Modulation of anaphylaxis by helminth-derived products in animal models
Purchase on Springer.com
$39.95 / €34.95 / £29.95*
Rent the article at a discountRent now
* Final gross prices may vary according to local VAT.
Helminths have a profound immunomodulatory effect upon the inductive and effector phases of inflammatory responses, including allergy. Several animal models of anaphylaxis have been established to investigate the mechanisms by which helminth infections or helminth-derived products interfere with the onset of allergic reactions. The focus of our studies was the immunosuppression induced by the intestinal roundworm Ascaris suum in the production of anaphylactic antibodies and the development of lung eosinophilic inflammation and hyperreactivity to its own allergens and to unrelated antigens. Thus, we identified a single protein affinity purified from the A. suum body extract, named PAS-1, which maintains all its immunosuppressive properties and promotes a significant increase in interleukin-10 production, an essential cytokine for the effectiveness of the suppressive mechanism. In addition, PAS-1 primes for regulatory T cells, which also mediate this mechanism. Therefore, this helminth molecule may be a promising target for therapeutic applications in allergic disorders.
- Maizels RM, Yazdanbakhsh M: Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 2003, 3:733–744. CrossRef
- Smits HH, Hartgers FC, Yazdanbakhsh M: Helminth infections: protection from atopic disorders. Curr Allergy Asthma Rep 2005, 5:42–50. CrossRef
- Raybourne R, Desowitz RS, Kliks MM, Deardoff TL: Anisakis simplex and Terranova sp: inhibition by larval excretory-secretory products of mitogen-induced rodent lymphoblast proliferation. Exp Parasitol 1983, 55:289–298. CrossRef
- Ferreira AP, Faquim-Mauro EL, Abrahamsohn IA, Macedo MS: Immunization with Ascaris suum extract impairs T cell functions in mice. Cell Immunol 1995, 162:202–210. CrossRef
- Boitelle A, Scales HE, Di Lorenzo C, et al.: Investigating the impact of helminth products on immune responsiveness using a TCR transgenic adoptive transfer system. J Immunol 2003, 17:447–454.
- Chow SC, Brown A, Pritchard D: The human hookworm pathogen Necator americanus induces apoptosis in T lymphocytes. Parasite Immunol 2000, 22:21–29. CrossRef
- Cross DA, Klesius PH: Soluble extracts from larval Ostertagia ostertagi modulating immune function. Int J Parasitol 1989, 19:57–61. CrossRef
- Faquim-Mauro EL, Macedo MS: The immunosuppressive activity of Ascaris suum is due to high molecular weight components. Clin Exp Immunol 1998, 114:245–251. CrossRef
- Langlet C, Mazingue C, Dessaint JP, Capron A: Inhibition of primary and secondary IgE-response by a schistosome-derived inhibitory factor. Int Arch Allergy Appl Immunol 1984, 73:225–230.
- Soares MF, Mota I, Macedo MS: Isolation of Ascaris suum components which suppress IgE antibody responses. Int Arch Allergy Immunol 1992, 97:37–43. CrossRef
- Lima C, Perini A, Garcia ML, et al.: Eosinophilic inflammation and airway hyper-responsiveness are profoundly inhibited by a helminth (Ascaris suum) extract in a murine model of asthma. Clin Exp Allergy 2002, 32:1659–1666. CrossRef
- Itami DM, Oshiro TM, Araujo CA, et al.: Modulation of murine experimental asthma by Ascaris suum components. Clin Exp Allergy 2005, 35:873–879. CrossRef
- Doetze A, Satoguina J, Burchard G, et al.: Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by Th3/Tr1-type cytokines IL-10 and transforming growth factor-beta but not by a TH1 to TH2 shift. Int Immunol 2000, 12:623–630. CrossRef
- Moncayo AL, Cooper PJ: Geohelminth infections: impact on allergic diseases. Int J Biochem Cell Biol 2006, 38:1031–1035. CrossRef
- Nacher M, Gay F, Singhasivanon P, et al.: Ascaris lumbricoides infection is associated with protection from cerebral malaria. Parasite Immunol 2000, 22:107–113. CrossRef
- Nacher M, Singhasivanon P, Silachamroon U, et al.: Helminth infections are associated with protection from malaria-related acute renal failure and jaundice in Thailand. Am J Trop Med Hyg 2001, 65:834–836.
- Fox JG, Beck P, Dangler CA, et al.: Concurrent enteric helminth infection modulates inflammation and gastric immune responses and reduces helicobacter-induced gastric atrophy. Nat Med 2000, 6:536–542. CrossRef
- Elliott DE, Setiawan T, Metwali A, et al.: Heligmosomoides polygyrus inhibits established colites in IL-10-deficient mice. Eur J Immunol 2004, 34:2690–2698. CrossRef
- Hunter MM, Wanq A, Hirota CL, McKay DM: Neutralizing anti-IL-10 antibody blocks the protective effect of tapeworm infection in a murine model of chemically induced colitis. J Immunol 2005, 174:7368–7375.
- van den Biggelaar AH, van Ree R, Rodríguez LC, et al.: Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 2000, 356:1723–1727. CrossRef
- Lynch NR, Hagel I, Perez M, et al.: Effect of anthelmintic treatment on the allergic reactivity of children in a tropical slum. J Allergy Clin Immunol 1993, 92:404–411. CrossRef
- Araújo MI, Hoppe B, Mederiros M Jr, et al.: Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma. J Infect Dis 2004, 190:1797–1803. CrossRef
- Wang CC, Nolan TJ, Schad GA, Abraham D: Infection of mice with the helminth Strongyloides stercoralis suppresses pulmonary allergic responses to ovalbumin. Clin Exp Allergy 2001, 31:495–503. CrossRef
- Furze RC, Hussell T, Selkirk ME: Amelioration of influenza-induced pathology in mice by coinfection with Trichinella spiralis. Infect Immun 2006, 74:1924–1932. CrossRef
- Mangan NE, Fallon RE, Smith P, et al.: Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J Immunol 2004, 173:6346–6356.
- Mangan NE, van Rooijen N, McKenzie AN, Fallon PG.: Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness. J Immunol 2006, 176:138–147.
- Bashir ME, Andersen P, Fuss IJ, et al.: An enteric helminth infection protects against an allergic response to dietary antigen. J Immunol 2002, 169:3284–3292.
- Wohlleben G, Trujillo C, Muller J, et al.: Helminth infection modulates the development of allergy induced airway inflammation. Int Immunol 2004, 16:585–596. CrossRef
- Soares MF, Macedo MS, Mota I: Suppressive effect of an Ascaris suum extract on IgE and IgG antibody responses in mice. Braz J Med Biol Res 1987, 20:203–211.
- Macedo MS, Faquim-Mauro ES, Ferreira AP, Abrahamsohn IA: Immunomodulation induced by Ascaris suum extract in mice: effect of anti-interleukin-4 and anti-interleukin-10 antibodies. Scand J Immunol 1998, 47:10–18. CrossRef
- Souza VM, Jacysyn JF, Macedo MS: IL-4 and IL-10 are essential for immunosuppression induced by high molecular weight proteins from Ascaris suum. Cytokine 2004, 28:92–100. CrossRef
- Maizels RM, Balic A, Gomez-Escobar N, et al.: Helminth parasite—masters of regulation. Immunol Rev 2004, 201:89–116. CrossRef
- Wilson MS, Maizels RM: Regulatory T cells induced by parasite and the modulation of allergic responses. Chem Immunol Allergy 2006, 90:176–195. CrossRef
- Wilson MS, Taylor MD, Balic A, et al.: Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 2005, 202:1199–1212. CrossRef
- Schopf L, Luccioli S, Bundoc V, et al.: Differential modulation of allergic eye disease by chronic and acute Ascaris infection. Invest Ophthalmol Vis Sci 2005, 46:2772–2780. CrossRef
- Falcone FH, Loukas A, Quinell RJ, Pritchard DI: The innate allergenicity of helminth parasites. Clin Rev Allergy Immunol 2004, 26:61–72. CrossRef
- Gomez-Escobar N, Lewis E, Maizels RM: A novel member of the transforming growth factor-beta (TGF-beta) super-family from the filarial nematodes Brugia malayi and B. pahangi. Exp Parasitol 1998, 88:200–209. CrossRef
- Gomez-Escobar N, Gregory WF, Maizels RM: Identification of tgh-2, a filarial nematode homology of Caenorhabditis elegans daf-7 and human transforming growth factor beta, expressed in microfilarial and adult stages of Brugia malayi. Infect Immun 2000, 68:6402–6410. CrossRef
- Hirata M, Hirata K, Hara T, et al.: Expression of TGF-beta-like molecules in the life cycle of Schistosoma japonicum. Parasitol Res 2005, 95:367–373. CrossRef
- Barrett AJ. The cystatins: a diverse superfamily of cysteine peptidase inhibitors. Biomed Biochim Acta 1986, 45:1363–1374.
- Watts C: Antigen processing in the endocytic compartment. Curr Opin Immunol 2001, 13:26–31. CrossRef
- Pierre T, Mellaman I: Developmental regulation of invariant chain proteolysis controls MHC class II trafficking in mouse dendritic cells. Cell 1998, 93:1135–1145. CrossRef
- Dainichi T, Maekawa Y, Ishii K, et al.: Nippocystatin, a cysteine protease inhibitor from Nippostrongylus brasiliensis, inhibits antigen processing and modulates antigen-specific immune response. Infect Immun 2001, 69:7380–7386. CrossRef
- Pfaff AW, Schulz-Key H, Soboslay PT, et al.: Litomosoides sigmodontis cystatin acts as an immunomodulator during experimental filariasis. Int J parasitol 2002, 32:171–178. CrossRef
- Lustigman S, Brotman B, Huima T, et al.: Molecular cloning and characterization of onchocystatin, a cystein proteinase inhibitor of Onchocerca volvulus. J Biol Chem 1992, 267:17739–17346.
- Hartmann S, Kyewski B, Sonnenburg B, et al.: A filarial cysteine protease inhibitor down-regulates T-cell proliferation and enhances interleukin-10 production. Eur J Immunol 1997, 27:2253–2260. CrossRef
- Schönemeyer A, Lucius R, Sonnenburg B, et al.: Modulation of human T-cell responses and macrophage functions by onchocystatin, a secreted protein of the filarial nematode Onchocerca volvulus. J Immunol 2001, 167:3207–3215.
- Goodridge HS, Wilson EH, Harnett W, et al.: Modulation of macrophage cytokine production by ES-62, a secreted product of the filarial nematode Acanthocheilonema viteae. J Immunol 2001, 167:940–945.
- Balic A, Harcus Y, Holland MJ, Maizels RM: Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives the immune responses. Eur J Immunol 2004, 34:3047–3059. CrossRef
- Tawill, S, Le Goff L, Ali F, et al.: Both free-living and parasitic nematodes induce a characteristic Th2 response that is dependent on the presence of intact glycans. Infec Immun 2004, 72:398–407. CrossRef
- van der Kleij D, Latz E, Brouwers JF, et al.: A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J Biol Chem 2002, 277:48122–48129. CrossRef
- Terrazas LI, Walsh KL, Piskorska D, et al.: The schistosome oligosaccharide lacto-N-neotetraose expands Gr1(+) cells that secrete anti-inflammatory cytokines and inhibit proliferation of naive CD4(+) cells: a potential mechanism for immune polarization in helminth infections. J Immunol 2001, 167:5294–5303.
- Balckburn CC, Selkirk ME: Inactivation of platelet-activating factor by a putative acetylhydrolase from the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunology 1992, 75:41–46.
- Culley FJ, Brown A, Conroy DM, et al.: Eotaxin is specifically cleaved by hookworm metalloproteases preventing its action in vitro and in vivo. J Immunol 2000, 165:6447–6453.
- Oshiro TM, Rafael A, Enobe CS, et al.: Comparison of different monoclonal antibodies against immunosuppressive proteins of Ascaris suum. Braz J Med Biol Res 2004, 37:223–226. CrossRef
- Oshiro TM, Enobe CS, Araujo CA, et al.: PAS-1, a protein affinity purified from Ascaris suum worms, maintains the ability to modulate the immune response to a bystander antigen. Immunol Cell Biol 2006, 84:138–144. CrossRef
- Pires RR, Oshiro TM, Itami DM, et al.: Production and characterization of a monoclonal antibody against an Ascaris suum allergenic component. Braz J Med Biol Res 2001, 34:1033–1036. CrossRef
- Oshiro TM, Macedo MS, Macedo-Soares MF: Anti-inflammatory activity of PAS-1, a protein component of Ascaris suum. Inflamm Res 2005, 54:17–21. CrossRef
- Modulation of anaphylaxis by helminth-derived products in animal models
Current Allergy and Asthma Reports
Volume 7, Issue 1 , pp 56-61
- Cover Date
- Print ISSN
- Online ISSN
- Current Science Inc.
- Additional Links
- Industry Sectors