Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-19T23:33:11.959Z Has data issue: false hasContentIssue false
  • English
  • Français

Induction of protection in murine experimental models against Trichinella spiralis: an up-to-date review

Published online by Cambridge University Press:  12 March 2015

G. Ortega-Pierres ,
A. Vaquero-Vera ,
R. Fonseca-Liñán ,
R.M. Bermúdez-Cruz  and
R. Argüello-García
G. Ortega-Pierres*
Affiliation:
Departamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, México City, México
A. Vaquero-Vera
Affiliation:
Departamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, México City, México
R. Fonseca-Liñán
Affiliation:
Departamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, México City, México
R.M. Bermúdez-Cruz
Affiliation:
Departamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, México City, México
R. Argüello-García
Affiliation:
Departamento de Genética y Biología Molecular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, México City, México
*
*E-mail: gortega@cinvestav.mx
Get access Rights & Permissions [Opens in a new window]

Abstract

The parasitic nematode Trichinella spiralis, an aetiological agent of the disease known as trichinellosis, infects wild and domestic animals through contaminated pig meat, which is the major source for Trichinella transmission. Prevention of this disease by interrupting parasite transmission includes vaccine development for livestock; however, major challenges to this strategy are the complexity of the T. spiralis life cycle, diversity of stage-specific antigens, immune-evasion strategies and the modulatory effect of host responses. Different approaches have been taken to induce protective immune responses by T. spiralis immunogens. These include the use of whole extracts or excretory–secretory antigens, as well as recombinant proteins or synthesized epitopes, using murine experimental models for trichinellosis. Here these schemes are reviewed and discussed, and new proposals envisioned to block the zoonotic transmission of this parasite.

Type
Review Articles
Information
Journal of Helminthology , Volume 89 , Issue 5 , September 2015 , pp. 526 - 539
Copyright
Copyright © Cambridge University Press 2015 

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

Abdel-Rahman, E.H., Abouel Ezz, N.M. & Abdel Megeed, K.N. (2005) Trichinella spiralis: affinity purified antigen based diagnosis and immunoprophylaxis. Journal of the Egyptian Society of Parasitology 35, 379–393.Google ScholarPubMed
Alizadeh, H. & Murrell, K.D. (1984) The intestinal mast cell response to Trichinella spiralis infection in mast cell-deficient w/wv mice. Journal of Parasitology 70, 767–773.CrossRefGoogle ScholarPubMed
Allen, J.E. & Maizels, R.M. (2011) Diversity and dialogue in immunity to helminths. Nature Reviews Immunology 11, 375–388.CrossRefGoogle ScholarPubMed
Artis, D., Wang, M.L., Keilbaugh, S.A., He, W., Brenes, M., Swain, G.P., Knight, P.A., Donaldson, D.D., Lazar, M.A., Miller, H.R., Schad, G.A., Scott, P. & Wu, G.D. (2004) RELMbeta/FIZZ2 is a goblet cell-specific immune-effector molecule in the gastrointestinal tract. Proceedings of the National Academy of Sciences, USA 101, 13596–13600.CrossRefGoogle ScholarPubMed
Aucouturier, J., Deville, S., Perret, C., Vallée, I. & Boireau, P. (2001) Assessment of efficacy and safety of various adjuvant formulations with a total soluble extract of Trichinella spiralis. Parasite 8, S126–S132.CrossRefGoogle ScholarPubMed
Beaumier, C.M., Gillespie, P.M., Hotez, P.J. & Bottazzi, M.E. (2013) New vaccines for neglected parasitic diseases and dengue. Translational Research 162, 144–155.CrossRefGoogle ScholarPubMed
Behnke, J.M., Dehlawi, M.S., Rose, R., Spyropoulos, P.N. & Wakelin, D. (1994) The response of hamsters to primary and secondary infection with Trichinella spiralis and to vaccination with parasite antigens. Journal of Helminthology 68, 287–294.CrossRefGoogle ScholarPubMed
Beiting, D.P., Gagliardo, L.F., Hesse, M., Bliss, S.K., Meskill, D. & Appleton, J.A. (2007) Coordinated control of immunity to muscle stage Trichinella spiralis by IL-10, regulatory T cells, and TGF-beta. Journal of Immunology 178, 1039–1047.CrossRefGoogle ScholarPubMed
Belyakov, I.M. & Ahlers, J.D. (2009) What role does the route of immunization play in the generation of protective immunity against mucosal pathogens? Journal of Immunology 183, 6883–6892.CrossRefGoogle ScholarPubMed
Billiau, A. & Matthys, P. (2001) Modes of action of Freund's adjuvants in experimental models of autoimmune diseases. Journal of Leukocyte Biology 70, 849–860.CrossRefGoogle ScholarPubMed
Bolás-Fernandez, F. & Corral Bezara, L.D. (2006) TSL-1 antigens of Trichinella: an overview of their potential role in parasite invasion, survival and serodiagnosis of trichinellosis. Research in Veterinary Science 81, 297–303.CrossRefGoogle ScholarPubMed
Bruschi, F., Korenaga, M. & Watanabe, N. (2008) Eosinophils and Trichinella infection: toxic for the parasite and the host? Trends in Parasitology 24, 462–467.CrossRefGoogle ScholarPubMed
Castillo-Alvarez, A.M., Vaquero-Vera, A., Fonseca-Liñán, R., Ruiz-Pérez, F., Villegas-Sepúlveda, N. & Ortega-Pierres, G. (2013) A prime-boost vaccination of mice with attenuated Salmonella expressing a 30-mer peptide from the Trichinella spiralis gp43 antigen. Veterinary Parasitology 194, 202–206.CrossRefGoogle ScholarPubMed
Cui, J., Ren, H.J., Liu, R.D., Wang, L., Zhang, Z.F. & Wang, Z.Q. (2013) Phage-displayed specific polypeptide antigens induce significant protective immunity against Trichinella spiralis infection in BALB/c mice. Vaccine 31, 1171–1177.CrossRefGoogle ScholarPubMed
Dea-Ayuela, M.A., Martinez-Fernandez, A.R. & Bolas-Fernandez, F. (2000) Comparison of IgG3 responses to carbohydrates following mouse infection or immunization with six species of Trichinella. Journal of Immunology 74, 215–223.Google ScholarPubMed
Dea-Ayuela, M.A., Rama-Iñiguez, S., Torrado-Santiago, S. & Bolas-Fernandez, F. (2006a) Microcapsules formulated in the enteric coating copolymer Eudragit L100 as delivery systems for oral vaccination against infections by gastrointestinal nematode parasites. Journal of Drug Targeting 14, 567–575.CrossRefGoogle ScholarPubMed
Dea-Ayuela, M.A., Rama-Iñiguez, S. & Bolas-Fernández, F. (2006b) Vaccination of mice against intestinal Trichinella spiralis infections by oral administration of antigens microencapsulated in methacrylic acid copolymers. Vaccine 24, 2772–2780.CrossRefGoogle Scholar
Deville, S., Pooter, A.D., Aucouturier, J., Lainé-Prade, V., Cote, M., Boireau, P. & Vallée, I. (2005) Influence of adjuvant formulation on the induced protection of mice immunized with total soluble antigen of Trichinella spiralis. Veterinary Parasitology 132, 75–80.CrossRefGoogle ScholarPubMed
Dixon, H., Blanchard, C., Deschoolmeester, M.L., Yuill, N.C., Christie, J.W., Rothenberg, M.E. & Else, K.J. (2006) The role of Th2 cytokines, chemokines and parasite products in eosinophil recruitment to the gastrointestinal mucosa during helminth infection. European Journal of Immunology 36, 1753–1763.CrossRefGoogle Scholar
Donaldson, L.E., Schmitt, E., Huntley, J.F., Newlands, G.F. & Grencis, R.K. (1996) A critical role for stem cell factor and c-kit in host protective immunity to an intestinal helminth. International Immunology 8, 559–567.CrossRefGoogle Scholar
Dupouy-Camet, J. (2000) Trichinellosis: a worldwide zoonosis. Veterinary Parasitology 93, 191–200.CrossRefGoogle ScholarPubMed
Dvorožňáková, E., Hurníková, Z. & Kołodziej-Sobocińska, M. (2010) Kinetics of specific humoral immune response of mice infected with low doses of Trichinella spiralis, T. britovi, and T. pseudospiralis larvae. Helminthologia 47, 152–157.CrossRefGoogle Scholar
Dvorožňáková, E., Hurníková, Z. & Kołodziej-Sobocińska, M. (2011) Development of cellular immune response of mice to infection with low doses of Trichinella spiralis, Trichinella britovi and Trichinella pseudospiralis larvae. Parasitology Research 108, 169–176.CrossRefGoogle ScholarPubMed
Dzik, J.M., Gołos, B., Jagielska, E., Zielinski, Z. & Wałajtys-Rode, E. (2004) A non-classical type of alveolar macrophage response to Trichinella spiralis infection. Parasite Immunology 26, 197–205.CrossRefGoogle ScholarPubMed
Eissa, M.M., el-Azzouni, M.Z., Baddour, N.M. & Boulos, L.M. (2003) Vaccination trial against experimental trichinellosis using autoclaved Trichinella spiralis larvae vaccine (ATSLV). Journal of the Egyptian Society of Parasitology 33, 219–228.Google ScholarPubMed
Fabre, V., Beiting, D.P., Bliss, S.K., Gebreselassie, N.G., Gagliardo, L.F., Lee, N.A., Lee, J.J. & Appleton, J.A. (2009) Eosinophil deficiency compromises parasite survival in chronic nematode infection. Journal of Immunology 182, 1577–1583.CrossRefGoogle ScholarPubMed
Faulkner, H., Humphreys, N., Renauld, J.C., Van Snick, J. & Grencis, R. (1997) Interleukin-9 is involved in host protective immunity to intestinal nematode infection. European Journal of Immunology 27, 2536–2540.CrossRefGoogle ScholarPubMed
Feng, S., Wu, X., Wang, X., Bai, X., Shi, H., Tang, B., Liu, X., Song, Y., Boireau, P., Wang, F., Zhao, Y. & Liu, M. (2013) Vaccination of mice with an antigenic serine protease-like protein elicits a protective immune response against Trichinella spiralis infection. Journal of Parasitology 99, 426–432.CrossRefGoogle ScholarPubMed
Field, M. (2003) Intestinal ion transport and the pathophysiology of diarrhea. Journal of Clinical Investigation 111, 931–943.CrossRefGoogle ScholarPubMed
Finkelman, F.D., Shea-Donohue, T., Morris, S.C., Gildea, L., Strait, R., Madden, K.B., Schopf, L. & Urban, J.F. Jr (2004) Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunological Reviews 201, 139–155.CrossRefGoogle ScholarPubMed
Fu, Y., Wang, W., Tong, J., Pan, Q., Long, Y., Qian, W. & Hou, X. (2009) Th17: a new participant in gut dysfunction in mice infected with Trichinella spiralis. Mediators of Inflammation 2009, 517052.CrossRefGoogle ScholarPubMed
Gamble, H.R. (1985) Trichinella spiralis: immunization of mice using monoclonal antibody affinity-isolated antigens. Experimental Parasitology 59, 398–404.CrossRefGoogle ScholarPubMed
Gebreselassie, N.G., Moorhead, A.R., Fabre, V., Gagliardo, L.F., Lee, N.A., Lee, J.J. & Appleton, J.A. (2012) Eosinophils preserve parasitic nematode larvae by regulating local immunity. Journal of Immunology 188, 417–425.CrossRefGoogle ScholarPubMed
Gold, A.M., Despommier, D.D. & Buck, S.W. (1990) Partial characterization of two antigens secreted by L1 larvae of Trichinella spiralis. Molecular and Biochemical Parasitology 44, 187–196.CrossRefGoogle Scholar
Goyal, P.K., Bolas-Fernandez, F. & Wakelin, D. (1997) Immunization of mice against Trichinella spiralis and T. britovi using excretory and secretory antigens. Journal of Immunology 71, 109–112.Google Scholar
Grove, D.I., Mahmoud, A.A. & Warren, K.S. (1977) Eosinophils and resistance to Trichinella spiralis. Journal of Experimental Medicine 145, 755–759.CrossRefGoogle ScholarPubMed
Gu, Y., Li, J., Zhu, X., Yang, J., Li, Q., Liu, Z., Yu, S. & Li, Y. (2008) Trichinella spiralis: characterization of phage-displayed specific epitopes and their protective immunity in BALB/c mice. Experimental Parasitology 118, 66–74.CrossRefGoogle ScholarPubMed
Gu, Y., Zhan, B., Yang, Y., Yang, X., Zhao, X., Wang, L., Yang, J., Bi, K., Wang, Y. & Zhu, X. (2014) Protective effect of a prime-boost strategy with the Ts87 vaccine against Trichinella spiralis infection in mice. Biomedical Research International 2014, 326860.CrossRefGoogle ScholarPubMed
Gurish, M.F., Humbles, A., Tao, H., Finkelstein, S., Boyce, J.A., Gerard, C., Friend, D.S. & Austen, K.F. (2002) CCR3 is required for tissue eosinophilia and larval cytotoxicity after infection with Trichinella spiralis. Journal of Immunology 168, 5730–5736. Errata in Journal of Immunology 169, 2797 and 4054.CrossRefGoogle ScholarPubMed
Gurish, M.F., Bryce, P.J., Tao, H., Kisselgof, A.B., Thornton, E.M., Miller, H.R., Friend, D.S. & Oettgen, H.C. (2004) IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. Journal of Immunology 172, 1139–1145.CrossRefGoogle ScholarPubMed
Ha, T.Y., Reed, N.D. & Crowle, P.K. (1983) Delayed expulsion of adult Trichinella spiralis by mast cell-deficient W/Wv mice. Infection and Immunity 41, 445–447.CrossRefGoogle ScholarPubMed
Hasnain, S.Z., Wang, H., Ghia, J.E., Haq, N., Deng, Y., Velcich, A., Grencis, R.K., Thornton, D.J. & Khan, W.I. (2010) Mucin gene deficiency in mice impairs host resistance to an enteric parasitic infection. Gastroenterology 138, 1763–1771.CrossRefGoogle Scholar
Hasnain, S.Z., Evans, C.M., Roy, M., Gallagher, A.L., Kindrachuk, K.N., Barron, L., Dickey, B.F., Wilson, M.S., Wynn, T.A., Grencis, R.K. & Thornton, D.J. (2011) Muc5ac: a critical component mediating the rejection of enteric nematodes. Journal of Experimental Medicine 208, 893–900.CrossRefGoogle ScholarPubMed
Helmby, H. & Grencis, R.K. (2002) IL-18 regulates intestinal mastocytosis and Th2 cytokine production independently of IFN-gamma during Trichinella spiralis infection. Journal of Immunology 169, 2553–2560.CrossRefGoogle ScholarPubMed
Herbert, D.R., Yang, J.Q., Hogan, S.P., Groschwitz, K., Khodoun, M., Munitz, A., Orekov, T., Perkins, C., Wang, Q., Brombacher, F., Urban, J.F. Jr, Rothenberg, M.E. & Finkelman, F.D. (2009) Intestinal epithelial cell secretion of RELM-beta protects against gastrointestinal worm infection. Journal of Experimental Medicine 206, 2947–2957.CrossRefGoogle ScholarPubMed
Herndon, F.J. & Kayes, S.G. (1992) Depletion of eosinophils by anti-IL-5 monoclonal antibody treatment of mice infected with Trichinella spiralis does not alter parasite burden or immunologic resistance to reinfection. Journal of Immunology 149, 3642–3647.CrossRefGoogle ScholarPubMed
Huang, L., Gebreselassie, N.G., Gagliardo, L.F., Ruyechan, M.C., Lee, N.A., Lee, J.J. & Appleton, J.A. (2014) Eosinophil-derived IL-10 supports chronic nematode infection. Journal of Immunology 193, 4178–4187.CrossRefGoogle ScholarPubMed
Khan, W.I., Blennerhasset, P., Ma, C., Matthaei, K.I. & Collins, S.M. (2001a) Stat6 dependent goblet cell hyperplasia during intestinal nematode infection. Parasite Immunology 23, 39–42.CrossRefGoogle ScholarPubMed
Khan, W.I., Blennerhassett, P.A., Deng, Y., Gauldie, J., Vallance, B.A. & Collins, S.M. (2001b) IL-12 gene transfer alters gut physiology and host immunity in nematode-infected mice. American Journal of Physiology. Gastrointestinal and Liver Physiology 281, G102–G110.CrossRefGoogle ScholarPubMed
Khan, W.I., Vallance, B.A., Blennerhassett, P.A., Deng, Y., Verdu, E.F., Matthaei, K.I. & Collins, S.M. (2001c) Critical role for signal transducer and activator of transcription factor 6 in mediating intestinal muscle hypercontractility and worm expulsion in Trichinella spiralis-infected mice. Infection and Immunity 69, 838–844.CrossRefGoogle ScholarPubMed
Khan, W.I., Richard, M., Akiho, H., Blennerhasset, P.A., Humphreys, N.E., Grencis, R.K., Van Snick, J. & Collins, S.M. (2003) Modulation of intestinal muscle contraction by interleukin-9 (IL-9) or IL-9 neutralization: correlation with worm expulsion in murine nematode infections. Infection and Immunity 71, 2430–2438.CrossRefGoogle ScholarPubMed
Kim, Y.S. & Ho, S.B. (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Current Gastroenterology Reports 12, 319–330.CrossRefGoogle ScholarPubMed
Knight, P.A., Wright, S.H., Lawrence, C.E., Paterson, Y.Y. & Miller, H.R. (2000) Delayed expulsion of the nematode Trichinella spiralis in mice lacking the mucosal mast cell-specific granule chymase, mouse mast cell protease-1. Journal of Experimental Medicine 192, 1849–1856.CrossRefGoogle ScholarPubMed
Knight, P.A., Pemberton, A.D., Robertson, K.A., Roy, D.J., Wright, S.H. & Miller, H.R. (2004) Expression profiling reveals novel innate and inflammatory responses in the jejunal epithelial compartment during infection with Trichinella spiralis. Infection and Immunity 72, 6076–6086.CrossRefGoogle ScholarPubMed
Knight, P.A., Brown, J.K. & Pemberton, A.D. (2008) Innate immune response mechanisms in the intestinal epithelium: potential roles for mast cells and goblet cells in the expulsion of adult Trichinella spiralis. Parasitology 135, 655–670.CrossRefGoogle ScholarPubMed
Kreider, T., Anthony, R.M., Urban, J.F. Jr & Gause, W.C. (2007) Alternatively activated macrophages in helminth infections. Current Opinion in Immunology 19, 448–453.CrossRefGoogle ScholarPubMed
Li, X., Yao, J.P., Pan, A.H., Liu, W., Hu, X.C., Wu, Z.D. & Zhou, X.W. (2013) An antigenic recombinant serine protease from Trichinella spiralis induces protective immunity in BALB/c mice. Parasitology Research 112, 3229–3238.CrossRefGoogle ScholarPubMed
Liu, M.Y., Wang, X.L., Fu, B.Q., Li, C.Y., Wu, X.P., Le Rhun, D., Chen, Q.J. & Boireau, P. (2007) Identification of stage-specifically expressed genes of Trichinella spiralis by suppression subtractive hybridization. Parasitology 134, 1443–1455.CrossRefGoogle ScholarPubMed
Liu, X.D., Wang, X.L., Bai, X., Liu, X.L., Wu, X.P., Zhao, Y., Sun, S.M., Yu, L., Su, X.Z., Wang, Z.Q., Wang, F. & Liu, M.Y. (2014) Oral administration with attenuated Salmonella encoding a Trichinella cystatin-like protein elicited host immunity. Experimental Parasitology 141, 1–11.CrossRefGoogle ScholarPubMed
Madden, K.B., Yeung, K.A., Zhao, A., Gause, W.C., Finkelman, F.D., Katona, I.M., Urban, J.F. Jr & Shea-Donohue, T. (2004) Enteric nematodes induce stereotypic STAT6-dependent alterations in intestinal epithelial cell function. Journal of Immunology 172, 5616–5621.CrossRefGoogle ScholarPubMed
Maizels, R.M., Hewitson, J.P. & Smith, K.A. (2012) Susceptibility and immunity to helminth parasites. Current Opinion in Immunology 24, 459–466.CrossRefGoogle ScholarPubMed
Marti, H.P., Murrell, K.D. & Gamble, H.R. (1987) Trichinella spiralis: immunization of pigs with newborn larval antigens. Experimental Parasitology 63, 68–73.CrossRefGoogle ScholarPubMed
McDermott, J.R., Bartram, R.E., Knight, P.A., Miller, H.R., Garrod, D.R. & Grencis, R.K. (2003) Mast cells disrupt epithelial barrier function during enteric nematode infection. Proceedings of the National Academy of Sciences, USA 100, 7761–7766.CrossRefGoogle ScholarPubMed
McGuire, C., Chan, W.C. & Wakelin, D. (2002) Nasal immunization with homogenate and peptide antigens induces protective immunity against Trichinella spiralis. Infection and Immunity 70, 7149–7152.CrossRefGoogle ScholarPubMed
Mitreva, M., Jasmer, D.P., Zarlenga, D.S., Wang, Z., Abubucker, S., Martin, J., Taylor, C.M., Yin, Y., Fulton, L., Minx, P., Yang, S.P., Warren, W.C., Fulton, R.S., Bhonagiri, V., Zhang, X., Hallsworth-Pepin, K., Clifton, S.W., McCarter, J.P., Appleton, J., Mardis, E.R. & Wilson, R.K. (2011) The draft genome of the parasitic nematode Trichinella spiralis. Nature Genetics 43, 228–235.CrossRefGoogle ScholarPubMed
Moncada, D.M., Kammanadiminti, S.J. & Chadee, K. (2003) Mucin and Toll-like receptors in host defense against intestinal parasites. Trends in Parasitology 19, 305–311.CrossRefGoogle ScholarPubMed
Murrell, K.D. (1985) Trichinella spiralis: acquired immunity in swine. Experimental Parasitology 59, 347–354.CrossRefGoogle ScholarPubMed
Murrell, K.D. & Pozio, E. (2011) Worldwide occurrence and impact of human trichinellosis, 1986–2009. Emerging Infectious Diseases 17, 2194–2202.CrossRefGoogle ScholarPubMed
Ortega-Pierres, G., Muñiz, E., Coral-Vázquez, R. & Parkhouse, R.M. (1989) Protection against Trichinella spiralis induced by purified stage-specific surface antigens of infective larvae. Parasitology Research 75, 563–567.CrossRefGoogle ScholarPubMed
Patarroyo, M.E., Bermúdez, A. & Moreno-Vranich, A. (2012) Towards the development of a fully protective Plasmodium falciparum antimalarial vaccine. Expert Review of Vaccines 11, 1057–1070.CrossRefGoogle ScholarPubMed
Pemberton, A.D., Knight, P.A., Wright, S.H. & Miller, H.R. (2004a) Proteomic analysis of mouse jejunal epithelium and its response to infection with the intestinal nematode, Trichinella spiralis. Proteomics 4, 1101–1108.CrossRefGoogle ScholarPubMed
Pemberton, A.D., Knight, P.A., Gamble, J., Colledge, W.H., Lee, J.K., Pierce, M. & Miller, H.R. (2004b) Innate BALB/c enteric epithelial responses to Trichinella spiralis: inducible expression of a novel goblet cell lectin, intelectin-2, and its natural deletion in C57BL/10 mice. Journal of Immunology 173, 1894–1901.CrossRefGoogle ScholarPubMed
Pompa-Mera, E.N., Yépez-Mulia, L., Ocaña-Mondragón, A., García-Zepeda, E.A., Ortega-Pierres, G. & González-Bonilla, C.R. (2011) Trichinella spiralis: intranasal immunization with attenuated Salmonella enterica carrying a gp43 antigen-derived 30mer epitope elicits protection in BALB/c mice. Experimental Parasitology 129, 393–401.CrossRefGoogle ScholarPubMed
Pompa-Mera, E.N., Arroyo-Matus, P., Ocaña-Mondragón, A., González-Bonilla, C.R. & Yépez-Mulia, L. (2014) Protective immunity against enteral stages of Trichinella spiralis elicited in mice by live attenuated Salmonella vaccine that secretes a 30-mer parasite epitope fused to the molecular adjuvant C3d-P28. Research in Veterinary Science 97, 533–545.CrossRefGoogle Scholar
Pozio, E. (2007) World distribution of Trichinella spp. infections in animals and humans. Veterinary Parasitology 149, 3–21.CrossRefGoogle ScholarPubMed
Pozio, E. (2013) The opportunistic nature of Trichinella – exploitation of new geographies and habitats. Veterinary Parasitology 194, 128–132.CrossRefGoogle ScholarPubMed
Pozio, E. (2014) Searching for Trichinella: not all pigs are created equal. Trends in Parasitology 30, 4–11.CrossRefGoogle Scholar
Pozio, E. & Zarlenga, D.S. (2013) New pieces of the Trichinella puzzle. International Journal for Parasitology 43, 983–997.CrossRefGoogle ScholarPubMed
Robinson, K., Bellaby, T. & Wakelin, D. (1994) Vaccination against the nematode Trichinella spiralis in high- and low-responder mice. Effects of different adjuvants upon protective immunity and immune responsiveness. Immunology 82, 261–267.Google ScholarPubMed
Robinson, K., Bellaby, T. & Wakelin, D. (1995) Oral and parenteral vaccination against Trichinella spiralis infections in high- and low-responder mice. International Journal for Parasitology 25, 989–992.CrossRefGoogle ScholarPubMed
Scales, H.E., Ierna, M.X. & Lawrence, C.E. (2007) The role of IL-4, IL-13 and IL-4Ralpha in the development of protective and pathological responses to Trichinella spiralis. Parasite Immunology 29, 81–91.CrossRefGoogle ScholarPubMed
Scalfone, L.K., Nel, H.J., Gagliardo, L.F., Cameron, J.L., Al-Shokri, S., Leifer, C.A., Fallon, P.G. & Appleton, J.A. (2013) Participation of MyD88 and interleukin-33 as innate drivers of Th2 immunity to Trichinella spiralis. Infection and Immunity 81, 1354–1363.CrossRefGoogle ScholarPubMed
Scudamore, C.L., Thornton, E.M., McMillan, L., Newlands, G.F. & Miller, H.R. (1995) Release of the mucosal mast cell granule chymase, rat mast cell protease-II, during anaphylaxis is associated with the rapid development of paracellular permeability to macromolecules in rat jejunum. Journal of Experimental Medicine 182, 1871–1881.CrossRefGoogle ScholarPubMed
Stills, H.F. Jr (2005) Adjuvants and antibody production: dispelling the myths associated with Freund's complete and other adjuvants. ILAR Journal 46, 280–293.CrossRefGoogle ScholarPubMed
Strait, R.T., Morris, S.C., Smiley, K., Urban, J.F. Jr & Finkelman, F.D. (2003) IL-4 exacerbates anaphylaxis. Journal of Immunology 170, 3835–3842.CrossRefGoogle ScholarPubMed
Suzuki, T., Sasaki, T., Takagi, H., Sato, K. & Ueda, K. (2008) The effectors responsible for gastrointestinal nematode parasites, Trichinella spiralis, expulsion in rats. International Journal for Parasitology 103, 1289–1295.CrossRefGoogle ScholarPubMed
Tang, F., Xu, L., Yan, R., Song, X. & Li, X. (2012) Evaluation of the immune response induced by DNA vaccines expressing MIF and MCD-1 genes of Trichinella spiralis in BALB/c mice. Journal of Helminthology 86, 430–439.CrossRefGoogle ScholarPubMed
Tang, F., Xu, L., Yan, R., Song, X. & Li, X. (2013) A DNA vaccine co-expressing Trichinella spiralis MIF and MCD-1 with murine ubiquitin induces partial protective immunity in mice. Journal of Helminthology 87, 24–33.CrossRefGoogle ScholarPubMed
Temann, U.A., Ray, P. & Flavell, R.A. (2002) Pulmonary overexpression of IL-9 induces Th2 cytokine expression, leading to immune pathology. Journal of Clinical Investigation 109, 29–39.CrossRefGoogle ScholarPubMed
Temann, U.A., Laouar, Y., Eynon, E.E., Homer, R. & Flavell, R.A. (2007) IL9 leads to airway inflammation by inducing IL13 expression in airway epithelial cells. International Immunology 19, 1–10.CrossRefGoogle ScholarPubMed
Urban, J.F. Jr, Schopf, L., Morris, S.C., Orekhova, T., Madden, K.B., Betts, C.J., Gamble, H.R., Bird, C., Donaldson, D., Else, K. & Finkelman, F.D. (2000) Stat6 signaling promotes protective immunity against Trichinella spiralis through a mast cell- and T cell-dependent mechanism. Journal of Immunology 164, 2046–2052.CrossRefGoogle ScholarPubMed
Wang, Z.Q., Cui, J., Wei, H.Y., Han, H.M., Zhang, H.W. & Li, Y.L. (2006) Vaccination of mice with DNA vaccine induces the immune response and partial protection against T. spiralis infection. Vaccine 24, 1205–1212.CrossRefGoogle ScholarPubMed
Williams, N.A., Hirst, T.R. & Nashar, T.O. (1999) Immune modulation by the cholera-like enterotoxins: from adjuvant to therapeutic. Immunology Today 20, 95–101.CrossRefGoogle ScholarPubMed
Yang, J., Yang, Y., Gu, Y., Li, Q., Wei, J., Wang, S., Boireau, P. & Zhu, X. (2008) Identification and characterization of a full-length cDNA encoding paramyosin of Trichinella spiralis. Biochemical and Biophysical Research Communications 365, 528–533.CrossRefGoogle ScholarPubMed
Yang, J., Gu, Y., Yang, Y., Wei, J., Wang, S., Cui, S., Pan, J., Li, Q. & Zhu, X. (2010a) Trichinella spiralis: immune response and protective immunity elicited by recombinant paramyosin formulated with different adjuvants. Experimental Parasitology 124, 403–408.CrossRefGoogle ScholarPubMed
Yang, Y., Zhang, Z., Yang, J., Chen, X., Cui, S. & Zhu, X. (2010b) Oral vaccination with Ts87 DNA vaccine delivered by attenuated Salmonella typhimurium elicits a protective immune response against Trichinella spiralis larval challenge. Vaccine 28, 2735–2742.CrossRefGoogle ScholarPubMed
Yépez-Mulia, L., Montaño-Escalona, C., Fonseca-Liñán, R., Muñoz-Cruz, S., Arizmendi-Puga, N., Boireau, P. & Ortega-Pierres, G. (2009) Differential activation of mast cells by antigens from Trichinella spiralis muscle larvae, adults, and newborn larvae. Veterinary Parasitology 159, 253–257.CrossRefGoogle ScholarPubMed
Zhang, Y., Wang, Z., Li, L. & Cui, J. (2013) Molecular characterization of Trichinella spiralis aminopeptidase and its potential as a novel vaccine candidate antigen against trichinellosis in BALB/c mice. Parasites & Vectors 6, 246.CrossRefGoogle ScholarPubMed
Zhao, A., Urban, J.F. Jr, Anthony, R.M., Sun, R., Stiltz, J., van Rooijen, N., Wynn, T.A., Gause, W.C. & Shea-Donohue, T. (2008) Th2 cytokine-induced alterations in intestinal smooth muscle function depend on alternatively activated macrophages. Gastroenterology 135, 217–225.CrossRefGoogle ScholarPubMed