About this Journal Submit a Manuscript Table of Contents
Journal of Biomedicine and Biotechnology
Volume 2011 (2011), Article ID 821578, 18 pages
http://dx.doi.org/10.1155/2011/821578
Review Article

Modulation of Specific and Allergy-Related Immune Responses by Helminths

Department of Molecular Parasitology, Humboldt University of Berlin, Philippstraße 13, Building 14, 10115 Berlin, Germany

Received 15 July 2011; Accepted 9 September 2011

Academic Editor: Luis I. Terrazas

Copyright © 2011 Emilia Daniłowicz-Luebert et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. D. Finkelman, T. Shea-Donohue, S. C. Morris et al., “Interleukin-4- and interleukin-13-mediated host protection against intestinal nematode parasites,” Immunological Reviews, vol. 201, pp. 139–155, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. R. M. Anthony, L. I. Rutitzky, J. F. Urban Jr., et al., “Protective immune mechanisms in helminth infection,” Nature Reviews Immunology, vol. 7, no. 12, pp. 975–987, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. R. M. Maizels and M. Yazdanbakhsh, “Immune regulation by helminth parasites: cellular and molecular mechanisms,” Nature Reviews Immunology, vol. 3, no. 9, pp. 733–744, 2003. View at Publisher · View at Google Scholar · View at Scopus
  4. S. J. Jenkins, D. Ruckerl, P. C. Cook et al., “Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation,” Science, vol. 332, no. 6035, pp. 1284–1288, 2011. View at Publisher · View at Google Scholar
  5. J. E. Allen and R. M. Maizels, “Diversity and dialogue in immunity to helminths,” Nature Reviews Immunology, vol. 11, no. 6, pp. 375–388, 2011. View at Publisher · View at Google Scholar
  6. H. H. Smits, B. Everts, F. C. Hartgers, et al., “Chronic helminth infections protect against allergic diseases by active regulatory processes,” Current Allergy and Asthma Reports, vol. 10, no. 1, pp. 3–12, 2010. View at Publisher · View at Google Scholar · View at Scopus
  7. S. P. Patel, M. R. Jarvelin, and M. P. Little, “Systematic review of worldwide variations of the prevalence of wheezing symptoms in children,” Environmental Health, vol. 7, article 57, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. P. G. Fallon and N. E. Mangan, “Suppression of TH2-type allergic reactions by helminth infection,” Nature Reviews Immunology, vol. 7, no. 3, pp. 220–230, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Cooke, “Review series on helminths, immune modulation and the hygiene hypothesis: how might infection modulate the onset of type 1 diabetes?” Immunology, vol. 126, no. 1, pp. 12–17, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. R. M. Maizels, A. Balic, N. Gomez-Escobar, et al., “Helminth parasites-masters of regulation,” Immunological Reviews, vol. 201, pp. 89–116, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. C. L. King and T. B. Nutman, “Regulation of the immune response in lymphatic filariasis and onchocerciasis,” Immunology Today, vol. 12, no. 3, pp. A54–A58, 1991. View at Scopus
  12. E. A. Ottesen, P. F. Weller, and L. Heck, “Specific cellular immune unresponsiveness in human filariasis,” Immunology, vol. 33, no. 3, pp. 413–421, 1977. View at Scopus
  13. P. F. Weller, E. A. Ottesen, L. Heck, et al., “Endemic filariasis on a Pacific island. I. Clinical, epidemiologic, and parasitologic aspects,” American Journal of Tropical Medicine and Hygiene, vol. 31, no. 5, pp. 942–952, 1982. View at Scopus
  14. E. A. Ottesen, “Immunopathology of lymphatic filariasis in man,” Springer Seminars in Immunopathology, vol. 2, no. 4, pp. 373–385, 1980. View at Scopus
  15. E. A. Ottesen and T. B. Nutman, “Tropical pulmonary eosinophilia,” Annual Review of Medicine, vol. 43, pp. 417–424, 1992. View at Scopus
  16. N. W. Brattig, “Pathogenesis and host responses in human onchocerciasis: impact of Onchocerca filariae and Wolbachia endobacteria,” Microbes and Infection, vol. 6, no. 1, pp. 113–128, 2004. View at Publisher · View at Google Scholar · View at Scopus
  17. R. Rigano, B. Buttari, E. Profumo et al., “Echinococcus granulosus antigen B impairs human dendritic cell differentiation and polarizes immature dendritic cell maturation towards a Th2 cell response,” Infection and Immunity, vol. 75, no. 4, pp. 1667–1678, 2007. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Donnelly, S. M. O'Neill, C. M. Stack et al., “Helminth cysteine proteases inhibit TRIF-dependent activation of macrophages via degradation of TLR3,” Journal of Biological Chemistry, vol. 285, no. 5, pp. 3383–3392, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. D. van der Kleij, E. Latz, J. F. Brouwers, et al., “A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization,” Journal of Biological Chemistry, vol. 277, no. 50, pp. 48122–48129, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. E. van Riet, B. Everts, K. Retra et al., “Combined TLR2 and TLR4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlates for Th1/Th2 polarization,” BMC Immunology, vol. 10, article 9, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. E. Aksoy, C. S. Zouain, F. Vanhoutte, et al., “Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells,” Journal of Biological Chemistry, vol. 280, no. 1, pp. 277–283, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. F. Vanhoutte, L. Breuilh, J. Fontaine et al., “Toll-like receptor (TLR)2 and TLR3 sensing is required for dendritic cell activation, but dispensable to control Schistosoma mansoni infection and pathology,” Microbes and Infection, vol. 9, no. 14-15, pp. 1606–1613, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Steinfelder, J. F. Andersen, J. L. Cannons et al., “The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1),” Journal of Experimental Medicine, vol. 206, no. 8, pp. 1681–1690, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. B. Everts, G. Perona-Wright, H. H. Smits et al., “Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses,” Journal of Experimental Medicine, vol. 206, no. 8, pp. 1673–1680, 2009. View at Publisher · View at Google Scholar · View at Scopus
  25. P. Zaccone, O. T. Burton, S. E. Gibbs, et al., “The S. mansoni glycoprotein omega-1 induces Foxp3 expression in NOD mouse CD4(+) T cells,” European Journal of Immunology, vol. 41, no. 9, pp. 2709–2718, 2011. View at Publisher · View at Google Scholar
  26. G. Schramm, K. Mohrs, M. Wodrich et al., “Cutting edge: IPSE/alpha-1, a glycoprotein from Schistosoma mansoni eggs, induces IgE-dependent, antigen-independent IL-4 production by murine basophils in vivo,” Journal of Immunology, vol. 178, no. 10, pp. 6023–6027, 2007. View at Scopus
  27. P. Smith, R. E. Fallon, N. E. Mangan et al., “Schistosoma mansoni secretes a chemokine binding protein with antiinflammatory activity,” Journal of Experimental Medicine, vol. 202, no. 10, pp. 1319–1325, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. T. M. Oshiro, M. S. Macedo, and M. F. Macedo-Soares, “Anti-inflammatory activity of PAS-1, a protein component of Ascaris suum,” Inflammation Research, vol. 54, no. 1, pp. 17–21, 2005. View at Publisher · View at Google Scholar · View at Scopus
  29. M. A. Bower, S. L. Constant, and S. Mendez, “Necator americanus the Na-ASP-2 protein secreted by the infective larvae induces neutrophil recruitment in vivo and in vitro,” Experimental Parasitology, vol. 118, no. 4, pp. 569–575, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. F. J. Culley, A. Brown, D. M. Conroy, I. Sabroe, D. I. Pritchard, and T. J. Williams, “Eotaxin is specifically cleaved by hookworm metalloproteases preventing its action in vitro and in vivo,” Journal of Immunology, vol. 165, no. 11, pp. 6447–6453, 2000. View at Scopus
  31. M. E. Grigg, K. Gounaris, and M. E. Selkirk, “Characterization of a platelet-activating factor acetylhydrolase secreted by the nematode parasite Nippostrongylus brasiliensis,” Biochemical Journal, vol. 317, no. 2, pp. 541–547, 1996. View at Scopus
  32. T. H. Tan, S. A. Edgerton, R. Kumari et al., “Macrophage migration inhibitory factor of the parasitic nematode Trichinella spiralis,” Biochemical Journal, vol. 357, no. 2, pp. 373–383, 2001. View at Publisher · View at Google Scholar · View at Scopus
  33. R. K. Grencis and G. M. Entwistle, “Production of an interferon-gamma homologue by an intestinal nematode: functionally significant or interesting artefact?” Parasitology, vol. 115, supplement, pp. S101–S106, 1997.
  34. S. Hartmann, B. Kyewski, B. Sonnenburg, and R. Lucius, “A filarial cysteine protease inhibitor down-regulates T cell proliferation and enhances interleukin-10 production,” European Journal of Immunology, vol. 27, no. 9, pp. 2253–2260, 1997. View at Publisher · View at Google Scholar · View at Scopus
  35. C. Klotz, T. Ziegler, A. S. Figueiredo et al., “A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages,” PLoS Pathogens, vol. 7, no. 1, article e1001248, 2011. View at Publisher · View at Google Scholar
  36. F. A. Marshall, A. M. Grierson, P. Garside, et al., “ES-62, an immunomodulator secreted by filarial nematodes, suppresses clonal expansion and modifies effector function of heterologous antigen-specific T cells in vivo,” Journal of Immunology, vol. 175, no. 9, pp. 5817–5826, 2005. View at Scopus
  37. H. S. Goodridge, E. H. Wilson, W. Harnett, et al., “Modulation of macrophage cytokine production by ES-62, a secreted product of the filarial nematode Acanthocheilonema viteae,” Journal of Immunology, vol. 167, no. 2, pp. 940–945, 2001. View at Scopus
  38. H. S. Goodridge, F. A. Marshall, K. J. Else et al., “Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62,” Journal of Immunology, vol. 174, no. 1, pp. 284–293, 2005. View at Scopus
  39. H. S. Goodridge, F. A. Marshall, E. H. Wilson et al., “In vivo exposure of murine dendritic cell and macrophage bone marrow progenitors to the phosphorylcholine-containing filarial nematode glycoprotein ES-62 polarizes their differentiation to an anti-inflammatory phenotype,” Immunology, vol. 113, no. 4, pp. 491–498, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. N. Gomez-Escobar, C. Bennett, L. Prieto-Lafuente, et al., “Heterologous expression of the filarial nematode alt gene products reveals their potential to inhibit immune function,” BMC Biology, vol. 3, article 8, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. B. Manoury, W. F. Gregory, R. M. Maizels, et al., “Bm-CPI-2, a cystatin homolog secreted by the filarial parasite Brugia malayi, inhibits class II MHC-restricted antigen processing,” Current Biology, vol. 11, no. 6, pp. 447–451, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. J. Murray, B. Manoury, A. Balic, et al., “Bm-CPI-2, a cystatin from Brugia malayi nematode parasites, differs from Caenorhabditis elegans cystatins in a specific site mediating inhibition of the antigen-processing enzyme AEP,” Molecular and Biochemical Parasitology, vol. 139, no. 2, pp. 197–203, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. N. Gomez-Escobar, W. F. Gregory, and R. M. Maizels, “Identification of tgh-2, a filarial nematode homolog of Caenorhabditis elegans daf-7 and human transforming growth factor β, expressed in microfilarial and adult stages of Brugia malayi,” Infection and Immunity, vol. 68, no. 11, pp. 6402–6410, 2000. View at Publisher · View at Google Scholar · View at Scopus
  44. A. W. Pfaff, H. Schulz-Key, P. T. Soboslay, et al., “Litomosoides sigmodontis cystatin acts as an immunomodulator during experimental filariasis,” International Journal for Parasitology, vol. 32, no. 2, pp. 171–178, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. A. Schönemeyer, R. Lucius, B. Sonnenburg et al., “Modulation of human T cell responses and macrophage functions by onchocystatin, a secreted protein of the filarial nematode Onchocerca volvulus,” Journal of Immunology, vol. 167, no. 6, pp. 3207–3215, 2001. View at Scopus
  46. S. Lustigman, B. Brotman, T. Huima, et al., “Molecular cloning and characterization of onchocystatin, a cysteine proteinase inhibitor of Onchocerca volvulus,” Journal of Biological Chemistry, vol. 267, no. 24, pp. 17339–17346, 1992. View at Scopus
  47. S. Babu, S. Q. Bhat, N. P. Kumar et al., “Attenuation of toll-like receptor expression and function in latent tuberculosis by coexistent filarial infection with restoration following antifilarial chemotherapy,” PLoS Neglected Tropical Diseases, vol. 3, no. 7, article e489, 2009. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Metenou, B. Dembele, S. Konate et al., “Filarial infection suppresses malaria-specific multifunctional Th1 and Th17 responses in malaria and filarial coinfections,” Journal of Immunology, vol. 186, no. 8, pp. 4725–4733, 2011. View at Publisher · View at Google Scholar
  49. P. J. Cooper, M. Chico, C. Sandoval, et al., “Human infection with Ascaris lumbricoides is associated with suppression of the interleukin-2 response to recombinant cholera toxin B subunit following vaccination with the live oral cholera vaccine CVD 103-HgR,” Infection and Immunity, vol. 69, no. 3, pp. 1574–1580, 2001. View at Publisher · View at Google Scholar · View at Scopus
  50. D. P. Strachan, “Hay fever, hygiene, and household size,” British Medical Journal, vol. 299, no. 6710, pp. 1259–1260, 1989. View at Scopus
  51. M. Yazdanbakhsh, P. G. Kremsner, and R. van Ree, “Allergy, parasites, and the hygiene hypothesis,” Science, vol. 296, no. 5567, pp. 490–494, 2002. View at Publisher · View at Google Scholar · View at Scopus
  52. C. Flohr, R. J. Quinnell, and J. Britton, “Do helminth parasites protect against atopy and allergic disease?” Clinical and Experimental Allergy, vol. 39, no. 1, pp. 20–32, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. A. H. van den Biggelaar, R. van Ree, L. C. Rodrigues et al., “Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10,” Lancet, vol. 356, no. 9243, pp. 1723–1727, 2000. View at Scopus
  54. M. I. Araujo, A. A. Lopes, M. Medeiros et al., “Inverse association between skin response to aeroallergens and Schistosoma mansoni infection,” International Archives of Allergy and Immunology, vol. 123, no. 2, pp. 145–148, 2000. View at Scopus
  55. M. Medeiros Jr., J. P. Figueiredo, M. C. Almeida, et al., “Schistosoma mansoni infection is associated with a reduced course of asthma,” Journal of Allergy and Clinical Immunology, vol. 111, no. 5, pp. 947–951, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. P. J. Cooper, M. E. Chico, L. C. Rodrigues et al., “Reduced risk of atopy among school-age children infected with geohelminth parasites in a rural area of the tropics,” Journal of Allergy and Clinical Immunology, vol. 111, no. 5, pp. 995–1000, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. S. Scrivener, H. Yemaneberhan, M. Zebenigus et al., “Independent effects of intestinal parasite infection and domestic allergen exposure on risk of wheeze in Ethiopia: s nested case-control study,” Lancet, vol. 358, no. 9292, pp. 1493–1499, 2001. View at Publisher · View at Google Scholar · View at Scopus
  58. O. A. Nyan, G. E. Walraven, W. A. Banya et al., “Atopy, intestinal helminth infection and total serum IgE in rural and urban adult Gambian communities,” Clinical and Experimental Allergy, vol. 31, no. 11, pp. 1672–1678, 2001. View at Publisher · View at Google Scholar · View at Scopus
  59. A. H. van den Biggelaar, L. C. Rodrigues, R. van Ree, et al., “Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren,” Journal of Infectious Diseases, vol. 189, no. 5, pp. 892–900, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. N. R. Lynch, I. Hagel, M. Perez, et al., “Effect of anthelmintic treatment on the allergic reactivity of children in a tropical slum,” Journal of Allergy and Clinical Immunology, vol. 92, no. 3, pp. 404–411, 1993. View at Scopus
  61. C. Flohr, L. N. Tuyen, R. J. Quinnell et al., “Reduced helminth burden increases allergen skin sensitization but not clinical allergy: a randomized, double-blind, placebo-controlled trial in Vietnam,” Clinical and Experimental Allergy, vol. 40, no. 1, pp. 131–142, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Endara, M. Vaca, M. E. Chico, et al., “Long-term periodic anthelmintic treatments are associated with increased allergen skin reactivity,” Clinical and Experimental Allergy, vol. 40, no. 11, pp. 1669–1677, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. L. C. Rodrigues, P. J. Newcombe, S. S. Cunha et al., “Early infection with Trichuris trichiura and allergen skin test reactivity in later childhood,” Clinical and Experimental Allergy, vol. 38, no. 11, pp. 1769–1777, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. S. L. Huang, P. F. Tsai, and Y. F. Yeh, “Negative association of Enterobius infestation with asthma and rhinitis in primary school children in Taipei,” Clinical and Experimental Allergy, vol. 32, no. 7, pp. 1029–1032, 2002. View at Publisher · View at Google Scholar · View at Scopus
  65. L. S. Cardoso, S. C. Oliveira, A. M. Goes et al., “Schistosoma mansoni antigens modulate the allergic response in a murine model of ovalbumin-induced airway inflammation,” Clinical and Experimental Immunology, vol. 160, no. 2, pp. 266–274, 2010. View at Publisher · View at Google Scholar · View at Scopus
  66. S. K. Park, M. K. Cho, H. K. Park, et al., “Macrophage migration inhibitory factor homologs of Anisakis simplex suppress Th2 response in allergic airway inflammation model via CD4 +CD25+Foxp3+ T cell recruitment,” Journal of Immunology, vol. 182, no. 11, pp. 6907–6914, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. D. M. Itami, T. M. Oshiro, C. A. Araujo, et al., “Modulation of murine experimental asthma by Ascaris suum components,” Clinical and Experimental Allergy, vol. 35, no. 7, pp. 873–879, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. C. A. Araujo, A. Perini, M. A. Martins, et al., “PAS-1, a protein from Ascaris suum, modulates allergic inflammation via IL-10 and IFN-γ, but not IL-12,” Cytokine, vol. 44, no. 3, pp. 335–341, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. C. A. de Araujo, A. Perini, M. A. Martins, et al., “PAS-1, an Ascaris suum protein, modulates allergic airway inflammation via CD8+ γδTCR+ and CD4+ CD25+ FoxP3+ T Cells,” Scandinavian Journal of Immunology, vol. 72, no. 6, pp. 491–503, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. T. Dainichi, Y. Maekawa, K. Ishii et al., “Nippocystatin, a cysteine protease inhibitor from Nippostrongylus brasiliensis, inhibits antigen processing and modulates antigen-specific immune response,” Infection and Immunity, vol. 69, no. 12, pp. 7380–7386, 2001. View at Publisher · View at Google Scholar · View at Scopus
  71. C. Schnoeller, S. Rausch, S. Pillai et al., “A helminth immunomodulator reduces allergic and inflammatory responses by induction of IL-10-producing macrophages,” Journal of Immunology, vol. 180, no. 6, pp. 4265–4272, 2008. View at Scopus
  72. A. J. Melendez, M. M. Harnett, P. N. Pushparaj et al., “Inhibition of FcεRI-mediated mast cell responses by ES-62, a product of parasitic filarial nematodes,” Nature Medicine, vol. 13, no. 11, pp. 1375–1381, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. N. E. Mangan, R. E. Fallon, P. Smith, et al., “Helminth infection protects mice from anaphylaxis via IL-10-producing B cells,” Journal of Immunology, vol. 173, no. 10, pp. 6346–6356, 2004. View at Scopus
  74. N. E. Mangan, N. Van Rooijen, A. N. McKenzie, et al., “Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness,” Journal of Immunology, vol. 176, no. 1, pp. 138–147, 2006. View at Scopus
  75. L. G. Pacifico, F. A. Marinho, C. T. Fonseca et al., “Schistosoma mansoni antigens modulate experimental allergic asthma in a murine model: a major role for CD4+ CD25+ Foxp3 + T cells independent of interleukin-10,” Infection and Immunity, vol. 77, no. 1, pp. 98–107, 2009. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Yang, J. Zhao, Y. Yang et al., “Schistosoma japonicum egg antigens stimulate CD4+ CD25 + T cells and modulate airway inflammation in a murine model of asthma,” Immunology, vol. 120, no. 1, pp. 8–18, 2007. View at Publisher · View at Google Scholar · View at Scopus
  77. C. Lima, A. Perini, M. L. Garcia, et al., “Eosinophilic inflammation and airway hyper-responsiveness are profoundly inhibited by a helminth (Ascaris suum) extract in a murine model of asthma,” Clinical and Experimental Allergy, vol. 32, no. 11, pp. 1659–1666, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. K. Kitagaki, T. R. Businga, D. Racila, et al., “Intestinal helminths protect in a murine model of asthma,” Journal of Immunology, vol. 177, no. 3, pp. 1628–1635, 2006. View at Scopus
  79. M. S. Wilson, M. D. Taylor, A. Balic, et al., “Suppression of allergic airway inflammation by helminth-induced regulatory T cells,” Journal of Experimental Medicine, vol. 202, no. 9, pp. 1199–1212, 2005. View at Publisher · View at Google Scholar · View at Scopus
  80. M. S. Wilson, M. D. Taylor, M. T. O'Gorman, et al., “Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation,” European Journal of Immunology, vol. 40, no. 6, pp. 1682–1696, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. M. E. Bashir, P. Andersen, I. J. Fuss, et al., “An enteric helminth infection protects against an allergic response to dietary antigen,” Journal of Immunology, vol. 169, no. 6, pp. 3284–3292, 2002. View at Scopus
  82. J. R. Grainger, K. A. Smith, J. P. Hewitson, et al., “Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway,” Journal of Experimental Medicine, vol. 207, no. 11, pp. 2331–2341, 2010. View at Publisher · View at Google Scholar · View at Scopus
  83. G. Wohlleben, C. Trujillo, J. Muller, et al., “Helminth infection modulates the development of allergen-induced airway inflammation,” International Immunology, vol. 16, no. 4, pp. 585–596, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. C. M. Trujillo-Vargas, M. Werner-Klein, G. Wohlleben et al., “Helminth-derived products inhibit the development of allergic responses in mice,” American Journal of Respiratory and Critical Care Medicine, vol. 175, no. 4, pp. 336–344, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. C. C. Wang, T. J. Nolan, G. A. Schad, and D. Abraham, “Infection of mice with the helminth Strongyloides stercoralis suppresses pulmonary allergic responses to ovalbumin,” Clinical and Experimental Allergy, vol. 31, no. 3, pp. 495–503, 2001. View at Publisher · View at Google Scholar · View at Scopus
  86. D. Negrão-Corrêa, M. R. Silveira, C. M. Borges, et al., “Changes in pulmonary function and parasite burden in rats infected with Strongyloides venezuelensis concomitant with induction of allergic airway inflammation,” Infection and Immunity, vol. 71, no. 5, pp. 2607–2614, 2003. View at Publisher · View at Google Scholar · View at Scopus
  87. H. K. Park, M. K. Cho, S. H. Choi, et al., “Trichinella spiralis: infection reduces airway allergic inflammation in mice,” Experimental Parasitology, vol. 127, no. 2, pp. 539–544, 2011. View at Publisher · View at Google Scholar
  88. A. M. Dittrich, A. Erbacher, S. Specht et al., “Helminth infection with Litomosoides sigmodontis induces regulatory T cells and inhibits allergic sensitization, airway inflammation, and hyperreactivity in a murine asthma model,” Journal of Immunology, vol. 180, no. 3, pp. 1792–1799, 2008. View at Scopus
  89. U. Herz, A. Braun, R. Ruckert, et al., “Various immunological phenotypes are associated with increased airway responsiveness,” Clinical and Experimental Allergy, vol. 28, no. 5, pp. 625–634, 1998. View at Publisher · View at Google Scholar · View at Scopus
  90. A. M. Dittrich, M. Krokowski, H. A. Meyer, et al., “Lipocalin2 protects against airway inflammation and hyperresponsiveness in a murine model of allergic airway disease,” Clinical and Experimental Allergy, vol. 40, no. 11, pp. 1689–1700, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. M. J. Makela, A. Kanehiro, L. Borish et al., “IL-10 is necessary for the expression of airway hyperresponsiveness but not pulmonary inflammation after allergic sensitization,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 11, pp. 6007–6012, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. E. Hamelmann, K. Tadeda, A. Oshiba, et al., “Role of IgE in the development of allergic airway inflammation and airway hyperresponsiveness—a murine model,” Allergy, vol. 54, no. 4, pp. 297–305, 1999. View at Publisher · View at Google Scholar · View at Scopus
  93. E. Hamelmann, U. Wahn, and E. W. Gelfand, “Role of the Th2 cytokines in the development of allergen-induced airway inflammation and hyperresponsiveness,” International Archives of Allergy and Immunology, vol. 118, no. 2-4, pp. 90–94, 1999. View at Scopus
  94. A. Heinzmann, X. Q. Mao, M. Akaiwa et al., “Genetic variants of IL-13 signalling and human asthma and atopy,” Human Molecular Genetics, vol. 9, no. 4, pp. 549–559, 2000. View at Scopus
  95. K. Arima, R. Umeshita-Suyama, Y. Sakata et al., “Upregulation of IL-13 concentration in vivo by the IL13 variant associated with bronchial asthma,” Journal of Allergy and Clinical Immunology, vol. 109, no. 6, pp. 980–987, 2002. View at Publisher · View at Google Scholar · View at Scopus
  96. P. S. Gao, N. M. Heller, W. Walker et al., “Variation in dinucleotide (GT) repeat sequence in the first exon of the STAT6 gene is associated with atopic asthma and differentially regulates the promoter activity in vitro,” Journal of Medical Genetics, vol. 41, no. 7, pp. 535–539, 2004. View at Scopus
  97. K. Tamura, H. Arakawa, M. Suzuki, et al., “Novel dinucleotide repeat polymorphism in the first exon of the STAT-6 gene is associated with allergic diseases,” Clinical and Experimental Allergy, vol. 31, no. 10, pp. 1509–1514, 2001. View at Publisher · View at Google Scholar · View at Scopus
  98. C. V. Scirica and J. C. Celedon, “Genetics of asthma potential implications for reducing asthma disparities,” Chest, vol. 132, supplement 5, pp. 770S–781S, 2007. View at Publisher · View at Google Scholar
  99. K. C. Barnes, A. V. Grant, N. N. Hansel, et al., “African Americans with asthma: genetic insights,” Proceedings of the American Thoracic Society, vol. 4, no. 1, pp. 58–68, 2007. View at Publisher · View at Google Scholar · View at Scopus
  100. J. R. Joubert, D. J. van Schalkwyk, and K. J. Turner, “Ascaris lumbricoides and the human immunogenetic response. Enhanced IgE-mediated reactivity to common inhaled allergens,” South African Medical Journal, vol. 57, no. 11, pp. 409–412, 1980. View at Scopus
  101. S. Dold, J. Heinrich, H. E. Wichmann, et al., “Ascaris-specific IgE and allergic sensitization in a cohort of school children in the former East Germany,” Journal of Allergy and Clinical Immunology, vol. 102, no. 3, pp. 414–420, 1998. View at Scopus
  102. L. J. Palmer, J. C. Celedon, S. T. Weiss, et al., “Ascaris lumbricoides infection is associated with increased risk of childhood asthma and atopy in rural China,” American Journal of Respiratory and Critical Care Medicine, vol. 165, no. 11, pp. 1489–1493, 2002. View at Publisher · View at Google Scholar · View at Scopus
  103. J. Leonardi-Bee, D. Pritchard, and J. Britton, “Asthma and current intestinal parasite infection: systematic review and meta-analysis,” American Journal of Respiratory and Critical Care Medicine, vol. 174, no. 5, pp. 514–523, 2006. View at Publisher · View at Google Scholar · View at Scopus
  104. H. Takeuchi, K. Zaman, J. Takahashi et al., “High titre of anti-Ascaris immunoglobulin E associated with bronchial asthma symptoms in 5-year-old rural Bangladeshi children,” Clinical and Experimental Allergy, vol. 38, no. 2, pp. 276–282, 2008. View at Publisher · View at Google Scholar · View at Scopus
  105. I. Hagel, M. Cabrera, M. A. Hurtado et al., “Infection by Ascaris lumbricoides and bronchial hyper reactivity: an outstanding association in Venezuelan school children from endemic areas,” Acta Tropica, vol. 103, no. 3, pp. 231–241, 2007. View at Publisher · View at Google Scholar · View at Scopus
  106. N. M. Alcantara-Neves, S. J. Badaro, M. C. dos Santos, et al., “The presence of serum anti-Ascaris lumbricoides IgE antibodies and of Trichuris trichiura infection are risk factors for wheezing and/or atopy in preschool-aged Brazilian children,” Respiratory Research, vol. 11, p. 114, 2010. View at Publisher · View at Google Scholar
  107. C. S. Enobe, C. A. Araujo, A. Perini, et al., “Early stages of Ascaris suum induce airway inflammation and hyperreactivity in a mouse model,” Parasite Immunology, vol. 28, no. 9, pp. 453–461, 2006. View at Publisher · View at Google Scholar · View at Scopus
  108. N. Acevedo and L. Caraballo, “IgE cross-reactivity between Ascaris lumbricoides and mite allergens: possible influences on allergic sensitization and asthma,” Parasite Immunology, vol. 33, no. 6, pp. 309–321, 2011. View at Publisher · View at Google Scholar
  109. G. Reese, R. Ayuso, and S. B. Lehrer, “Tropomyosin: an invertebrate pan-allergen,” International Archives of Allergy and Immunology, vol. 119, no. 4, pp. 247–258, 1999. View at Publisher · View at Google Scholar · View at Scopus
  110. N. Acevedo, J. Sanchez, A. Erler et al., “IgE cross-reactivity between Ascaris and domestic mite allergens: the role of tropomyosin and the nematode polyprotein ABA-1,” Allergy, vol. 64, no. 11, pp. 1635–1643, 2009. View at Publisher · View at Google Scholar · View at Scopus
  111. N. Acevedo, A. Erler, P. Briza, et al., “Allergenicity of Ascaris lumbricoides tropomyosin and IgE sensitization among asthmatic patients in a tropical environment,” International Archives of Allergy and Immunology, vol. 154, no. 3, pp. 195–206, 2010. View at Publisher · View at Google Scholar · View at Scopus
  112. A. Gonzalez-Quintela, F. Gude, J. Campos, et al., “Toxocara infection seroprevalence and its relationship with atopic features in a general adult population,” International Archives of Allergy and Immunology, vol. 139, no. 4, pp. 317–324, 2006. View at Publisher · View at Google Scholar · View at Scopus
  113. O. Barbuzza, F. Guarneri, G. Galtieri, et al., “Protein contact dermatitis and allergic asthma caused by Anisakis simplex,” Contact Dermatitis, vol. 60, no. 4, pp. 239–240, 2009. View at Publisher · View at Google Scholar · View at Scopus
  114. A. Daschner, C. Cuellar, and A. Valls, “Towards a differential definition of atopy: Anisakis simplex and the relationship between parasites and arthropods in respiratory allergy,” Parasite Immunology, vol. 30, no. 8, pp. 417–424, 2008. View at Publisher · View at Google Scholar · View at Scopus
  115. A. Daschner, C. De Frutos, A. Valls, et al., “Anisakis simplex sensitization-associated urticaria: short-lived immediate type or prolonged acute urticaria,” Archives of Dermatological Research, vol. 302, no. 8, pp. 625–629, 2010. View at Publisher · View at Google Scholar · View at Scopus
  116. E. Sartono, Y. C. Kruize, A. Kurniawan et al., “Elevated cellular immune responses and interferon-γ release after long- term diethylcarbamazine treatment of patients with human lymphatic filariasis,” Journal of Infectious Diseases, vol. 171, no. 6, pp. 1683–1687, 1995. View at Scopus
  117. A. A. Da'dara and D. A. Harn, “Elimination of helminth infection restores HIV-1C vaccine-specific T cell responses independent of helminth-induced IL-10,” Vaccine, vol. 28, no. 5, pp. 1310–1317, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. D. Elias, D. Wolday, H. Akuffo, et al., “Effect of deworming on human T cell responses to mycobacterial antigens in helminth-exposed individuals before and after bacille Calmette-Guerin (BCG) vaccination,” Clinical and Experimental Immunology, vol. 123, no. 2, pp. 219–225, 2001. View at Publisher · View at Google Scholar · View at Scopus
  119. A. Balic, Y. Harcus, M. J. Holland, et al., “Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses,” European Journal of Immunology, vol. 34, no. 11, pp. 3047–3059, 2004. View at Publisher · View at Google Scholar · View at Scopus
  120. M. Segura, Z. Su, C. Piccirillo, et al., “Impairment of dendritic cell function by excretory-secretory products: a potential mechanism for nematode-induced immunosuppression,” European Journal of Immunology, vol. 37, no. 7, pp. 1887–1904, 2007. View at Publisher · View at Google Scholar · View at Scopus
  121. R. T. Semnani, H. Sabzevari, R. Iyer, et al., “Filarial antigens impair the function of human dendritic cells during differentiation,” Infection and Immunity, vol. 69, no. 9, pp. 5813–5822, 2001. View at Publisher · View at Google Scholar · View at Scopus
  122. R. T. Semnani, P. G. Venugopal, C. A. Leifer, et al., “Inhibition of TLR3 and TLR4 function and expression in human dendritic cells by helminth parasites,” Blood, vol. 112, no. 4, pp. 1290–1298, 2008. View at Publisher · View at Google Scholar · View at Scopus
  123. C. A. Terrazas, L. I. Terrazas, and L. Gomez-Garcia, “Modulation of dendritic cell responses by parasites: a common strategy to survive,” Journal of Biomedicine & Biotechnology, vol. 2010, Article ID 357106, 19 pages, 2010. View at Scopus
  124. L. Carvalho, J. Sun, C. Kane, et al., “Review series on helminths, immune modulation and the hygiene hypothesis: mechanisms underlying helminth modulation of dendritic cell function,” Immunology, vol. 126, no. 1, pp. 28–34, 2009. View at Publisher · View at Google Scholar · View at Scopus
  125. R. T. Semnani, A. Y. Liu, H. Sabzevari et al., “Brugia malayi microfilariae induce cell death in human dendritic cells, inhibit their ability to make IL-12 and IL-10, and reduce their capacity to activate CD4+ T cells,” Journal of Immunology, vol. 171, no. 4, pp. 1950–1960, 2003. View at Scopus
  126. J. C. Massacand, R. C. Stettler, R. Meier, et al., “Helminth products bypass the need for TSLP in Th2 immune responses by directly modulating dendritic cell function,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 33, pp. 13968–13973, 2009. View at Publisher · View at Google Scholar · View at Scopus
  127. C. A. Terrazas, L. Gomez-Garcia, and L. I. Terrazas, “Impaired pro-inflammatory cytokine production and increased Th2-biasing ability of dendritic cells exposed to Taenia excreted/secreted antigens: a critical role for carbohydrates but not for STAT6 signaling,” International Journal for Parasitology, vol. 40, no. 9, pp. 1051–1062, 2010. View at Publisher · View at Google Scholar · View at Scopus
  128. D. J. Dowling, C. M. Noone, P. N. Adams et al., “Ascaris lumbricoides pseudocoelomic body fluid induces a partially activated dendritic cell phenotype with Th2 promoting ability in vivo,” International Journal for Parasitology, vol. 41, no. 2, pp. 255–261, 2010. View at Publisher · View at Google Scholar · View at Scopus
  129. K. A. Smith, K. Hochweller, G. J. Hammerling, et al., “Chronic helminth infection promotes immune regulation in vivo through dominance of CD11cloCD103- dendritic cells,” Journal of Immunology, vol. 186, no. 12, pp. 7098–7109, 2011. View at Publisher · View at Google Scholar
  130. A. T. Phythian-Adams, P. C. Cook, R. J. Lundie et al., “CD11c depletion severely disrupts Th2 induction and development in vivo,” Journal of Experimental Medicine, vol. 207, no. 10, pp. 2089–2096, 2010. View at Publisher · View at Google Scholar · View at Scopus
  131. A. Hoerauf, J. Satoguina, M. Saeftel, et al., “Immunomodulation by filarial nematodes,” Parasite Immunology, vol. 27, no. 10-11, pp. 417–429, 2005. View at Publisher · View at Google Scholar · View at Scopus
  132. S. Gordon and F. O. Martinez, “Alternative activation of macrophages: mechanism and functions,” Immunity, vol. 32, no. 5, pp. 593–604, 2010. View at Publisher · View at Google Scholar · View at Scopus
  133. J. L. Reyes and L. I. Terrazas, “The divergent roles of alternatively activated macrophages in helminthic infections,” Parasite Immunology, vol. 29, no. 12, pp. 609–619, 2007. View at Publisher · View at Google Scholar · View at Scopus
  134. J. T. Pesce, T. R. Ramalingam, M. M. Mentink-Kane, et al., “Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis,” PLoS Pathogens, vol. 5, no. 4, Article ID e1000371, 2009. View at Publisher · View at Google Scholar · View at Scopus
  135. P. Loke, A. S. MacDonald, and J. E. Allen, “Antigen-presenting cells recruited by Brugia malayi induce Th2 differentiation of naive CD4(+) T cells,” European Journal of Immunology, vol. 30, no. 4, pp. 1127–1135, 2000. View at Publisher · View at Google Scholar · View at Scopus
  136. S. Babu, V. Kumaraswami, and T. B. Nutman, “Alternatively activated and immunoregulatory monocytes in human filarial infections,” Journal of Infectious Diseases, vol. 199, no. 12, pp. 1827–1837, 2009. View at Publisher · View at Google Scholar · View at Scopus
  137. D. M. Mosser and J. P. Edwards, “Exploring the full spectrum of macrophage activation,” Nature Reviews Immunology, vol. 8, no. 12, pp. 958–969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  138. M. Munder, F. Mollinedo, J. Calafat, et al., “Arginase I is constitutively expressed in human granulocytes and participates in fungicidal activity,” Blood, vol. 105, no. 6, pp. 2549–2556, 2005. View at Publisher · View at Google Scholar · View at Scopus
  139. G. Raes, R. Van Den Bergh, P. De Baetselier et al., “Arginase-1 and Ym1 are markers for murine, but not human, alternatively activated myeloid cells,” Journal of Immunology, vol. 174, no. 11, pp. 6561–6562, 2005. View at Scopus
  140. J. E. Allen, R. A. Lawrence, and R. M. Maizels, “APC from mice harbouring the filarial nematode, Brugia malayi, prevent cellular proliferation but not cytokine production,” International Immunology, vol. 8, no. 1, pp. 143–151, 1996. View at Publisher · View at Google Scholar · View at Scopus
  141. P. Loke, A. S. MacDonald, A. Robb, et al., “Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact,” European Journal of Immunology, vol. 30, no. 9, pp. 2669–2678, 2000. View at Publisher · View at Google Scholar · View at Scopus
  142. D. R. Herbert, T. Orekov, A. Roloson, et al., “Arginase I suppresses IL-12/IL-23p40-driven intestinal inflammation during acute schistosomiasis,” Journal of Immunology, vol. 184, no. 11, pp. 6438–6446, 2010. View at Publisher · View at Google Scholar · View at Scopus
  143. A. Zhao, J. F. Urban Jr., R. M. Anthony, et al., “Th2 cytokine-induced alterations in intestinal smooth muscle function depend on alternatively activated macrophages,” Gastroenterology, vol. 135, no. 1, article e211, pp. 217–225, 2008. View at Publisher · View at Google Scholar · View at Scopus
  144. M. G. Nair, Y. Du, J. G. Perrigoue et al., “Alternatively activated macrophage-derived RELM-α is a negative regulator of type 2 inflammation in the lung,” Journal of Experimental Medicine, vol. 206, no. 4, pp. 937–952, 2009. View at Publisher · View at Google Scholar · View at Scopus
  145. J. T. Pesce, T. R. Ramalingam, M. S. Wilson, et al., “Retnla (relmalpha/fizz1) suppresses helminth-induced Th2-type immunity,” PLoS Pathogens, vol. 5, no. 4, Article ID e1000393, 2009. View at Publisher · View at Google Scholar · View at Scopus
  146. M. S. Wilson and R. M. Maizels, “Regulatory T cells induced by parasites and the modulation of allergic responses,” Chemical Immunology and Allergy, vol. 90, pp. 176–195, 2006. View at Scopus
  147. K. J. Else, “Have gastrointestinal nematodes outwitted the immune system?” Parasite Immunology, vol. 27, no. 10-11, pp. 407–415, 2005. View at Publisher · View at Google Scholar · View at Scopus
  148. M. Hesse, C. A. Piccirillo, Y. Belkaid et al., “The pathogenesis of schistosomiasis is controlled by cooperating IL-10-producing innate effector and regulatory T cells,” Journal of Immunology, vol. 172, no. 5, pp. 3157–3166, 2004. View at Scopus
  149. A. S. McKee and E. J. Pearce, “CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development,” Journal of Immunology, vol. 173, no. 2, pp. 1224–1231, 2004. View at Scopus
  150. J. J. Taylor, M. Mohrs, and E. J. Pearce, “Regulatory T cell responses develop in parallel to Th responses and control the magnitude and phenotype of the Th effector population,” Journal of Immunology, vol. 176, no. 10, pp. 5839–5847, 2006. View at Scopus
  151. S. Metenou, B. Dembele, S. Konate et al., “At homeostasis filarial infections have expanded adaptive T regulatory but not classical Th2 cells,” Journal of Immunology, vol. 184, no. 9, pp. 5375–5382, 2010. View at Publisher · View at Google Scholar · View at Scopus
  152. S. Rausch, J. Huehn, D. Kirchhoff et al., “Functional analysis of effector and regulatory T cells in a parasitic nematode infection,” Infection and Immunity, vol. 76, no. 5, pp. 1908–1919, 2008. View at Publisher · View at Google Scholar · View at Scopus
  153. S. Rausch, J. Huehn, C. Loddenkemper et al., “Establishment of nematode infection despite increased Th2 responses and immunopathology after selective depletion of Foxp3+ cells,” European Journal of Immunology, vol. 39, no. 11, pp. 3066–3077, 2009. View at Publisher · View at Google Scholar · View at Scopus
  154. N. Harris and W. C. Gause, “To B or not to B: B cells and the Th2-type immune response to helminths,” Trends in Immunology, vol. 32, no. 2, pp. 80–88, 2010. View at Publisher · View at Google Scholar · View at Scopus
  155. H. J. Hernandez, Y. Wang, and M. J. Stadecker, “In infection with Schistosoma mansoni, B cells are required for T helper type 2 cell responses but not for granuloma formation,” Journal of Immunology, vol. 158, no. 10, pp. 4832–4837, 1997. View at Scopus
  156. D. Jankovic, A. W. Cheever, M. C. Kullberg et al., “CD4+ T cell-mediated granulomatous pathology in schistosomiasis is downregulated by a B cell-dependent mechanism requiring Fc receptor signaling,” Journal of Experimental Medicine, vol. 187, no. 4, pp. 619–629, 1998. View at Publisher · View at Google Scholar · View at Scopus
  157. T. Adjobimey and A. Hoerauf, “Induction of immunoglobulin G4 in human filariasis: an indicator of immunoregulation,” Annals of Tropical Medicine and Parasitology, vol. 104, no. 6, pp. 455–464, 2010. View at Publisher · View at Google Scholar · View at Scopus
  158. E. A. Ottesen, F. Skvaril, S. P. Tripathy, et al., “Prominence of IgG4 in the IgG antibody response to human filariasis,” Journal of Immunology, vol. 134, no. 4, pp. 2707–2712, 1985. View at Scopus
  159. R. Hussain, R. G. Hamilton, V. Kumaraswami, et al., “IgE responses in human filariasis. I. Quantitation of filaria-specific IgE,” Journal of Immunology, vol. 127, no. 4, pp. 1623–1629, 1981. View at Scopus
  160. R. A. Lawrence, “Immunity to filarial nematodes,” Veterinary Parasitology, vol. 100, no. 1-2, pp. 33–44, 2001. View at Publisher · View at Google Scholar · View at Scopus
  161. J. S. van der Zee, P. van Swieten, and R. C. Aalberse, “Inhibition of complement activation by IgG4 antibodies,” Clinical and Experimental Allergy, vol. 64, no. 2, pp. 415–422, 1986. View at Scopus
  162. L. Hussaarts, L. E. van der Vlugt, M. Yazdanbakhsh, et al., “Regulatory B-cell induction by helminths: implications for allergic disease,” Journal of Allergy and Clinical Immunology. In press. View at Publisher · View at Google Scholar
  163. S. Amu, S. P. Saunders, M. Kronenberg, et al., “Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model,” Journal of Allergy and Clinical Immunology, vol. 125, no. 5, article e1118, pp. 1114–1124, 2010. View at Publisher · View at Google Scholar · View at Scopus
  164. S. Hartmann, C. Schnoeller, A. Dahten, et al., “Gastrointestinal nematode infection interferes with experimental allergic airway inflammation but not atopic dermatitis,” Clinical and Experimental Allergy, vol. 39, no. 10, pp. 1585–1596, 2009. View at Publisher · View at Google Scholar · View at Scopus
  165. N. Gomez-Escobar, E. Lewis, and R. M. Maizels, “A novel member of the transforming growth factor-β (TGF-β) superfamily from the filarial nematodes Brugia malayi and B. pahangi,” Experimental Parasitology, vol. 88, no. 3, pp. 200–209, 1998. View at Publisher · View at Google Scholar · View at Scopus
  166. S. J. Davies, C. B. Shoemaker, and E. J. Pearce, “A divergent member of the transforming growth factor β receptor family from Schistosoma mansoni is expressed on the parasite surface membrane,” Journal of Biological Chemistry, vol. 273, no. 18, pp. 11234–11240, 1998. View at Publisher · View at Google Scholar · View at Scopus
  167. M. J. Beall and E. J. Pearce, “Human Transforming Growth Factor-β Activates a Receptor Serine/Threonine Kinase from the Intravascular Parasite Schistosoma mansoni,” Journal of Biological Chemistry, vol. 276, no. 34, pp. 31613–31619, 2001. View at Publisher · View at Google Scholar · View at Scopus
  168. J. L. Pennock, J. M. Behnke, Q. D. Bickle et al., “Rapid purification and characterization of L-dopachrome-methyl ester tautomerase (macrophage-migration-inhibitory factor) from Trichinella spiralis, Trichuris muris and Brugia pahangi,” Biochemical Journal, vol. 335, no. 3, pp. 495–498, 1998. View at Scopus
  169. J. J. Vermeire, Y. Cho, E. Lolis, et al., “Orthologs of macrophage migration inhibitory factor from parasitic nematodes,” Trends in Parasitology, vol. 24, no. 8, pp. 355–363, 2008. View at Publisher · View at Google Scholar · View at Scopus
  170. X. Zang, P. Taylor, J. M. Wang et al., “Homologues of human macrophage migration inhibitory factor from a parasitic nematode: Gene cloning, protein activity, and crystal structure,” Journal of Biological Chemistry, vol. 277, no. 46, pp. 44261–44267, 2002. View at Publisher · View at Google Scholar · View at Scopus
  171. C. Klotz, T. Ziegler, E. Daniłowicz-Luebert, et al., “Cystatins of parasitic organisms,” Advances in Experimental Medicine and Biology, vol. 712, pp. 208–221, 2011.
  172. T. Dainichi, Y. Maekawa, K. Ishii, et al., “Molecular cloning of a cystatin from parasitic intestinal nematode, Nippostrongylus brasiliensis,” The Journal of Medical Investigation, vol. 48, no. 1-2, pp. 81–87, 2001. View at Scopus
  173. X. Zang, M. Yazdanbakhsh, H. Jiang, et al., “A novel serpin expressed by blood-borne microfilariae of the parasitic nematode Brugia malayi inhibits human neutrophil serine proteinases,” Blood, vol. 94, no. 4, pp. 1418–1428, 1999. View at Scopus
  174. P. Stanley and P. E. Stein, “BmSPN2, a serpin secreted by the filarial nematode Brugia malayi, does not inhibit human neutrophil proteinases but plays a noninhibitory role,” Biochemistry, vol. 42, no. 20, pp. 6241–6248, 2003. View at Publisher · View at Google Scholar · View at Scopus
  175. W. Harnett, I. B. McInnes, and M. M. Harnett, “ES-62, a filarial nematode-derived immunomodulator with anti-inflammatory potential,” Immunology Letters, vol. 94, no. 1-2, pp. 27–33, 2004. View at Publisher · View at Google Scholar · View at Scopus
  176. M. M. Harnett, A. J. Melendez, and W. Harnett, “The therapeutic potential of the filarial nematode-derived immunodulator, ES-62 in inflammatory disease,” Clinical and Experimental Immunology, vol. 159, no. 3, pp. 256–267, 2010. View at Publisher · View at Google Scholar · View at Scopus
  177. F. A. Marshall, K. A. Watson, P. Garside, et al., “Effect of activated antigen-specific B cells on ES-62-mediated modulation of effector function of heterologous antigen-specific T cells in vivo,” Immunology, vol. 123, no. 3, pp. 411–425, 2008. View at Publisher · View at Google Scholar · View at Scopus
  178. M. Okano, K. Nishizaki, M. Abe, et al., “Strain-dependent induction of allergic rhinitis without adjuvant in mice,” Allergy, vol. 54, no. 6, pp. 593–601, 1999. View at Publisher · View at Google Scholar · View at Scopus
  179. M. Wuhrer, C. I. Balog, M. I. Catalina et al., “IPSE/alpha-1, a major secretory glycoprotein antigen from schistosome eggs, expresses the Lewis X motif on core-difucosylated N-glycans,” FEBS Journal, vol. 273, no. 10, pp. 2276–2292, 2006. View at Publisher · View at Google Scholar · View at Scopus
  180. M. Okano, A. R. Satoskar, K. Nishizaki, et al., “Lacto-N-fucopentaose III found on Schistosoma mansoni egg antigens functions as adjuvant for proteins by inducing Th2-type response1,” Journal of Immunology, vol. 167, no. 1, pp. 442–450, 2001. View at Scopus
  181. R. R. Pires, T. M. Oshiro, D. M. Itami, et al., “Production and characterization of a monoclonal antibody against an Ascaris suum allergenic component,” Brazilian Journal of Medical and Biological Research, vol. 34, no. 8, pp. 1033–1036, 2001. View at Scopus
  182. T. M. Oshiro, A. Rafael, C. S. Enobe, et al., “Comparison of different monoclonal antibodies against immunosuppresive proteins of Ascaris suum,” Brazilian Journal of Medical and Biological Research, vol. 37, no. 2, pp. 223–226, 2004. View at Scopus
  183. S. T. Holgate and R. Polosa, “Treatment strategies for allergy and asthma,” Nature Reviews Immunology, vol. 8, no. 3, pp. 218–230, 2008. View at Publisher · View at Google Scholar · View at Scopus