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Biological role of excretory–secretory proteins in endemic parasites of Latin America and the Caribbean

Published online by Cambridge University Press:  16 May 2019

S. Gomez-Fuentes
Affiliation:
Unidad Periférica para el estudio de la Neuroinflamación en patologías Neurológicas del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, 14269 Mexico City, Mexico
V. Morales-Ruiz
Affiliation:
Unidad Periférica para el estudio de la Neuroinflamación en patologías Neurológicas del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, 14269 Mexico City, Mexico
D. López-Recinos
Affiliation:
Unidad Periférica para el estudio de la Neuroinflamación en patologías Neurológicas del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, 14269 Mexico City, Mexico
A. Guevara-Salinas
Affiliation:
Unidad Periférica para el estudio de la Neuroinflamación en patologías Neurológicas del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, 14269 Mexico City, Mexico
A. Arce-Sillas
Affiliation:
Unidad Periférica para el estudio de la Neuroinflamación en patologías Neurológicas del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, 14269 Mexico City, Mexico
J.F. Rodríguez
Affiliation:
Unidad Periférica para el estudio de la Neuroinflamación en patologías Neurológicas del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, 14269 Mexico City, Mexico
C. Parada-Colin
Affiliation:
Departamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, 04510 Mexico City, Mexico
L. Adalid-Peralta*
Affiliation:
Unidad Periférica para el estudio de la Neuroinflamación en patologías Neurológicas del Instituto de Investigaciones Biomédicas en el Instituto Nacional de Neurología y Neurocirugía, 14269 Mexico City, Mexico Instituto Nacional de Neurología y Neurocirugía, 14269 Mexico City, Mexico
*
Author for correspondence: L. Adalid-Peralta, E-mail: [email protected]

Abstract

Neglected tropical diseases (NTDs) share certain traits: they are parasitic infections, prevailing in tropical environments and affecting marginalized sectors of the population. Six NTDs – ascariasis, cysticercosis, echinococcosis, hookworm infection, onchocerciasis and trichuriasis – all of them endemic in Latin America and the Caribbean (LAC), are analysed in this work. This review aims to discuss key information on the function of excretory/secretory (E/S) proteins from these parasites in their infectivity, pathogeny and diagnosis. The modulation of the host immune system to favour the permanence and survival of the parasite is also discussed. An updated knowledge on the function of E/S molecules in endemic parasitoses in LAC may lead to new approaches for the clinical management and diagnosis of these diseases. In turn, this could allow us to optimize their treatment and make it more affordable – a relevant goal given the economic constraints that the region is facing.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2019 

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References

Adalid-Peralta, L, Arce-Sillas, A, Fragoso, G, et al. (2013) Cysticerci drive dendritic cells to promote in vitro and in vivo Tregs differentiation. Clinical and Developmental Immunology 2013, 981468.Google Scholar
Ali, F, Brown, A, Stanssens, P, Timothy, LM, Soule, HR and Pritchard, DI (2001) Vaccination with neutrophil inhibitory factor reduces the fecundity of the hookworm Ancylostoma ceylanicum. Parasite Immunology 23(5), 237249.Google Scholar
Antunes, MFP, Titz, TO, Batista, IFC, Marques-Porto, R, Oliveira, CF, Alves de Araujo, CA and Macedo-Soares, MF (2015) Immunosuppressive PAS-1 is an excretory/secretory protein released by larval and adult worms of the ascarid nematode Ascaris suum. Journal of Helminthology 89(3), 367374.Google Scholar
Atluri, SRV, Singhi, P, Khandelwal, N and Malla, N (2009) Evaluation of excretory secretory and 10-30 kDa antigens of Taenia solium Cysticerci by EITB assay for the diagnosis of neurocysticercosis. Parasite Immunology 31(3), 151155.Google Scholar
Baig, S, Damian, RT, Molinari, JL, Tato, P, Morales-Montor, J, Welch, M, Talhouk, J, Hashmey, R and White, AC (2005a) Purification and characterization of a metacestode cysteine proteinase from Taenia solium involved in the breakdown of human IgG. Parasitology 131(03), 411416.Google Scholar
Baig, S, Damian, RT, Morales-Montor, J, Olecki, P, Talhouk, J, Hashmey, R and White, AC (2005b) Characterization of excretory/secretory endopeptidase and metallo-aminopeptidases from Taenia crassiceps metacestodes. The Journal of Parasitology 91(5), 983987.Google Scholar
Barker, GC and Bundy, DAP (1999) Isolation of a gene family that encodes the porin-like proteins from the human parasitic nematode Trichuris trichiura. Gene 229(1–2), 131136.Google Scholar
Bethony, J, Brooker, S, Albonico, M, Geiger, SM, Loukas, A, Diemert, D and Hotez, PJ (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. The Lancet 367(9521), 15211532.Google Scholar
Beyhan, YE, Yilmaz, H and Hokelek, M (2016) Effects of acetic acid on the viability of Ascaris lumbricoides eggs. Is vinegar reliable enough to clean the vegetables? Saudi Medical Journal 37(3), 288292.Google Scholar
Boubaker, G, Gottstein, B, Hemphill, A, Babba, H and Spiliotis, M (2014) Echinococcus P29 antigen: molecular characterization and implication on post-surgery follow-up of CE patients infected with different species of the Echinococcus granulosus complex. PLoS ONE 9(5), e98357.Google Scholar
Bourke, CD, Maizels, RM and Mutapi, F (2011) Acquired immune heterogeneity and its sources in human helminth infection. Parasitology 138(2), 139159.Google Scholar
Brattig, NW, Henkle-Dührsen, KH, Hounkpatin, S, Liebau, E, Kruppa, TF and Zipfel, PF (1997) Characterization of human immune responses to the cytosolic superoxide dismutase and glutathione S-transferase from Onchocerca volvulus. Tropical Medicine & International Health 2(8), 788798.Google Scholar
Brooker, S, Bethony, J and Hotez, PJ (2004) Human hookworm infection in the 21st century. Advances in Parasitology 58, 197288.Google Scholar
Brophy, PM, Patterson, LH, Brown, A and Pritchard, DI (1995) Glutathione S-transferase (GST) expression in the human hookworm Necator americanus: potential roles for excretory-secretory forms of GST. Acta Tropica 59(3), 259263.Google Scholar
Cantacessi, C, Young, ND, Nejsum, P, Jex, AR, Campbell, BE, Hall, RS, Thamsborg, SM, Scheerlinck, J-P and Gasser, RB (2011) The transcriptome of Trichuris suis–first molecular insights into a parasite with curative properties for key immune diseases of humans. PLoS ONE 6(8), e23590.Google Scholar
Chiumiento, L and Bruschi, F (2009) Enzymatic antioxidant systems in helminth parasites. Parasitology Research 105(3), 593603.Google Scholar
Cho-Ngwa, F, Liu, J and Lustigman, S (2010) The Onchocerca volvulus cysteine proteinase inhibitor, Ov-CPI-2, is a target of protective antibody response that increases with age. PLoS Neglected Tropical Diseases 4(8), e800.Google Scholar
Coral-Almeida, M, Gabriël, S, Abatih, EN, Praet, N, Benitez, W and Dorny, P (2015) Taenia solium human cysticercosis: a systematic review of sero-epidemiological data from endemic zones around the world. PLoS Neglected Tropical Diseases 9(7), e0003919.Google Scholar
Cortez, MM, Rojas, GC and Parkhouse, RME (2018) The HP10 Taenia monoclonal antibody-based ELISA detects a similar protein in the vesicular fluid of Taenia hydatigena. Tropical Animal Health and Production 50(3), 697700.Google Scholar
De Araújo, CAA, Perini, A, Martins, MA, Macedo, MS and Macedo-Soares, MF (2010) PAS-1, an Ascaris suum protein, modulates allergic airway inflammation via CD8+ΓδTCR+ and CD4+CD25+FoxP3+ T cells. Scandinavian Journal of Immunology 72(6), 491503.Google Scholar
De Silva, NR, Brooker, S, Hotez, PJ, Montresor, A, Engels, D and Savioli, L (2003) Soil-transmitted helminth infections: updating the global picture. Trends in Parasitology 19(12), 547551.Google Scholar
Delunardo, F, Ortona, E, Margutti, P, Perdicchio, M, Vacirca, D, Teggi, A, Sorice, M and Siracusano, A (2010) Identification of a novel 19 kDa Echinococcus granulosus antigen. Acta Tropica 113(1), 4247.Google Scholar
Díaz, A, Ibarguren, S, Breijo, M, Willis, AC and Sim, RB (2000) Host-derived annexin II at the host-parasite interface of the Echinococcus granulosus hydatid cyst. Molecular and Biochemical Parasitology 110(1), 171176.Google Scholar
Diemert, DJ, Bethony, JM and Hotez, PJ (2008) Hookworm vaccines. Clinical Infectious Diseases 46(2), 282288.Google Scholar
Drake, L, Korchev, Y, Bashford, L, Djamgoz, M, Wakelin, D, Ashall, F and Bundy, D (1994) The major secreted product of the whipworm, Trichuris, is a pore-forming protein. Proceedings of the Royal Society of London. Series B: Biological Sciences 257(1350), 255261.Google Scholar
Dzik, JM (2006) Molecules released by helminth parasites involved in host colonization. Acta Biochimica Polonica 53(1), 3364.Google Scholar
Fernández, V, Chalar, C, Martínez, C, Musto, H, Zaha, A and Fernández, C (2000) Echinococcus granulosus: molecular cloning and phylogenetic analysis of an inducible glutathione S-transferase. Experimental Parasitology 96(3), 190194.Google Scholar
Fleury, A, Hernandez, M, Avila, M, et al. (2007) Detection of HP10 antigen in serum for diagnosis and follow-up of subarachnoidal and intraventricular human neurocysticercosis. Journal of Neurology, Neurosurgery & Psychiatry 78(9), 970974.Google Scholar
Franco-Paredes, C, Jones, D, Rodríguez-morales, AJ and Santos-Preciado, JI (2007) Commentary: improving the health of neglected populations in Latin America. BMC Public Health 7(1), 11.Google Scholar
Gao, Y-J, Yan, H-L, Ding, F-X, Lu, Y-M and Sun, S-H (2007) Annexin B1 at the host–parasite interface of the Taenia solium cysticercus: secreted and associated with inflammatory reaction. Acta Tropica 101(3), 192199.Google Scholar
Geng, J, Plenefisch, J, Komuniecki, PR and Komuniecki, R (2002) Secretion of a novel developmentally regulated chitinase (family 19 glycosyl hydrolase) into the perivitelline fluid of the parasitic nematode, Ascaris suum. Molecular and Biochemical Parasitology 124(1–2), 1121.Google Scholar
Gomez, S, Adalid-Peralta, L, Palafox-Fonseca, H, et al. (2015) Genome analysis of Excretory/Secretory proteins in Taenia solium reveals their Abundance of Antigenic Regions (AAR). Scientific Reports 5(1), 9683.Google Scholar
González, G, Spinelli, P, Lorenzo, C, Hellman, U, Nieto, A, Willis, A and Salinas, G (2000) Molecular characterization of P-29, a metacestode-specific component of Echinococcus granulosus which is immunologically related to, but distinct from, antigen 5. Molecular and Biochemical Parasitology 105(2), 177184.Google Scholar
Gustavsen, K, Hopkins, A and Sauerbrey, M (2011) Onchocerciasis in the Americas: from arrival to (near) elimination. Parasites and Vectors 4(1), 205.Google Scholar
Hawdon, JM, Datu, B and Crowell, M (2003) Molecular cloning of a novel multidomain Kunitz-type proteinase inhibitor from the hookworm Ancylostoma caninum 89(2), 402407.Google Scholar
Hiemstra, IH, Klaver, EJ, Vrijland, K, Kringel, H, Andreasen, A, Bouma, G, Kraal, G, van Die, I and den Haan, JMM (2014) Excreted/secreted Trichuris suis products reduce barrier function and suppress inflammatory cytokine production of intestinal epithelial cells. Molecular Immunology 60(1), 17.Google Scholar
Hewitson, JP, Grainger, JR and Maizels, RM (2009) Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Molecular and Biochemical Parasitology 167(1), 111.Google Scholar
Hill, DE and Sakanari, JA (1997) Trichuris suis: thiol protease activity from adult worms. Experimental Parasitology 85(1), 5562.Google Scholar
Hill, DE, Gamble, HR, Rhoads, ML, Fetterer, RH and Urban, JF (1993) Trichuris suis: a zinc metalloprotease from culture fluids of adult parasites. Experimental Parasitology 77(2), 170178.Google Scholar
Hotez, PJ, Bottazzi, ME, Franco-paredes, C, Ault, SK and Periago, MR (2008) The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination. PLoS Neglected Tropical Diseases 2(9), e300.Google Scholar
Hotez, PJ, Diemert, D, Bacon, KM, et al. (2013) The human hookworm vaccine. Vaccine 31(Suppl 2), 227232.Google Scholar
Ibáñez-Shimabukuro, M, Florencia Rey-Burusco, M, Cooper, A, Kennedy, MW, Córsico, B and Smith, BO (2014) Resonance assignment of As-P18, a fatty acid binding protein secreted by developing larvae of the parasitic nematode Ascaris suum. Biomolecular NMR Assignments 8(1), 3336.Google Scholar
Jex, AR, Nejsum, P, Schwarz, EM, et al. (2014) Genome and transcriptome of the porcine whipworm Trichuris suis. Nature Genetics 46(7), 701706.Google Scholar
Kasper, G, Brown, A, Eberl, M, et al. (2001) A calreticulin-like molecule from the human hookworm Necator americanus interacts with C1q and the cytoplasmic signalling domains of some integrins. Parasite Immunology 23(3), 141152.Google Scholar
Kennedy, MW and Qureshi, F (1986) Stage-specific secreted antigens of the parasitic larval stages of the nematode Ascaris. Immunology 58(3), 515522.Google Scholar
Laclette, JP, Landa, A, Arcos, L, Willms, K, Davis, AE and Shoemaker, CB (1991) Paramyosin is the Schistosoma mansoni (Trematoda) homologue of antigen B from Taenia solium (Cestoda). Molecular and Biochemical Parasitology 44(2), 287295.Google Scholar
Laclette, JP, Shoemaker, CB, Richter, D, Arcos, L, Pante, N, Cohen, C, Bing, D and Nicholson-Weller, A (1992) Paramyosin inhibits complement C1. The Journal of Immunology 148(1), 124128.Google Scholar
Leon, N, Padilla, C, Pajuelo, M, Sheen, P and Zimic, M (2013) Cathepsin L cysteine protease from Taenia solium: its biological role in the infection and potential use for the immunodiagnosis of neurocysticercosis. Rev Peru Med Exp Salud Publica 30(3), 446454.Google Scholar
Levine, MZ, Calderón, JC, Wilkins, PP, et al. (2004) Characterization, cloning, and expression of two diagnostic antigens for Taenia solium tapeworm infection. Journal of Parasitology 90(3), 631638.Google Scholar
Li, DA, He, Y, Guo, YJ, Wang, F, Song, SX, Wang, Y, Yang, F, He, XW and Sun, SH (2007) Comparative proteomics analysis to annexin B1 DNA and protein vaccination in mice. Vaccine 25(5), 932938.Google Scholar
Liebau, E, Walter, RD and Henkle-Duhrsen, K (1994) Onchocerca volvulus: isolation and sequence of a second glutathione S- transferase cDNA. Experimental Parasitology 79(1), 6871.Google Scholar
Lillywhite, JE, Cooper, ES, Needham, CS, Venugopal, S, Bundy, DAP and Bianco, AE (1995) Identification and characterization of excreted/secreted products of Trichuris trichiura. Parasite Immunology 17(1), 4754.Google Scholar
Lorenzatto, KR, Monteiro, KM, Paredes, R, Paludo, GP, Da Fonsêca, MM, Galanti, N, Zaha, A and Ferreira, HB (2012) Fructose-bisphosphate aldolase and enolase from Echinococcus granulosus: genes, expression patterns and protein interactions of two potential moonlighting proteins. Gene 506(1), 7684.Google Scholar
Loukas, A and Prociv, P (2001) Immune responses in hookworm infections. Clinical Microbiology Reviews 14(4), 689703.Google Scholar
Loukas, A, Brown, AP and Pritchard, DI (2002) Na-Ctl-2, a CDNA encoding a C-type lectin expressed exclusively in adult Necator americanus hookworms. DNA Sequence 13(1), 6165.Google Scholar
Loukas, A, Bethony, J, Brooker, S and Hotez, P (2006) Hookworm vaccines: past, present, and future. The Lancet Infectious Diseases 6(11), 733741.Google Scholar
Lustigman, S, Prichard, RK, Gazzinelli, A, Grant, WN, Boatin, BA, McCarthy, JS and Basáñez, MG (2012) A research agenda for helminth diseases of humans: the problem of helminthiases. PLoS Neglected Tropical Diseases 6(4), e1582.Google Scholar
Mahalakshmi, N, Aparnaa, R, Vishal, LA and Kaliraj, P (2013) Molecular characterization and evaluation of Onchocerca volvulus-secreted larval acidic protein 1 (SLAP1) as a putative vaccine candidate on endemic population of lymphatic filariasis. Parasitology Research 112(9), 32033211.Google Scholar
Mazumder, DN, Santra, A, Dutta, G, Ghosh, N and Chowdhury, MK (1992) Hepatic lesions caused by excretory and secretory products of Ascaris lumbricoides in golden hamster. Indian Journal of Gastroenterology 11(3), 117120.Google Scholar
Mc Gibbon, AM and Lee, TDG (1995) Structural characteristics of the Ascaris allergen, ABA-1. Parasite 2(1), 4148.Google Scholar
Mei, B, Kennedy, MW, Beauchamp, J, Komuniecki, PR and Komuniecki, R (1997) Secretion of a novel, developmentally regulated fatty acid-binding protein into the perivitelline fluid of the parasitic nematode, Ascaris suum. The Journal of Biological Chemistry 272(15), 99339941.Google Scholar
Melo, CFOR, Esteves, CZ, de Oliveira, RN, Guerreiro, TM, de Oliveira, DN, de Oliveira Lima, E, Miné, JC, Allegretti, SM and Catharino, RR (2016) Early developmental stages of Ascaris lumbricoides featured by high-resolution mass spectrometry. Parasitology Research 115(11), 41074114.Google Scholar
Monteiro, KM, Lorenzatto, KR, de Lima, JC, dos Santos, GB, Förster, S, Paludo, GP, Carvalho, PC, Brehm, K and Ferreira, HB (2017) Comparative proteomics of hydatid fluids from two Echinococcus multilocularis isolates. Journal of Proteomics 162, 4051.Google Scholar
Moreno, Y, Gros, PP, Tam, M, Segura, M, Valanparambil, R, Geary, TG and Stevenson, MM (2011) Proteomic analysis of excretory-secretory products of Heligmosomoides polygyrus assessed with next-generation sequencing transcriptomic information. PLoS Neglected Tropical Diseases 5(10), e1370.Google Scholar
Muto, R, Imai, S, Tezuka, H, Furuhashi, Y and Fujita, K (2001) The biological activity of ABA-1-like protein from Ascaris lumbricoides. Journal of Medical and Dental Sciences 48(3), 95104.Google Scholar
Nirmalan, N, Cordeiro, NJV, Kläger, SL, Bradley, JE and Allen, JE (1999) Comparative analysis of glycosylated and nonglycosylated filarial homologues of the 20-kilodalton retinol binding protein from Onchocerca volvulus (Ov20). Infection and Immunity 67(12), 63296334.Google Scholar
Ortona, E, Margutti, P, Delunardo, F, et al. (2005) Screening of an Echinococcus granulosus CDNA library with IgG4 from patients with cystic echinococcosis identifies a new tegumental protein involved in the immune escape. Clinical and Experimental Immunology 142(3), 528538.Google Scholar
Oshiro, TM, Enobe, CS, Araújo, CA, Macedo, MS and Macedo-Soares, MF (2006) PAS-1, a protein affinity purified from Ascaris suum worms, maintains the ability to modulate the immune response to a bystander antigen. Immunology and Cell Biology 84(2), 138144.Google Scholar
Parthasarathy, G and Mansfield, LS (2005) Trichuris suis excretory secretory products (ESP) elicit interleukin-6 (IL-6) and IL-10 secretion from intestinal epithelial cells (IPEC-1). Veterinary Parasitology 131(3–4), 317324.Google Scholar
Plenefisch, J, Xiao, H, Mei, B, Geng, J, Komuniecki, PR and Komuniecki, R (2000) Secretion of a novel class of IFABPs in nematodes: coordinate use of the Ascaris/Caenorhabditis model systems. Molecular and Biochemical Parasitology 105(2), 223236.Google Scholar
PNUD. (2019) Sobre América Latina y El Caribe. Available at http://www.latinamerica.undp.org/content/rblac/es/home/regioninfo.htmlGoogle Scholar
Prieto-Perez, L, Perez-Tanoira, R, Cabello-Ubeda, A, Petkova-Saiz, E and Gorgolas-Hernandez-Mora, M (2016) Geohelminths. Enfermedades infecciosas y microbiologia clinica 34(6), 384389.Google Scholar
Reddy, A and Fried, B (2009) An update on the use of helminths to treat Crohn's and other autoimmunune diseases. Parasitology Research 104(2), 217221.Google Scholar
Rhoads, ML and Fetterer, RH (1998) Purification and characterisation of a secreted aminopeptidase from adult Ascaris suum. International Journal for Parasitology 28(11), 16811690.Google Scholar
Rhoads, ML, Fetterer, RH, Hill, DE and Urban, JF (2000) Trichuris suis: a secretory chymotrypsin/elastase inhibitor with potential as an immunomodulator. Experimental Parasitology 95(1), 3644.Google Scholar
Ridi, RE and Tallima, H (2009) Schistosoma mansoni ex vivo lung-stage larvae excretory–secretory antigens as vaccine candidates against schistosomiasis. Vaccine 27(5), 666673.Google Scholar
Rosales Borjas, D and Ortiz Ortiz, L (2008) Infecciones parasitarias: mecanismos de evasión de la respuesta inmune. Revista Médica de La Extensión Portuguesa – ULA 2, 8998.Google Scholar
Saboyá, MI, Catalá, L, Nicholls, RS and Ault, SK (2013) Update on the mapping of prevalence and intensity of infection for soil-transmitted helminth infections in Latin America and the Caribbean: a call for action. PLoS Neglected Tropical Diseases 7(9), e2419.Google Scholar
Salinas, G, Braun, G and Taylor, DW (1994) Molecular characterisation and localisation of an Onchocerca volvulus π-class glutathione S-transferase. Molecular and Biochemical Parasitology 66(1), 19.Google Scholar
Santra, A, Chowdhury, A, Ghosh, A and Mazumder, DN (2000) Development of an animal model of hepatic fibrosis by excretory-secretory antigen of Ascaris suum. Indian Journal of Gastroenterology: Official Journal of the Indian Society of Gastroenterology 19(3), 119121.Google Scholar
Schneider, MC, Aguilera, XP, da Silva Junior, JB, et al. (2011) Elimination of neglected diseases in Latin America and the Caribbean: a mapping of selected diseases. PLoS Neglected Tropical Diseases 5(2), e964.Google Scholar
Shalaby, NM and Shalaby, NM (2016) Effect of Ascaris lumbricoides infection on T helper cell type 2 in rural Egyptian children. Therapeutics and Clinical Risk Management 12, 379385.Google Scholar
Siles-Lucas, M, Nunes, CP, Zaha, A and Breijo, M (2000) The 14-3-3 protein is secreted by the adult worm of Echinococcus granulosus. Parasite Immunology 22(10), 521528.Google Scholar
Song, X, Hu, D, Zhong, X, Wang, N, Gu, X, Wang, T, Peng, X and Yang, G (2016) Characterization of a secretory annexin in Echinococcus granulosus. American Journal of Tropical Medicine and Hygiene 94(3), 626633.Google Scholar
Summers, RW, Elliot, DE, Urban, JF, Thompson, R and Weinstock, JV (2005) Trichuris suis therapy in Crohn's disease. Gut 54(1), 8790.Google Scholar
Tato, P, Castro, AM, Rodríguez, D, Soto, R, Arechavaleta, F and Molinari, JL (1995) Suppression of murine lymphocyte proliferation induced by a small RNA purified from the Taenia solium metacestode. Parasitology Research 81(3), 181187.Google Scholar
Tato, P, White, AC, Willms, K, Rodríguez, D, Solano, S, Sepúlveda, J and Molinari, JL (1996) Immunosuppression and inhibition of inflammation in mice induced by a small Taenia solium RNA-peptide to implanted T. solium metacestodes. Parasitology Research 82(7), 590597.Google Scholar
Vibanco-Pérez, N and Landa-Piedra, A (1998) Glutathione S-transferase in helminth parasites. Revista Latinoamericana de Microbiologia 40(1–2), 7385.Google Scholar
Victor, B, Dorny, P, Kanobana, K, Polman, K, Lindh, J, Deelder, AM, Palmblad, M and Gabriël, S (2013) Use of expressed sequence tags as an alternative approach for the identification of Taenia solium metacestode excretion/secretion proteins. BMC Research Notes 6, 224.Google Scholar
Virginio, VG, Monteiro, KM, Drumond, F, de Carvalho, MO, Vargas, DM, Zaha, A and Ferreira, HB (2012) Excretory/secretory products from in vitro-cultured Echinococcus granulosus protoscoleces. Molecular and Biochemical Parasitology 183(1), 1522.Google Scholar
Wang, L, Liu, H, Chen, X, Zhang, M, Xie, K and Ma, Q (2012) Immune sculpting of norepinephrine on MHC-I, B7-1, IDO and B7-H1 expression and regulation of proliferation and invasion in pancreatic carcinoma cells. PLoS ONE 7(9), e45491.Google Scholar
Wang, T, Van Steendam, K, Dhaenens, M, Vlaminck, J, Deforce, D, Jex, AR, Gasser, RB and Geldhof, P (2013) Proteomic analysis of the excretory-secretory products from larval stages of Ascaris suum reveals high abundance of glycosyl hydrolases. PLoS Neglected Tropical Diseases 7(10), e2467.Google Scholar
Wang, Y, Xiao, D, Shen, Y, et al. (2015) Proteomic analysis of the excretory/secretory products and antigenic proteins of Echinococcus granulosus adult worms from infected dogs. BMC Veterinary Research 11(1), 119.Google Scholar
WHO (World Health Organization). (2016) World health statistics 2016: monitoring health for the SDGs, sustainable development goals. World Health Organization. http://www.who.int/iris/handle/10665/206498Google Scholar
WHO. (2017a) OMS | Equinococosis. Available at http://www.who.int/mediacentre/factsheets/fs377/es/ (accessed 9 January 2018).Google Scholar
WHO. (2017b) OMS | Oncocercosis. Available at http://www.who.int/mediacentre/factsheets/fs374/es/ (accessed 9 January 2018).Google Scholar
Williamson, AL, Lustigman, S, Oksov, Y, et al. (2006) Ancylostoma caninum MTP-1, an astacin-like metalloprotease secreted by infective hookworm larvae, is involved in tissue migration. Infection and Immunity 74(2), 961967.Google Scholar
Wu, Y, Egerton, G, Pappin, DJC, Harrison, RA, Wilkinson, MC, Underwood, A and Bianco, AE (2004) The Secreted Larval Acidic Proteins (SLAPs) of Onchocerca spp. are encoded by orthologues of the alt gene family of Brugia malayi and have host protective potential. Molecular and Biochemical Parasitology 134(2), 213224.Google Scholar
Xia, Y, Spence, HJ, Moore, J, et al. (2000) The ABA-1 allergen of Ascaris Lumbricoides: sequence polymorphism, stage and tissue-specific expression, lipid binding function, and protein biophysical properties. Parasitology 120(Pt 2), 211224.Google Scholar
Zhan, B, Gupta, R, Wong, S, Bier, S, Jiang, D, Goud, G and Hotez, P (2008) Molecular cloning and characterization of Ac-TMP-2, a tissue inhibitor of metalloproteinase secreted by adult Ancylostoma caninum. Molecular and Biochemical Parasitology 162(2), 142148.Google Scholar
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