Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-28T00:47:49.887Z Has data issue: false hasContentIssue false
  • English
  • Français

The beneficial helminth parasite?

Published online by Cambridge University Press:  21 September 2005

D. M. McKAY
D. M. McKAY
Affiliation:
Intestinal Disease Research Programme, McMaster University, Hamilton, Ontario, Canada
Get access Rights & Permissions [Opens in a new window]

Abstract

There is unequivocal evidence that parasites influence the immune activity of their hosts, and many of the classical examples of this are drawn from assessment of helminth infections of their mammalian hosts. Thus, helminth infections can impact on the induction or course of other diseases that the host might be subjected to. Epidemiological studies demonstrate that world regions with high rates of helminth infections consistently have reduced incidences of autoimmune and other allergic/inflammatory-type conditions. Here I review and assess the possible ways by which helminth infections can block or modulate concomitant disease processes. There is much to be learned from careful analysis of immuno-regulation in helminth-infected rodents and from an understanding of the immune status of acutely and chronically infected humans. The ultimate reward from this type of investigation will likely be a more comprehensive knowledge of immunity, novel ways to intervene in the immune response to alleviate autoimmune and allergic diseases (growing concerns in economically developed areas), and perhaps the development of helminth therapy for patients suffering from specific inflammatory, autoimmune or allergic disorders.

Keywords

allergyinflammationimmunomodulationHymenolepis sppnematodeSchistosoma spp
Type
Review Article
Information
Parasitology , Volume 132 , Issue 1 , January 2006 , pp. 1 - 12
Copyright
© 2005 Cambridge University Press

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

Allen, J. E. and Maizels, R. M. ( 1996). Immunology of human helminth infection. International Archives of Allergy and Immunology 109, 3–10.CrossRefGoogle Scholar
Allen, J. E. and Maizels, R. M. ( 1997). Th1-Th2: reliable paradigm or dangerous dogma. Immunology Today 18, 387–392.CrossRefGoogle Scholar
Araujo, M. I., Hoppe, B., Medeiros, M. J. R., Alcantara, L., Almeida, M. C., Schriefer, A., Oliveira, R. R., Kruschewsky, R., Figueiredo, J. P., Cruz, A. A. and Carvalho, E. M. ( 2004 a). Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma. Journal of Infectious Diseases 190, 1797–1803.Google Scholar
Araujo, M. I., Hoppe, B. S., Medeiros, M. J. R. and Carvalho, E. M. ( 2004 b). Schistosoma mansoni infection modulates the immune response against allergic and auto-immune diseases. Memorias do Instituto Oswaldo Cruz 99, 27–32.Google Scholar
Arechavaleta, F., Molinari, J. L. and Tato, P. ( 1998). A Taenia solium metacestode factor non-specifically inhibits cytokine production. Parasitology Research 84, 117–122.Google Scholar
Bain, K., Zhong, M., Harari, Y., Lai, M., Weisbrodt, N. and Murad, F. ( 2005). Helminth regualtion of host IL-4α/STAT6 signaling: mechnaism underlying NOS-2 inhibiton by Trichinella spiralis. Proceedings of the National Academy of Sciences, USA 102, 3936–3941.CrossRefGoogle Scholar
Bashir, M. E. H., Andersen, P., Fuss, I. J., Shi, H. N. and Nagler-anderson, C. ( 2002). An enteric helminth infection protects against an allergic response to dietary antigen. Journal of Immunology 169, 3284–3292.CrossRefGoogle Scholar
Behnke, J. M., Barnard, C. J. and Wakelin, D. ( 1992). Understanding chronic nematode infections: evolutionary considerations, current hypotheses and the way forward. International Journal for Parasitology 22, 861–907.CrossRefGoogle Scholar
Bonini, S., Rasi, G., Bracci-Laudiero, M. L., Procoli, A. and Aloe, L. ( 2003). Nerve growth factor: neurotrophin or cytokine? International Archives of Allergy and Immunology 131, 80–84.Google Scholar
Borkow, G., Leng, Q., Weisman, Z., Stein, M., Galai, N., Kalinkovich, A. and Bentwich, Z. ( 2000). Chronic immune activation associated with intestinal helminth infections results in impaired signal transduction and anergy. Journal of Clinical Investigation 106, 1053–1060.CrossRefGoogle Scholar
Bradley, J. E. and Jackson, J. A. ( 2004). Immunity, immunoregulation and the ecology of trichuriasis and ascariasis. Parasite Immunology 26, 429–441.CrossRefGoogle Scholar
Castro, G. A. ( 1989). Immunophysiology of enteric parasitism. Parasitology Today 5, 11–19.CrossRefGoogle Scholar
Castrodeza, C. ( 1979). Non-progressive evolution, the Red Queen hypothesis, and the balance of nature. Acta Biotheories 28, 11–18.CrossRefGoogle Scholar
Cooper, P. J. ( 2004). The potential impact of early exposures to geohelminth infections on the development of atopy. Clinical Reviews of Allergy and Immunology 26, 5–14.CrossRefGoogle Scholar
Crompton, D. W. ( 1999). How much human helminthiasis is there in the world? Journal of Parasitology 85, 397–403.Google Scholar
Delgado, M. and Ganea, D. ( 2001). Vasoactive intestinal peptide and pituitary adenylate cyclase-activating polypeptide inhibit expression of Fas ligand in activated T lymphocytes by regulating c-Myc, NF-κβ, NF-AT and early growth factors 2/3. Journal of Immunology 166, 1028–1040.CrossRefGoogle Scholar
Desowitz, M. ( 1981). Harmonious parasites. In New Guinea Tapeworms and Jewish Grandmothers. Tales of People and Parasites pp. 179–205. N. W. Norton & Co., London.
Donnelly, S., O'neill, S. M., Sekiya, M., Mulcahy, G. and Dalton, J. P. ( 2005). Thioredoxin peroxidase secreted by Fasciola hepatica induces the alternative activation of macrophages. Infection and Immunity 73, 166–173.CrossRefGoogle Scholar
Dzik, J. M., Golos, B., Jagielska, E., Zielinski, Z. and Walajtys-rode, E. ( 2004). A non-classical type of alveolar macrophage response to Trichinella spiralis infection. Parasite Immunology 26, 197–205.CrossRefGoogle Scholar
Elliott, D. E., Setiawan, T., Metwali, A., Blum, A., Urban, J. F. Jr. and Weinstock, J. V. ( 2004). Heligmosomoides polygyrus inhibits established colitis in IL-10-deficient mice. European Journal of Immunology 34, 2690–2698.CrossRefGoogle Scholar
Elliott, D. E., Li, J., Blum, A., Metwali, A., Qadir, K., Urban, J. F. Jr. and Weinstock, J. V. ( 2003). Exposure to schistosome eggs protects mice from TNBS-induced colitis. American Journal of Physiology (Gastrointestinal Liver Physiology) 284, G385–G391.CrossRefGoogle Scholar
Elliott, D. E., Urban, J. F. Jr., Argo, C. K. and Weinstock, J. V. ( 2000). Does failure to acquire helminthic parasites predispose to Crohn's disease? FASEB Journal 14, 1848–1855.Google Scholar
Farrokhyar, F., Swarbrick, E. T. and Irvine, E. J. ( 2001). A critical review of epidemiological studies in inflammatory bowel disease. Scandinavian Journal of Gastroenterology 36, 2–15.CrossRefGoogle Scholar
Finkelman, F. D., Shea-donohue, T., Morris, S. C., Gildea, L., Strait, R., Madden, K. B., Schopf, L. and Urban, J. F. Jr. ( 2004). Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites. Immunological Reviews 201, 139–155.CrossRefGoogle Scholar
Foster, N. and Lee, D. ( 1995). A vasoactive intestinal polypeptide like protein excreted/secreted by Nippostrongylus brasiliensis and its effect on contraction of uninfected rat intestine. Parasitology 110, 97–104.Google Scholar
Fox, J. G., Beck, P., Dangler, C. A., Whary, M. T., Wang, T. C., Ning shi, H. and Nagler-anderson, C. ( 2000). Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy. Nature Medicine 6, 536–542.CrossRefGoogle Scholar
Gause, W. C., Urban, J. F. Jr. and Stadecker, J. M. ( 2003). The immune response to parasitic helminths: insights from murine models. Trends in Immunology 24, 269–277.CrossRefGoogle Scholar
Gomez-Escobar, N., Lewis, E. and Maizels, R. M. ( 1998). A novel member of the transforming growth factor-beta (TGF-β) superfamily from the filarial nematodes Brugia malayi and B. phangi. Experimental Parasitology 88, 200–209.CrossRefGoogle Scholar
Gordon, S. ( 2003). Alternative activation of macrophages. Nature Reviews in Immunology 3, 23–35.CrossRefGoogle Scholar
Grencis, R. K. ( 2003). Cytokine regulation of resistance and susceptibility to intestinal nematode infection – from host to parasite. Veterinary Parasitology 100, 45–50.Google Scholar
Grencis, R. K. and Entwistle, G. M. ( 1997). Production of an interferon-γ homologue by an intestinal nematode: functionally significant or interesting artifact? Parasitology 115, S101–S105.Google Scholar
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, London 389, 737–742.CrossRefGoogle Scholar
Hartmann, S. and Lucius, R. ( 2003). Modulation of host immune responses by nematode cystatins. International Journal for Parasitology 33, 1291–1302.CrossRefGoogle Scholar
Hayes, K. S., Bancroft, A. J. and Grencis, R. K. ( 2004). Immune-mediated regulation of chronic nematode infection. Immunological Reviews 201, 75–88.CrossRefGoogle Scholar
Hesse, M., Piccirillo, C. A., Belkaid, Y., Prufer, J., Mentink-kane, M., Leusink, M., Cheever, A. W., Shevach, E. M. and Wynn, T. A. ( 2004). The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells. Journal of Immunology 172, 3157–3166.CrossRefGoogle Scholar
Hogaboam, C. M., Valalnce, B. A., Kumar, A., Addison, C. L., Grahmam, F. L., Gauldie, J. and Collins, S. M. ( 1997). Therapeutic effects of interleukin-4 gene transfer in experimental inflammatory bowel disease. Journal of Clinical Investigation 100, 2766–2776.CrossRefGoogle Scholar
Holcomb, I. N., Kabakoff, R. C., Chan, B., Baker, T. W., Gurney, A., Henzel, W., Nelson, C., Lowman, H. B., Wright, B. D., Skelton, N. J., Frantz, G. D., Tumas, D. B., Peale, F. V. Jr., Shelton, D. L. and Hebert, C. C. ( 2000). FIZZ1, a novel cysteine-rich secreted protein associated with pulmonary inflammation, defines a new gene family. EMBO J 19, 4046–4055.CrossRefGoogle Scholar
Hunter, M. M. and McKay, D. M. ( 2004). Review article: Helminths as therapeutic agents for inflammatory bowel disease. Alimentary Pharmacology and Therapeutics 19, 167–177.CrossRefGoogle Scholar
Hunter, M. M., Wang, A., Hirota, C. L. and McKay, D. M. ( 2005). Neutralizing anti-IL-10 antibody blocks the protective effect of tapeworm infection in a murine model of chemically-induced colitis. Journal of Immunology 174, 7368–7375.CrossRefGoogle Scholar
Ito, A., Nakao, M. and Wandra, T. ( 2003). Human taeniasis and cysticercosis in Asia. Lancet 362, 1918–1920.CrossRefGoogle Scholar
Jackson, J. A., Turner, J. D., Rentoul, L., Faulkner, H., Behnke, J. M., Hoyle, M., Grencis, R. K., Else, K. J., Kamgno, J., Boussinesq, M. and Bradley, J. E. ( 2004). T helper cell type 2 responsiveness predicts future susceptibility to gastrointestinal nematodes in humans. Journal of Infectious Diseases 190, 1804–1811.CrossRefGoogle Scholar
Jenkins, D. C. and Phillipson, R. F. ( 1972). Increased establishment and longevity of Nippostrongylus brasiliensis in immune rats given repeated small infections. International Journal for Parasitology 2, 105–111.CrossRefGoogle Scholar
Kalinkovich, A., Weisman, Z., Leng, Q., Borkow, G., Stein, M., Greenberg, Z., Zlotnikov, S., Eitan, S. and Bentwich, Z. ( 1999). Increased CCR5 expression with decreased beta-chemokine secretion in Ethiopians: relevance to AIDS in Africa. Journal of Human Virology 2, 283–289.Google Scholar
Kane, C. M., Cervi, L., Sun, J., Mckee, A. S., Masek, K. S., Shapira, S., Hunter, C. A. and Pearce, E. J. ( 2004). Helminth antigens modulate TLR-initiated dendritic cell activation. Journal of Immunology 173, 7454–7461.CrossRefGoogle Scholar
Khan, W. I., Blennerhassett, P. A., Varghese, A. K., Chowdhury, S. K., Omsted, P., Deng, Y. and Collins, S. M. ( 2002). Intestinal nematode infection ameliorates experimental colitis in mice. Infection and Immunity 71, 5931–5937.CrossRefGoogle Scholar
La Flamme, A. C., Ruddenklau, K. and Backstrom, B. T. ( 2003). Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infection and Immunity 71, 4996–5004.CrossRefGoogle Scholar
Lawrence, R. A., Allen, J. E. and Gray, C. A. ( 2000). Requirements for in vivo IFN-γ induction by live microfilariae of the parasitic nematode, Brugia malayi. Parasitology 120, 631–640.CrossRefGoogle Scholar
Li, M. C. and He, S. H. ( 2004). IL-10 and its related cytokines for treatment of inflammatory bowel disease. World Journal of Gastroenterology 10, 620–625.CrossRefGoogle Scholar
Liu, T., Jin, H., Ullenbruch, M., Hu, B., Hashimoto, N., Moore, B., McKenzie, A., Lukacs, N. W. and Phan, S. H. ( 2004). Regulation of found in inflammatory zone 1 expression in bleomycin-induced lung fibrosis: role of IL-4/IL-13 and mediation via STAT-6. Journal of Immunology 173, 3425–3431.CrossRefGoogle Scholar
Loke, P., MacDonald, A. S., Robb, A., Maizels, R. M. and Allen, J. E. ( 2000). Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. European Journal of Immunology 30, 2669–2678.3.0.CO;2-1>CrossRefGoogle Scholar
Maizels, R. M., Balic, A., Gomez-Escobar, N., Nair, M., Taylor, M. D. and Allen, J. E. ( 2004). Helminth parasites – masters of regulation. Immunological Reviews 201, 89–116.CrossRefGoogle Scholar
Maizels, R. M. and Yazdanbakhsh, M. ( 2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733–744.CrossRefGoogle Scholar
Maldonado-Lopez, R. and Moser, M. ( 2001). Dendritic cell subsets and the regulation of Th1/Th2 responses. Seminar in Immunology 13, 275–282.CrossRefGoogle Scholar
Mangan, N. E., Fallon, R. E., Smith, P., Van Rooijen, N., McKenzie, A. N. and Fallon, P. G. ( 2004). Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. Journal of Immunology 173, 6346–6356.CrossRefGoogle Scholar
Masson, S. D., McKay, D. M., Stead, R. H., Agro, A., Stanisz, A. and Perdue, M. H. ( 1996). Nippostrongylus brasiliensis infection causes neuronal abnormalities and altered neurally regulated ion secretion in rat jejunum. Parasitology 113, 173–182.CrossRefGoogle Scholar
Mayer, L. ( 2005). A novel approach to the treatment of ulcerative colitis: is it kosher? (editorial). Gastroenterology 128, 1117–1119.CrossRefGoogle Scholar
McGuirk, P. and Mills, K. H. ( 2002). Pathogen-specific regulatory T cells provoke a shift in the Th1/Th2 paradigm in immunity to infectious diseases. Trends in Immunology 23, 450–455.CrossRefGoogle Scholar
McInnes, I. B., Leung, B. P., Harnett, M., Gracie, J. A., Liew, F. Y. and Harnett, W. ( 2003). A novel therapeutic approach targeting articular inflammation using the filarial nematode-derived phosphorylcholine-containing glycoprotein ES-62. Journal of Immunology 171, 2127–2133.CrossRefGoogle Scholar
McKay, D. M. and Khan, W. I. ( 2003). STAT-6 is an absolute requirement for murine rejection of Hymenolepis diminuta. Journal of Parasitology 89, 188–189.CrossRefGoogle Scholar
McKay, D. M. and Fairweather, I. ( 1997). A role for the enteric nervous system in the response to helminth infections. Parasitology Today 13, 63–69.CrossRefGoogle Scholar
McKay, D. M., Halton, D. W., Johnston, C. F., Fairweather, I. and Shaw, C. ( 1990 a). Hymenolepis diminuta: changes in intestinal morphology and the enterochromaffin cell population associated with infection in male C57 mice. Parasitology 101, 107–113.Google Scholar
McKay, D. M., Halton, D. W., McCaigue, M. D., Johnston, C. F., Fairweather, I. and Shaw, C. ( 1990 b). Hymenolepis diminuta: intestinal goblet cell response in male C57 mice. Experimental Parasitology 71, 9–20.Google Scholar
McKee, A. S. and Pearce, E. J. ( 2004). CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. Journal of Immunology 173, 1224–1231.CrossRefGoogle Scholar
Mills, C. D., Kincaid, K., Alt, J. M., Heilman, M. J. and Hill, A. M. ( 2000). M-1/M-2 macrophages and the Th1-Th2 paradigm. Journal of Immunology 164, 6166–6173.CrossRefGoogle Scholar
Moreels, T. G., Nieuwendijk, R. J., De Man, J. G., De Winter, B. Y., Herman, A. G., Van Marck, E. A. and Pelckmans, P. A. ( 2004). Concurrent infection with Schistosoma mansoni attenuates inflammation induced changes in colonic morphology, cytokine levels, and smooth muscle contractility of trinitrobenzene sulphonic acid induced colitis in rats. Gut 53, 99–107.CrossRefGoogle Scholar
Mosmann, T. R., Cherwinski, H., Bond, M. W., Giedlin, M. A. and Coffman, R. L. ( 1986). Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. Journal of Immunology 136, 2348–2357.Google Scholar
Mosmann, T. R., Li, L. and Sad, S. ( 1997). Functions of CD8 T-cell subsets secreting different cytokine patterns. Seminars in Immunology 9, 87–92.CrossRefGoogle Scholar
Nair, M. G., Gallagher, I. J., Taylor, M. D., Loke, P., Coulson, P. S., Wilson, R. A., Maizels, R. M. and Allen, J. E. ( 2005). Chitinase and Fizz family members are a generalized feature of nematode infection with selective upregulation of Ym1 and Fizz1 by antigen-presenting cells. Infection and Immunity 73, 385–394.CrossRefGoogle Scholar
Oberhelman, R. A., Guerrero, E. S., Fernandez, M. L., Silio, M., Mercado, D., Comiskey, N., Ihenacho, G. and Mera, R. ( 1998). Correlations between intestinal parasitosis, physical growth, and psychomotor development among infants and children from rural Nicaragua. American Journal of Tropical Medicine 58, 470–475.CrossRefGoogle Scholar
O'Garra, A. and Vieira, P. ( 2004). Regulatory T cells and mechanisms of immune system control. Nature Medicine 10, 801–805.CrossRefGoogle Scholar
Omer, F. M., De Souza, J. B., Corran, P. H., Sultan, A. A. and Riley, E. M. ( 2003). Activation of transforming growth factor-β by malaria parasite-derived metalloproteinases and a thrombospondin-like molecule. Journal of Experimental medicine 198, 1817–1827.CrossRefGoogle Scholar
Omer, F. M., Kurtzhals, J. A. and Riley, E. M. ( 2000). Maintaining the immunological balance in parasitic infections: a role for TGF-β? Parasitology Today 16, 18–23.Google Scholar
Oyewole, F., Ariyo, F., Sanyaolu, A., Oyibo, W. A., Faweya, T., Monye, P., Ukpong, M. and Okoro, C. ( 2002). Intestinal helminthiases and their control with albendazole among primary school children in riverine communities of Ondo state, Nigeria. Southeast Asian Journal of Tropical Medicine and Public Health 33, 214–217.Google Scholar
Paalangara, R., McClure, S. and McCullagh, P. ( 2003). Intestinal exposure to a parasite antigen in utero depresses cellular and cytokine responses of the mucosal immune system. Veterinary Immunology and Immunopathology 93, 91–105.CrossRefGoogle Scholar
Perdue, M. H. and McKay, D. M. ( 1994). Integrative immunophysiology in the intestinal mucosa. American Journal of Physiology (Gastrointestinal Liver Physiology) 267, G151–G165.CrossRefGoogle Scholar
Ramaswamy, K., Kumar, P. and He, Y. X. ( 2000). A role for parasite-induced PGE2 in IL-10-mediated host immunoregulation by skin stage schistosomula of Schistosoma mansoni. Journal of Immunology 165, 4567–4574.CrossRefGoogle Scholar
Reardon, C., Sanchez, A., Hogaboam, C. M. and McKay, D. M. ( 2001). Tapeworm infection reduces the ion transport abnormalities induced by dextran sulphate sodium (DSS) colitis. Infection and Immunity 69, 4417–4423.CrossRefGoogle Scholar
Reiner, S. L. ( 2001). Helper T cell differentiation, inside and out. Current Opinion in Immunology 13, 351–355.CrossRefGoogle Scholar
Rigano, R., Profumo, E., Bruschi, F., Carulli, G., Azzara, A., Ioppolo, S., Buttari, B., Ortona, E., Margutti, P., Teggi, A. and Siracusano, A. ( 2001). Modulation of human immune response by Echinococcus granulosus antigen B and its possible role in evading host defenses. Infection and Immunity 69, 288–296.CrossRefGoogle Scholar
Rodriguez-Sosa, M., Satoskar, A. R., Calderon, R., Gomez-Garcia, L., Saavedra, R., Bojalil, R. and Terrazas, L. I. ( 2002). Chronic helminth infection induces alternatively activated macrophages expressing high levels of CCR5 with low interleukin-12 production and Th2-biasing ability. Infection and Immunity 70, 3656–3664.CrossRefGoogle Scholar
Romagnani, S. ( 2004). Immunologic influences on allergy and the TH1/TH2 balance. Journal of Allergy and Clinical Immunology 113, 395–400.CrossRefGoogle Scholar
Saldiva, S. R., Silveira, A. S., Philippi, S. T., Torres, D. M., Mangini, A. C., Dias, R. M., Da Silva, R. M., Buratini, M. N. and Massad, E. ( 1999). Ascaris-Trichuris association and malnutrition in Brazilian children. Paediatric Perinatal Epidemiology 13, 89–98.CrossRefGoogle Scholar
Sasaki, A. ( 2000). Host-parasite co-evolution in a multi-locus gene-for-gene system. Proceedings in Biological Sciences 267, 2183–2188.CrossRefGoogle Scholar
Satoguina, J., Mempel, M., Larbi, J., Badusche, M., Loliger, C., Adjei, O., Gachelin, G., Fleischer, B. and Hoerauf, A. ( 2002). Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes and Infection 4, 1291–1300.CrossRefGoogle Scholar
Sawa, Y., Oshitani, N., Adachi, K., Higuchi, K., Matsumoto, T. and Arakawa, T. ( 2003). Comprehensive analysis of intestinal cytokine messenger RNA profile by real-time quantitative polymerase chain reaction in patients with inflammatory bowel disease. International Journal for Molecular Medicine 11, 175–179.CrossRefGoogle Scholar
Schopf, L. R., Hoffman, K. F., Cheever, A. W., Urban, J. F. Jr. and Wynn, T. ( 2002). IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. Journal of Immunology 168, 2383–2392.CrossRefGoogle Scholar
Shea-Donohue, T., Sullivan, C., Finkelman, F. D., Madden, K. B., Morris, S. C., Goldhill, J., Pineiro-Carrero, V. and Urban, J. F. Jr. ( 2001). The role of IL-4 in Heligosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. Journal of Immunology 167, 2234–2239.CrossRefGoogle Scholar
Smith, P., Walsh, C. M., Mangan, N. E., Fallon, R. E., Sayers, J. R., McKenzie, A. N. and Fallon, P. G. ( 2004). Schistosoma mansoni worms induce anergy of T cells via selective up-regulation of programmed death ligand 1 on macrophages. Journal of Immunology 173, 1240–1248.CrossRefGoogle Scholar
Summers, R. W., Elliott, D. E., Urban, J. F. Jr., Thompson, R. and Weinstock, J. V. ( 2005 a). Trichuris suis therapy in Crohn's disease. Gut 54, 87–90.Google Scholar
Summers, R. W., Elliott, D. E., Urban, J. F. Jr., Thompson, R. and Weinstock, J. V. ( 2005 b). Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128, 825–832.Google Scholar
Suzuki, R., Furuno, T., McKay, D. M., Wolvers, D., Teshima, R., Nakanishi, M. and Bienenstock, J. ( 1999). Direct neurite-mast cell (RBL) communication in vitro occurs via the neuropetide substance P. Journal of Immunology 163, 2410–2415.Google Scholar
Tchuem-Tchuente, L.-A., Behnke, J. M., Gilbert, F. S., Southgate, V. R. and Vercruysse, J. ( 2003). Polyparasitism with Schistosoma haematobium and soil-transmitted helminth infections among school children in Loum, Cameroon. Tropical Medicine and International Health 8, 975–986.CrossRefGoogle Scholar
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 Scholar
Toenjes, S. A. and Kuhn, R. E. ( 2003). The initial immune response during experimental cysticercosis is of the mixed Th1/Th2 type. Parasitology Research 89, 407–413.Google Scholar
Turner, J. D., Faulkner, H., Kamgno, J., Cormont, F., Van Snick, J., Else, K. J., Grencis, R. K., Behnke, J. M., Boussinesq, M. and Bradley, J. E. ( 2003). Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. Journal of Infectious Diseases 188, 1768–1775.CrossRefGoogle Scholar
Udani, V. ( 2005). Pediatric epilepsy – an Indian perspective. Indian Journal of Pediatrics 72, 309–313.CrossRefGoogle Scholar
Vallance, B. A., Blennerhassett, P. A. and Collins, S. M. ( 1997). Increased intestinal muscle contractility and worm expulsion in nematode-infected mice. American Journal of Physiology (Gastrointestinal Liver Physiology) 272, G321–G327.CrossRefGoogle Scholar
Van Der Biggelaar, A. H., Rodrigues, L. C., Van Ree, R., Van Der Zee, J. S., Hoeksma-Kruize, Y. C., Souverijn, J. H., Missinou, M. A., Borrmann, S., Kremsner, P. G. and Yazdanbakhsh, M. ( 2004). Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese school children. Journal of Infectious Diseases 189, 892–900.Google Scholar
Van Den Biggelaar, A. H., Van Ree, R., Rodrigues, L. C., Lell, B., Deelder, A. M., Kremsner, P. G. and Yazdanbakhsh, M. ( 2000). Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 356, 1723–1727.CrossRefGoogle Scholar
Van Der Kleij, D., Latz, E., Brouwers, J. F. H. M., Kruize, Y. C. M., Schmitz, M., Kurt-Jones, E. A., Espevik, T., De Jong, E. C., Kapsenberg, M. L., Golenbock, D. T., Tielens, A. G. M. and Yazdanbakhsh, M. ( 2002). A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. Journal of Biological Chemistry 277, 48122–48129.CrossRefGoogle Scholar
Van Der Kleij, D., Van Den Biggelaar, A. H., Kruize, Y. C., Reta, R., Fillie, Y., Schmitz, M., Kremsner, P. G., Tielns, A. G. and Yazdanbakhsh, M. ( 2004). Responses to Toll-like receptor ligands in children living in areas where schistosome infections are endemic. Journal of Infectious Diseases 189, 1044–1051.CrossRefGoogle Scholar
Velazquez, P., Wei, B. and Braun, J. ( 2005). Surveillance B lymphocytes and mucosal immunoregulation. Springer Seminars in Immunopathology 26, 453–462.CrossRefGoogle Scholar
Wang, A. and McKay, D. M. ( 2005). Immune modulation by a high molecular weight protein from the rat tapeworm Hymenolepis diminuta. Parasitology 130, 575–585.CrossRefGoogle Scholar
Wei, B., Velazquez, P., Turovskaya, O., Spricher, K., Aranda, R., Kronenberg, M., Birnbaumer, L. and Braun, J. ( 2005). Mesenteric B cells centrally inhibit CD4+ T cell colitis through interaction with regulatory T cell subsets. Proceedings of the National Academy of Sciences, USA 102, 2010–2015.CrossRefGoogle Scholar
Weinstock, J. V., Summers, R. W., Elliott, D. E., Qadir, K., Urban, J. F. Jr. and Thompson, R. ( 2002). The possible link between de-worming and the emergence of immunological disease. Journal of Laboratory and Clinical Medicine 139, 334–338.CrossRefGoogle Scholar
Welch, J. S., Escoubet-Lozach, L., Sykes, D. B., Liddiard, K., Greaves, D. R. and Glass, C. K. ( 2002). TH2 cytokines and allergic challenge induce Ym1 expression in macrophages by a STAT6-dependent mechanism. Journal of Biological Chemistry 277, 42821–42829.CrossRefGoogle Scholar
Wescott, R. B. and Colwell, D. A. ( 1980). Influence of numbers of Nematospiroides dubius upon delayed rejection of Nippostrongylus brasiliensis in mice. Journal of Parasitology 66, 858–859.CrossRefGoogle Scholar
West, A. B. ( 2005). Letter to the Editor. Potential danger in the medical use of Trichuis suis for the treatment of inflammatory bowel disease. Inflammatory Bowel Disease 11, 515.Google Scholar
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 Scholar
Wilson, M. S. and Maizels, R. M. ( 2004). Regulation of allergy and autoimmunity in helminth infection. Clinical Reviews in Allergy and Immunology 26, 35–50.CrossRefGoogle Scholar
Wohlleben, G., Trujillo, C., Muller, J., Ritze, Y., Grunewald, S., Tatsch, U. and Erb, K. J. ( 2004). Helminth infection modulates the development of allergen-induced airway inflammation. International Immunology 16, 585–596.CrossRefGoogle Scholar
Yazdanbakhsh, M., Van Den Biggelaar, A. and Maizels, R. ( 2001). Th2 responses without atopy: immunoregulation in chronic helminth infections and reduced allergic disease. Trends in Immunology 22, 372–377.CrossRefGoogle Scholar
Yazdanbakhsh, M., Kremsner, P. G. and Van Ree, R. ( 2002). Allergy, parasites and the hygiene hypothesis. Science 296, 490–494.CrossRefGoogle Scholar
Zang, X., Taylor, P., Wang, J. M., Meyer, D. J., Scott, A. L., Walkinshaw, M. D. and Maizels, R. M. ( 2002). Homologues of human macrophage migration inhibitory factor from a parasitic nematode. Gene cloning, protein activity, and crystal structure. Journal of Biological Chemistry 277, 44261–44267.CrossRefGoogle Scholar
Zhao, A., McDermitt, J., Urban, J. F. Jr., Gause, W. C., Madden, K. B., Yeung, K. A., Morris, S. C., Finkelman, F. D. and Shea-Donohue, T. ( 2003). Dependence of IL-4, IL-13 and nematode-induced alterations in murine small intestinal smooth muscle contractility on stat6 and enteric nerves. Journal of Immunology 171, 948–954.CrossRefGoogle Scholar