Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-26T00:48:00.746Z Has data issue: false hasContentIssue false
  • English
  • Français

Triggering and modulation of the host-parasite interplay by Echinococcus multilocularis: a review

Published online by Cambridge University Press:  07 December 2009

N. MEJRI ,
A. HEMPHILL  and
B. GOTTSTEIN
N. MEJRI
Affiliation:
Institute of Parasitology, University of Bern, Laenggass-Strasse 122, CH-3001Bern, Switzerland
A. HEMPHILL
Affiliation:
Institute of Parasitology, University of Bern, Laenggass-Strasse 122, CH-3001Bern, Switzerland
B. GOTTSTEIN*
Affiliation:
Institute of Parasitology, University of Bern, Laenggass-Strasse 122, CH-3001Bern, Switzerland
*
*Corresponding author: Institute of Parasitology, University of Bern, Laenggass-Strasse 122, CH-3001, Bern, Switzerland. Tel: +41 31 631 24 18. Fax: +41 31 631 24 77. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

As more facts emerge regarding the ways in which E. multilocularis-derived molecules trigger the host immune response and modulate the host-parasite interplay, it becomes possible to envisage how the parasite can survive and proliferate in its intermediate host, while in other hosts it dies out. Through effects on cells of both the innate and adaptive arms of the immune response, E. multilocularis can orchestrate a range of outcomes that are beneficial not only to the parasite, in terms of facilitating its intrahepatic proliferation and maturation, and thus life cycle over all, but also to its intermediate host, in limiting pathology. The present review deals with the role of metacestode surface molecules as well as excretory/secretory (E/S) metabolic products of the parasite in the modulation of the host responses such as to optimize its own survival.

Keywords

Echinococcus multilocularisalveolar echinococcosisimmunologymetabolitesimmune modulation
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 3: Development and applications of cestode and trematode laboratory models , March 2010 , pp. 557 - 568
Copyright
Copyright © Cambridge University Press 2009

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

Abbas, A. K., Murphy, K. M. and Sher, A. (1996). Functional diversity of helper T lymphocytes. Nature 383, 787–793.CrossRefGoogle ScholarPubMed
Amiot, F., Vuong, P., Defontaines, M., Pater, C., Dautry, F. and Uance, M. (1999). Secondary alveolar echinococcosis in lymphotoxinalpha and tumour necrosis factor-alpha deficient mice: exacerbation of Echinococcus multilocularis larval growth is associated with cellular changes in the periparasitic granuloma. Parasite Immunology 21, 475–483.CrossRefGoogle ScholarPubMed
Andrade, M. A., Siles-Lucas, M., Espinoza, E., Pérez Arellano, J. L., Gottstein, B. and Muro, A. (2004). Echinococcus multilocularis laminated-layer components and the E14t 14-3-3 recombinant protein decrease activated rat macrophages NO production in vitro. Nitric Oxide 10, 150–155.CrossRefGoogle Scholar
Auer, H., Hermentin, K. and Aspöck, H. (1988). Demonstration of a specific Echinococcus multilocularis antigen in the supernatant of in vitro maintained protoscolices. Zentralblatt für Bakteriologie und Mikrobiologie, Hyg A 268, 416–423.Google ScholarPubMed
Aumüller, E., Schramm, G., Gronow, A., Brehm, K., Gibbs, B. F., Doenhoff, M. J. and Haas, H. (2004). Echinococcus multilocularis metacestode extract triggers human basophils to release interleukin-4. Parasite Immunology 26, 387–395.CrossRefGoogle ScholarPubMed
Bahram, S. (2000). MIC genes: from genetics to biology. Advances in Immunology 76, 1–60.Google ScholarPubMed
Baz, A., Ettlin, G. M. and Dematteis, S. (2006). Complexity and function of cytokine responses in experimental infection by Echinococcus granulosus. Immunobiology 211, 3–9.CrossRefGoogle ScholarPubMed
Boonstra, A., Asselin-Paturel, C., Gilliet, M., Crain, C., Trinchieri, G., Liu, Y. J. and O'Garra, A. (2003). Flexibility of mouse classical and plasmacytoid-derived dendritic cells in directing T helper type 1 and 2 cell development: dependency on antigen dose and differential toll-like receptor ligation. Journal of Experimental Medicine 197, 101–109.CrossRefGoogle ScholarPubMed
Brehm, K., Spiliotis, M., Zavala-Góngora, R., Konrad, C. and Frosch, M. (2006). The molecular mechanisms of larval cestode development: first steps into an unknown world. Parasitology International 55 (Suppl.), S15–S21.CrossRefGoogle ScholarPubMed
Bresson-Hadni, S., Koch, S., Miguet, J. P., Gillet, M., Mantion, G. A., Heyd, B. and Vuitton, D. A. (2003). European group of clinicians. Indications and results of liver transplantation for Echinococcus alveolar infection: an overview. Langenbecks Archive of Surgery 388, 231–238.CrossRefGoogle Scholar
Bresson-Hadni, S., Liance, M., Meyer, J. P., Houin, R., Bresson, J. L. and Vuitton, D. A. (1990). Cellular immunity in experimental Echinococcus multilocularis infection. II. Sequential and comparative phenotypic study of the periparasitic mononuclear cells in resistant and sensitive mice. Clinical and Experimental Immunology 82, 378–383.CrossRefGoogle ScholarPubMed
Burden, D. J., Bland, A. P., Hammet, N. C. and Hughes, D. L. (1983). Fasciola hepatica: migration of newly excysted juveniles in resistant rats. Experimental Parasitology 56, 277–288.CrossRefGoogle ScholarPubMed
Castriconi, R., Cantoni, C., Della Chiesa, M., Vitale, M., Marcenaro, E., Conte, R., Biassoni, R., Bottino, C., Moretta, L. and Moretta, A. (2003). Transforming growth factor beta 1 inhibits expression of NKp30 and NKG2D receptors: consequences for the NK-mediated killing of dendritic cells. Proceedings of the National Academy of Sciences, USA 100, 4120–4125.CrossRefGoogle ScholarPubMed
Cox, D. A., Marshall-Clarke, S. and Dixon, J. B. (1989). Activation of normal murine B cells by Echinococcus granulosus. Immunology 67, 16–20.Google ScholarPubMed
Dai, W. J. and Gottstein, B. (1999). Nitric oxide-mediated immunosuppression following murine Echinococcus multilocularis infection. Immunology 97, 107–116.CrossRefGoogle ScholarPubMed
Dai, W. J., Hemphill, A., Waldvogel, A., Ingold, K., Deplazes, P., Mossmann, H. and Gottstein, B. (2001). Major carbohydrate antigen of Echinococcus multilocularis induces an immunoglobulin G response independent of alphabeta+ CD4+ T cells. Infection and Immunity 69, 6074–6083.CrossRefGoogle ScholarPubMed
Dai, W. J., Waldvogel, A., Jungi, T., Stettler, M. and Gottstein, B. (2003). Inducible nitric oxide synthase-deficiency in mice increases resistance to chronic infection with Echinococcus multilocularis. Immunology 10, 238–244.CrossRefGoogle Scholar
Dai, W. J., Waldvogel, A., Siles-Lucas, M. and Gottstein, B. (2004). Echinococcus multilocularis proliferation in mice and respective parasite 14-3-3 gene expression is mainly controlled by an alphabeta CD4 T-cell-mediated immune response. Immunology 112, 481–488.CrossRefGoogle ScholarPubMed
Devouge, M. and Ali-Khan, Z. (1983). Intraperitoneal murine alveolar hydatidosis: relationship between the size of the larval cyst mass, immigrant inflammatory cells, splenomegaly and thymus involution. Tropenmedizin und Parasitologie 34, 15–20.Google ScholarPubMed
Doubrovina, E. S., Doubrovin, M. M., Vider, E., Sisson, R. B., O'Reilly, R. J., Dupont, B. and Vyas, Y. M. (2003). Evasion from NK cell immunity by MHC class I chain-related molecules expressing colon adenocarcinoma. Journal of Immunology 171, 6891–6899.CrossRefGoogle ScholarPubMed
Dreweck, C. M., Soboslay, P. T., Schulz-Key, H., Gottstein, B. and Kern, P. (1999). Cytokine and chemokine secretion by human peripheral blood cells in response to viable Echinococcus multilocularis metacestode vesicles. Parasite Immunology 21, 433–438.CrossRefGoogle ScholarPubMed
Emery, I., Leclerc, C., Sengphommachanh, K., Vuitton, D. A. and Liance, M. (1998). In vivo treatment with recombinant IL-12 protects C57BL/6J mice against secondary alveolar echinococcosis. Parasite Immunology 20, 81–91.CrossRefGoogle ScholarPubMed
Emery, I., Liance, M., Deriaud, E., Vuitton, D. A., Houin, R. and Leclerc, C. (1996). Characterization of T-cell immune responses of Echinococcus multilocularis-infected C57BL/6J mice. Parasite Immunology 18, 463–472.CrossRefGoogle ScholarPubMed
Falcone, F. H., Dahinden, C. A., Gibbs, B. F., Noll, T., Amon, U., Hebestreit, H., Abrahamsen, O., Klaucke, J., Schlaak, M. and Haas, H. (1996). Human basophils release interleukin-4 after stimulation with Schistosoma mansoni egg antigen. European Journal of Immunology 26, 1147–1155.CrossRefGoogle ScholarPubMed
Fallon, P. G., Ballantyne, S. J., Mangan, N. E., Barlow, J. L., Dasvarma, A., Hewett, D. R., McIlgorm, A., Jolin, H. E. and McKenzie, A. N. (2006). Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. Journal of Experimental Medicine 203, 1105–1116.CrossRefGoogle ScholarPubMed
Faria, A. M. and Weiner, H. L. (2005). Oral tolerance. Immunological Reviews 206, 232–259.CrossRefGoogle ScholarPubMed
Fort, M. M., Cheung, J., Yen, D., Li, J., Zurawski, S. M., Lo, S., Menon, S., Clifford, T., Hunte, B., Lesley, R., Muchamuel, T., Hurst, S. D., Zurawski, G., Leach, M. W., Gorman, D. M. and Rennick, D. M. (2001). IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15, 985–995.CrossRefGoogle ScholarPubMed
Foti, M., Granucci, F., Pelizzola, M., Beretta, O. and Ricciardi-Castagnoli, P. (2006). Dendritic cells in pathogen recognition and induction of immune responses: a functional genomics approach. Journal of Leukocyte Biology 79, 913–916.CrossRefGoogle ScholarPubMed
Frosch, P. M., Frosch, M., Pfister, T., Schaad, V. and Bitter-Suermann, D. (1991). Cloning and characterization an immunodominant major surface antigen of Echinococcus multilocularis. Molecular and Biochemical Parasitology 48, 121–130.CrossRefGoogle ScholarPubMed
Gauci, C., Merli, M., Muller, V., Chow, C., Yagi, K., Mackenstedt, U. and Lightowlers, M. W. (2002). Molecular cloning of a vaccine antigen against infection with the larval stage of Echinococcus multilocularis. Infection and Immunity 70, 3969–3972.CrossRefGoogle ScholarPubMed
Germain, R. N. (1994). MHC-dependent antigen processing and peptide presentation: providing ligands for T lymphocyte activation. Cell 76, 287–299.CrossRefGoogle ScholarPubMed
Ghiringhelli, F., Puig, P. E., Roux, S., Parcellier, A., Schmitt, E., Solary, E., Kroemer, G., Martin, F., Chauffert, B. and Zitvogel, L. (2005). Tumor cells convert immature myeloid dendritic cells into TGF-beta-secreting cells inducing CD4+CD25+ regulatory T cell proliferation. Journal of Experimental Medicine 202, 919–929.CrossRefGoogle ScholarPubMed
Godot, V., Harraga, S., Beurton, I., Deschaseaux, M., Sarciron, E., Gottstein, B. and Vuitton, D. A. (2000). Resistance/susceptibility to Echinococcus multilocularis infection and cytokine profile in humans. I. Comparison of patients with progressive and abortive lesions. Clinical Experimental Immunology 121, 484–490.CrossRefGoogle ScholarPubMed
Godot, V., Harraga, S., Deschaseaux, M., Bresson-Hadni, S., Gottstein, B., Emilie, D. and Vuitton, D. A. (1997). Increased basal production of interleukin-10 by peripheral blood mononuclear cells in human alveolar echinococcosis. European Cytokine Network 8, 401–408.Google ScholarPubMed
Godot, V., Harraga, S., Podoprigora, G., Liance, M., Bardonnet, K. and Vuitton, D. A. (2003). IFN alpha-2a protects mice against a helminth infection of the liver and modulates immune responses. Gastroenterology 124, 1441–1450.CrossRefGoogle ScholarPubMed
Gottstein, B., Dai, W. J., Walker, M., Stettler, M., Muller, N. and Hemphill, A. (2002). An intact laminated layer is important for the establishment of secondary Echinococcus multilocularis infection. Parasitology Research 88, 822–828.CrossRefGoogle ScholarPubMed
Gottstein, B., Saucy, F., Deplazes, P., Reichen, J., Demierre, G., Zürcher, C., Busato, A. and Pugin, P. (2001). Is a high prevalence of Echinococcus multilocularis in wild and domestic animals associated with increased disease incidence in humans? Emerging Infectious Diseases 7, 408–412.CrossRefGoogle ScholarPubMed
Gottstein, B., Dai, W. J., Walker, M., Stettler, M., Muller, N. and Hemphill, A. (1992). An intact laminated layer is important for the establishment of secondary Echinococcus multilocularis infection. Parasitology Research 88, 822–828.CrossRefGoogle Scholar
Gottstein, B. and Hemphill, A. (2008). Echinococcus multilocularis: the parasite-host interplay. Experimental Parasitology 119, 447–452.CrossRefGoogle ScholarPubMed
Groh, V., Rhinehart, R., Randolph-Habecker, J., Topp, M. S., Riddell, S. R. and Spies, T. (2001). Costimulation of CD8αβ T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nature Immunology 2, 255–260.CrossRefGoogle ScholarPubMed
Groux, H., O'Garra, A., Bigler, M., Rouleau, M., Antonenko, S., de Vries, J. E. and Roncarolo, M. G. (1997). A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389, 737–742.CrossRefGoogle ScholarPubMed
Holdenrieder, S., Stieber, P., Peterfi, A., Nagel, D., Steinle, A. and Salih, H. R. (2006). Soluble MICA in malignant diseases. International Journal of Cancer 118, 684–687.CrossRefGoogle ScholarPubMed
Honey, K. (2005). Immunotherapy: CD8+CD25+ regulatory T cells get the OK. Nature Reviews Immunology 5, 832–833.CrossRefGoogle Scholar
Hori, S., Nomura, T. and Sakaguchi, S. (2003). Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1030–1031.CrossRefGoogle ScholarPubMed
Hübner, M. P., Manfras, B. J., Margos, M. C., Eiffler, D., Hoffmann, W. H., Schulz-Key, H., Kern, P. and Soboslay, P. T. (2006). Echinococcus multilocularis metacestodes modulate cellular cytokine and chemokine release by peripheral blood mononuclear cells in alveolar echinococcosis patients. Clinical and Experimental Immunology 145, 243–251.CrossRefGoogle ScholarPubMed
Huelsmeier, A. J., Gehrig, P. M., Geyer, R., Sack, R., Gottstein, B., Deplazes, P. and Kohler, P. (2002). A major Echinococcus multilocularis antigen is a mucin-type glycoprotein. Journal of Biological Chemistry 277, 5742–5748.CrossRefGoogle Scholar
Ingold, K., Gottstein, B. and Hemphill, A. (1998). Identification of a laminated layer-associated protein in Echinococcus multilocularis metacestodes. Parasitology 116, 363–372.CrossRefGoogle ScholarPubMed
Ingold, K., Gottstein, B. and Hemphill, A. (2000). High molecular mass glycans are major structural elements associated with the laminated layer of in vitro cultivated Echinococcus multilocularis metacestodes. International Journal for Parasitology 30, 207–214.CrossRefGoogle ScholarPubMed
Ito, A., Schantz, P. M. and Wilson, J. F. (1995). Em18, a new serodiagnostic marker for differentiation of active and inactive cases of alveolar hydatid disease. American Journal of Tropical Medicine and Hygiene 52, 41–44.CrossRefGoogle ScholarPubMed
Jenkins, P., Dixon, J. B., Rakha, N. K. and Carter, S. D. (1990). Regulation of macrophage-mediated larvicidal activity in Echinococcus granulosus and Mesocestoides corti (Cestoda) infection in mice. Parasitology 100, 309–315.CrossRefGoogle ScholarPubMed
Jenne, L., Arrighi, J. F., Sauter, B. and Kern, P. (2001). Dendritic cells pulsed with unfractionated helminthic proteins to generate antiparasitic cytotoxic T lymphocyte. Parasite Immunology 23, 195–201.CrossRefGoogle ScholarPubMed
Jenne, L., Kilwinski, J., Radloff, P., Flick, W. and Kern, P. (1998). Clinical efficacy of and immunologic alterations caused by interferon gamma therapy for alveolar echinococcosis. Clinical Infectious Diseases 26, 492–494.CrossRefGoogle ScholarPubMed
Jinushi, M., Takehara, T., Tatsumi, T., Hiramatsu, N., Sakamori, R., Yamaguchi, S. and Hayashi, N. (2005). Impairment of natural killer cell and dendritic cell functions by the soluble form of MHC class I-related chain A in advanced human hepatocellular carcinomas. Journal of Hepatology 43, 1013–1020.CrossRefGoogle ScholarPubMed
Kilwinski, J., Jenne, L., Jellen-Ritter, A., Radloff, P., Flick, W. and Kern, P. (1999). T lymphocyte cytokine profile at a single cell level in alveolar echinococcosis. Cytokine 11, 373–381.CrossRefGoogle Scholar
Kizaki, T., Kobayashi, S., Ogasawara, K., Day, N. K., Good, R. A. and Onoé, K. (1991). Immune suppression induced by protoscoleces of Echinococcus multilocularis in mice. Evidence for the presence of CD8dull suppressor cells in spleens of mice intraperitoneally infected with E. multilocularis. Journal of Immunology 147, 1659–1666.CrossRefGoogle ScholarPubMed
Kizaki, T., Ishige, M., Bingyan, W., Day, N. K., Good, R. A. and Onoe, K. (1993). Generation of CD8+ suppressor T cells by protoscoleces of Echinococcus multilocularis in vitro. Immunology 79, 412–417.Google ScholarPubMed
Kocherscheidt, L., Flakowski, A. K., Grüner, B., Hamm, D. M., Dietz, K., Kern, P. and Soboslay, P. T. (2008). Echinococcus multilocularis: inflammatory and regulatory chemokine responses in patients with progressive, stable and cured alveolar echinococcosis. Experimental Parasitology 119, 467–474.CrossRefGoogle ScholarPubMed
Kouguchi, H., Matsumoto, J., Katoh, Y., Oku, Y., Suzuki, T. and Yagi, K. (2007). The vaccination potential of EMY162 antigen against Echinococcus multilocularis infection. Biochemical and Biophysical Research Communications 363, 915–920.CrossRefGoogle ScholarPubMed
Koizumi, A., Hada, N., Kaburaki, A., Yamano, K., Schweizer, F. and Takeda, T. (2009). Synthetic studies on the carbohydrate moiety of the antigen from the parasite Echinococcus multilocularis. Carbohydrate Research 344, 856–868.CrossRefGoogle ScholarPubMed
Korkmaz, M., Inceboz, T., Celebi, F., Babaoglu, A. and Uner, A. (2004). Use of two sensitive and specific immunoblot markers, em70 and em90, for diagnosis of alveolar echinococcosis. Journal of Clinical Microbiology 42, 3350–3352.CrossRefGoogle ScholarPubMed
Liance, M., Aicard-Blum, S., Emery, I., Houin, A. and Vuitton, D. A. (1998). Echinococcus multilocularis infection in mice: in vivo treatment with a low dose of IFN-gamma decreases metacestode growth and liver fibrogenesis. Parasite 5, 231–237.CrossRefGoogle ScholarPubMed
Lin, R. Y., Wang, J. H., Lu, X. M., Zhou, X. T., Mantion, G., Wen, H., Vuitton, D. A. and Richert, L. (2009). Components of the mitogen-activated protein kinase cascade are activated in hepatic cells by Echinococcus multilocularis metacestode. World Journal of Gastroenterology 15, 2116–2124.CrossRefGoogle ScholarPubMed
MacDonald, A. S., Straw, A. D., Bauman, B. and Pearce, E. J. (2001). CD8− dendritic cell activation status plays an integral role in influencing Th2 response development. Journal of Immunology 167, 1982–1988.CrossRefGoogle ScholarPubMed
Machado, E. R., Ueta, M. T., Lourenço, E. V., Anibal, F. F., Sorgi, C. A., Soares, E. G., Roque-Barreira, M. C., Medeiros, A. I. and Faccioli, L. H. (2005). Leukotrienes play a role in the control of parasite burden in murine strongyloidiasis. Journal of Immunology 175, 3892–3899.CrossRefGoogle ScholarPubMed
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. (2004). Helminth parasites–masters of regulation. Immunology Reviews 201, 89–116.CrossRefGoogle ScholarPubMed
Mbow, M. L., Christe, M., Rutti, B. and Brossard, M. (1994). Absence of acquired resistance to nymphal Ixodes ricinus ticks in BALB/c mice developing cutaneous reactions. Journal of Parasitology 80, 81–87.CrossRefGoogle ScholarPubMed
Mejri, N. and Gottstein, B. (2006). Intraperitoneal Echinococcus multilocularis infection in C57BL/6 mice inhibits the up-regulation of B7-1 and B7-2 co-stimulator expression on peritoneal macrophages and causes failure to enhance peritoneal T cell activation. Parasite Immunology 28, 373–385.CrossRefGoogle Scholar
Mejri, N. and Gottstein, B. (2009). Echinococcus multilocularis metacestode metabolites contain a cysteine protease that digests eotaxin, a CC pro-inflammatory chemokine. Parasitology Research 105, 1253–1260.CrossRefGoogle ScholarPubMed
Mishra, A., Hogan, S. P., Lee, J. J., Foster, P. S. and Rothenberg, M. E. (1999). Fundamental signals that regulate eosinophil homing to the gastrointestinal tract. Journal of Clinical Investigations 103, 1719–1727.CrossRefGoogle ScholarPubMed
Morelli, A. E. and Thomson, A. W. (2007). Tolerogenic dendritic cells and the quest for transplant tolerance. Nature Review in Immunology 7, 610–621.CrossRefGoogle ScholarPubMed
Müller, N., Gottstein, B., Vogel, M., Flury, K. and Seebeck, T. (1989). Application of a recombinant Echinococcus multilocularis antigen in an ELISA for diagnosis of human alveolar echinococcosis. Molecular and Biochemical Parasitology 36, 151–160.CrossRefGoogle Scholar
O'Garra, A. (1998). Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity 8, 275–283.CrossRefGoogle ScholarPubMed
Ovington, K. S. and Behm, C. A. (1997). The enigmatic eosinophil: investigation of the biological role of eosinophils in parasitic helminth infection. Memorias do Instituto Oswaldo Cruz 2, 93–104.CrossRefGoogle Scholar
Persat, F., Bouhours, J.-F., Mojon, M. and Petavy, A.-F. (1992). Glycosphingolipids with Gal beta 1–6Gal sequences in metacestodes of the parasite Echinococcus multilocularis. Journal of Biological Chemistry 267, 8764–8769.CrossRefGoogle ScholarPubMed
Persat, F., Vincent, C., Schmitt, D. and Mojon, M. (1996). Inhibition of human peripheral blood mononuclear cell proliferative response by glycosphingolipids from metacestodes of Echinococcus multilocularis. Infection and Immunity 64, 3682–3687.CrossRefGoogle ScholarPubMed
Pennock, J. L. and Grencis, R. K. (2006). The mast cell and gut nematodes: damage and defence. Chemical Immunology and Allergy 90, 128–140.Google ScholarPubMed
Playford, M. C. and Kamiya, M. (1992). Immune response to Echinococcus multilocularis infection in the mouse model. Japanese Journal of Veterinary Research 40, 113–130.Google ScholarPubMed
Playford, M. C., Ooi, H. K., Oku, Y. and Kamiya, M. (1992). Secondary Echinococcus multilocularis infection in severe combined immunodeficient (scid) mice: biphasic growth of the larval cyst mass. International Journal for Parasitology 22, 975–982.CrossRefGoogle ScholarPubMed
Reis e Sousa, C., Sher, A. and Kaye, P. (1999). The role of dendritic cells in the induction and regulation of immunity to microbial infection. Current Opinion in Immunology 11, 392–399.CrossRefGoogle ScholarPubMed
Rigano, R., Buttari, B., De Falco, E., Profumo, E., Ortona, E., Margutti, P., Scottà, C., Teggi, A. and Siracusano, A. (2004). Echinococcus granulosus-specific T-cell lines derived from patients at various clinical stages of cystic echinococcosis. Parasite Immunology 26, 45–52.CrossRefGoogle ScholarPubMed
Riley, E. M. and Dixon, J. B. (1987). Experimental Echinococcus granulosus infection in mice: immunocytochemical analysis of lymphocyte populations in local lymphoid infections during early infection. Parasitology 94, 523–532.CrossRefGoogle ScholarPubMed
Rojas, R. E., Balaji, K. N., Subramanian, A. and Boom, W. H. (1999). Regulation of human CD4(+) alpha-beta T-cell-receptor-positive (TCR(+)) and gamma-delta TCR(+) T-cell responses to Mycobacterium tuberculosis by interleukin-10 and transforming growth factor beta. Infection and Immunity 67, 6461–6472.CrossRefGoogle ScholarPubMed
Romagnoli, G., Nisini, R., Chiani, P., Mariotti, S., Teloni, R., Cassone, A. and Torosantucci, A. (2004). The interaction of human dendritic cells with yeast and germ-tube forms of Candida albicans leads to efficient fungal processing, dendritic cell maturation, and acquisition of a Th1 response-promoting function. Journal of Leukocyte Biology 75, 117–126.CrossRefGoogle ScholarPubMed
Rutitzky, L. I., Hernandez, H. J., Yim, Y. S., Ricklan, D. E., Finger, E., Mohan, C., Peter, I., Wakeland, E. K. and Stadecker, M. J. (2005). Enhanced egg-induced immunopathology correlates with high IFN-gamma in murine schistosomiasis: identification of two epistatic genetic intervals. Journal of Immunology 175, 3920–3926.CrossRefGoogle Scholar
Sailer, M., Soelder, B., Allerberger, F., Zaknun, D., Feichtinger, H. and Gottstein, B. (1997). Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. Journal of Pediatrics 130, 320–323.CrossRefGoogle Scholar
Sako, Y., Yamasaki, H., Nakaya, K., Nakao, M. and Ito, A. (2007). Cloning and characterization of cathepsin L-like peptidases of Echinococcus multilocularis metacestodes. Molecular and Biochemical Parasitology 154, 181–189.CrossRefGoogle ScholarPubMed
Saraswathi, T. R., Nalinkumar, S., Ranganathan, K., Umadevi, R. and Elizabeth, J. (2003). Eosinophils in health and disease. Journal of Oral Maxillofacial Pathology 7, 31–33.Google Scholar
Sato, C. and Furuya, K. (1994). Isolation and characterization of a diagnostic polysaccharide antigen from larval Echinococcus multilocularis. Japanese Journal of Medicine and Science Biology 47, 65–71.Google ScholarPubMed
Sher, A., Pearce, E. and Kaye, P. (2003). Shaping the immune response to parasites: role of dendritic cells. Current Opinion Immunology 15, 421–429.CrossRefGoogle ScholarPubMed
Siles Lucas, M., Felleisen, R. S. J., Hemphill, A., Wilson, W. and Gottstein, B. (1998). Stage-specific expression of the 14-3-3 gene in Echinococcus multilocularis. Molecular and Biochemical Parasitology 91, 281–293.Google ScholarPubMed
Siles-Lucas, M. and Gottstein, B. (2003). The 14-3-3 protein: a key molecule in parasites as in other organisms. Trends in Parasitology 19, 575–581.CrossRefGoogle ScholarPubMed
Siles-Lucas, M., Merli, M., Mackenstedt, U. and Gottstein, B. (2003). The Echinococcus multilocularis 14-3-3 protein protects mice against primary but not secondary alveolar echinococcosis. Vaccine 21, 431–439.CrossRefGoogle Scholar
Siracusano, A., Rigano, R., Ortona, E., Profumo, E., Margutti, P., Buttari, B., Delunardo, F. and Teggi, A. (2008). Immunomodulatory mechanisms during Echinococcus granulosus infection. Experimental Parasitology 119, 483–489.CrossRefGoogle ScholarPubMed
Spiliotis, M., Konrad, C., Gelmedin, V., Tappe, D., Brückner, S., Mösch, H. U. and Brehm, K. (2006). Characterisation of EmMPK1, an ERK-like MAP kinase from Echinococcus multilocularis which is activated in response to human epidermal growth factor. International Journal for Parasitology 36, 1097–1112.CrossRefGoogle ScholarPubMed
Sturm, D., Menzel, J., Gottstein, B., Kern, P. (1995). Interleukin-5 is the predominant cytokine produced by peripheral blood – mononuclear cells in alveolar echinococcosis. Infection and Immunity 63, 1688–1697.CrossRefGoogle ScholarPubMed
Takeda, K., Kaisho, T. and Akira, S. (2003). Toll-like receptors. Annual Review Immunology 21, 335–376.CrossRefGoogle ScholarPubMed
Thomas, P. G., Carter, M. R., Atochina, O., Da'Dara, A. A., Piskorska, D., McGuire, E. and Harn, D. A. (2003). Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. Journal of Immunology 171, 5837–5841.CrossRefGoogle ScholarPubMed
Vogel, M., Gottstein, B., Müller, N. and Seebeck, T. (1988). Expression of a species-specific Echinococcus multilocularis antigen in Escherichia coli. Molecular and Biochemical Parasitology 31, 117–126.CrossRefGoogle Scholar
Vuitton, D. A. (2003). The ambiguous role of immunity in echinococcosis: protection of the host or of the parasite? Acta Tropica 85, 119–132.CrossRefGoogle ScholarPubMed
Walker, M., Baz, A., Dematteis, S., Stettler, M., Gottstein, B., Schaller, J. and Hemphill, A. (2004). Isolation and characterization of a secretory fraction of Echinococcus multilocularis metacestode potentially involved in modulating the host-parasite interface. Infection and Immunity 72, 527–536.CrossRefGoogle ScholarPubMed
Weenink, S., Averdunk, H., Boston, T., Boswarva, V., Guery, J. C., Adorini, L., Mellins, E., McCluskey, J. and Gautam, A. M. (1997). Impaired antigen presentation by murine I-Ad class II MHC molecules expressed in normal and HLA-DM-defective human B cell lines. International Immunology 9, 889–896.CrossRefGoogle ScholarPubMed
Wellinghausen, N., Gebert, P. and Kern, P. (1999). Interleukin (IL)-4, IL-10 and IL-12 profile in serum of patients with alveolar echinococcosis. Acta Tropica 73, 165–174.CrossRefGoogle ScholarPubMed
Whelan, M., Harnett, M. M., Houston, K. M., Patel, V., Harnett, W. and Rigley, K. P. (2000). A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. Journal of Immunology 164, 6453–6460.CrossRefGoogle ScholarPubMed
Wu, P., Wei, H., Zhang, C., Zhang, J. and Tian, Z. (2005). Regulation of NK cell activation by stimulatory and inhibitory receptors in tumor escape from innate immunity. Frontiers in Bioscience 10, 3132–3142.CrossRefGoogle ScholarPubMed
Yamaguchi, Y., Hayashi, Y., Sugama, Y., Miura, Y., Kasahara, T., Kitamura, S., Torisu, M., Mita, S., Tominaga, A. and Takatsu, K. (1988). Highly purified murine interleukin 5 (IL-5) stimulates eosinophil function and prolongs in vitro survival. IL-5 as an eosinophil chemotactic factor. Journal of Experimental Medicine 167, 1737–1742.CrossRefGoogle ScholarPubMed
Zaccone, P., Burton, O. T. and Cooke, A. (2008). Interplay of parasite-driven immune responses and autoimmunity. Trends in Parasitology 24, 35–42.CrossRefGoogle ScholarPubMed
Zhang, S., Hüe, S., Sène, D., Penfornis, A., Bresson-Hadni, S., Kantelip, B., Caillat-Zucman, S. and Vuitton, D. A. (2008). Expression of major histocompatibility complex class I chain-related molecule A, NKG2D, and transforming growth factor-beta in the liver of humans with alveolar echinococcosis: new actors in the tolerance to parasites? Journal of Infectious Diseases 197, 1341–1349.CrossRefGoogle Scholar
Zingg, W., Renner-Schneiter, E. C., Pauli-Magnus, C., Renner, E. L., van Overbeck, J., Schläpfer, E., Weber, M., Weber, R., Opravil, M., Gottstein, B., Speck, R. F. and the Swiss HIV Cohort Study (2004). Alveolar echinococcosis of the liver in an adult with human immunodeficiency virus type-1 infection. Infection 32, 299–302.CrossRefGoogle Scholar