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Babesia parasites develop and are transmitted by the non-vector soft tick Ornithodoros moubata (Acari: Argasidae)

Published online by Cambridge University Press:  18 September 2006

B. BATTSETSEG
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
T. MATSUO
Affiliation:
Department of Infectious Diseases, Kyorin University, School of Medicine, Mitaka, Tokyo 181-8611, Japan
X. XUAN
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
D. BOLDBAATAR
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
S. H. CHEE
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
R. UMEMIYA
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
T. SAKAGUCHI
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
T. HATTA
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
J. ZHOU
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
A. R. VERDIDA
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan
D. TAYLOR
Affiliation:
Graduate School of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8577, Japan
K. FUJISAKI
Affiliation:
National Research Center for Protozoan Diseases, Obihiro University of Agriculture and Veterinary Medicine, Inada-cho, Obihiro, Hokkaido 080-8555, Japan

Abstract

Ornithodoros moubata ticks were fed on blood infected with Babesia equi. However, the parasites were quickly cleared as evidenced by the disappearance of B. equi-specific ribosomal RNA from the ticks. We hypothesized that if the Babesia parasite can escape midgut-associated barriers a non-vector tick can become infected with Babesia. To test this hypothesis, B. equi parasite-infected blood from in vitro culture was injected into the haemocoel of ticks. B. equi-specific rRNA was surprisingly detected 45 days after injection even in the eggs. Babesia-free dogs were infested with O. moubata ticks that were infected by inoculation with B. gibsoni-infected red blood cells. Parasitaemia and antibody production against Bg-TRAP of B. gibsoni increased gradually. These results indicate that O. moubata may be a useful vector model for Babesia parasites and also a very important tool for studies on tick immunity against Babesia parasites and tick-Babesia interactions.

Type
Research Article
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Abraham, E. G. and Jacobs-Lorena, M. ( 2004). Mosquito midgut barriers to malaria parasite development. Insect Biochemistry and Molecular Biology 34, 667671.CrossRefGoogle Scholar
Avarzed, A., de Waal, D. T., Igarashi, I., Saito, A., Oyamada, T., Toyoda, Y. and Suzuki, N. ( 1997). Prevalence of equine piroplasmosis in central Mongolia. Onderstepoort Journal of Veterinary Research 64, 141145.Google Scholar
Ceraul, S. M., Sonenshine, D. E. and Hynes, W. L. ( 2002). Resistance of the tick Dermacentor variabilis (Acari Ixodidae) following challenge with the bacterium Escherichia coli (Enterobacteriales: Entero-bacteriaceae). Journal of Medical Entomology 39, 376383.CrossRefGoogle Scholar
Ceraul, S. M., Sonenshine, D. E., Ratzlaff, R. E. and Hynes, W. L. ( 2003). An arthropod defensin expressed by hemocytes of the American dog tick, Dermacentor variabilis (Acari Ixodidae). Insect Biochemistry and Molecular Biology 33, 10991103.CrossRefGoogle Scholar
Chinzei, Y. ( 1983). Quantitative changes of vitellogenin and vitellin in adult female ticks, Ornithodoros moubata, during vitellogenesis. Mie Medical Journal 32, 117127.Google Scholar
Chomczyski, P. and Sacchi, N. ( 1987). Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156159.Google Scholar
Fogaca, A. C., da Silva, P. I. Jr., Miranda, M. T., Bianchi, A. G., Miranda, A., Ribolla, P. E. and Daffre, S. ( 1999). Antimicrobial activity of a bovine hemoglobin fragment in the tick Boophilus microplus. Journal of Biological Chemistry 274, 2533025334.CrossRefGoogle Scholar
Fogaca, A. C., Lorenzini, D. M., Kaku, L. M., Esteves, E., Bulet, P. and Daffre, S. ( 2004). Cysteine-rich antimicrobial peptides of the cattle tick Boophilus microplus: isolation, structural characterization and tissue expression profile. Developmental and Comparative Immunology 28, 191200.CrossRefGoogle Scholar
Fukumoto, S., Sekine, Y., Xuan, X., Igarashi, I., Sugimoto, C., Fujisaki, K., Nagasawa, H., Makimura, S. and Suzuki, H. ( 2004). Serodiagnosis of canine Babesia gibsoni infection by enzyme-linked immunosorbent assay with recombinant P50 expressed in Escherichia coli. The Journal of Parasitology 90, 387391.CrossRefGoogle Scholar
Fukumoto, S., Xuan, X., Igarashi, I., Zhang, S., Suzuki, N. and Mikami, T. ( 2000). Morphological changes of Babesia gibsoni grown in canine red blood cell-substituted severe combined immune deficiency mice. Journal of Parasitology 86, 956958.CrossRefGoogle Scholar
Fukumoto, S., Xuan, X., Nishikawa, Y., Inoue, N., Igarashi, I., Nagasawa, H., Fujisaki, K. and Mikami, T. ( 2001 a). Identification and expression of a 50-kilodalton surface antigen of Babesia gibsoni and evaluation of its diagnostic potential in an enzyme-linked immunosorbent assay. Journal of Clinical Microbiology 39, 26032609.Google Scholar
Fukumoto, S., Xuan, X., Shigeno, S., Kimbita, E., Igarashi, I., Nagasawa, H., Fujisaki, K. and Mikami, T. ( 2001 b). Development of a polymerase chain reaction method for diagnosing Babesia gibsoni infection in dogs. Journal of Veterinary Medical Science 63, 977981.Google Scholar
Gillespie, J. P., Kanost, M. R. and Trenczek, T. ( 1997). Biological mediators of insect immunity. Annual Review of Entomology 42, 611643.CrossRefGoogle Scholar
Grandjean, O. ( 1983). Blood digestion in Ornithodorus moubata Murray sensu stricto Walton females (Ixodoidea: Argasidae) II. Modifications of midgut cells related to the digestive cycle and to the triggering action of mating. Annales de Parasitologie Humaine et Comparee 58, 493514.Google Scholar
Homer, J. M., Aguilar-Delfin, I., Telford, III S. R., Krause, P. J. and Persing, D. H. ( 2000). Babesiosis. Clinical Microbiology Reviews 13, 451469.CrossRefGoogle Scholar
Inoue, N., Hanada, K., Tsuji, N., Igarashi, I., Nagasawa, H., Mikami, T. and Fujisaki, K. ( 2001). Characterization of phagocytic hemocytes in Ornithodoros moubata (Acari Ixodidae). Journal of Medical Entomology 38, 514519.CrossRefGoogle Scholar
Johns, R., Sonenshine, D. E. and Hynes, W. L. ( 1998). Control of bacterial infections in the hard tick Dermacentor variabilis (Acari Ixodidae): evidence for the existence of antimicrobial proteins in tick hemolymph. Journal of Medical Entomology 35, 458464.CrossRefGoogle Scholar
Johns, R., Sonenshine, D. E. and Hynes, W. L. ( 2001). Identification of a defensin from the hemolymph of the American dog tick, Dermacentor variabilis. Insect Biochemistry and Molecular Biology 31, 857865.CrossRefGoogle Scholar
Kadota, K., Satoh, E., Ochiai, M., Inoue, N., Tsuji, N., Igarashi, I., Nagasawa, H., Mikami, T., Claveria, F. G. and Fujisaki, K. ( 2002). Existence of phenol oxidase in the argasid tick Ornithodoros moubata. Parasitology Research 88, 781784.CrossRefGoogle Scholar
Kappmeyer, L. S., Perryman, L. E. and Knowles, D. P. ( 1993). A Babesia equi gene encodes a surface protein with homology to Theileria species. Molecular and Biochemical Parasitology 62, 121124.CrossRefGoogle Scholar
Kjemtrup, A. M. and Conrad, P. A. ( 2000). Human babesiosis: an emerging tick-borne disease. International Journal for Parasitology 30, 13231337.CrossRefGoogle Scholar
Knowles, D. P., Perryman, L. E. and Kappmeyer, L. S. ( 1997). Genetic and biochemical analysis of erythrocyte-stage surface antigens belonging to a family of highly conserved proteins of Babesia equi and Theileria species. Molecular and Biochemical Parasitology 90, 6979.CrossRefGoogle Scholar
Kopacek, P., Vogt, R., Jindrak, L., Weise, C. and Safarik, I. ( 1999). Purification and characterization of the lysozyme from the gut of the soft tick Ornithodoros moubata. Insect Biochemistry and Molecular Biology 29, 989997.CrossRefGoogle Scholar
Kopacek, P., Weice, C., Saravanan, T., Vitova, K. and Grubhoffer, L. ( 2000). Characterization of an α-macroglobulin-like glycoprotein isolated from the plasma of the soft tick Ornithodoros moubata. European Journal of Biochemistry 267, 465475.CrossRefGoogle Scholar
Kryuchechnikov, V. N. ( 1991). Protective responses of Ixodoidea hemocytes. In Modern Acarology ( ed. Dusbábek, F. and Bukva, V.), vol. 1. pp. 331334. Academia/SPB Academic Publishing, Prague/The Hague.
Kuttler, K. L. ( 1988). Worldwide impact of babesiosis. In Babesiosis of Domestic Animals and Man ( ed. Ristic, M.), pp. 122. Boca Raton, FL, CRC Press.
Lai, R., Lomas, L. O., Jonczy, J., Turner, P. C. and Rees, H. H. ( 2004). Two novel non-cationic defensin-like antimicrobial peptides from haemolymph of the female tick, Amblyomma hebraeum. The Biochemical Journal 379, 681685.CrossRefGoogle Scholar
Matsuo, T., Okoda, Y., Badgar, B., Inoue, N., Xuan, X., Taylor, D. and Fujisaki, K. ( 2004). Fate of GFP-expressing Escherichia coli in the midgut and response to ingestion in a tick, Ornithodoros moubata (Acari: Argasidae). Experimental Parasitology 108, 6773.CrossRefGoogle Scholar
Nakajima, Y., van der Goes van Naters-Yasui, A., Taylor, D. and Yamakawa, M. ( 2001). Two isoforms of a member of the arthropod defensin family from the soft tick, Ornithodoros moubata (Acari: Argasidae). Insect Biochemistry and Molecular Biology 31, 747751.CrossRefGoogle Scholar
Nakajima, Y., Taylor, D. and Yamakawa, M. ( 2002 a). Involvement of antibacterial peptide defensin in tick midgut defense. Experimental and Applied Acarology 28, 135140.Google Scholar
Nakajima, Y., van der Goes van Naters-Yasui, A., Taylor, D. and Yamakawa, M. ( 2002 b). Antibacterial peptide defensin is involved in midgut immunity of the soft tick, Ornithodoros moubata (Acari: Argasidae). Insect Molecular Biology 11, 611618.Google Scholar
Nakajima, Y., Ogihara, K., Taylor, D. and Yamakawa, M. ( 2003). Antibacterial hemoglobin fragments from the midgut of the soft tick, Ornithodoros moubata (Acari: Argasidae). Journal of Medical Entomology 40, 7881.CrossRefGoogle Scholar
Nakajima, Y., Saido-Sakanaka, H., Ogihara, K., Taylor, D. and Yamakawa, M. ( 2005). Antibacterial peptides are secreted into the midgut lumen to provide antibacterial midgut defense in the soft tick, Ornithodoros moubata (Acari: Argasidae). Applied Entomology and Zoology 40, 391397.CrossRefGoogle Scholar
Saravanan, T., Weise, C., Sojka, D. and Kopacek, P. ( 2003). Molecular cloning, structure and bait region splice variants of α2-macroglobulin from the soft tick Ornithodoros moubata. Insect Biochemistry and Molecular Biology 33, 841851.CrossRefGoogle Scholar
Shen, Z., Dimopoulos, G., Kafatos, F. C. and Jacobs-Lorena, M. ( 1999). A cell surface mucin specifically expressed in the midgut of the malaria mosquito Anopheles gambiae. Proceedings of the National Academy of Sciences, USA 96, 56105615.CrossRefGoogle Scholar
Simser, J. A., Mulenga, A., Macaluso, K. R. and Azad, A. F. ( 2004). An immune responsive factor D-like serine proteinase homologue identified from the American dog tick, Dermacentor variabilis. Insect Molecular Biology 13, 2535.CrossRefGoogle Scholar
Sinden, R. E. and Billingsley, P. F. ( 2001). Plasmodium invasion of mosquito cells: hawk or dove? Trends in Parasitology 17, 209211.Google Scholar
Sonenshine, D. E., Hynes, W. L., Ceraul, S. M., Mitchell, R. and Benzine, T. ( 2005). Host blood proteins and peptides in the midgut of the tick Dermacentor variabilis contribute to bacterial control. Experimental and Applied Acarology 36, 207223.CrossRefGoogle Scholar
Waladde, S. M., Ocheing, S. A. and Gichuhi, P. M. ( 1991). Artificial-membrane feeding of the ixodid tick, Rhipicephalus appendiculatus, to repletion. Experimental and Applied Acarology 11, 297306.CrossRefGoogle Scholar
Wei, Q., Tsuji, M., Zamoto, A., Kohsaki, M., Matsui, T., Shiota, T., Telford, III S. R. and Ishihara, C. ( 2001). Human babesiosis in Japan: isolation of Babesia microti-like parasites from an asymptomatic transfusion donor and from a rodent from an area where babesiosis is endemic. Journal of Clinical Microbiology 39, 21782183.CrossRefGoogle Scholar
Zhou, J., Fukumoto, S., Jia, H., Yokoyama, N., Zhang, G., Fujisaki, K., Lin, J. and Xuan, X. ( 2006). Characterization of the Babesia gibsoni p18 as a homologue of thrombospondin related adhesive protein. Molecular and Biochemical Parasitology 148, 190198.CrossRefGoogle Scholar