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The Hygiene Theory Harnessing Helminths and Their Ova to Treat Autoimmunity

Ben-Ami Shor, Dana, Harel, Michal, Eliakim, Rami, Shoenfeld, Yehuda·2013·Clinical Reviews in Allergy & Immunology
DOI 10.1007/s12016-012-8352-9
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Abstract

The incidence of autoimmune diseases is increasing in Western countries, possibly due to the improved sanitary conditions and reduced exposure to infections in childhood (the hygiene hypothesis). There is an ongoing debate whether infection prevents or precipitates autoimmune diseases. Various helminths species used in several animal models were shown to limit inflammatory activity in a variety of diseases including inflammatory bowel disease, multiple sclerosis, type 1 diabetes, rheumatoid arthritis, and systemic lupus erythematosus. At present the scientific data is based mostly on experimental animal models; however, there is an increasing body of evidence in a number of clinical trials being conducted. Herein we review several clinical trials evaluating the anti-inflammatory effects of helminths and assessing their association with different autoimmune diseases, including inflammatory bowel disease, multiple sclerosis, and autoimmune liver diseases. We also describe the common pathways by which helminths induce immune modulation and the key changes observed in the host immune system following exposure to helminths. These common pathways include the inhibition of IFN-γ and IL-17 production, promotion of IL-4, IL-10 and TGF-β release, induction of CD4(+) T cell FoxP3(+) expression, and generation of regulatory macrophages, dendritic cells, and B cells. Helminths products are becoming significant candidates for anti-inflammatory agents in this context. However, further resea…

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Research works printed but not linked: 55

  1. Strachan DP (1989) Hay fever, hygiene, and household size. BMJ 299:1259–1260 · DOI · Paper page
  2. Motomura Y, Wang H, Deng Y, El-Sharkawy RT, Verdu EF, Khan WI (2009) Helminth antigen-based strategy to ameliorate inflammation in an experimental model of colitis. Clin Exp Immunol 155:88–95 · DOI
  3. Reardon C, Sanchez A, Hogaboam CM, McKay DM (2001) Tapeworm infection reduces epithelial ion transport abnormalities in murine dextran sulfate sodium-induced colitis. Infect Immun 69:4417–4423 · DOI
  4. Marshall FA, Watson KA, Garside P, Harnett MM, Harnett W (2008) Effect of activated antigen-specific B cells on ES-62-mediated modulation of effector function of heterologous antigen-specific T cells in vivo. Immunology 123:411–425 · DOI
  5. Harnett MM, Kean DE, Boitelle A et al (2008) The phosphorycholine moiety of the filarial nematode immunomodulator ES-62 is responsible for its anti-inflammatory action in arthritis. Ann Rheum Dis 67:518–523 · DOI
  6. Sagi L, Baum S, Agmon-Levin N et al (2011) Autoimmune bullous diseases the spectrum of infectious agent antibodies and review of the literature. Autoimmun Rev 10:527–535 · DOI
  7. Saunders KA, Raine T, Cooke A, Lawrence CE (2007) Inhibition of autoimmune type 1 diabetes by gastrointestinal helminth infection. Infect Immun 75:397–407 · DOI
  8. Cooke A, Tonks P, Jones FM et al (1999) Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol 21:169–176 · DOI
  9. Cooke A (2009) Review series on helminths, immune modulation and the hygiene hypothesis: how might infection modulate the onset of type 1 diabetes? Immunology 126:12–17 · DOI
  10. Summers RW, Elliott DE, Urban JF Jr, Thompson R, Weinstock JV (2005) Trichuris suis therapy in Crohn's disease. Gut 54:87–90 · DOI · Paper page
  11. Summers RW, Elliott DE, Urban JF Jr, Thompson RA, Weinstock JV (2005) Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology 128:825–832 · DOI · Paper page
  12. Summers RW, Elliott DE, Weinstock JV (2005) Is there a role for helminths in the therapy of inflammatory bowel disease? Nat Clin Pract Gastroenterol Hepatol 2:62–63 · DOI
  13. Kahana E (2000) Epidemiologic studies of multiple sclerosis: a review. Biomed Pharmacother 54:100–102 · DOI
  14. Fleming JO, Cook TD (2006) Multiple sclerosis and the hygiene hypothesis. Neurology 67:2085–2086 · DOI
  15. Butterworth AE, Curry AJ, Dunne DW et al (1994) Immunity and morbidity in human schistosomiasis mansoni. Trop Geogr Med 46:197–208
  16. Sewell D, Qing Z, Reinke E et al (2003) Immunomodulation of experimental autoimmune encephalomyelitis by helminth ova immunization. Int Immunol 15:59–69 · DOI
  17. La Flamme AC, Ruddenklau K, Backstrom BT (2003) Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect Immun 71:4996–5004 · DOI
  18. Zheng X, Hu X, Zhou G et al (2008) Soluble egg antigen from Schistosoma japonicum modulates the progression of chronic progressive experimental autoimmune encephalomyelitis via Th2-shift response. J Neuroimmunol 194:107–114 · DOI
  19. Gruden-Movsesijan A, Ilic N, Mostarica-Stojkovic M, Stosic-Grujicic S, Milic M, Sofronic-Milosavljevic L (2008) Trichinella spiralis: modulation of experimental autoimmune encephalomyelitis in DA rats. Exp Parasitol 118:641–647 · DOI
  20. Walsh KP, Brady MT, Finlay CM, Boon L, Mills KH (2009) Infection with a helminth parasite attenuates autoimmunity through TGF-beta-mediated suppression of Th17 and Th1 responses. J Immunol 183:1577–1586 · DOI
  21. Elliott DE, Weinstock JV (2012) Helminth-host immunological interactions: prevention and control of immune-mediated diseases. Ann N Y Acad Sci 1247:83–96 · DOI
  22. Zaccone P, Fehervari Z, Jones FM et al (2003) Schistosoma mansoni antigens modulate the activity of the innate immune response and prevent onset of type 1 diabetes. Eur J Immunol 33:1439–1449 · DOI
  23. Elliott DE, Metwali A, Leung J et al (2008) Colonization with Heligmosomoides polygyrus suppresses mucosal IL-17 production. J Immunol 181:2414–2419 · DOI
  24. Elliott DE, Urban JJ, Argo CK, Weinstock JV (2000) Does the failure to acquire helminthic parasites predispose to Crohn's disease? FASEB J 14:1848–1855 · DOI
  25. Elliott DE, Li J, Blum A et al (2003) Exposure to schistosome eggs protects mice from TNBS-induced colitis. Am J Physiol Gastrointest Liver Physiol 284:G385–G391 · DOI
  26. Kuijk LM, van Die I (2010) Worms to the rescue: can worm glycans protect from autoimmune diseases? IUBMB Life 62:303–312 · DOI
  27. Moreels TG, Nieuwendijk RJ, De Man JG et al (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 · DOI
  28. Ruyssers NE, De Winter BY, De Man JG et al (2009) Therapeutic potential of helminth soluble proteins in TNBS-induced colitis in mice. Inflamm Bowel Dis 15:491–500 · DOI
  29. Ruyssers NE, De Winter BY, De Man JG et al (2010) Schistosoma mansoni proteins attenuate gastrointestinal motility disturbances during experimental colitis in mice. World J Gastroenterol 16:703–712 · DOI
  30. Hunter MM, Wang A, McKay DM (2007) Helminth infection enhances disease in a murine TH2 model of colitis. Gastroenterology 132:1320–1330 · DOI
  31. Smith P, Mangan NE, Walsh CM et al (2007) Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism. J Immunol 178:4557–4566 · DOI
  32. Hsu SJ, Tseng PH, Chen PJ (2005) Trichuris suis therapy for ulcerative colitis: nonresponsive patients may need anti-helminth therapy. Gastroenterology 129:768–769, author reply 9
  33. Croese J, O'Neil J, Masson J et al (2006) A proof of concept study establishing Necator americanus in Crohn's patients and reservoir donors. Gut 55:136–137 · DOI · Paper page
  34. Mortimer K, Brown A, Feary J et al (2006) Dose-ranging study for trials of therapeutic infection with Necator americanus in humans. AmJTrop Med Hyg 75:914–920 · DOI
  35. Correale J, Farez M (2007) Association between parasite infection and immune responses in multiple sclerosis. Ann Neurol 61:97–108 · DOI
  36. Correale J, Farez MF (2011) The impact of parasite infections on the course of multiple sclerosis. J Neuroimmunol 233:6–11 · DOI · Paper page
  37. Correale J, Farez M, Razzitte G (2008) Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann Neurol 64:187–199 · DOI
  38. Aoyama H, Hirata T, Sakugawa H et al (2007) An inverse relationship between autoimmune liver diseases and Strongyloides stercoralis infection. AmJTrop Med Hyg 76:972–976 · DOI
  39. Gause WC, Urban JF Jr, Stadecker MJ (2003) The immune response to parasitic helminths: insights from murine models. Trends Immunol 24:269–277 · DOI
  40. Lammas DA, Casanova JL, Kumararatne DS (2000) Clinical consequences of defects in the IL-12-dependent interferon-gamma (IFN-gamma) pathway. Clin Exp Immunol 121:417–425 · DOI
  41. Krug N, Madden J, Redington AE et al (1996) T-cell cytokine profile evaluated at the single cell level in BAL and blood in allergic asthma. Am J Respir Cell Mol Biol 14:319–326 · DOI
  42. Klunker S, Trautmann A, Akdis M et al (2003) A second step of chemotaxis after transendothelial migration: keratinocytes undergoing apoptosis release IFN-gamma-inducible protein 10, monokine induced by IFN-gamma, and IFN-gamma-inducible alpha-chemoattractant for T cell chemotaxis toward epidermis in atopic dermatitis. J Immunol 171:1078–1084 · DOI
  43. Park H, Li Z, Yang XO et al (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6:1133–1141 · DOI · Paper page
  44. Osada Y, Kanazawa T (2010) Parasitic helminths: new weapons against immunological disorders. J Biomed Biotechnol 2010:1–9 · DOI
  45. Tozawa K, Hanai H, Sugimoto K et al (2003) Evidence for the critical role of interleukin-12 but not interferon-gamma in the pathogenesis of experimental colitis in mice. J Gastroenterol Hepatol 18:578–587 · DOI
  46. Zhang Z, Zheng M, Bindas J, Schwarzenberger P, Kolls JK (2006) Critical role of IL-17 receptor signaling in acute TNBS-induced colitis. Inflamm Bowel Dis 12:382–388 · DOI
  47. Martin-Orozco N, Chung Y, Chang SH, Wang YH, Dong C (2009) Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur J Immunol 39:216–224 · DOI
  48. Harnett MM, Melendez AJ, Harnett W (2010) The therapeutic potential of the filarial nematode-derived immunodulator, ES-62 in inflammatory disease. Clin Exp Immunol 159:256–267 · DOI
  49. Wu Z, Nagano I, Asano K, Takahashi Y (2010) Infection of non-encapsulated species of Trichinella ameliorates experimental autoimmune encephalomyelitis involving suppression of Th17 and Th1 response. Parasitol Res 107:1173–1188 · DOI
  50. Osada Y, Shimizu S, Kumagai T, Yamada S, Kanazawa T (2009) Schistosoma mansoni infection reduces severity of collagen-induced arthritis via down-regulation of pro-inflammatory mediators. Int J Parasitol 39:457–464 · DOI
  51. Mo HM, Liu WQ, Lei JH, Cheng YL, Wang CZ, Li YL (2007) Schistosoma japonicum eggs modulate the activity of CD4+ CD25+ Tregs and prevent development of colitis in mice. Exp Parasitol 116:385–389 · DOI
  52. Zaccone P, Burton OT, Gibbs S et al (2010) Immune modulation by Schistosoma mansoni antigens in NOD mice: effects on both innate and adaptive immune systems. J Biomed Biotechnol 2010:795210 · DOI
  53. Duez C, Gosset P, Tonnel AB (2006) Dendritic cells and toll-like receptors in allergy and asthma. Eur J Dermatol 16:12–16
  54. Kane CM, Cervi L, Sun J et al (2004) Helminth antigens modulate TLR-initiated dendritic cell activation. J Immunol 173:7454–7461 · DOI
  55. Rocha FA, Leite AK, Pompeu MM et al (2008) Protective effect of an extract from Ascaris suum in experimental arthritis models. Infect Immun 76:2736–2745 · DOI

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Metadata

Authors
Ben-Ami Shor, D., Harel, M., Eliakim, R., & Shoenfeld, Y.
Venue
Clinical Reviews in Allergy & Immunology
Publisher
Springer Science and Business Media LLC
Published
2013-01-17
Volume
45
Issue
2
Pages
211-216
ISSN
  • 1080-0549
  • 1559-0267
DOI
10.1007/s12016-012-8352-9
Cited by
57
References
1
Language
en
Licence
www.springer.com/tdm (tdm)

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