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Pathogen induced regulatory cell populations preventing allergy through the Th1/Th2 paradigm point of view

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Abstract

Epidemiological studies have demonstrated an inverse correlation between prevalence of helminth infections and allergic diseases both associated to Th2 immune responses. On the other hand, such an inverse correlation has also been evidenced between allergies and bacterial infections, associated to Th1 responses. In this review, we will examine and compare the various mechanisms by which Th1- or Th2-inducing infectious agents regulate the development of atopic diseases. We will emphasize the key role of various regulatory cell populations associated to the immune responses toward pathogen.

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Abbreviations

Foxp3:

Forkhead box P3, member of the forkhead/winged-helix family of transcriptional regulators

References

  1. Levy DA. Parasites and allergy: from IgE to Th1/Th2 and beyond. Clin Rev Allergy Immunol 2004;26:1–4.

    Article  PubMed  Google Scholar 

  2. Shirakawa T, Enomoto T, Shimazu S, Hopkin JM. The inverse association between tuberculin responses and atopic disorder. Science 1997;275:77–9.

    Article  PubMed  CAS  Google Scholar 

  3. Droste JH, Wieringa MH, Weyler JJ, Nelen VJ, Vermeire PA, Van Bever HP. Does the use of antibiotics in early childhood increase the risk of asthma and allergic disease? Clin Exp Allergy 2000;30:1547–53.

    Article  PubMed  CAS  Google Scholar 

  4. Neaville WA, Tisler C, Bhattacharya A, Anklam K, Gilbertson-White S, Hamilton R, Adler K, Dasilva DF, Roberg KA, Carlson-Dakes KT, Anderson E, Yoshihara D, Gangnon R, Mikus LD, Rosenthal LA, Gern JE, Lemanske RF Jr.Developmental cytokine response profiles and the clinical and immunologic expression of atopy during the first year of life. J Allergy Clin Immunol 2003;112:740–6.

    Article  PubMed  CAS  Google Scholar 

  5. van den Biggelaar AH, van Ree R, Rodrigues LC, Lell B, Deelder AM, Kremsner PG, Yazdanbakhsh M. Decreased atopy in children infected with Schistosoma haematobium: a role for parasite-induced interleukin-10. Lancet 2000;356:1723–7.

    Article  PubMed  Google Scholar 

  6. Yazdanbakhsh M, Kremsner PG, van Ree R. Allergy, parasites, and the hygiene hypothesis. Science 2002;296:490–4.

    Article  PubMed  CAS  Google Scholar 

  7. Sakaguchi S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004;22:531–62.

    Article  PubMed  CAS  Google Scholar 

  8. Powrie F. T cells in inflammatory bowel disease: protective and pathogenic roles. Immunity 1995;3:171–4.

    Article  PubMed  CAS  Google Scholar 

  9. Weiner HL. Induction and mechanism of action of transforming growth factor-beta-secreting Th3 regulatory cells. Immunol Rev 2001;182:207–14.

    Article  PubMed  CAS  Google Scholar 

  10. Groux H, O’Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, Roncarolo MG. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997;389:737–42.

    Article  PubMed  CAS  Google Scholar 

  11. Chess L, Jiang H. Resurrecting CD8+ suppressor T cells. Nat Immunol 2004;5:469–71.

    Article  PubMed  CAS  Google Scholar 

  12. Lahn M, Kanehiro A, Takeda K, Joetham A, Schwarze J, Kohler G, O’Brien R, Gelfand EW, Born W. Negative regulation of airway responsiveness that is dependent on gammadelta T cells and independent of alphabeta T cells. Nat Med 1999;5:1150–6.

    Article  PubMed  CAS  Google Scholar 

  13. Hansen G, Yeung VP, Berry G, Umetsu DT, DeKruyff RH. Vaccination with heat-killed Listeria as adjuvant reverses established allergen-induced airway hyperreactivity and inflammation: role of CD8+ T cells and IL-18. J Immunol 2000;164:223–30.

    PubMed  CAS  Google Scholar 

  14. Stock P, Kallinich T, Akbari O, Quarcoo D, Gerhold K, Wahn U, Umetsu DT, Hamelmann E. CD8(+) T cells regulate immune responses in a murine model of allergen-induced sensitization and airway inflammation. Eur J Immunol 2004;34:1817–27.

    Article  PubMed  CAS  Google Scholar 

  15. Ho LP, Urban BC, Jones L, Ogg GS, McMichael AJ. CD4(-)CD8alphaalpha subset of CD1d-restricted NKT cells controls T cell expansion. J Immunol 2004;172:7350–8.

    PubMed  CAS  Google Scholar 

  16. O’Garra A, Vieira P. Regulatory T cells and mechanisms of immune system control. Nat Med 2004;10:801–5.

    Article  PubMed  CAS  Google Scholar 

  17. Maizels RM. Infections and allergy—helminths, hygiene and host immune regulation. Curr Opin Immunol 2005;17:656–61.

    Article  PubMed  CAS  Google Scholar 

  18. Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 2003;3:733–44.

    Article  PubMed  CAS  Google Scholar 

  19. Mosmann TR, Cherwinski H, Bond MW, Giedlin MA, Coffman RL. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986;136:2348–57.

    PubMed  CAS  Google Scholar 

  20. Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM, Weaver CT. Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 2005;6:1123–32.

    Article  PubMed  CAS  Google Scholar 

  21. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005;6:1133–41.

    Article  PubMed  CAS  Google Scholar 

  22. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235–8.

    Article  PubMed  CAS  Google Scholar 

  23. Mangan PR, Harrington LE, O’Quinn DB, Helms WS, Bullard DC, Elson CO, Hatton RD, Wahl SM, Schoeb TR, Weaver CT. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006;441:231–4.

    Article  PubMed  CAS  Google Scholar 

  24. Weaver CT, Harrington LE, Mangan PR, Gavrieli M, Murphy KM. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 2006;24:677–88.

    Article  PubMed  CAS  Google Scholar 

  25. Schnyder-Candrian S, Togbe D, Couillin I, Mercier I, Brombacher F, Quesniaux V, Fossiez F, Ryffel B, Schnyder B. Interleukin-17 is a negative regulator of established allergic asthma. J Exp Med 2006;203:2715–25.

    Article  PubMed  CAS  Google Scholar 

  26. Gershon RK, Kondo K. Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology 1970;18:723–37.

    PubMed  CAS  Google Scholar 

  27. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003;4:330–6.

    Article  PubMed  CAS  Google Scholar 

  28. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057–61.

    Article  PubMed  CAS  Google Scholar 

  29. Read S, Malmstrom V, Powrie F. Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J Exp Med 2000;192:295–302.

    Article  PubMed  CAS  Google Scholar 

  30. Nakamura K, Kitani A, Strober W. Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med 2001;194:629–44.

    Article  PubMed  CAS  Google Scholar 

  31. Verginis P, Li HS, Carayanniotis G. Tolerogenic semimature dendritic cells suppress experimental autoimmune thyroiditis by activation of thyroglobulin-specific CD4+CD25+ T cells. J Immunol 2005;174:7433–9.

    PubMed  CAS  Google Scholar 

  32. Fukaura H, Kent SC, Pietrusewicz MJ, Khoury SJ, Weiner HL, Hafler DA. Induction of circulating myelin basic protein and proteolipid protein-specific transforming growth factor-beta1-secreting Th3 T cells by oral administration of myelin in multiple sclerosis patients. J Clin Invest 1996;98:70–7.

    PubMed  CAS  Google Scholar 

  33. Wakkach A, Fournier N, Brun V, Breittmayer JP, Cottrez F, Groux H. Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity 2003;18:605–17.

    Article  PubMed  CAS  Google Scholar 

  34. Endharti AT, Rifa IMs, Shi Z, Fukuoka Y, Nakahara Y, Kawamoto Y, Takeda K, Isobe K, Suzuki H. Cutting edge: CD8+CD122+ regulatory T cells produce IL-10 to suppress IFN-gamma production and proliferation of CD8+ T cells. J Immunol 2005;175:7093–7.

    PubMed  CAS  Google Scholar 

  35. Seo N, Tokura Y, Takigawa M, Egawa K. Depletion of IL-10- and TGF-beta-producing regulatory gamma delta T cells by administering a daunomycin-conjugated specific monoclonal antibody in early tumor lesions augments the activity of CTLs and NK cells. J Immunol 1999;163:242–9.

    PubMed  CAS  Google Scholar 

  36. Hachem P, Lisbonne M, Michel ML, Diem S, Roongapinun S, Lefort J, Marchal G, Herbelin A, Askenase PW, Dy M, Leite-de-Moraes MC. Alpha-galactosylceramide-induced iNKT cells suppress experimental allergic asthma in sensitized mice: role of IFN-gamma. Eur J Immunol 2005;35:2793–802.

    Article  PubMed  CAS  Google Scholar 

  37. Harada M, Magara-Koyanagi K, Watarai H, Nagata Y, Ishii Y, Kojo S, Horiguchi S, Okamoto Y, Nakayama T, Suzuki N, Yeh WC, Akira S, Kitamura H, Ohara O, Seino KI, Taniguchi M. IL-21-induced B{varepsilon} cell apoptosis mediated by natural killer T cells suppresses IgE responses. J Exp Med 2006;203:2929–37.

    Google Scholar 

  38. Dieli F, Taniguchi M, Kronenberg M, Sidobre S, Ivanyi J, Fattorini L, Iona E, Orefici G, De Leo G, Russo D, Caccamo N, Sireci G, Di Sano C, Salerno A. An anti-inflammatory role for V alpha 14 NK T cells in Mycobacterium bovis bacillus Calmette-Guerin-infected mice. J Immunol 2003;171:1961–8.

    PubMed  CAS  Google Scholar 

  39. Mallevaey T, Zanetta JP, Faveeuw C, Fontaine J, Maes E, Platt F, Capron M, de-Moraes ML, Trottein F. Activation of invariant NKT cells by the helminth parasite schistosoma mansoni. J Immunol 2006;176:2476–85.

    PubMed  CAS  Google Scholar 

  40. Ford MS, Young KJ, Zhang Z, Ohashi PS, Zhang L. The immune regulatory function of lymphoproliferative double negative T cells in vitro and in vivo. J Exp Med 2002;196:261–7.

    Article  PubMed  CAS  Google Scholar 

  41. Khan Q, Penninger JM, Yang L, Marra LE, Kozieradzki I, Zhang L. Regulation of apoptosis in mature alphabeta+CD4-CD8- antigen-specific suppressor T cell clones. J Immunol 1999;162:5860–7.

    PubMed  CAS  Google Scholar 

  42. Zhang C, Zhang J, Tian Z. The regulatory effect of natural killer cells: do “NK-reg cells” exist? Cell Mol Immunol 2006;3:241–54.

    PubMed  CAS  Google Scholar 

  43. Kapsenberg ML. Dendritic-cell control of pathogen-driven T-cell polarization. Nat Rev Immunol 2003;3:984–93.

    Article  PubMed  CAS  Google Scholar 

  44. Levings MK, Gregori S, Tresoldi E, Cazzaniga S, Bonini C, Roncarolo MG. Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells. Blood 2005;105:1162–9.

    Article  PubMed  CAS  Google Scholar 

  45. Atochina O, Daly-Engel T, Piskorska D, McGuire E, Harn DA. A schistosome-expressed immunomodulatory glycoconjugate expands peritoneal Gr1(+) macrophages that suppress naive CD4(+) T cell proliferation via an IFN-gamma and nitric oxide-dependent mechanism. J Immunol 2001;167:4293–302.

    PubMed  CAS  Google Scholar 

  46. Loke P, MacDonald AS, Robb A, Maizels RM, Allen JE. Alternatively activated macrophages induced by nematode infection inhibit proliferation via cell-to-cell contact. Eur J Immunol 2000;30:2669–78.

    Article  PubMed  CAS  Google Scholar 

  47. Terrazas LI, Montero D, Terrazas CA, Reyes JL, Rodriguez-Sosa M. Role of the programmed Death-1 pathway in the suppressive activity of alternatively activated macrophages in experimental cysticercosis. Int J Parasitol 2005;35:1349–58.

    Article  PubMed  CAS  Google Scholar 

  48. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol 2002;3:944–50.

    Article  PubMed  CAS  Google Scholar 

  49. Mangan NE, van Rooijen N, McKenzie AN, Fallon PG. Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness. J Immunol 2006;176:138–47.

    PubMed  CAS  Google Scholar 

  50. Mizoguchi A, Mizoguchi E, Takedatsu H, Blumberg RS, Bhan AK. Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 2002;16:219–30.

    Article  PubMed  CAS  Google Scholar 

  51. Parekh VV, Prasad DV, Banerjee PP, Joshi BN, Kumar A, Mishra GC. B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8+ T cells: role of TGF-beta 1. J Immunol 2003;170:5897–911.

    PubMed  CAS  Google Scholar 

  52. Wei B, Velazquez P, Turovskaya O, Spricher K, Aranda R, Kronenberg M, Birnbaumer L, Braun J. Mesenteric B cells centrally inhibit CD4+ T cell colitis through interaction with regulatory T cell subsets. Proc Natl Acad Sci U S A 2005;102:2010–5.

    Article  PubMed  CAS  Google Scholar 

  53. Mizoguchi A, Mizoguchi E, Smith RN, Preffer FI, Bhan AK. Suppressive role of B cells in chronic colitis of T cell receptor alpha mutant mice. J Exp Med 1997;186:1749–56.

    Article  PubMed  CAS  Google Scholar 

  54. Maizels RM, Balic A, Gomez-Escobar N, Nair M, Taylor MD, Allen JE. Helminth parasites–masters of regulation. Immunol Rev 2004;201:89–116.

    Article  PubMed  CAS  Google Scholar 

  55. Kitagaki K, Businga TR, Racila D, Elliott DE, Weinstock JV, Kline JN. Intestinal helminths protect in a murine model of asthma. J Immunol 2006;177:1628–35.

    PubMed  CAS  Google Scholar 

  56. Wilson MS, Taylor MD, Balic A, Finney CA, Lamb JR, Maizels RM. Suppression of allergic airway inflammation by helminth-induced regulatory T cells. J Exp Med 2005;202:1199–212.

    Article  PubMed  CAS  Google Scholar 

  57. Bashir ME, Andersen P, Fuss IJ, Shi HN, Nagler-Anderson C. An enteric helminth infection protects against an allergic response to dietary antigen. J Immunol 2002;169:3284–292.

    PubMed  CAS  Google Scholar 

  58. Moore KW, O’Garra A, de Waal Malefyt R, Vieira P, Mosmann TR. Interleukin-10. Annu Rev Immunol 1993;11:165–90.

    Article  PubMed  CAS  Google Scholar 

  59. Wohlleben G, Trujillo C, Muller J, Ritze Y, Grunewald S, Tatsch U, Erb KJ. Helminth infection modulates the development of allergen-induced airway inflammation. Int Immunol 2004;16:585–96.

    Article  PubMed  CAS  Google Scholar 

  60. Mangan NE, Fallon RE, Smith P, van Rooijen N, McKenzie AN, Fallon PG. Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J Immunol 2004;173:6346–56.

    PubMed  CAS  Google Scholar 

  61. Schopf L, Luccioli S, Bundoc V, Justice P, Chan CC, Wetzel BJ, Norris HH, Urban JF Jr, Keane-Myers A. Differential modulation of allergic eye disease by chronic and acute ascaris infection. Invest Ophthalmol Vis Sci 2005;46:2772–80.

    Article  PubMed  Google Scholar 

  62. McKee AS, Pearce EJ. CD25+CD4+ cells contribute to Th2 polarization during helminth infection by suppressing Th1 response development. J Immunol 2004;173:1224–31.

    PubMed  CAS  Google Scholar 

  63. Pedras-Vasconcelos JA, Pearce EJ. Type 1 CD8+ T cell responses during infection with the helminth Schistosoma mansoni. J Immunol 1996;157:3046–53.

    PubMed  CAS  Google Scholar 

  64. Yang J, Zhao J, Yang Y, Zhang L, Yang X, Zhu X, Ji M, Sun N, Su C. Schistosoma japonicum egg antigens stimulate CD4 CD25 T cells and modulate airway inflammation in a murine model of asthma. Immunology 2006;120:8–18.

    PubMed  Google Scholar 

  65. Summers RW, Elliott DE, Qadir K, Urban JF Jr, Thompson R, Weinstock JV. Trichuris suis seems to be safe and possibly effective in the treatment of inflammatory bowel disease. Am J Gastroenterol 2003;98:2034–41.

    Article  PubMed  Google Scholar 

  66. Wickelgren I. Immunotherapy. Can worms tame the immune system? Science 2004;305:170–1.

    Article  PubMed  CAS  Google Scholar 

  67. Erb KJ, Holloway JW, Sobeck A, Moll H, Le Gros G. Infection of mice with Mycobacterium bovis-Bacillus Calmette-Guerin (BCG) suppresses allergen-induced airway eosinophilia. J Exp Med 1998;187:561–9.

    Article  PubMed  CAS  Google Scholar 

  68. Hopfenspirger MT, Agrawal DK. Airway hyperresponsiveness, late allergic response, and eosinophilia are reversed with mycobacterial antigens in ovalbumin-presensitized mice. J Immunol 2002;168:2516–22.

    PubMed  CAS  Google Scholar 

  69. Koh YI, Choi IS, Kim WY. BCG infection in allergen-presensitized rats suppresses Th2 immune response and prevents the development of allergic asthmatic reaction. J Clin Immunol 2001;21:51–9.

    Article  PubMed  CAS  Google Scholar 

  70. Yang X, Fan Y, Wang S, Han X, Yang J, Bilenki L, Chen L. Mycobacterial infection inhibits established allergic inflammatory responses via alteration of cytokine production and vascular cell adhesion molecule-1 expression. Immunology 2002;105:336–43.

    Article  PubMed  CAS  Google Scholar 

  71. Major T, Wohlleben G, Reibetanz B, Erb KJ. Application of heat killed Mycobacterium bovis-BCG into the lung inhibits the development of allergen-induced Th2 responses. Vaccine 2002;20:1532–40.

    Article  PubMed  CAS  Google Scholar 

  72. Daugelat S, Ladel CH, Kaufmann SH. Influence of mouse strain and vaccine viability on T-cell responses induced by Mycobacterium bovis bacillus Calmette-Guerin. Infect Immun 1995;63:2033–40.

    PubMed  CAS  Google Scholar 

  73. Tsuji S, Matsumoto M, Takeuchi O, Akira S, Azuma I, Hayashi A, Toyoshima K, Seya T. Maturation of human dendritic cells by cell wall skeleton of Mycobacterium bovis bacillus Calmette-Guerin: involvement of toll-like receptors. Infect Immun 2000;68:6883–90.

    Article  PubMed  CAS  Google Scholar 

  74. Krieg AM. CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 2002;20:709–60.

    Article  PubMed  CAS  Google Scholar 

  75. Korf JE, Pynaert G, Tournoy K, Boonefaes T, Van Oosterhout A, Ginneberge D, Haegeman A, Verschoor JA, De Baetselier P, Grooten J. Macrophage reprogramming by mycolic acid promotes a tolerogenic response in experimental asthma. Am J Respir Crit Care Med 2006;174:152–60.

    Article  PubMed  CAS  Google Scholar 

  76. Zuany-Amorim C, Manlius C, Trifilieff A, Brunet LR, Rook G, Bowen G, Pay G, Walker C. Long-term protective and antigen-specific effect of heat-killed Mycobacterium vaccae in a murine model of allergic pulmonary inflammation. J Immunol 2002;169:1492–9.

    PubMed  CAS  Google Scholar 

  77. Zuany-Amorim C, Sawicka E, Manlius C, Le Moine A, Brunet LR, Kemeny DM, Bowen G, Rook G, Walker C. Suppression of airway eosinophilia by killed Mycobacterium vaccae-induced allergen-specific regulatory T-cells. Nat Med 2002;8:625–9.

    Article  PubMed  CAS  Google Scholar 

  78. Adams VC, Hunt JR, Martinelli R, Palmer R, Rook GA, Brunet LR. Mycobacterium vaccae induces a population of pulmonary CD11c+ cells with regulatory potential in allergic mice. Eur J Immunol 2004;34:631–38.

    Article  PubMed  CAS  Google Scholar 

  79. Kuipers H, Heirman C, Hijdra D, Muskens F, Willart M, van Meirvenne S, Thielemans K, Hoogsteden HC, Lambrecht BN. Dendritic cells retrovirally overexpressing IL-12 induce strong Th1 responses to inhaled antigen in the lung but fail to revert established Th2 sensitization. J Leukoc Biol 2004;76:1028–38.

    Article  PubMed  CAS  Google Scholar 

  80. Akbari O, DeKruyff RH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol 2001;2:725–31.

    Article  PubMed  CAS  Google Scholar 

  81. Quinn KM, McHugh RS, Rich FJ, Goldsack LM, de Lisle GW, Buddle BM, Delahunt B, Kirman JR. Inactivation of CD4+ CD25+ regulatory T cells during early mycobacterial infection increases cytokine production but does not affect pathogen load. Immunol Cell Biol 2006;84:467–74.

    Article  PubMed  CAS  Google Scholar 

  82. Emoto M, Emoto Y, Buchwalow IB, Kaufmann SH. Induction of IFN-gamma-producing CD4+ natural killer T cells by Mycobacterium bovis bacillus Calmette Guerin. Eur J Immunol 1999;29:650–9.

    Article  PubMed  CAS  Google Scholar 

  83. Han X, Fan Y, Wang S, Yang J, Bilenki L, Qiu H, Jiao L, Yang X. Dendritic cells from Chlamydia-infected mice show altered Toll-like receptor expression and play a crucial role in inhibition of allergic responses to ovalbumin. Eur J Immunol 2004;34:981–9.

    Article  PubMed  CAS  Google Scholar 

  84. Moser M, Murphy KM. Dendritic cell regulation of TH1-TH2 development. Nat Immunol 2000;1:199–205.

    Article  PubMed  CAS  Google Scholar 

  85. Han X, Wang S, Fan Y, Yang J, Jiao L, Qiu H, Yang X. Chlamydia infection induces ICOS ligand-expressing and IL-10-producing dendritic cells that can inhibit airway inflammation and mucus overproduction elicited by allergen challenge in BALB/c mice. J Immunol 2006;176:5232–9.

    PubMed  CAS  Google Scholar 

  86. Stock P, Akbari O, Berry G, Freeman GJ, Dekruyff RH, Umetsu DT. Induction of T helper type 1-like regulatory cells that express Foxp3 and protect against airway hyper-reactivity. Nat Immunol 2004;5:1149–56.

    Article  PubMed  CAS  Google Scholar 

  87. Bilsborough J, George TC, Norment A, Viney JL. Mucosal CD8alpha+ DC, with a plasmacytoid phenotype, induce differentiation and support function of T cells with regulatory properties. Immunology 2003;108:481–92.

    Article  PubMed  CAS  Google Scholar 

  88. Akbari O, Freeman GJ, Meyer EH, Greenfield EA, Chang TT, Sharpe AH, Berry G, DeKruyff RH, Umetsu DT. Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat Med 2002;8:1024–32.

    Article  PubMed  CAS  Google Scholar 

  89. Lauener RP, Birchler T, Adamski J, Braun-Fahrlander C, Bufe A, Herz U, von Mutius E, Nowak D, Riedler J, Waser M, Sennhauser FH. Expression of CD14 and Toll-like receptor 2 in farmers’ and non-farmers’ children. Lancet 2002;360:465–6.

    Article  PubMed  CAS  Google Scholar 

  90. Kondo Y, Matsuse H, Machida I, Kawano T, Saeki S, Tomari S, Obase Y, Fukushima C, Kohno S. Regulation of mite allergen-pulsed murine dendritic cells by respiratory syncytial virus. Am J Respir Crit Care Med 2004;169:494–8.

    Article  PubMed  Google Scholar 

  91. Marsland BJ, Harris NL, Camberis M, Kopf M, Hook SM, Le Gros G. Bystander suppression of allergic airway inflammation by lung resident memory CD8+ T cells. Proc Natl Acad Sci U S A 2004;101:6116–21.

    Article  PubMed  CAS  Google Scholar 

  92. Wohlleben G, Muller J, Tatsch U, Hambrecht C, Herz U, Renz H, Schmitt E, Moll H, Erb KJ. Influenza A virus infection inhibits the efficient recruitment of Th2 cells into the airways and the development of airway eosinophilia. J Immunol 2003;170:4601–11.

    PubMed  CAS  Google Scholar 

  93. Menager-Marcq IN, Pomie CI, Romagnoli PA, Van Meerwijk JO. CD8(+)CD28(−) Regulatory T lymphocytes prevent experimental inflammatory bowel disease in mice. Gastroenterology 2006;131(6)1775-85.

    Google Scholar 

  94. Montagnoli C, Fallarino F, Gaziano R, Bozza S, Bellocchio S, Zelante T, Kurup WP, Pitzurra L, Puccetti P, Romani L. Immunity and tolerance to Aspergillus involve functionally distinct regulatory T cells and tryptophan catabolism. J Immunol 2006;176:1712–23.

    PubMed  CAS  Google Scholar 

  95. Strachan DP. Hay fever, hygiene, and household size. BMJ 1989;299:1259–60.

    PubMed  CAS  Google Scholar 

  96. Lynch NR, Hagel I, Perez M, Di Prisco MC, Lopez R, Alvarez N. Effect of anthelmintic treatment on the allergic reactivity of children in a tropical slum. J Allergy Clin Immunol 1993;92:404–11.

    Google Scholar 

  97. van den Biggelaar AH, Rodrigues LC, van Ree R, van der Zee JS, Hoeksma-Kruize YC, Souverijn JH, Missinou MA, Borrmann S, Kremsner PG, Yazdanbakhsh M. Long-term treatment of intestinal helminths increases mite skin-test reactivity in Gabonese schoolchildren. J Infect Dis 2004;189:892–900.

    Article  PubMed  Google Scholar 

  98. Araujo MI, Hoppe B, Medeiros M Jr, Alcantara L, Almeida MC, Schriefer A, Oliveira RR, Kruschewsky R, Figueiredo JP, Cruz AA, Carvalho EM. Impaired T helper 2 response to aeroallergen in helminth-infected patients with asthma. J Infect Dis 2004;190:1797–803.

    Article  PubMed  CAS  Google Scholar 

  99. Medeiros M Jr, Figueiredo JP, Almeida MC, Matos MA, Araujo MI, Cruz AA, Atta AM, Rego MA, de Jesus AR, Taketomi EA, Carvalho EM. Schistosoma mansoni infection is associated with a reduced course of asthma. J Allergy Clin Immunol 2003;111:947–51.

    Article  PubMed  Google Scholar 

  100. Araujo MI, Lopes AA, Medeiros M, Cruz AA, Sousa-Atta L, Sole D, Carvalho EM. Inverse association between skin response to aeroallergens and Schistosoma mansoni infection. Int Arch Allergy Immunol 2000;123:145–8.

    Article  PubMed  CAS  Google Scholar 

  101. Wilson MS, Maizels RM. Regulation of allergy and autoimmunity in helminth infection. Clin Rev Allergy Immunol 2004;26:35–50.

    Article  PubMed  CAS  Google Scholar 

  102. King CL, Medhat A, Malhotra I, Nafeh M, Helmy A, Khaudary J, Ibrahim S, El-Sherbiny M, Zaky S, Stupi RJ, Brustoski K, Shehata M, Shata MT. Cytokine control of parasite-specific anergy in human urinary schistosomiasis. IL-10 modulates lymphocyte reactivity. J Immunol 1996;156:4715–21.

    PubMed  CAS  Google Scholar 

  103. Ottesen EA, Weller PF, Heck L. Specific cellular immune unresponsiveness in human filariasis. Immunology 1977;33:413–21.

    PubMed  CAS  Google Scholar 

  104. Piessens WF, McGreevy PB, Piessens PW, McGreevy M, Koiman I, Saroso JS, Dennis DT. Immune responses in human infections with Brugia malayi: specific cellular unresponsiveness to filarial antigens. J Clin Invest 1980;65:172–9.

    Article  PubMed  CAS  Google Scholar 

  105. Sartono E, Kruize YC, Kurniawan A, Maizels RM, Yazdanbakhsh M. Depression of antigen-specific interleukin-5 and interferon-gamma responses in human lymphatic filariasis as a function of clinical status and age. J Infect Dis 1997;175:1276–80.

    Article  PubMed  CAS  Google Scholar 

  106. Taylor A, Verhagen J, Akdis CA, Akdis M. T regulatory cells in allergy and health: a question of allergen specificity and balance. Int Arch Allergy Immunol 2004;135:73–82.

    Article  PubMed  CAS  Google Scholar 

  107. Doetze A, Satoguina J, Burchard G, Rau T, Loliger C, Fleischer B, Hoerauf A. Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T(h)3/T(r)1-type cytokines IL-10 and transforming growth factor-beta but not by a T(h)1 to T(h)2 shift. Int Immunol 2000;12:623–30.

    Article  PubMed  CAS  Google Scholar 

  108. von Hertzen L, Klaukka T, Mattila H, Haahtela T. Mycobacterium tuberculosis infection and the subsequent development of asthma and allergic conditions. J Allergy Clin Immunol 1999;104:1211–4.

    Article  Google Scholar 

  109. Trujillo C, Erb KJ. Inhibition of allergic disorders by infection with bacteria or the exposure to bacterial products. Int J Med Microbiol 2003;293:123–31.

    Article  PubMed  CAS  Google Scholar 

  110. Choi IS, Koh YI. Therapeutic effects of BCG vaccination in adult asthmatic patients: a randomized, controlled trial. Ann Allergy Asthma Immunol 2002;88:584–91.

    Article  PubMed  Google Scholar 

  111. Cavallo GP, Elia M, Giordano D, Baldi C, Cammarota R. Decrease of specific and total IgE levels in allergic patients after BCG vaccination: preliminary report. Arch Otolaryngol Head Neck Surg 2002;128:1058–60.

    PubMed  Google Scholar 

  112. Camporota L, Corkhill A, Long H, Lordan J, Stanciu L, Tuckwell N, Cross A, Stanford JL, Rook GA, Holgate ST, Djukanovic R. The effects of Mycobacterium vaccae on allergen-induced airway responses in atopic asthma. Eur Respir J 2003;21:287–93.

    Article  PubMed  CAS  Google Scholar 

  113. Arkwright PD, David TJ. Intradermal administration of a killed Mycobacterium vaccae suspension (SRL 172) is associated with improvement in atopic dermatitis in children with moderate-to-severe disease. J Allergy Clin Immunol 2001;107:531–4.

    Article  PubMed  CAS  Google Scholar 

  114. Bilenki L, Wang S, Fan Y, Yang J, Han X, Yang X. Chlamydia trachomatis infection inhibits airway eosinophilic inflammation induced by ragweed. Clin Immunol 2002;102:28–36.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

T.R. is supported by a post-doctoral fellowship from Fondation pour la Recherche Médicale (FRM).

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Authors and Affiliations

  1. Inserm U547 – Univ. Lille 2 – Institut Pasteur de Lille, 1, rue du Professeur Calmette, Lille, 59019, France

    Thomas Roumier, Monique Capron, David Dombrowicz & Christelle Faveeuw

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  1. Thomas Roumier
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  2. Monique Capron
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  3. David Dombrowicz
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  4. Christelle Faveeuw
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Correspondence to David Dombrowicz.

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D.D. and C.F. contributed equally to this work

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Roumier, T., Capron, M., Dombrowicz, D. et al. Pathogen induced regulatory cell populations preventing allergy through the Th1/Th2 paradigm point of view. Immunol Res 40, 1–17 (2008). https://doi.org/10.1007/s12026-007-0058-3

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