Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-15T21:14:32.659Z Has data issue: false hasContentIssue false
  • English
  • Français

Vaccines against bovine babesiosis: where we are now and possible roads ahead

Published online by Cambridge University Press:  28 July 2014

MONICA FLORIN-CHRISTENSEN ,
CARLOS E. SUAREZ ,
ANABEL E. RODRIGUEZ ,
DANIELA A. FLORES  and
LEONHARD SCHNITTGER
MONICA FLORIN-CHRISTENSEN*
Affiliation:
Instituto de Patobiologia, CICVyA, INTA-Castelar, 1686 Hurlingham, Argentina CONICET, C1033AAJ Ciudad Autonoma de Buenos Aires, Argentina
CARLOS E. SUAREZ
Affiliation:
Department of Veterinary Microbiology and Pathology, Washington State University, Pullman, WA 99164-7040, USA ADRU-ARS, United States Department of Agriculture, Pullman, WA 99164-6630, USA
ANABEL E. RODRIGUEZ
Affiliation:
Instituto de Patobiologia, CICVyA, INTA-Castelar, 1686 Hurlingham, Argentina
DANIELA A. FLORES
Affiliation:
Instituto de Patobiologia, CICVyA, INTA-Castelar, 1686 Hurlingham, Argentina ANPCyT, C1425FQD Ciudad Autonoma de Buenos Aires, Argentina
LEONHARD SCHNITTGER
Affiliation:
Instituto de Patobiologia, CICVyA, INTA-Castelar, 1686 Hurlingham, Argentina CONICET, C1033AAJ Ciudad Autonoma de Buenos Aires, Argentina
*
*Corresponding author: Instituto de Patobiologia, CICVyA, INTA-Castelar, Los Reseros y Nicolas Repetto, s/n, 1686 Hurlingham, Argentina. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Bovine babesiosis caused by the tick-transmitted haemoprotozoans Babesia bovis, Babesia bigemina and Babesia divergens commonly results in substantial cattle morbidity and mortality in vast world areas. Although existing live vaccines confer protection, they have considerable disadvantages. Therefore, particularly in countries where large numbers of cattle are at risk, important research is directed towards improved vaccination strategies. Here a comprehensive overview of currently used live vaccines and of the status quo of experimental vaccine trials is presented. In addition, pertinent research fields potentially contributing to the development of novel non-live and/or live vaccines are discussed, including parasite antigens involved in host cell invasion and in pathogen-tick interactions, as well as the protective immunity against infection. The mining of available parasite genomes is continuously enlarging the array of potential vaccine candidates and, additionally, the recent development of a transfection tool for Babesia can significantly contribute to vaccine design. However, the complication and high cost of vaccination trials hinder Babesia vaccine research, and have so far seriously limited the systematic examination of antigen candidates and prevented an in-depth testing of formulations using different immunomodulators and antigen delivery systems.

Keywords

Bovine babesiosislive vaccinessubunit vaccinestransfectionerythrocyteinvasiontick-parasite interactionimmune response
Type
Research Article
Information
Parasitology , Volume 141 , Issue 12 , October 2014 , pp. 1563 - 1592
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

AbouLaila, M., Terkawi, M. A., Seuseu, F. J., Ota, N., de Macedo, A. C., Yokoyama, N., Xuan, X. and Igarashi, I. (2012). Expression and immunological characterization of the heat shock protein-70 homologue from Babesia bigemina. Veterinary Parasitology 190, 401–410.Google Scholar
Adl, S. M., Simpson, A. G., Farmer, M. A., Andersen, R. A., Anderson, O. R., Barta, J. R., Bowser, S. S., Brugerolle, G., Fensome, R. A., Fredericq, S., James, T. Y., Karpov, S., Kugrens, P., Krug, J., Lane, C. E., Lewis, L. A., Lodge, J., Lynn, D. H., Mann, D. G., Mc Court, R. M., Mendoza, L., Moestrup, O., Mozley-Standridge, S. E., Nerad, T. A., Shearer, C. A., Smirnov, A. V., Spiegel, F. W. and Taylor, M. F. (2005). The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. Journal of Eukaryotic Microbiology 52, 399–451.Google Scholar
Adl, S. M., Simpson, A. G., Lane, C. E., Lukeš, J., Bass, D., Bowser, S. S., Brown, M. W., Burki, F., Dunthorn, M., Hampl, V., Heiss, A., Hoppenrath, M., Lara, E., Le Gall, L., Lynn, D. H., McManus, H., Mitchell, E. A., Mozley-Stanridge, S. E., Parfrey, L. W., Pawlowski, J., Rueckert, S., Shadwick, R. S., Schoch, C. L., Smirnov, A. and Spiegel, F. W. (2012). The revised classification of eukaryotes. Journal of Eukaryotic Microbiology 59, 429–493.Google Scholar
Agarwal, S., Singh, M. K., Garg, S., Chitnis, C. E. and Singh, S. (2013). Ca(2+) -mediated exocytosis of subtilisin-like protease 1: a key step in egress of Plasmodium falciparum merozoites. Cell Microbiology 15, 910–921.Google Scholar
Aikawa, M., Rabbege, J., Uni, S., Ristic, M. and Miller, L. H. (1985). Structural alteration of the membrane of erythrocytes infected with Babesia bovis. American Journal of Tropical Medicine and Hygiene 34, 45–49.Google Scholar
Allred, D. R. and Al-Khedery, B. (2006). Antigenic variation as an exploitable weakness of babesial parasites. Veterinary Parasitology 138, 50–60.Google Scholar
Alvarez, A. J., Lopez, U., Rojas, C., Borgonio, V. M., Sanchez, V., Castañeda, R., Vargas, P. and Figueroa, J. V. (2010). Immunization of Bos taurus steers with Babesia bovis recombinant antigens MSA-1, MSA-2c and 12D3. Transboundary and Emerging Diseases 57, 87–90.Google Scholar
Angus, B. M. (1996). The history of the cattle tick Boophilus microplus in Australia and achievements in its control. International Journal for Parasitology 26, 1341–1355.Google Scholar
Antunes, S., Galindo, R. C., Almazán, C., Rudenko, N., Golovchenko, M., Grubhoffer, L., Shkap, V., do Rosário, V., de la Fuente, J. and Domingos, A. (2012). Functional genomics studies of Rhipicephalus (Boophilus) annulatus ticks in response to infection with the cattle protozoan parasite, Babesia bigemina. International Journal for Parasitology 42, 187–195.Google Scholar
Arama, C. and Troye-Blomberg, M. (2014). The path of malaria vaccine development: challenges and perspectives. Journal of Internal Medicine 275, 456–466.Google Scholar
Arevalo-Pinzon, G., Curtidor, H., Reyes, C., Pinto, M., Vizcaíno, C., Patarroyo, M. A. and Patarroyo, M. E. (2010). Fine mapping of Plasmodium falciparum ribosomal phosphoprotein PfP0 revealed sequences with highly specific binding activity to human red blood cells. Journal of Molecular Medicine 88, 61–74.Google Scholar
Asada, M., Goto, Y., Yahata, K., Yokoyama, N., Kawai, S., Inoue, N., Kaneko, O. and Kawazu, S. (2012 a). Gliding motility of Babesia bovis merozoites visualized by time-lapse video microscopy. PLOS ONE 7, e35227. doi: 10.1371/journal.pone.0035227.Google Scholar
Asada, M., Tanaka, M., Goto, Y., Yokoyama, N., Inoue, N. and Kawazu, S. (2012 b). Stable expression of green fluorescent protein and targeted disruption of thioredoxin peroxidase-1 gene in Babesia bovis with the WR99210/dhfr selection system. Molecular and Biochemical Parasitology 181, 162–170.Google Scholar
Aurrecoechea, C., Barreto, A., Brestelli, J., Brunk, B. P., Cade, S., Doherty, R., Fischer, S., Gajria, B., Gao, X., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Hu, S., Iodice, J., Kissinger, J. C., Kraemer, E. T., Li, W., Pinney, D. F., Pitts, B., Roos, D. S., Srinivasamoorthy, G., Stoeckert, C. J. Jr., Wang, H. and Warrenfeltz, S. (2013). EuPathDB: the eukaryotic pathogen database. Nucleic Acids Research 41, D684–D691.Google Scholar
Babes, V. (1888). Sur l'hemoglobinurie bacterienne du boeuf. Comptes rendus hebdomadaires des seances de l'Academie des Sciences, Paris 107, 692–694.Google Scholar
Bacchi, C. J., Nathan, H. C., Hutner, S. H., Duch, D. S. and Nichol, C. A. (1981). Prevention by polyamines of the curative effect of amicarbalide and imidocarb for Trypanosoma brucei infections in mice. Biochemical Pharmacology 30, 883–886.Google Scholar
Baravalle, M. E., Thompson, C., de Echaide, S. T., Palacios, C., Valentini, B., Suárez, C. E., Christensen, M. F. and Echaide, I. (2010). The novel protein BboRhop68 is expressed by intraerythrocytic stages of Babesia bovis. Parasitology International 59, 571–578.Google Scholar
Baravalle, M. E., Thompson, C., Valentini, B., Ferreira, M., Torioni de Echaide, S., Florin-Christensen, M. and Echaide, I. (2012). Babesia bovis biological clones and the inter-strain allelic diversity of the Bv80 gene support subpopulation selection as a mechanism involved in the attenuation of two virulent isolates. Veterinary Parasitology 190, 391–400.Google Scholar
Bastos, R. G., Johnson, W. C., Mwangi, W., Brown, W. C. and Goff, W. L. (2008). Bovine NK cells acquire cytotoxic activity and produce IFN-gamma after stimulation by Mycobacterium bovis BCG- or Babesia bovis-exposed splenic dendritic cells. Veterinary Immunology and Immunopathology 124, 302–312.Google Scholar
Bastos, R. G., Ueti, M. W., Knowles, D. P. and Scoles, G. A. (2010). The Rhipicephalus (Boophilus) microplus Bm86 gene plays a critical role in the fitness of ticks fed on cattle during acute Babesia bovis infection. Parasites and Vectors 3, 111.Google Scholar
Bastos, R. G., Suarez, C. E., Laughery, J. M., Johnson, W. C., Ueti, M. W. and Knowles, D. P. (2013). Differential expression of three members of the multidomain adhesion CCp family in Babesia bigemina, Babesia bovis and Theileria equi. PLOS ONE 8, e67765.Google Scholar
Bautista, C. R., Alvarez, J. A., Mosqueda, J. J., Falcon, A., Ramos, J. A., Rojas, C., Figueroa, J. V. and Ku, M. (2008). Enhancement of the Mexican bovine babesiosis vaccine efficacy by using Lactobacillus casei. Annals of the New York Academy of Sciences 1149, 126–130.Google Scholar
Bautista, C. R., Castañeda, R., Alvarez, J. A., Rojas, C., Figueroa, J. V. and Rodriguez, A. (2012). The simultaneous vaccination of bovines with Lactobacillus casei and the bivalent vaccine against bovine babesiosis induces a better protection against Babesia bovis and B. bigemina transmitted by ticks in extreme field conditions. Veterinaria México 43, 189–200.Google Scholar
Beard, L. A., Pelzel, A. M., Rush, B. R., Wright, A. M., Galgut, B. I., Hennager, S. G., King, A. O. and Traub-Dargatz, J. L. (2013). Babesia equi-induced anemia in a Quarter Horse and subsequent regulatory response. Journal of the American Veterinary Medical Association 242, 992–996.Google Scholar
Becker, C. A. M., Malandrin, L., Depoix, D., Larcher, T., David, P. H., Chauvin, A., Bischoff, E. and Bonnet, S. (2010). Identification of three CCp genes in Babesia divergens: novel markers for sexual stages parasites. Molecular and Biochemical Parasitology 174, 36–43.Google Scholar
Benavides, E., Vizcaino, O., Britto, C. M., Romero, A. and Rubio, A. (2000). Attenuated trivalent vaccine against babesiosis and anaplasmosis in Colombia. Annals of the New York Academy of Sciences 916, 613–616.Google Scholar
Benavides, M. V. and Sacco, A. M. (2007). Differential Bos taurus cattle response to Babesia bovis infection. Veterinary Parasitology 150, 54–64.Google Scholar
Benitez, D., Cetrá, B. and Florin-Christensen, M. (2012). Rhipicephalus (Boophilus) microplus ticks can complete their life cycle on the water buffalo (Bubalus bubalis). Journal of Buffalo Science 1, 193–197.Google Scholar
Ben Musa, N. and Phillips, R. S. (1991). The adaptation of three isolates of Babesia divergens to continuous culture in rat erythrocytes. Parasitology 103, 165–170.Google Scholar
Besteiro, S., Dubremetz, J. F. and Lebrun, M. (2011). The moving junction of apicomplexan parasites: a key structure for invasion. Cell Microbiology 13, 797–805.Google Scholar
Bock, R. E. and de Vos, A. J. (2001). Immunity following use of Australian tick fever vaccine: a review of the evidence. Australian Veterinary Journal 79, 832–839.Google Scholar
Bock, R. E., de Vos, A. J., Kingston, T. G., Shiels, I. A. and Dalgliesh, R. J. (1992). Investigations of breakdowns in protection provided by living Babesia bovis vaccine. Veterinary Parasitology 43, 45–56.Google Scholar
Bock, R. E., de Vos, A. J., Kingston, T. G. and McLellan, D. J. (1997). Effect of breed of cattle on innate resistance to infection with Babesia bovis, B. bigemina and Anaplasma marginale. Australian Veterinary Journal 75, 337–340.Google Scholar
Bock, R., Jackson, L., de Vos, A. and Jorgensen, W. (2004). Babesiosis of cattle. Parasitology 129(Suppl.), S247–S269.Google Scholar
Bork, S., Okamura, M., Matsuo, T., Kumar, S., Yokoyama, N. and Igarashi, I. (2005). Host serum modifies the drug susceptibility of Babesia bovis in vitro. Parasitology 130, 489–492.Google Scholar
Bradley, P. J. and Sibley, L. D. (2007). Rhoptries: an arsenal of secreted virulence factors. Current Opinion in Microbiology 10, 582–587.Google Scholar
Bram, R. A., George, J. E., Reichar, R. E. and Tabaciinic, W. J. (2002). Threat of foreign arthropod-borne pathogens to livestock in the United States. Journal of Medical Entomology 39, 405–416.Google Scholar
Brasseur, P., Lecoublet, S., Kapel, N., Favennec, L. and Ballet, J. J. (1998). In vitro evaluation of drug susceptibilities of Babesia divergens isolates. Antimicrobial Agents and Chemotherapy 42, 818–820.Google Scholar
Brayton, K. A., Lau, A. O., Herndon, D. R., Hannick, L., Kappmeyer, L. S., Berens, S. J., Bidwell, S. L., Brown, W. C., Crabtree, J., Fadrosh, D., Feldblum, T., Forberger, H. A., Haas, B. J., Howell, J. M., Khouri, H., Koo, H., Mann, D. J., Norimine, J., Paulsen, I. T., Radune, D., Ren, Q., Smith, R. K. Jr., Suarez, C. E., White, O., Wortman, J. R., Knowles, D. P. Jr., McElwain, T. F. and Nene, V. M. (2007). Genome sequence of Babesia bovis and comparative analysis of apicomplexan hemoprotozoa. PLOS Pathogens 3, 1401–1413.Google Scholar
Brown, W. C. and Corral, R. S. (2002). Stimulation of B lymphocytes, macrophages, and dendritic cells by protozoan DNA. Microbes and Infection 4, 969–974.Google Scholar
Brown, W. C. and Palmer, G. H. (1999). Designing blood-stage vaccines against Babesia bovis and B. bigemina. Parasitology Today (personal ed.) 15, 275–281.Google Scholar
Brown, W. C., Estes, D. M., Chantler, S. E., Kegerreis, K. A. and Suarez, C. E. (1998). DNA and a CpG oligonucleotide derived from Babesia bovis are mitogenic for bovine B cells. Infection and Immunity 66, 5423–5432.Google Scholar
Brown, W. C., McElwain, T. F., Palmer, G. H., Chantler, S. E. and Estes, D. M. (1999 a). Bovine CD4(+) T-lymphocyte clones specific for rhoptry-associated protein 1 of Babesia bigemina stimulate enhanced immunoglobulin G1 (IgG1) and IgG2 synthesis. Infection and Immunity 67, 155–164.Google Scholar
Brown, W. C., Suarez, C. E., Shoda, L. K. and Estes, D. M. (1999 b). Modulation of host immune responses by protozoal DNA. Veterinary Immunology and Immunopathology 72, 87–94.Google Scholar
Brown, W. C., Ruef, B. J., Norimine, J., Kegerreis, K. A., Suarez, C. E., Conley, P. G., Stich, R. W., Carson, K. H. and Rice-Ficht, A. C. (2001). A novel 20-kilodalton protein conserved in Babesia bovis and B. bigemina stimulates memory CD4(+) T lymphocyte responses in B. bovis-immune cattle. Molecular and Biochemical Parasitology 118, 97–109.Google Scholar
Brown, W. C., Norimine, J., Knowles, D. P. and Goff, W. L. (2006 a). Immune control of Babesia bovis infection. Veterinary Parasitology 138, 75–87.Google Scholar
Brown, W. C., Norimine, J., Goff, W. L., Suarez, C. E. and McElwain, T. F. (2006 b). Prospects for recombinant vaccines against Babesia bovis and related parasites. Parasite Immunology 28, 315–327.Google Scholar
Buling, A., Criado-Fornelio, A., Asenzo, G., Benitez, D., Barba-Carretero, J. C. and Florin-Christensen, M. (2007). A quantitative PCR assay for the detection and quantification of Babesia bovis and B. bigemina. Veterinary Parasitology 147, 16–25.Google Scholar
Caballero, M. C., Pedroni, M. J., Palmer, G. H., Suarez, C. E., Davitt, C. and Lau, A. O. (2012). Characterization of acyl carrier protein and LytB in Babesia bovis apicoplast. Molecular and Biochemical Parasitology 181, 125–133.Google Scholar
Callow, L. L. (1979). Some aspects of the epidemiology and control of bovine babesiosis in Australia. Journal of the South African Veterinary Association 50, 353–356.Google Scholar
Cantó Alarcón, G. J., Martínez, J. A. Á., Rojas Ramírez, E. E., Ramos Aragón, J. A., Mosqueda Gualito, J. J., Vega y Murguía, C. A. and Figueroa Millán, J. V. (2003). Protección contra babesiosis bovina con una vacuna mixta de Babesia bovis y Babesia bigemina derivada de cultivo in Vitro bajo una confrontación de campo. Veterinaria México 34, 323–332.Google Scholar
Cantu, A., Ortega-S, J. A., Mosqueda, J., Garcia-Vazquez, Z., Henke, S. E. and George, J. E. (2007). Immunologic and molecular identification of Babesia bovis and Babesia bigemina in free-ranging white-tailed deer in northern Mexico. Journal of Wildlife Diseases 43, 504–507.Google Scholar
Carcy, B., Précigout, E., Valentin, A., Gorenflot, A., Reese, R. T. and Schrével, J. (1991). Heat shock response of Babesia divergens and identification of the hsp70 as an immunodominant early antigen during ox, gerbil and human babesiosis. Biology of the Cell 72, 93–102.Google Scholar
Carcy, B., Precigout, E., Valentin, A., Gorenflot, A. and Schrevel, J. (1995). A 37-kilodalton glycoprotein of Babesia divergens is a major component of a protective fraction containing low-molecular-mass culture-derived exoantigens. Infection and Immunity 63, 811–817.Google Scholar
Carcy, B., Précigout, E., Schetters, T. and Gorenflot, A. (2006). Genetic basis for GPI anchor merozoite surface antigen polymorphism of Babesia and resulting antigenic diversity. Veterinary Parasitology 138, 33–49.Google Scholar
Carson, C. A., Timms, P., Cowman, A. F. and Stewart, N. P. (1990). Babesia bovis: evidence for selection of subpopulations during attenuation. Experimental Parasitology 70, 404–410.Google Scholar
Chauvin, A., Valentin, A., Malandrin, L. and L'Hostis, M. (2002). Sheep as a new experimental host for Babesia divergens. Veterinary Research 33, 429–433.Google Scholar
Chhabra, S., Ranjan, R., Uppal, S. K. and Singla, L. D. (2012). Transplacental transmission of Babesia equi (Theileria equi) from carrier mares to foals. Journal of Parasitic Diseases 36, 31–33.Google Scholar
Clark, J. S. (1951). Texas fever in Oklahoma. In Oklahoma´s Historical Society´s Chronicles of Oklahoma (ed. Oklahoma Historical Society), vol. 29, pp. 429–444. Electronic Publishing Center, Oklahoma State University, Oklahoma City, OK, USA.Google Scholar
Combrink, M. P., Troskie, P. C., Pienaar, R., Latif, A. A. and Mans, B. J. (2014). Genotypic diversity in Babesia bovis field isolates and vaccine strains from South Africa. Veterinary Parasitology 199, 144–152.Google Scholar
Connaway, J. W. and Francis, M. C. (1899). Texas fever. Experiments made by the Missouri Experimental Station and the Missouri State Board of Agriculture in cooperation with Texas Experimental Station in immunizing northern breeding cattle against Texas fever from the southern state. Missouri Agricultural Experiment Station Bulletins 48, 1–64.Google Scholar
Cornillot, E., Hadj-Kaddour, K., Dassouli, A., Noel, B., Ranwez, V., Vacherie, B., Augagneur, Y., Brès, V., Duclos, A., Randazzo, S., Carcy, B., Debierre-Grockiego, F., Delbecq, S., Moubri-Ménage, K., Shams-Eldin, H., Usmani-Brown, S., Bringaud, F., Wincker, P., Vivarès, C. P., Schwarz, R. T., Schetters, T. P., Krause, P. J., Gorenflot, A., Berry, V., Barbe, V. and BenMamoun, C. (2012). Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti. Nucleic Acids Research 40, 9102–9114.Google Scholar
Court, R. A., Jackson, L. A. and Lee, R. P. (2001). Elevated anti-parasitic activity in peripheral blood monocytes and neutrophils of cattle infected with Babesia bovis. International Journal for Parasitology 31, 29–37.Google Scholar
Criado-Fornelio, A., Buling, A., Asenzo, G., Benitez, D., Florin-Christensen, M., Gonzalez-Oliva, A., Henriques, G., Silva, M., Alongi, A., Agnone, A., Torina, A. and Madruga, C. R. (2009). Development of fluorogenic probe-based PCR assays for the detection and quantification of bovine piroplasmids. Veterinary Parasitology 162, 200–206.Google Scholar
Crompton, P. D., Pierce, S. K. and Miller, L. H. (2010). Advances and challenges in malaria vaccine development. Journal of Clinical Investigation 120, 4168–4178.Google Scholar
Cursino-Santos, J. R., Halverson, G., Rodriguez, M., Narla, M. and Lobo, C. A. (2014). Identification of binding domains on red blood cell glycophorins for Babesia divergens. Transfusion 54, 982–989.Google Scholar
Dalgliesh, R. J., Callow, L. L., Mellors, L. T. and McGregor, W. (1981). Development of a highly infective Babesia bigemina vaccine of reduced virulence. Australian Veterinary Journal 57, 8–11.Google Scholar
Dalgliesh, R. J., Jorgensen, W. K. and de Vos, A. J. (1990). New Australian vaccines for the control of babesiosis and anaplasmosis in the world cattle trade. Tropical Animal Health Production 22, 44–52.Google Scholar
da Silveira, J. A., Rabelo, E. M. and Ribeiro, M. F. (2011). Detection of Theileria and Babesia in brown brocket deer (Mazama gouazoubira) and marsh deer (Blastocerus dichotomus) in the State of Minas Gerais, Brazil. Veterinary Parasitology 177, 61–66.Google Scholar
Davis, W. C., Wyatt, C. R., Hamilton, M. J. and Goff, W. L. (1992). A rapid, reliable method of evaluating growth and viability of intraerythrocytic protozoan hemoparasites using fluorescence flow cytometry. Memórias do instituto Oswaldo Cruz 87, 235–239.Google Scholar
de la Fuente, J. (2012). Vaccines for vector control: exciting possibilities for the future. Veterinary Journal 194, 139–140.Google Scholar
de la Fuente, J. and Merino, O. (2013). Vaccinomics, the new road to tick vaccines. Vaccine 31, 5923–5929.Google Scholar
de la Fuente, J., Rodríguez, M., Montero, C., Redondo, M., García-García, J. C., Méndez, L., Serrano, E., Valdés, M., Enríquez, A., Canales, M., Ramos, E., Boué, O., Machado, H. and Lleonart, R. (1999). Vaccination against ticks (Boophilus spp.): the experience with the Bm86-based vaccine Gavac. Genetic Analysis 15, 143–148.Google Scholar
de Vos, A. J. (1979). Epidemiology and control of bovine babesiosis in South Africa. Journal of the South African Veterinary Association 50, 357–362.Google Scholar
de Vos, A. J., Dalgliesh, R. J. and McGregor, W. (1986). Effect of imidocarb dipropionate prophylaxis on the infectivity and immunogenicity of a Babesia bovis vaccine in cattle. Australian Veterinary Journal 63, 174–178.Google Scholar
de Vries, E., Corton, C., Harris, B., Cornelissen, A. W. and Berriman, M. (2006). Expressed sequence tag (EST) analysis of the erythrocytic stages of Babesia bovis. Veterinary Parasitology 138, 61–74.Google Scholar
de Waal, D. T. (1996). Vaccination against babesiosis. Acta Parasitologica Turcica 20, 487–499.Google Scholar
de Waal, D. T. and Combrink, M. P. (2006). Live vaccines against bovine babesiosis. Veterinary Parasitology 138, 88–96.Google Scholar
Delbecq, S., Precigout, E., Vallet, A., Carcy, B., Schetters, T. P. and Gorenflot, A. (2002). Babesia divergens: cloning and biochemical characterization of Bd37. Parasitology 125, 305–312.Google Scholar
Delbecq, S., Hadj-Kaddour, K., Randazzo, S., Kleuskens, J., Schetters, T., Gorenflot, A. and Précigout, E. (2006). Hydrophobic moeties in recombinant proteins are crucial to generate efficient saponin-based vaccine against Apicomplexan Babesia divergens. Vaccine 24, 613–621.Google Scholar
Delbecq, S., Auguin, D., Yang, Y. S., Löhr, F., Arold, S., Schetters, T., Précigout, E., Gorenflot, A. and Roumestand, C. (2008). The solution structure of the adhesion protein Bd37 from Babesia divergens reveals structural homology with eukaryotic proteins involved in membrane trafficking. Journal of Molecular Biology 375, 409–424.Google Scholar
Dhawan, S., Dua, M., Chishti, A. H. and Hanspal, M. (2003). Ankyrin peptide blocks falcipain-2-mediated malaria parasite release from red blood cells. Journal of Biological Chemistry 278, 30180–30186.Google Scholar
Dominguez, M., Echaide, I., Echaide, S. T., Mosqueda, J., Cetrá, B., Suarez, C. E. and Florin-Christensen, M. (2010). In silico predicted conserved B-cell epitopes in the merozoite surface antigen-2 family of B. bovis are neutralization sensitive. Veterinary Parasitology 167, 216–226.Google Scholar
Dominguez, M., Ferreri, L. and Schnittger, L. (2011). Canonical and variant histone repertoire in Babesia bovis and their possible relevance in epigenetic regulation. In Proceedings of the 23rd International Conference of the World Association for the Advancement of Veterinary Parasitology, p. 326.Google Scholar
Dominguez, M., Echaide, I., de Echaide, S. T., Wilkowsky, S., Zabal, O., Mosqueda, J. J., Schnittger, L. and Florin-Christensen, M. (2012). Validation and field evaluation of a competitive enzyme-linked immunosorbent assay for diagnosis of Babesia bovis infections in Argentina. Clinical and Vaccine Immunology 19, 924–928.Google Scholar
Dowling, S. C., Perryman, L. E. and Jasmer, D. P. (1996). A Babesia bovis 225-kilodalton spherical-body protein: localization to the cytoplasmic face of infected erythrocytes after merozoite invasion. Infection and Immunity 64, 2618–2626.Google Scholar
Dubremetz, J. F., Garcia-Reguet, N., Conseil, V. and Fourmaux, M. N. (1998). Apical organelles and host-cell invasion by Apicomplexa. International Journal for Parasitology 28, 1007–1013.Google Scholar
Echaide, I. E. (2008). Bovine Babesiosis: vaccines. In Proceedings of the XV Congreso Brasileiro de Parasitología Veterinaria. Curitiba, Brazil. http://www.docstoc.com/docs/122076821/BOVINE-BABESIOSIS-VACCINES-BABESIOSES-DOS-BOVINOS-pdf.Google Scholar
Echaide, I. E., de Echaide, S. T. and Guglielmone, A. A. (1993 a). Live and soluble antigens for cattle protection to Babesia bigemina. Veterinary Parasitology 51, 35–40.Google Scholar
Echaide, I. E., de Echaide, S. T.Mangold, A. J. and Guglielmone, A. A. (1993 b). Live and soluble antigens from in vitro culture to vaccinate cattle against Babesia bovis. In Proceedings of the IX International Veterinary Hemoparasite Disease Conference. Mérida, México, p. 13.Google Scholar
Edelhofer, R., Kanout, A., Schuh, M. and Kutzer, E. (1998). Improved disease resistance after Babesia divergens vaccination. Parasitology Research 84, 181–187.Google Scholar
Ellse, L. and Wall, R. (2013). The use of essential oils in veterinary ectoparasite control: a review. Medical and Veterinary Entomology. doi: 10.1111/mve.12033. [Epub ahead of print]Google Scholar
Estes, D. M. and Brown, W. C. (2002). Type 1 and type 2 responses in regulation of Ig isotype expression in cattle. Veterinary Immunology and Immunopathology 90, 1–10.Google Scholar
Fernandez-Becerra, C., de Azevedo, M. F., Yamamoto, M. M. and del Portillo, H. A. (2003). Plasmodium falciparum: new vector with bi-directional promoter activity to stably express transgenes. Experimental Parasitology 103, 88–91.Google Scholar
Ferreri, L., Benitez, D., Dominguez, M., Rodriguez, A., Asenzo, G., Mesplet, M., Florin-Christensen, M. and Schnittger, L. (2008). Water buffalos as carriers of Babesia bovis in Argentina. Annals of the New York Academy of Sciences 1149, 149–151.Google Scholar
Fish, L., Leibovich, B., Krigel, Y., McElwain, T. and Shkap, V. (2008). Vaccination of cattle against B. bovis infection with live attenuated parasites and non-viable immunogens. Vaccine 26, G29–G33.Google Scholar
Fisher, T. G., McElwain, T. F. and Palmer, G. H. (2001). Molecular basis for variable expression of merozoite surface antigen gp45 among American isolates of Babesia bigemina. Infection and Immunity 69, 3782–3790.Google Scholar
Fletcher, T. I., Wigg, J. L., Rolls, P. J. and de Vos, A. J. (2009). Viability assays of intraerythrocytic organisms using fluorescent dyes. Veterinary Parasitology 163, 144–147.Google Scholar
Flores, D., Minichiello, Y., Araujo, F. R., Shkap, V., Benitez, D., Echaide, I., Rolls, P., Mosqueda, J., Pacheco, G. M., Petterson, M., Florin-Christensen, M. and Schnittger, L. (2013). Evidence for extensive genetic diversity and substructuring of the Babesia bovis metapopulation. Transboundary and Emerging Diseases 60, 131–136.Google Scholar
Florin-Christensen, M. and Schnittger, L. (2009). Piroplasmids and ticks: a long-lasting intimate relationship. Frontiers Bioscience (Landmark Ed) 14, 3064–3073.Google Scholar
Florin-Christensen, J., Suarez, C. E., Florin-Christensen, M., Hines, S. A., McElwain, T. F. and Palmer, G. H. (2000). Phosphatidylcholine formation is the predominant lipid biosynthetic event in the hemoparasite Babesia bovis. Molecular and Biochemical Parasitology 106, 147–156.Google Scholar
Florin-Christensen, M., Schnittger, L., Dominguez, M., Mesplet, M., Rodriguez, A., Ferreri, L., Asenzo, G., Wilkowsky, S., Farber, M., Echaide, I. and Suarez, C. (2007). Search for Babesia bovis vaccine candidates. Parassitologia 49, 9–12.Google Scholar
Freeman, J. M., Kappmeyer, L. S., Ueti, M. W., McElwain, T. F., Baszler, T. V., Echaide, I., Nene, V. M. and Knowles, D. P. (2010). A Babesia bovis gene syntenic to Theileria parva p67 is expressed in blood and tick stage parasites. Veterinary Parasitology 173, 211–218.Google Scholar
Gaffar, F. R., Franssen, F. F. and de Vries, E. (2003). Babesia bovis merozoites invade human, ovine, equine, porcine and caprine erythrocytes by a sialic acid-dependent mechanism followed by developmental arrest after a single round of cell fission. International Journal for Parasitology 33, 1595–1603.Google Scholar
Gaffar, F. R., Yatsuda, A. P., Franssen, F. F. and de Vries, E. (2004 a). Erythrocyte invasion by Babesia bovis merozoites is inhibited by polyclonal antisera directed against peptides derived from a homologue of Plasmodium falciparum apical membrane antigen 1. Infection and Immunity 72, 2947–2955.Google Scholar
Gaffar, F. R., Yatsuda, A. P., Franssen, F. F. and de Vries, E. (2004 b). A Babesia bovis merozoite protein with a domain architecture highly similar to the thrombospondin-related anonymous protein (TRAP) present in Plasmodium sporozoites. Molecular and Biochemical Parasitology 136, 25–34.Google Scholar
Galay, R. L., Maeda, H., Aung, K. M., Umemiya-Shirafuji, R., Xuan, X., Igarashi, I., Tsuji, N., Tanaka, T. and Fujisaki, K. (2011). Anti-babesial activity of a potent peptide fragment derived from longicin of Haemaphysalis longicornis. Tropical Animal Health and Production 44, 343–348.Google Scholar
Gardner, M. J., Bishop, R., Shah, T., de Villiers, E. P., Carlton, J. M., Hall, N., Ren, Q., Paulsen, I. T., Pain, A., Berriman, M., Wilson, R. J., Sato, S., Ralph, S. A., Mann, D. J., Xiong, Z., Shallom, S. J., Weidman, J., Jiang, L., Lynn, J., Weaver, B., Shoaibi, A., Domingo, A. R., Wasawo, D., Crabtree, J., Wortman, J. R., Haas, B., Angiuoli, S. V., Creasy, T. H., Lu, C., Suh, B., Silva, J. C., Utterback, T. R., Feldblyum, T. V., Pertea, M., Allen, J., Nierman, W. C., Taracha, E. L., Salzberg, S. L., White, O. R., Fitzhugh, H. A., Morzaria, S., Venter, J. C., Fraser, C. M. and Nene, V. (2005). Genome sequence of Theileria parva, a bovine pathogen that transforms lymphocytes. Science 309, 134–137.Google Scholar
Ghosh, S., Azhahianambi, P. and Yadav, M. P. (2007). Upcoming and future strategies of tick control: a review. Journal of Vector Borne Diseases 44, 79–89.Google Scholar
Gimenez, G., Magalhaes, K. G., Belaunzarán, M. L., Poncini, C. V., Lammel, E. M., Gonzalex-Cappa, S. M., Bozza, P. T. and Isola, E. L. (2010). Lipids from attenuated and virulent Babesia bovis strains induce differential TLR2-mediated macrophage activation. Molecular Immunology 47, 747–755.Google Scholar
Gimenez, G., Belaunzarán, M. L., Poncini, C. V., Blanco, F. C., Echaide, I., Zamorano, P. I., Lammel, E. M., González Cappa, S. M. and Isola, E. L. (2013). Babesia bovis: lipids from virulent S2P and attenuated R1A strains trigger differential signalling and inflammatory responses in bovine macrophages. Parasitology 140, 530–540.Google Scholar
Goff, W. L. and Yunker, C. E. (1986). Babesia bovis: increased percentage parasitized erythrocytes in cultures and assessment of growth by incorporation of [3H] hypoxanthine. Experimental Parasitology 62, 202–210.Google Scholar
Goff, W. L., Johnson, W. C., Parish, S. M., Barrington, G. M., Tuo, W. and Valdez, R. A. (2001). The age-related immunity in cattle to Babesia bovis infection involves the rapid induction of interleukin-12, interferon-gamma and inducible nitric oxide synthase mRNA expression in the spleen. Parasite Immunology 23, 463–471.Google Scholar
Goff, W. L., Johnson, W. C., Parish, S. M., Barrington, G. M., Elsasser, T. H., Davis, W. C. and Valdez, R. A. (2002 a). IL-4 and IL-10 inhibition of IFN-gamma- and TNFalpha-dependent nitric oxide production from bovine mononuclear phagocytes exposed to Babesia bovis merozoites. Veterinary Immunology and Immunopathology 84, 237–251.Google Scholar
Goff, W. L., Johnson, W. C., Tuo, W., Valdez, R. A., Parish, S. M., Barrington, G. M. and Davis, W. C. (2002 b). Age-related innate immune response in calves to Babesia bovis involves IL-12 induction and IL-10 modulation. Annals of the New York Academy of Sciences 969, 164–168.Google Scholar
Goff, W. L., Johnson, W. C., Horn, R. H., Barrington, G. M. and Knowles, D. P. (2003). The innate immune response in calves to Boophilus microplus tick transmitted Babesia bovis involves type-1 cytokine induction and NK-like cells in the spleen. Parasite Immunology 25, 185–188.Google Scholar
Goff, W. L., Molloy, J. B., Johnson, W. C., Suarez, C. E., Pino, I., Rhalem, A., Sahibi, H., Ceci, L., Carelli, G., Adams, D. S., McGuire, T. C., Knowles, D. P. and McElwain, T. F. (2006 a). Validation of a competitive enzyme-linked immunosorbent assay for detection of antibodies against Babesia bovis. Clinical and Vaccine Immunology 13, 1212–1216.Google Scholar
Goff, W. L., Storset, A. K., Johnson, W. C. and Brown, W. C. (2006 b). Bovine splenic NK cells synthesize IFN-gamma in response to IL-12-containing supernatants from Babesia bovis-exposed monocyte cultures. Parasite Immunology 28, 221–228.Google Scholar
Goff, W. L., Johnson, W. C., Molloy, J. B., Jorgensen, W. K., Waldron, S. J., Figueroa, J. V., Matthee, O., Adams, D. S., McGuire, T. C., Pino, I., Mosqueda, J., Palmer, G. H., Suarez, C. E., Knowles, D. P. and McElwain, T. F. (2008). Validation of a competitive enzyme-linked immunosorbent assay for detection of Babesia bigemina antibodies in cattle. Clinical and Vaccine Immunology 15, 1316–1321.Google Scholar
Goff, W. L., Bastos, R. G., Brown, W. C., Johnson, W. C. and Schneider, D. A. (2010). The bovine spleen: interactions among splenic cell populations in the innate immunologic control of hemoparasitic infections. Veterinary Immunology and Immunopathology 138, 1–14.Google Scholar
Gohil, S., Kats, L. M., Sturm, A. and Cooke, B. M. (2010). Recent insights into alteration of red blood cells by Babesia bovis: moovin' forward. Trends in Parasitology 26, 591–599.Google Scholar
Gohil, S., Kats, L. M., Seemann, T., Fernandez, K. M., Siddiqui, G. and Cooke, B. M. (2013). Bioinformatic prediction of the exportome of Babesia bovis and identification of novel proteins in parasite-infected red blood cells. International Journal for Parasitology 43, 409–416.Google Scholar
Goodger, B. V., Commins, M. A., Waltisbuhl, D. J., Wright, I. G. and Rode-Bramanis, K. (1990). Babesia bovis: immunity induced by vaccination with a lipid enriched fraction. International Journal for Parasitology 20, 685–687.Google Scholar
Goodswen, S. J., Kennedy, P. J. and Ellis, J. T. (2012). Evaluating high-throughput Ab initio gene finders to discover proteins encoded in eurkaryotic pathogen genomes missed by laboratory techniques. PLOS ONE 7, e50609.Google Scholar
Goodswen, S. J., Kennedy, P. J. and Ellis, J. T. (2013). A novel strategy for classifying the output from an in silico vaccine discovery pipeline for eukaryotic pathogens using machine learning algorithms. BMC Bioinformatics 14, 315.Google Scholar
Graf, J. F., Gogolewski, R., Leach-Bing, N., Sabatini, G. A., Molento, M. B., Bordin, E. L. and Arantes, G. J. (2004). Tick control: an industry point of view. Parasitology 129(Suppl.), S427–S442.Google Scholar
Graham, O. H. and Hourrigan, J. L. (1977). Eradication programs for the arthropod parasites of livestock. Journal of Medical Entomology 13, 629–658.Google Scholar
Grande, N., Precigout, E., Ancelin, M. L., Moubri, K., Carcy, B., Lemesre, J. L., Vial, H. and Gorenflot, A. (1997). Continuous in vitro culture of Babesia divergens in a serumfree medium. Parasitology 115, 451–469.Google Scholar
Gray, J. S. (1983). Chemotherapy of Babesia divergens in the gerbil, Meriones unguiculatus. Research in Veterinary Science 35, 318–324.Google Scholar
Gray, J. S. (2006). Identity of the causal agents of human babesiosis in Europe. International Journal of Medical Microbiology 40, 131S–136S.Google Scholar
Gubbels, M. J. and Duraisingh, M. T. (2012). Evolution of apicomplexan secretory organelles. International Journal for Parasitology 42, 1071–1081.Google Scholar
Guerrero, F. D., Bendele, K. G., Davey, R. B. and George, J. E. (2007). Detection of Babesia bigemina infection in strains of Rhipicephalus (Boophilus) microplus collected from outbreaks in south Texas. Veterinary Parasitology 145, 156–163.Google Scholar
Guillemi, E., Ruybal, P., Lia, V., González, S., Farber, M. and Wilkowsky, S. E. (2013). Multi-locus typing scheme for Babesia bovis and Babesia bigemina reveals high levels of genetic variability in strains from Northern Argentina. Infection, Genetics and Evolution 14, 214–222.Google Scholar
Guthrie, C. C. (1905). A contribution to the clinical knowledge of Texas fever. Journal of Infectious Diseases 2, 529–554.Google Scholar
Hadj-Kaddour, K., Carcy, B., Vallet, A., Randazzo, S., Delbecq, S., Kleuskens, J., Schetters, T., Gorenflot, A. and Precigout, E. (2007). Recombinant protein Bd37 protected gerbils against heterologous challenges with isolates of Babesia divergens polymorphic for the bd37 gene. Parasitology 134(Pt 2), 187–196.Google Scholar
Hayashida, K., Hara, Y., Abe, T., Yamasaki, C., Toyoda, A., Kosuge, T., Suzuki, Y., Sato, Y., Kawashima, S., Katayama, T., Wakaguri, H., Inoue, N., Homma, K., Tada-Umezaki, M., Yagi, Y., Fujii, Y., Habara, T., Kanehisa, M., Watanabe, H., Ito, K., Gojobori, T., Sugawara, H., Imanishi, T., Weir, W., Gardner, M., Pain, A., Shiels, B., Hattori, M., Nene, V. and Sugimoto, C. (2012). Comparative genome analysis of three eukaryotic parasites with differing abilities to transform leukocytes reveals key mediators of Theileria-induced leukocyte transformation. MBio 3, e00204–e00212.Google Scholar
Hayashida, K., Abe, T., Weir, W., Nakao, R., Ito, K., Kajino, K., Suzuki, Y., Jongejan, F., Geysen, D. and Sugimoto, C. (2013). Whole-genome sequencing of Theileria parva strains provides insight into parasite migration and diversification in the African continent. DNA Research 20, 209–220.Google Scholar
Heekin, A. M., Guerrero, F. D., Bendele, K. G., Saldivar, L., Scoles, G. A., Gondro, C., Nene, V., Djikeng, A. and Brayton, K. A. (2012). Analysis of Babesia bovis infection induced gene expression changes in larvae from the cattle tick, Rhipicephalus (Boophilus) microplus. Parasites and Vectors 5, 162.Google Scholar
Heekin, A. M., Guerrero, F. D., Bendele, K. G., Saldivar, L., Scoles, G. A., Dowd, S. E., Gondro, C., Nene, V., Djikeng, A. and Brayton, K. A. (2013). Gut transcriptome of replete adult female cattle ticks, Rhipicephalus (Boophilus) microplus, feeding upon a Babesia bovis-infected bovine host. Parasitology Research 112, 3075–3090.Google Scholar
Hinaidy, H. K. (1981). Bovine babesiasis in Austria. IV. Studies with killed vaccines. Berliner und Münchener tieärztliche Wochenschrift 94, 121–125.Google Scholar
Hines, S. A., McElwain, T. F., Buening, G. M. and Palmer, G. H. (1989). Molecular characterization of Babesia bovis merozoite surface proteins bearing epitopes immunodominant in protected cattle. Molecular and Biochemical Parasitology 37, 1–9.Google Scholar
Hines, S. A., Palmer, G. H., Jasmer, D. P., McGuire, T. C. and McElwain, T. F. (1992). Neutralization-sensitive merozoite surface antigens of Babesia bovis encoded by members of a polymorphic gene family. Molecular and Biochemical Parasitology 55, 85–94.Google Scholar
Hines, S. A., Palmer, G. H., Jasmer, D. P., Goff, W. L. and McElwain, T. F. (1995). Immunization of cattle with recombinant Babesia bovis merozoite surface antigen-1. Infection and Immunity 63, 349–352.Google Scholar
Holman, P. J., Carroll, J. E., Pugh, R. and Davis, D. S. (2011). Molecular detection of Babesia bovis and Babesia bigemina in white-tailed deer (Odocoileus virginianus) from Tom Green County in central Texas. Veterinary Parasitology 177, 298–304.Google Scholar
Homer, M. J., Aguilar-Delfin, I., Telford, S. R. III, Krause, P. J. and Persing, D. H. (2000). Babesiosis. Clinical Microbiology Reviews 13, 451–469.Google Scholar
Hope, M., Riding, G., Menzies, M., Colditz, I., Reverter, A. and Willadsen, P. (2005). Potential for recombinant Babesia bovis antigens to protect against a highly virulent isolate. Parasite Immunology 27, 439–445.Google Scholar
Huang, Y., Xiao, Y. P. and Allred, D. R. (2013). Unusual chromatin structure associated with monoparalogous transcription of the Babesia bovis ves multigen family. International Journal for Parasitology 43, 163–172.Google Scholar
Jackson, A. P., Otto, T. D., Darby, A., Ramaprasad, A., Xia, D., Echaide, I. E., Farber, M., Gahlot, S., Gamble, J., Gupta, D., Gupta, Y., Jackson, L., Malandrin, L., Malas, T. B., Moussa, E., Nair, M., Reid, A. J., Sanders, M., Sharma, J., Tracey, A., Quail, M. A., Weir, W., Wastling, J. M., Hall, N., Willadsen, P., Lingelbach, K., Shiels, B., Tait, A., Berriman, M., Allred, D. R. and Pain, A. (2014). The evolutionary dynamics of variant antigen genes in Babesia reveal a history of genomic innovation underlying host-parasite interaction. Nucleic Acids Research 42, 7113–7131.Google Scholar
Jackson, L. A., Waldron, S. J., Weier, H. M., Nicoll, C. L. and Cooke, B. M. (2001). Babesia ovis: culture of laboratory-adapted parasite lines and clinical isolates in a chemically defined medium. Experimental Parasitology 99, 168–174.Google Scholar
Johnson, W. C., Cluff, C. W., Goff, W. L. and Wyatt, C. R. (1996). Reactive oxygen and nitrogen intermediates and products from polyamine degradation are babesiacidal in vitro. Annals of the New York Academy of Sciences 791, 136–147.Google Scholar
Jonsson, N. N. (2006). The productivity effects of cattle tick (Boophilus microplus) infestation on cattle, with particular reference to Bos indicus cattle and their crosses. Veterinary Parasitology 137, 1–10.Google Scholar
Jonsson, N. N., Bock, R. E. and Jorgensen, W. K. (2008). Productivity and health effects of anaplasmosis and babesiosis on Bos indicus cattle and their crosses, and the effects of differing intensity of tick control in Australia. Veterinary Parasitology 155, 1–9.Google Scholar
Jonsson, N. N., Bock, R. E., Jorgensen, W. K., Morton, J. M. and Stear, M. J. (2012). Is endemic stability of tick-borne disease in cattle a useful concept? Trends in Parasitology 28, 85–89.Google Scholar
Joseph, J. T., Purtill, K., Wong, S. J., Munoz, J., Teal, A., Madison-Antenucci, S., Horowitz, H. W., Aguero-Rosenfeld, M. E., Moore, J. M., Abramowsky, C. and Wormser, G. P. (2012). Vertical transmission of Babesia microti, United States. Emerging Infectious Diseases 18, 1318–1321.Google Scholar
Kakoma, I. and Mehlhorn, H. (1994). Babesia of domestic ruminants. In Parasitic Protozoa 2 (ed. Kreier, J. P. and Baker, J. R.), Vol. 7, pp. 141–216. Academic Press, New York, NY, USA.Google Scholar
Kania, S. A., Allred, D. R. and Barbet, A. F. (1995). Babesia bigemina: host factors affecting the invasion of erythrocytes. Experimental Parasitology 80, 76–84.Google Scholar
Kappmeyer, L. S., Thiagarajan, M., Herndon, D. R., Ramsay, J. D., Caler, E., Djikeng, A., Gillespie, J. J., Lau, A. O., Roalson, E. H., Silva, J. C., Silva, M. G., Suarez, C. E., Ueti, M. W., Nene, V. M., Mealey, R. H., Knowles, D. P. and Brayton, K. A. (2012). Comparative genomic analysis and phylogenetic position of Theileria equi. BMC Genomics 13, 603.Google Scholar
Kessler, R. H., Madruga, C. R., Jesus, E. F. and Semprebom, D. V. (1987). Isolamento de cepas puras de Babesia bovis, Babesia bigemina e Anaplasma marginale em área enzoótica. Pesquisa Agropecuaria Brasileira 22, 747–752.Google Scholar
Kim, C. M., Blanco, L. B., Alhassan, A., Iseki, H., Yokoyama, N., Xuan, X. and Igarashi, I. (2008). Development of a rapid immunochromatographic test for simultaneous serodiagnosis of bovine babesioses caused by Babesia bovis and Babesia bigemina. American Journal of Tropical Medicine and Hygiene 78, 117–121.Google Scholar
Klinger, C. M., Nisbet, R. E., Ouologuem, D. T., Roos, D. S. and Dacks, J. B. (2013). Cryptic organelle homology in apicomplexan parasites: insights from evolutionary cell biology. Current Opinion in Microbiology 16, 424–431.Google Scholar
Krause, P. J., Daily, J., Telford, S. R., Vannier, E., Lantos, P. and Spielman, A. (2007). Shared features in the pathobiology of babesiosis and malaria. Trends in Parasitology 23, 605–610.Google Scholar
Krishnegowda, G., Hajjar, A. M., Zhu, J., Douglass, E. J., Uematsu, S., Akira, S., Woods, A. S. and Gowda, D. C. (2005). Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. Journal of Biological Chemistry 280, 8606–8616.Google Scholar
Kumar, B., Murugan, K., Ray, D. D. and Ghosh, S. (2012). Efficacy of rBm86 against Rhipicephalus (Boophilus) microplus (IVRI-I line) and Hyalomma anatolicum anatolicum (IVRI-II line) infestations on bovine calves. Parasitology Research 111, 629–635.Google Scholar
Lau, A. O. (2009). An overview of the Babesia, Plasmodium and Theileria genomes: a comparative perspective. Molecular and Biochemical Parasitology 164, 1–8.Google Scholar
Lau, A. O., Kalyanaraman, A., Echaide, I., Palmer, G. H., Bock, R., Pedroni, M. J., Rameshkumar, M., Ferreira, M. B., Fletcher, T. I. and McElwain, T. F. (2011). Attenuation of virulence in an apicomplexan hemoparasite results in reduced genome diversity at the population level. BMC Genomics 12, 410. doi: 10.1186/1471-2164-12-410CrossRefGoogle Scholar
Laughery, J. M., Knowles, D. P., Schneider, D. A., Bastos, R. G., McElwain, T. and Suarez, C. E. (2014). Targeted surface expression of an exogenous antigen in stably transfected Babesia bovis. PLOS ONE 9: e97890.Google Scholar
Lew, A. E., Dluzewski, A. R., Johnson, A. M. and Pinder, J. C. (2002). Myosins of Babesia bovis: molecular characterisation, erythrocyte invasion, and phylogeny. Cell Motility and the Cytoskeleton 52, 202–220.Google Scholar
Lewis, D. and Williams, H. (1979). Infection of the Mongolian gerbil with the cattle piroplasm Babesia divergens. Nature 278, 170–171.Google Scholar
Li, H., Child, M. A. and Bogyo, M. (2012). Proteases as regulators of pathogenesis: examples from the Apicomplexa. Biochimica et Biophysica Acta 1824, 177–185.Google Scholar
Liddell, K. G., Lucas, S. B. and Williams, H. (1980). Babesia divergens infections in the Mongolian gerbil: characteristics of a human strain. Parasitology 82, 205–224.Google Scholar
Lobo, C. A. (2005). Babesia divergens and Plasmodium falciparum use common receptors, glycophorins A and B, to invade the human red blood cell. Infection and Immunity 73, 649–651.Google Scholar
Lobo, C. A., Rodriguez, M. and Cursino-Santos, J. R. (2012). Babesia and red cell invasion. Current Opinion in Hematology 19, 170–175.Google Scholar
Machado, R., McElwain, T., Pancracio, H., Freschi, C. and Palmer, G. (1999). Babesia bigemina: immunization with purified rhoptries induces protection against acute parasitemia. Experimental Parasitology 93, 105–108.Google Scholar
Mafra, C. L., Patarroyo, J. H. and Silva, S. S. (1994). Babesia bovis: infectivity of an attenuated strain of Brazilian origin for the tick vector, Boophilus microplus. Veterinary Parasitology 52, 139–143.Google Scholar
Mahoney, D. F. (1967). Bovine babesiosis: the immunization of cattle with killed Babesia argentina. Experimental Parasitology 20, 125–129.Google Scholar
Mahoney, D. F. (1974). The application of epizootiological principals in the control of babesiosis in cattle. Bulletin-Office International des épizooties 81, 123–138.Google Scholar
Mahoney, D. F. (1986). In The Ruminant Immune System in Health and Disease (ed. Morrison, W. I.), pp. 539–545. Cambridge University Press, Cambridge, UK.Google Scholar
Malandrin, L., Marchand, A. M. and Chauvin, A. (2004). Development of a microtitre based spectrophotometric method to monitor Babesia divergens growth in vitro. Journal of Microbiological Methods 58, 303–312.Google Scholar
Malandrin, L., Jouglin, M., Sun, Y., Brisseau, N. and Chauvin, A. (2010). Redescription of Babesia capreoli (Enigk and Friedhoff, 1962) from roe deer (Capreolus capreolus): isolation, cultivation, host specificity, molecular characterisation and differentiation from Babesia divergens. International Journal for Parasitology 40, 277–284.Google Scholar
Mangold, A. J., Aguirre, D. H. and Guglielmone, A. A. (1990). Post-thawing viability of vaccines for bovine babesiosis and anaplasmosis cryopreserved with glycerol. Veterinary Parasitology 37, 301–306.Google Scholar
Mangold, A. J., Aguirre, D. H., Cafrune, M. M., de Echaide, S. T. and Guglielmone, A. A. (1993). Evaluation of the infectivity of a vaccinal and a pathogenic Babesia bovis strain from Argentina to Boophilus microplus. Veterinary Parasitology 51, 143–148.Google Scholar
Mangold, A. J., Vanzini, V. R., Echaide, I. E., de Eschaide, S. T., Volpogni, M. M. and Guglielmone, A. A. (1996). Viability after thawing and dilution of simultaneously cryopreserved vaccinal Babesia bovis and Babesia bigemina strains cultured in vitro. Veterinary Parasitology 61, 345–348.Google Scholar
Maritz-Olivier, C., van Zyl, W. and Stutzer, C. (2012). A systematic, functional genomics, and reverse vaccinology approach to the identification of vaccine candidates in the cattle tick, Rhipicephalus microplus. Ticks and Tick-borne Diseases 3, 179–187.Google Scholar
Martins, T. M., do Rosário, V. E. and Domingos, A. (2012). Expression and characterization of the Babesia bigemina cysteine protease BbiCPL1. Acta Tropica 121, 1–5.Google Scholar
Mazumdar, J. and Striepen, B. (2007). Make it or take it: fatty acid metabolism of apicomplexan parasites. Eukaryotic Cell 6, 1727–1735.Google Scholar
Mazuz, M. L., Molad, T., Fish, L., Leibovitz, B., Wolkomirsky, R., Fleiderovitz, L. and Shkap, V. (2012). Genetic diversity of Babesia bovis in virulent and attenuated strains. Parasitology 139, 317–323.Google Scholar
McAllister, M. M. (2014). Successful vaccines for naturally occurring protozoal diseases of animals should guide human vaccine research. A review of protozoal vaccines and their designs. Parasitology 141, 624–640.Google Scholar
McCosker, P. J. (1993). Ticks in a changing world. World Animal Review 74–75, 1. (www.fao.org/3/a-u9550t/u9550T01.htm#ticks%20in%20a%20changing%20world).Google Scholar
McElwain, T. F., Perryman, L. E., Musoke, A. J. and McGuire, T. C. (1991). Molecular characterization and immunogenicity of neutralization-sensitive Babesia bigemina merozoite surface proteins. Molecular and Biochemical Parasitology 47, 213–222.Google Scholar
McGuire, T. C., Musoke, A. J. and Kurtti, T. (1979). Functional properties of bovine IgG1 and IgG2: interaction with complement, macrophages, neutrophils, and skin. Immunology 38, 249–256.Google Scholar
McHardy, N., Woollon, R. M., Clampitt, R. B., James, J. A. and Crawley, R. J. (1986). Efficacy, toxicity and metabolism of imidocarb dipropionate in the treatment of Babesia ovis infection in sheep. Research in Veterinary Science 41, 14–20.Google Scholar
Mdachi, R. E., Murilla, G. A., Omukuba, J. N. and Cagnolati, V. (1995). Disposition of diminazene aceturate (Berenil) in trypanosome-infected pregnant and lactating cows. Veterinary Parasitogy 58, 215–225.Google Scholar
Merino, O., Almazán, C., Canales, M., Villar, M., Moreno-Cid, J. A., Galindo, R. C. and de la Fuente, J. (2011). Targeting the tick protective antigen subolesin reduces vector infestations and pathogen infection by Anaplasma marginale and Babesia bigemina. Vaccine 29, 8575–8579.Google Scholar
Merino, O., Antunes, S., Mosqueda, J., Moreno-Cid, J. A., Pérez de la Lastra, J. M., Rosario-Cruz, R., Rodríguez, S., Domingos, A. and de la Fuente, J. (2013). Vaccination with proteins involved in tick-pathogen interactions reduces vector infestations and pathogen infection. Vaccine 31, 5889–5896.Google Scholar
Mesplet, M., Echaide, I., Dominguez, M., Mosqueda, J. J., Suarez, C. E., Schnittger, L. and Florin-Christensen, M. (2010). Bovipain-2, the falcipain-2 ortholog, is expressed in intraerythrocytic stages of the tick-transmitted hemoparasite Babesia bovis. Parasites and Vectors 3, 113. doi: 10.1186/1756-3305-3-113.Google Scholar
Mesplet, M., Palmer, G. H., Pedroni, M. J., Echaide, I., Florin-Christensen, M., Schnittger, L. and Lau, A. O. (2011). Genome-wide analysis of peptidase content and expression in a virulent and attenuated Babesia bovis strain pair. Molecular and Biochemical Parasitology 179, 111–113.Google Scholar
Montealegre, F., Levy, M. G., Ristic, M. and James, M. A. (1985). Growth inhibition of Babesia bovis in culture by secretions from bovine mononuclear phagocytes. Infection and Immunity 50, 523–526.Google Scholar
Montenegro-James, S., Ristic, M., Toro Benitez, M., Leon, E. and Lopez, R. (1985). Heterologous strain immunity in bovine babesiosis using a culture-derive soluble Babesia bovis immunogen. Veterinary Parasitology 18, 321–337.Google Scholar
Montenegro-James, S., Toro Benitez, M., Leon, E., Lopez, R. and Risti, C. M. (1987). Bovine babesiosis: induction of protective immunity with culture-derived Babesia bovis and Babesia bigemina immunogens. Parasitology Research 74, 142–150.Google Scholar
Montenegro-James, S., Toro, M., Leon, E., Guillen, A. T., Lopez, R. and Lopez, W. (1992). Immunization of cattle with an inactivated polyvalent vaccine against anaplasmosis and babesiosis. Annals of the New York Academy of Sciences 653, 112–121.Google Scholar
Montero, E., Gonzalez, L. M., Rodriguez, M., Oksov, Y., Blackman, M. J. and Lobo, C. A. (2006). A conserved subtilisin protease identified in Babesia divergens merozoites. Journal of Biological Chemistry 281, 35717–35726.Google Scholar
Montero, E., Rodriguez, M., Gonzalez, L. M., and Lobo, C. A. (2008). Babesia divergens: identification and characterization of BdHSP-20, a small heat shock protein. Experimental Parasitology 119, 238–245.Google Scholar
Montero, E., Rodriguez, M., Oksov, Y. and Lobo, C. A. (2009). Babesia divergens apical membrane antigen 1 and its interaction with the human red blood cell. Infection and Immunity 77, 4783–4793.Google Scholar
Moreau, E., Jouglin, M., Chauvin, A. and Malandrin, L. (2009). Babesia divergens experimental infection of spleen-intact sheep results in long-lasting parasitemia despite a strong humoral response: preliminary results. Veterinary Parasitology 166, 205–211.Google Scholar
Mosqueda, J., McElwain, T. F. and Palmer, G. H. (2002 b). Babesia bovis merozoite surface antigen 2 proteins are expressed on the merozoite and sporozoite surface, and specific antibodies inhibit attachment and invasion of erythrocytes. Infection and Immunity 70, 6448–6455.Google Scholar
Mosqueda, J., McElwain, T. F., Stiller, D. and Palmer, G. H. (2002 a). Babesia bovis merozoite surface antigen 1 and rhoptry-associated protein 1 are expressed in sporozoites, and specific antibodies inhibit sporozoite attachment to erythrocytes. Infection and Immunity 70, 1599–1603.Google Scholar
Mosqueda, J., Falcon, A., Alvarez, A. J., Ramos, A. J., Oropeza-Hernandez, I. F. and Figueroa, J. V. (2004 a). Babesia bigemina sexual stages are induced in vitro and are specifically recognized by antibodies in the midgut of infected Boophilus microplus ticks. International Journal for Parasitology 34, 1229–1236.Google Scholar
Mosqueda, J., Ramos, J. A., Falcon, A., Alvarez, J. A., Aragon, V. and Figueroa, J. V. (2004 b). Babesia bigemina: sporozoite isolation from Boophilus microplus nymphs and initial immunomolecular characterization. Annals of the New York Academy of Sciences 26, 222–231.Google Scholar
Mosqueda, J., Olvera-Ramirez, A., Aguilar-Tipacamu, G. and Canto, G. J. (2012). Current advances in detection and treatment of babesiosis. Current Medicinal Chemistry 19, 1504–1518.Google Scholar
Mott, G. A., Wilson, R., Fernando, A., Robinson, A., MacGregor, P., Kennedy, D., Schaap, D., Matthews, J. B. and Matthews, K. R. (2011). Targeting cattle-borne zoonoses and cattle pathogens using a novel trypanosomatid-based delivery system. PLOS Pathogens 7, e1002340.Google Scholar
Mount, A., Koernig, S., Silva, A., Drane, D., Maraskovsky, E. and Morelli, A. B. (2013). Combination of adjuvants: the future of vaccine design. Expert Review of Vaccines 12, 733–746.Google Scholar
Müller, J. and Hemphill, A. (2013). In vitro culture systems for the study of apicomplexan parasites in farm animals. International Journal for Parasitology 43, 115–124.Google Scholar
Norimine, J., Suarez, C. E., McElwain, T. F., Florin-Christensen, M. and Brown, W. C. (2002). Immunodominant epitopes in Babesia bovis rhoptry-associated protein 1 that elicit memory CD4(+)-T-lymphocyte responses in B. bovis-immune individuals are located in the amino-terminal domain. Infection and Immunity 70, 2039–2048.Google Scholar
Norimine, J., Mosqueda, J., Suarez, C., Palmer, G. H., McElwain, T. F., Mbassa, G. and Brown, W. C. (2003). Stimulation of T-helper cell gamma interferon and immunoglobulin G responses specific for Babesia bovis rhoptry-associated protein 1 (RAP-1) or a RAP-1 protein lacking the carboxy-terminal repeat region is insufficient to provide protective immunity against virulent B. bovis challenge. Infection and Immunity 71, 5021–5032.Google Scholar
Norimine, J., Mosqueda, J., Palmer, G. H., Lewin, H. A. and Brown, W. C. (2004). Conservation of Babesia bovis small heat shock protein (Hsp20) among strains and definition of T helper cell epitopes recognized by cattle with diverse major histocompatibility complex class II haplotypes. Infection and Immunity 72, 1096–1106.Google Scholar
Norimine, J., Ruef, B. J., Palmer, G. H., Knowles, D. P., Herndon, D. R., Rice-Ficht, A. C. and Brown, W. C. (2006). A novel 78-kDa fatty acyl-CoA synthetase (ACS1) of Babesia bovis stimulates memory CD4+ T lymphocyte responses in B. bovis-immune cattle. Molecular and Biochemical Parasitology 147, 20–29.Google Scholar
O´Connor, R. M. and Allred, D. R. (2000). Selection of Babesia bovis-infected erythrocytes for adhesion to endothelial cells co-selects for altered variant erythrocyte surface antigen isoforms. Journal of Immunology 164, 2037–2045.Google Scholar
OIE World Organization for Animal Health (2010). OIE World Organization for Animal Health Terrestrial Manual. Bovine Babesiosis, Chapter 2.4.2 (2010). http://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/2.04.02_BOVINE_BABESIOSIS.pdfGoogle Scholar
Oliveira, M. C., Oliveira-Sequeira, T. C., Regitano, L. C., Alencar, M. M., Néo, T. A., Silva, A. M. and Oliveira, H. N. (2008). Detection of Babesia bigemina in cattle of different genetic groups and in Rhipicephalus (Boophilus) microplus tick. Veterinary Parasitology 155, 281–286.Google Scholar
Ottley, M. (1984). The Water Buffalo: New Prospects for an Underutilized Animal, 2nd Edn. Report of an Ad Hoc Panel of the Advisory Committee on Technology Innovation Board on Science and Technology for International Development Commission on International Relations, National Research Council, pp. 66–72. National Academy Press, Washington, DC, USA.Google Scholar
Pain, A., Renauld, H., Berriman, M., Murphy, L., Yeats, C. A., Weir, W., Kerhornou, A., Aslett, M., Bishop, R., Bouchier, C., Cochet, M., Coulson, R. M., Cronin, A., de Villiers, E. P., Fraser, A., Fosker, N., Gardner, M., Goble, A., Griffiths-Jones, S., Harris, D. E., Katzer, F., Larke, N., Lord, A., Maser, P., McKellar, S., Mooney, P., Morton, F., Nene, V., O'Neil, S., Price, C., Quail, M. A., Rabbinowitsch, E., Rawlings, N. D., Rutter, S., Saunders, D., Seeger, K., Shah, T., Squares, R., Squares, S., Tivey, A., Walker, A. R., Woodward, J., Dobbelaere, D. A., Langsley, G., Rajandream, M. A., McKeever, D., Shiels, B., Tait, A., Barrell, B. and Hall, N. (2005). Genome of the host-cell transforming parasite Theileria annulata compared with T . parva. Science 309, 131–133.Google Scholar
Parizi, L. F., Githaka, N. W., Logullo, C., Konnai, S., Masuda, A., Ohashi, K. and da Silva Vaz, I. Jr. (2012). The quest for a universal vaccine against ticks: cross-immunity insights. Veterinary Journal 194, 158–165.Google Scholar
Patarroyo, J. H., Prates, A. A., Tavares, C. A., Mafra, C. L. and Vargas, M. I. (1995). Exoantigens of an attenuated strain of Babesia bovis used as a vaccine against bovine babesiosis. Veterinary Parasitology 59, 189–199.Google Scholar
Pedroni, M. J., Sondgeroth, K. S., Gallego-Lopez, G. M., Echaide, I. and Lau, A. O. (2013). Comparative transcriptome analysis of geographically distinct virulent and attenuated Babesia bovis strains reveals similar gene expression changes through attenuation. BMC Genomics 14, 763.Google Scholar
Penichet, M., Rodriguez, M., Castellano, O., Mandado, S., Rojas, Y., Rubiera, R., Sanchez, P., Lleonart, R. and de la Fuente, J. (1994). Detection of Bm86 antigen in different strains of Boophilus microplus and effectiveness of immunization with recombinant Bm86. Parasite Immunology 16, 493–500.Google Scholar
Pérez de León, A. A., Strickman, D. A., Knowles, D. P., Fish, D., Thacker, E., de la Fuente, J., Krause, P. J., Wikel, S. K., Miller, R. S., Wagner, G. G., Almazán, C., Hillman, R., Messenger, M. T., Ugstad, P. O., Duhaime, R. A., Teel, P. D., Ortega-Santos, A., Hewitt, D. G., Bowers, E. J., Bent, S. J., Cochran, M. H., McElwain, T. F., Scoles, G. A., Suarez, C. E., Davey, R., Howell Freeman, J. M., Lohmeyer, K., Li, A. Y., Guerrero, F. D., Kammlah, D. M., Phillips, P., Pound, J. M. and Group for Emerging Babesioses and One Health Research and Development in the U.S. (2010). One Health approach to identify research needs in bovine and human babesioses: workshop report. Parasites and Vectors 3, 36. doi: 10.1186/1756-3305-3-36.Google Scholar
Perez-Llaneza, A., Caballero, M., Baravalle, E., Mesplet, M., Mosqueda, J., Suarez, C. E., Echaide, I., Katzer, F., Pacheco, G. M., Florin-Christensen, M. and Schnittger, L. (2010). Development of a tandem repeat-based multilocus typing system distinguishing Babesia bovis geographic isolates. Veterinary Parasitology 167, 196–204.Google Scholar
Pipano, E. (1981). Frozen vaccine against tick fevers of cattle. In XI International Congress on Diseases of Cattle, Haifa, Israel (ed. Mayer, E.), pp. 678–681. Bregman Press, Haifa, Israel.Google Scholar
Pipano, E. (1995). Live vaccines against hemoparasitic diseases in livestock. Veterinary Parasitology 57, 213–231.Google Scholar
Pipano, E. (1997). Vaccines against hemoparasitic diseases in Israel with special reference to quality assurance. Tropical Animal Health and Production 29, 86–90.Google Scholar
Pipano, E., Shkap, V., Kriegel, Y., Leibovitz, B., Savitsky, I. and Fish, L. (2002). Babesia bovis and B. bigemina: persistence of infection in Friesian cows following vaccination with live antibabesial vaccines. Veterinary Journal, 164, 64–68.Google Scholar
Posadas, J. B. and Lecuona, R. E. (2009). Selection of native isolates of Beauveria bassiana (Ascomycetes: Clavicipitaceae) for the microbial control of Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). Journal of Medical Entomology 46, 284–291.Google Scholar
Pradel, G., Hayton, K., Aravind, L., Iyer, L. M., Abrahamsen, M. S., Bonawitz, A., Mejia, C. and Templeton, T. J. (2004). A multidomain adhesion protein family expressed in Plasmodium falciparum is essential for transmission to the mosquito. Journal of Experimental Medicine 199, 1533–1544.Google Scholar
Precigout, E., Gorenflot, A., Valentin, A., Bissuel, G., Carcy, B., Brasseur, P., Moreau, Y. and Schrevel, J. (1991). Analysis of immune responses of different hosts to Babesia divergens isolates from different geographic areas and capacity of culture-derived exoantigens to induce efficient cross-protection. Infection and Immunity 59, 2799–2805.Google Scholar
Precigout, E., Delbecq, S., Vallet, A., Carcy, B., Camillieri, S., Hadj-Kaddour, K., Kleuskens, J., Schetters, T. and Gorenflot, A. (2004). Association between sequence polymorphism in an epitope of Babesia divergens Bd37 exoantigen and protection induced by passive transfer. International Journal for Parasitology 34, 585–593.Google Scholar
Rachinsky, A., Guerrero, F. D. and Scoles, G. A. (2007). Differential protein expression inovaries of uninfected and Babesia-infected southern cattle ticks, Rhipicephalus (Boophilus) microplus. Insect Biochemistry and Molecular Biology 37, 1291–1308.Google Scholar
Rachinsky, A., Guerrero, F. D. and Scoles, G. A. (2008). Proteomic profiling of Rhipicephalus (Boophilus) microplus midgut responses to infection with Babesia bovis. Veterinary Parasitology 152, 294–313.Google Scholar
Rajeshwari, K., Patel, K., Nambeesan, S., Mehta, M., Sehgal, A., Chakraborty, T. and Sharma, S. (2004). The P domain of the P0 protein of Plasmodium falciparum protects against challenge with malaria parasites. Infection and Immunity 72, 5515–5521.Google Scholar
Ramos, C. A., Araújo, F. R., Souza, I. I., Oliveira, R. H., Elisei, C., Soares, C. O., Sacco, A. M., Rosinha, G. M. and Alves, L. C. (2009). Molecular and antigenic characterisation of ribosomal phosphoprotein P0 from Babesia bovis. Memórias do Instituto Oswaldo Cruz 104, 998–1002.Google Scholar
Ramos, C. M., Cooper, S. M. and Holman, P. J. (2010). Molecular and serologic evidence for Babesia bovis-like parasites in white-tailed deer (Odocoileus virginianus) in south Texas. Veterinary Parasitology 172, 214–220.Google Scholar
Ribeiro, M. F., Bastos, C. V., Vasconcelos, M. M. and Passos, L. M. (2009). Babesia bigemina: in vitro multiplication of sporokinetes in Ixodes scapularis (IDE8) cells. Experimental Parasitology 122, 192–195.Google Scholar
Riek, R. F. (1966). The life cycle of Babesia argentina (Lignieres, 1903) (Sporozoa: piroplasmidea) in the tick vector Boophilus microplus (Canestrini). Australian Journal of Agricultural Research 17, 247–254.Google Scholar
Riek, J., Marcondes Klafke, G., Webster, A., Dall'Agnol, B., Scheffer, R., Araújo Souza, U., Bamberg Corassini, V., Vargas, R., Silveira dos Santos, J. and de Souza Martins, J. R. (2014). First report of fluazuron resistance in Rhipicephalus microplus: a field tick population resistant to six classes of acaricides. Veterinary Parasitology, in press, http://dx.doi.org/10.1016/j.vetpar.2014.01.012.Google Scholar
Rodriguez, A. E., Couto, A., Echaide, I., Schnittger, L. and Florin-Christensen, M. (2010). Babesia bovis contains an abundant parasite-specific protein-free glycerophosphatidylinositol and the genes predicted to be involved in its assembly. Veterinary Parasitology 167, 227–235.Google Scholar
Rodriguez, A. E., Schnittger, L., Tomazic, M. L. and Florin-Christensen, M. (2013 a). Current and prospective tools for the control of cattle-infecting Babesia parasites. In Protozoa: Biology, Classification and Role in Disease (ed. Castillo, V. and Harris, R.), pp. 1–44. Nova Publishers, Hauppauge, NY, USA.Google Scholar
Rodriguez, A. E., Zamorano, P., Wilkowsky, S., Torrá, F., Ferreri, L., Dominguez, M. and Florin-Christensen, M. (2013 b). Delivery of recombinant vaccines against bovine herpesvirus type 1 gD and Babesia bovis MSA-2c to mice using liposomes derived from egg yolk lipids. Veterinary Journal 196, 550–551.Google Scholar
Rodriguez, A. E., Florin-Christensen, M., Flores, D. A., Echaide, I., Suarez, C. and Schnittger, L. (2014). The glycosylphosphatidylinositol-anchored protein repertoire of Babesia bovis and its significance for erythrocyte invasion. Ticks and Tick-Borne Diseases 5, 343–348.Google Scholar
Rodriguez, R. I. and Trees, A. J. (1996). In vitro responsiveness of Babesia bovis to imidocarb dipropionate and the selection of a drug-adapted line. Veterinary Parasitology 62, 35–41.Google Scholar
Rodriguez, S. D., Buening, G. M., Green, T. J. and Carson, C. A. (1983). Cloning of Babesia bovis by in vitro cultivation. Infection and Immunity 42, 15–18.Google Scholar
Rodríguez-Hernández, E., Mosqueda, J., Alvarez-Sánchez, M. E., Neri, A. F., Mendoza-Hernández, G. and Camacho-Nuez, M. (2012). The identification of a VDAC like protein involved in the interaction of Babesia bigemina sexual stages with Rhipicephalus microplus midgut cells. Veterinary Parasitology 187, 538–541.Google Scholar
Rojas, C., Figueroa, J. V., Alvarado, A., Mejia, P., Mosqueda, J. J., Falcon, A., Vega, C. A. and Alvarez, A. (2006). Bovine babesiosis live vaccine production: use of gamma irradiation on the substrate. Annals of the New York Academy of Sciences 1081, 405–416.Google Scholar
Rudzinska, M. A., Trager, W., Lewengrub, S. J. and Gubert, E. (1976). An electron microscopic study of Babesia microti invading erythrocytes. Cell Tissue Research 169, 323–334.Google Scholar
Ruef, B. J., Dowling, S. C., Conley, P. G., Perryman, L. E., Brown, W. C., Jasmer, D. P. and Rice-Ficht, A. C. (2000 a). A unique Babesia bovis spherical body protein is conserved among geographic isolates and localizes to the infected erythrocyte membrane. Molecular and Biochemical Parasitology 105, 1–12.Google Scholar
Ruef, B. J., Ward, T. J., Oxner, C. R., Conley, P. G., Brown, W. C. and Rice-Ficht, A. C. (2000 b). Phylogenetic analysis with newly characterized Babesia bovis Hsp70 and Hsp90 provides strong support for paraphyly within the piroplasms. Molecular and Biochemical Parasitology 109, 67–72.Google Scholar
Sabio y García, J. V., Farber, M., Carrica, M., Cravero, S., Macedo, G. C., Bigi, F., Oliveira, S. C., Rossetti, O. and Campos, E. (2008). Expression of Babesia bovis rhoptry associated protein 1 (RAP1) in Brucella abortus S19. Microbes and Infection 10, 635–641.Google Scholar
Salama, A. A., Terkawi, M. A., Kawai, S., Aboulaila, M., Nayel, M., Mousa, A., Zaghawa, A., Yokoyama, N. and Igarashi, I. (2013). Specific antibody to a conserved region of Babesia apical membrane antigen-1 inhibited the invasion of B. bovis into the erythrocyte. Experimental Parasitology 135, 623–628.Google Scholar
Salas, J. H., González, M. M., Noa, M., Pérez, N. A., Díaz, G., Gutiérrez, R., Zazueta, H. and Osuna, I. (2003). Organophosphorus pesticide residues in Mexican commercial pasteurized milk. Journal of Agricultural and Food Chemistry 51, 4468–4471.Google Scholar
Sánchez, C., Campos, E. and Oliva, A. G. (2009). Babesia bovis: effect of Albumax II and orotic acid in a low-serum in vitro culture. Experimental Parasitology 121, 274–278.Google Scholar
Santangelo, M. P., McIntosh, D., Bigi, F., Armôa, G. R., Campos, A. S., Ruybal, P., Dellagostin, O. A., McFadden, J., Mendum, T., Gicquel, B., Winter, N., Farber, M. and Cataldi, A. (2007). Mycobacterium bovis BCG as a delivery system for the RAP-1 antigen from Babesia bovis. Vaccine 25, 1104–1113.Google Scholar
Schneider, D. A., Yan, H., Bastos, R. G., Johnson, W. C., Gavin, P. R., Allen, A. J., Barrington, G. M., Herrmann-Hoesing, L. M., Knowles, D. P. and Goff, W. L. (2011). Dynamics of bovine spleen cell populations during the acute response to Babesia bovis infection: an immunohistological study. Parasite Immunology 33, 34–44.Google Scholar
Schnittger, L., Rodriguez, A. E., Florin-Christensen, M. and Morrison, D. A. (2012). Babesia: a world emerging. Infection, Genetics and Evolution 12, 1788–1809.Google Scholar
Schuster, F. L. (2002). Cultivation of Babesia and Babesia-like blood parasites: agents of an emerging zoonotic disease. Clinical Microbiology Reviews 15, 365–373.Google Scholar
Shkap, V., Leibovitz, B., Krigel, Y., Hammerschlag, J., Marcovics, A., Fish, L., Molad, T., Savitsky, I. and Mazuz, M. (2005). Vaccination of older Bos taurus bulls against bovine babesiosis. Veterinary Parasitology 129, 235–242.Google Scholar
Shkap, V., de Vos, A. J., Zweygarth, E. and Jongejan, F. (2007 a). Attenuated vaccines for tropical theileriosis, babesiosis and heartwater: the continuing necessity. Trends in Parasitology 23, 420–426.Google Scholar
Shkap, V., Rasulov, I., Abdurasulov, S., Fish, L., Leibovitz, B., Krigel, Y., Molad, T., Mazuz, M. L. and Savitsky, I. (2007 b). Babesia bigemina: attenuation of an Uzbek isolate for immunization of cattle with live calf- or culture-derived parasites. Veterinary Parasitology 31, 221–226.Google Scholar
Shoda, L. K., Palmer, G. H., Florin-Christensen, J., Florin-Christensen, M., Godson, D. L. and Brown, W. C. (2000). Babesia bovis-stimulated macrophages express interleukin-1beta, interleukin-12, tumor necrosis factor alpha, and nitric oxide and inhibit parasite replication in vitro. Infection and Immunity 68, 5139–5145.Google Scholar
Shoda, L. K., Kegerreis, K. A., Suarez, C. E., Roditi, I., Corral, R. S., Bertot, G. M., Norimine, J. and Brown, W. C. (2001 ). DNA from protozoan parasites Babesia bovis, Trypanosoma cruzi, and T. brucei is mitogenic for B lymphocytes and stimulates macrophage expression of interleukin-12, tumor necrosis factor alpha, and nitric oxide. Infection and Immunity 69, 2162–2171.Google Scholar
Shonhai, A. (2010). Plasmodial heat shock proteins: targets for chemotherapy. FEMS Immunology and Medical Microbiology 58, 61–74.Google Scholar
Silva, M. G., Ueti, M. W., Norimine, J., Florin-Christensen, M., Bastos, R. G., Goff, W. L., Brown, W. C., Oliva, A. and Suarez, C. E. (2010 a). Babesia bovis expresses a neutralization-sensitive antigen that contains a microneme adhesive repeat (MAR) domain. Parasitology International 59, 294–297.Google Scholar
Silva, M. G., Ueti, M. W., Norimine, J., Florin-Christensen, M., Bastos, R. G., Goff, W. L., Brown, W. C., Oliva, A. and Suarez, C. E. (2010 b). Babesia bovis expresses Bbo-6cys-E, a member of a novel gene family that is homologous to the 6-cys family of Plasmodium. Parasitology International 50, 13–18.Google Scholar
Silva, M. G., Domingos, A., Esteves, M. A., Cruz, M. E. and Suarez, C. E. (2013). Evaluation of the growth-inhibitory effect of trifluralin analogues on in vitro cultured Babesia bovis parasites. International Journal of Parasitology Drugs and Drug Resistance 3, 59–68.Google Scholar
Silveira, J. A., Rabelo, E. M., Lacerda, A. C., Borges, P. A., Tomás, W. M., Pellegrin, A. O., Tomich, R. G. and Ribeiro, M. F. (2013). Molecular detection and identification of hemoparasites in pampas deer (Ozotoceros bezoarticus Linnaeus, 1758) from the Pantanal Brazil. Ticks and Tick-borne Diseases 4, 341–345.CrossRefGoogle Scholar
Simuunza, M., Bilgic, H., Karagenc, T., Syakalima, M., Shiels, B., Tait, A. and Weir, W. (2011). Population genetic analysis and sub-structuring in Babesia bovis. Molecular and Biochemical Parasitology 177, 106–115.Google Scholar
Skuce, P. J., Mallon, T. R. and Taylor, S. M. (1996). Molecular cloning of a putative rhoptry associated protein homologue from Babesia divergens. Molecular and Biochemical Parasitology 77, 99–102.Google Scholar
Smith, T. and Kilborne, F. L. (1893). Investigations into the nature, causation and prevention of Southern cattle fever. In Ninth Annual Report of the Bureau of Animal Industry for the Year 1892, pp. 177–304. Government Printing Office, Washington, DC, USA.Google Scholar
Solari, M. A., Nari, A. and Cardozo, H. (1992). Impact of Babesia bovis and Babesia bigemina on the production of beef cattle in Uruguay. Memorias Instituto Oswaldo Cruz, Rio de Janeiro 87, 143–149.CrossRefGoogle ScholarPubMed
Sondgeroth, K. S., McElwain, T. F., Allen, A. J., Chen, A. V. and Lau, A. O. (2013). Loss of neurovirulence is associated with reduction of cerebral capillary sequestration during acute Babesia bovis infection. Parasites and Vectors 6, 181. doi: 10.1186/1756-3305-6-181.Google Scholar
Sonenshine, D. E., Kocan, K. M. and de la Fuente, J. (2006). Tick control: further thoughts on a research agenda. Trends in Parasitology 22, 550–551.CrossRefGoogle ScholarPubMed
Standfast, N. F., Bock, R. E., Wiecek, M. M., Devos, A. J., Jorgensen, W. K. and Kingston, T. G. (2003). Overcoming constraints to meeting increased demand for Babesia bigemina vaccine in Australia. Veterinary Parasitology 115, 213–222.Google Scholar
Suarez, C. E. and McElwain, T. F. (2008). Transient transfection of purified Babesia bovis merozoites. Experimental Parasitology 118, 498–504.Google Scholar
Suarez, C. E. and McElwain, T. F. (2009). Stable expression of a GFP-BSD fusion protein in Babesia bovis merozoites. International Journal for Parasitology 39, 289–297.Google Scholar
Suarez, C. E. and Noh, S. (2011). Emerging perspectives in the research of bovine babesiosis and anaplasmosis. Veterinary Parasitology 180, 109–125.Google Scholar
Suarez, C. E., Palmer, G. H., Hötzel, I. and McElwain, T. F. (1998). Structure, sequence, and transcriptional analysis of the Babesia bovis rap-1 multigene locus. Molecular and Biochemical Parasitology 93, 215–224.Google Scholar
Suarez, C. E., Florin-Christensen, M., Hines, S. A., Palmer, G. H., Brown, W. C. and McElwain, T. F. (2000). Characterization of allelic variation in the Babesia bovis merozoite surface antigen 1 (MSA-1) locus and identification of a cross-reactive inhibition-sensitive MSA-1 epitope. Infection and Immunity 68, 6865–6870.Google Scholar
Suarez, C. E., Palmer, G. H., Florin-Christensen, M., Hines, S. A., Hotzel, I. and McElwain, T. F. (2003). Organization, transcription and expression of rhoptry associated protein genes in the Babesia bigemina rap-1 locus. Molecular and Biochemical Parasitology 127, 101–112.Google Scholar
Suarez, C. E., Palmer, G. H., LeRoith, T., Florin-Christensen, M., Crabb, B. and McElwain, T. F. (2004). Intergenic regions in the rhoptry associated protein-1 (rap-1) locus promote exogenous gene expression in Babesia bovis. International Journal for Parasitology 34, 1177–1184.Google Scholar
Suarez, C. E., Norimine, J., Lacy, P. and Mc Elwain, T. F. (2006). Characterization and gene expression of Babesia bovis elongation factor-1alpha. International Journal for Parasitology 36, 965–973.CrossRefGoogle ScholarPubMed
Suarez, C. E., Lacy, P., Laughery, J., Gonzalez, M. G. and Mc Elwain, T. (2007). Optimization of Babesia bovis transfection methods. Parassitologia 1, 67–70.Google Scholar
Suarez, C. E., Laughery, J. M., Bastos, R. G., Johnson, W. C., Norimine, J., Asenzo, G., Brown, W. C., Florin-Christensen, M. and Goff, W. L. (2011). A novel neutralization sensitive and subdominant RAP-1-related antigen (RRA) is expressed by Babesia bovis merozoites. Parasitology 18, 1–10.Google Scholar
Suarez, C. E., Laughery, J. M., Schneider, D. A., Sondgerot, K. S. and Mc Elwain, T. F. (2012). Acute and persistent infection by a transfected Mo7 strain of Babesia bovis. Molecular and Biochemical Parasitology 185, 52–57.Google Scholar
Sun, Y., Moreau, E., Chauvin, A. and Malandrin, L. (2011). The invasion process of bovine erythrocyte by Babesia divergens: knowledge from an in vitro assay. Veterinary Research 42, 62. doi: 10.1186/1297-9716-42-62.Google Scholar
Téllez, M., Matesanz, F. and Alcina, A. (2003). The C-terminal domain of the Plasmodium falciparum acyl-CoA synthetases PfACS1 and PfACS3 functions as ligand for ankyrin. Molecular and Biochemical Parasitology 129, 191–198.Google Scholar
Terkawi, M. A., Jia, H., Gabriel, A., Goo, Y. K., Nishikawa, Y., Yokoyama, N., Igarashi, I., Fujisaki, K. and Xuan, X. (2007). A shared antigen among Babesia species: ribosomal phosphoprotein P0 as a universal babesial vaccine candidate. Parasitology Research 102, 35–40.Google Scholar
Terkawi, M. A., Seuseu, F. J., Eko-Wibowo, P., Huyen, N. X., Minoda, Y., AbouLaila, M., Kawai, S., Yokoyama, N., Xuan, X. and Igarashi, I. (2011 a). Secretion of a new spherical body protein of Babesia bovis into the cytoplasm of infected erythrocytes. Molecular and Biochemical Parasitology 178, 40–45.Google Scholar
Terkawi, M. A., Huyen, N. X., Wibowo, P. E., Seuseu, F. J., Aboulaila, M., Ueno, A., Goo, Y. K., Yokoyama, N., Xuan, X. and Igarashi, I. (2011 b). Spherical body protein 4 is a new serological antigen for global detection of Babesia bovis infection in cattle. Clinical and Vaccine Immunology 18, 337–342.Google Scholar
Terkawi, M. A., Ratthanophart, J., Salama, A., Aboulaila, M., Asada, M., Ueno, A., Alhasan, H., Guswanto, A., Masatani, T., Yokoyama, N., Nishikawa, Y., Xuan, X. and Igarashi, I. (2013). Molecular characterization of a new Babesia bovis Thrombospondin-Related Anonymous Protein (BbTRAP2). PLOS ONE 8, e83305.Google Scholar
Timms, P., Dalgliesh, R. J., Barry, D. N., Dimmock, C. K. and Rodwell, B. J. (1983). Babesia bovis: comparison of culture-derived parasites, non-living antigen and conventional vaccine in the protection of cattle against heterologous challenge. Australian Veterinary Journal 60, 75–77.Google Scholar
Timms, P., Stewart, N. P., Rodwell, B. J. and Barry, D. N. (1984). Immune responses of cattle following vaccination with living and non-living Babesia bovis antigens. Veterinary Parasitology 16, 243–251.Google Scholar
Timms, P., Stewart, N. P. and De Vos, A. J. (1990). Study of virulence and vector transmission of Babesia bovis by use of cloned parasite lines. Infection and Immunity 58, 2171–2176.Google Scholar
Torina, A., Agnone, A., Sireci, G., Mosqueda, J. J., Blanda, V., Albanese, I., La Farina, M., Cerrone, A., Cusumano, F. and Caracappa, S. (2010). Characterization of the apical membrane antigen-1 in Italian strains of Babesia bigemina. Transboundary and Emerging Diseases 57, 52–56.Google Scholar
Torina, A., Moreno-Cid, J. A., Blanda, V., Fernández de Mera, I. G., de la Lastra, J. M., Scimeca, S., Blanda, M., Scariano, M. E., Briganò, S., Disclafani, R., Piazza, A., Vicente, J., Gortázar, C., Caracappa, S., Lelli, R. C. and de la Fuente, J. (2014). Control of tick infestations and pathogen prevalence in cattle and sheep farms vaccinated with the recombinant Subolesin-Major Surface Protein 1a chimeric antigen. Parasites and Vectors 7, 10.Google Scholar
Tjornehoj, K., Lawrence, J. A., Kafuwa, P. T., Whiteland, A. P. and Chimera, B. A. (1997). Immunisation of smallholder dairy cattle against anaplasmosis and babesiosis in Malawi. Tropical Animal Health Production 29, 77–82.Google Scholar
Tsuji, M., Fujioka, H., Arai, S., Taniyama, H., Ishihara, C. and Aikawa, M. (1996). A mouse model for cerebral babesiosis. Parasitology Today 12, 203–205.Google Scholar
Uematsu, S. and Akira, S. (2008). Toll-like receptors (TLRs) and their Ligands. In Toll-Like Receptors (TLRs) and Innate Immunity. Handbook of Experimental Pharmacology, 183 (ed. Bauer, S. and Hartmann, G.), pp. 1–20. Springer, Berlin, Germany.Google Scholar
Uilenberg, G. (1995). International collaborative research: significance of tick-borne hemoparasitic diseases to world animal health. Veterinary Parasitology 57, 19–41.Google Scholar
Uilenberg, G. (2006). Babesia – a historical overview. Veterinary Parasitology 138, 3–10.Google Scholar
Vaughan, A. M. and Kappe, S. H. (2012). Malaria vaccine development: persistent challenges. Current Opinions in Immunology 24, 324–331.Google Scholar
Vial, H. J. and Gorenflot, A. (2006). Chemotherapy against babesiosis. Veterinary Parasitology 138, 147–160.Google Scholar
Vichido, R., Falcon, A., Ramos, J. A., Alvarez, A., Figueroa, J. V., Norimine, J., Brown, W. C., Castro, L. A. and Mosqueda, J. (2008). Expression analysis of heat shock protein 20 and rhoptry-associated protein 1a in sexual stages and kinetes of Babesia bigemina. Annals of the New York Academy of Sciences 1149, 136–140.Google Scholar
Wickramasekara Rajapakshage, B. K., Yamasaki, M., Hwang, S. J., Sasaki, N., Murakami, M., Tamura, Y., Lim, S. Y., Nakamura, K., Ohta, H. and Takiguchi, M. (2012). Involvement of mitochondrial genes of Babesia gibsoni in resistance to diminazene aceturate. Journal of Veterinary Medical Science 74, 1139–1148.CrossRefGoogle ScholarPubMed
Wilkowsky, S. E., Farber, M., Echaide, I., Torioni de Echaide, S., Zamorano, P. I., Dominguez, M., Suarez, C. E. and Florin-Christensen, M. (2003). Babesia bovis merozoite surface protein-2c (MSA-2c) contains highly immunogenic, conserved B-cell epitopes that elicit neutralization-sensitive antibodies in cattle. Molecular and Biochemical Parasitology 127, 133–141.Google Scholar
Willadsen, P. (2006). Tick control: thoughts on a research agenda. Veterinary Parasitology 138, 161–168.Google Scholar
Willadsen, P., Riding, G. A., McKenna, R. V., Kemp, D. H., Tellam, R. L., Nielsen, J. N., Lahnstein, J., Cobon, G. S. and Gough, J. M. (1989). Immunologic control of a parasitic arthropod. Identification of a protective antigen from Boophilus microplus. Journal of Immunology 143, 1346–1351.CrossRefGoogle ScholarPubMed
Willadsen, P., Bird, P., Cobon, G. S. and Hungerford, J. (1995). Commercialisation of a recombinant vaccine against Boophilus microplus. Parasitology 110 (Suppl.), S43–S50.Google Scholar
Williamson, K. C., Keister, D. B., Muratova, O. and Kaslow, D. C. (1995). Recombinant Pfs230, a Plasmodium falciparum gametocyte protein, induces antisera that reduce the infectivity of Plasmodium falciparum to mosquitoes. Molecular and Biochemical Parasitology 75, 33–42.Google Scholar
Winger, C. M., Canning, E. U. and Culverhouse, J. D. (1987). Induction of protective immunity to Babesia divergens in Mongolian gerbils, Meriones unguiculatus, using culture-derived immunogens. Veterinary Parasitology 26, 43–53.Google Scholar
Winger, C. M., Canning, E. U. and Culverhouse, J. D. (1989). A strain of Babesia divergens, attenuated after long term culture. Research in Veterinary Science 46, 110–113.Google Scholar
Wright, I. G. and Goodger, B. V. (1988). Pathogenesis of babesiosis. In Babesiosis of Domestic Animals and Man (ed. Ristic, M.), pp. 99–118. CRC Press, Boca Raton, FL, USA.Google Scholar
Wright, I. G., Goodger, B. V., Leatch, G., Aylward, J. H., Rode-Bramanism, K. and Waltisbuhlm, D. J. (1987). Protection of Babesia bigemina-immune animals against subsequent challenge with virulent Babesia bovis. Infection and Immunity 55, 364–368.Google Scholar
Wright, I. G., Casua, R., Comminsa, M. A., Dalrymple, B. P., Gale, K. R., Goodger, B. V., Riddles, P. W., Waltisbuhl, D. J., Abetz, I., Berrie, D. A., Bowles, Y., Dimmock, C., Hayes, T., Kalnins, H., Leatch, G., McCrae, R., Montague, P. E., Nisbet, I. T., Parrodi, F., Peters, J. M., Scheiwe, P. C., Smith, W., Rode-Bramanis, K. and White, M. A. (1992). The development of a recombinant Babesia vaccine. Veterinary Parasitology 44, 3–13.Google Scholar
Wyatt, C. R., Goff, W. and Davis, W. C. (1991). A flow cytometric method for assessing viability of intraerythrocytic hemoparasites. Journal of Immunological Methods 140, 23–30.Google Scholar
Yokoyama, N., Okamura, M. and Igarashi, I. (2006). Erythrocyte invasion by Babesia parasites: current advances in the elucidation of the molecular interactions between the protozoan ligands and host receptors in the invasion stage. Veterinary Parasitology 138, 22–32.CrossRefGoogle ScholarPubMed
Yokoyama, N., Suthisak, B., Hirata, H., Matsuo, T., Inoue, N., Sugimoto, C. and Igarashi, I. (2012). Cellular localization of Babesia bovis merozoite rhoptry-associated protein 1 and its erythrocyte-binding activity. Infection and Immunity 70, 5822–5826.Google Scholar
Zintl, A., Westbrook, C., Mulcahy, G., Skerrett, H. E. and Gray, J. S. (2002 a). Invasion, and short-and long-term survival of Babesia divergens (Phylum Apicomplexa) cultures in non-bovine sera and erythrocytes. Parasitology 124, 583–588.Google Scholar
Zintl, A., Westbrook, C., Skerrett, H. E., Gray, J. S. and Mulcahy, G. (2002 b). Chymotrypsin and neuraminidase treatment inhibits host cell invasion by Babesia divergens (Phylum Apicomplexa). Parasitology 125, 45–50.Google Scholar
Zintl, A., Mulcahy, G., Skerrett, H. E., Taylor, S. M. and Gray, J. S. (2003). Babesia divergens: a bovine blood parasite of veterinary and zoonotic importance. Clinical Microbiology Reviews 16, 622–636.Google Scholar
Zintl, A., Gray, J. S., Skerrett, H. E. and Mulcahy, G. (2005). Possible mechanisms underlying age-related resistance to bovine babesiosis. Parasite Immunology 27, 115–120.Google Scholar
Zivkovic, Z., Torina, A., Mitra, R., Alongi, A., Scimeca, S., Kocan, K. M., Galindo, R. C., Almazán, C., Blouin, E. F., Villar, M., Nijhof, A. M., Mani, R., La Barbera, G., Caracappa, S., Jongejan, F. and de la Fuente, J. (2010). Subolesin expression in response to pathogen infection in ticks. BMC Immunology 11, 7.Google Scholar
Zweygarth, E. and Josemans, A. I. (2014). L-cysteine replaces microaerophilous culture conditions for the in vitro initiation of Theileria equi. Parasitology Research 113, 433–435. doi: 10.1007/s00436-013-3672-0.Google Scholar
Zweygarth, E., Van Niekerk, C., Just, M. C. and De Waal, D. T. (1995). In vitro cultivation of a Babesia sp. from cattle in South Africa. Onderstepoort Journal of Veterinary Research 62, 139–142.Google Scholar