Regulation of Th2 responses and allergic inflammation through bystander activation of CD8+ T lymphocytes in early life

Journal of Immunology

Volumn 185, Issue 2, 2010, Pages 884-891

  Dubois, Aurore ^a   Deruytter, Nathalie ^c,d,e   Adams, Brigitte ^a   Kanda, Akira ^c,d,e   Delbauve, Sandrine ^a   Fleury, Sebastien ^c,d,e   Torres, David ^a   François, Angélique ^b   Pétein, Michel ^b   Goldman, Michel ^a   Dombrowicz, David ^c,d,e   Flamand, Véronique ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^b INSTITUTE OF PATHOLOGY AND GENETICS   (Belgium)

^c INSERM   (France)

^d UNIV LILLE   (France)

^e INSTITUT PASTEUR DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIGEN; ALLOANTIGEN TC1; ALLOANTIGEN TC2; GAMMA INTERFERON; HERMES ANTIGEN; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G1; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; L SELECTIN; MESSENGER RNA; OVALBUMIN; UNCLASSIFIED DRUG; IMMUNOGLOBULIN G;

ADOPTIVE TRANSFER; ALLERGIC REACTION; ALLERGY AIRWAY INFLAMMATION; ALLOGENEIC STEM CELL TRANSPLANTATION; ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DENDRITIC CELL; EOSINOPHILIA; IMMUNIZATION; MEMORY T LYMPHOCYTE; MOUSE; NEWBORN; NEWBORN PERIOD; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; SPLEEN CELL; TH1 CELL; TH2 CELL; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; BLOOD; BYSTANDER EFFECT; C57BL MOUSE; CYTOLOGY; GENE EXPRESSION; GENETICS; IMMUNOLOGY; INFLAMMATION; LUNG; METABOLISM; MOUSE MUTANT; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN; TIME; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; ANIMALS, NEWBORN; ASTHMA; BYSTANDER EFFECT; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; GENE EXPRESSION; IMMUNOGLOBULIN E; IMMUNOGLOBULIN G; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-4; LUNG; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; OVALBUMIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN; TH1 CELLS; TH2 CELLS; TIME FACTORS;

EID: 77955499089     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0903287     Document Type: Article

References (47)

1. Adkins, B., C. Leclerc, and S. Marshall-Clarke. 2004. Neonatal adaptive immunity comes of age. Nat. Rev. Immunol. 4: 553-564.
2. Adkins, B., Y. Bu, and P. Guevara. 2001. The generation of Th memory in neonates versus adults: prolonged primary Th2 effector function and impaired development of Th1 memory effector function in murine neonates. J. Immunol. 166: 918-925. (Pubitemid 32060246)
3. Rose, S., M. Lichtenheld, M. R. Foote, and B. Adkins. 2007. Murine neonatal CD4+ cells are poised for rapid Th2 effector-like function. J. Immunol. 178: 2667-2678. (Pubitemid 46333143)
4. Li, L., H. H. Lee, J. J. Bell, R. K. Gregg, J. S. Ellis, A. Gessner, and H. Zaghouani. 2004. IL-4 utilizes an alternative receptor to drive apoptosis of Th1 cells and skews neonatal immunity toward Th2. Immunity 20: 429-440. (Pubitemid 38482121)
5. Holt, P. G. 2004. The role of genetic and environmental factors in the development of T-cell mediated allergic disease in early life. Paediatr. Respir. Rev. 5(Suppl. A): S27-S30.
6. +) T lymphocytes and IFN-γ. Eur. J. Immunol. 30: 1290-1296.
7. + T lymphocytes downregulate T helper cell type 2 cytokine secretion and pulmonary eosinophilia during experimental murine respiratory syncytial virus infection. J. Exp. Med. 186: 421-432.
8. + T cells. Eur. J. Immunol. 27: 2657-2665.
9. + T cells in murine experimental allergic encephalomyelitis. Science 256: 1213-1215.
10. Noble, A., G. A. Pestano, and H. Cantor. 1998. Suppression of immune responses by CD8 cells. I. Superantigen-activated CD8 cells induce unidirectional Fas-mediated apoptosis of antigen-activated CD4 cells. J. Immunol. 160: 559-565.
11. Laffont, S., J. D. Coudert, L. Garidou, L. Delpy, A. Wiedemann, C. Demur, C. Coureau, and J. C. Guéry. 2006. CD8+ T-cell-mediated killing of donor dendritic cells prevents alloreactive T helper type-2 responses in vivo. Blood 108: 2257-2264.
12. Srivastava, K. D., C. Qu, T. Zhang, J. Goldfarb, H. A. Sampson, and X.-M. Li. 2009. Food Allergy Herbal Formula-2 silences peanut-induced anaphylaxis for a prolonged posttreatment period via IFN-γ-producing CD8+ T cells. J. Allergy Clin. Immunol. 123: 443-451.
13. Suzuki, M., K. Maghni, S. Molet, A. Shimbara, Q. A. Hamid, and J. G. Martin. 2002. IFN-gamma secretion by CD8T cells inhibits allergen-induced airway eosinophilia but not late airway responses. J. Allergy Clin. Immunol. 109: 803-809.
14. Yamada, A., Y. Ohshima, M. Yasutomi, K. Ogura, S. Tokuriki, H. Naiki, and M. Mayumi. 2009. Antigen-primed splenic CD8+ T cells impede the development of oral antigen-induced allergic diarrhea. J. Allergy Clin. Immunol. 123: 889-894.
15. Salagianni, M., K. L. Wong, M. J. Thomas, A. Noble, and D. M. Kemeny. 2007. An essential role for IL-18 in CD8 T cell-mediated suppression of IgE responses. J. Immunol. 178: 4771-4778.
16. Thomas, M. J., A. Noble, E. Sawicka, P. W. Askenase, and D. M. Kemeny. 2002. CD8 T cells inhibit IgE via dendritic cell IL-12 induction that promotes Th1 T cell counter-regulation. J. Immunol. 168: 216-223.
17. + T cells provide innate immune protection against Listeria monocytogenes in the absence of cognate antigen. J. Exp. Med. 198: 1583-1593.
18. + T cells. Proc. Natl. Acad. Sci. USA 101: 6116-6121.
19. de Lavareille, A., C. Prigogine, F. Paulart, N. Nagy, C. Habran, N. O. Haddou, A. Le Moine, I. Salmon, M. Goldman, and V. Flamand. 2005. Regulatory role of host CD8+ T lymphocytes in experimental graft-versus-host disease across a single major histocompatibility complex class II incompatibility. Transplantation 80: 1293-1299.
20. Field, A.-C., L. Caccavelli, M.-F. Bloch, and B. Bellon. 2003. Regulatory CD8+ T cells control neonatal tolerance to a Th2-mediated autoimmunity. J. Immunol. 170: 2508-2515. (Pubitemid 36245640)
21. Adams, B., N. Nagy, F. Paulart, M. L. Vanderhaeghen, M. Goldman, and V. Flamand. 2003. CD8+ T lymphocytes regulating Th2 pathology escape neonatal tolerization. J. Immunol. 171: 5071-5076. (Pubitemid 37432788)
22. Kovarik, J., M. Gaillard, X. Martinez, P. Bozzotti, P.-H. Lambert, T. F. Wild, and C.-A. Siegrist. 2001. Induction of adult-like antibody, Th1, and CTL responses to measles hemagglutinin by early life murine immunization with an attenuated vaccinia-derived NYVAC(K1L) viral vector. Virology 285: 12-20. (Pubitemid 32589003)
23. Zhang, J., N. Silvestri, J. L. Whitton, and D. E. Hassett. 2002. Neonates mount robust and protective adult-like CD8(+)-T-cell responses to DNA vaccines. J. Virol. 76: 11911-11919.
24. Buonocore, S., F. Paulart, A. Le Moine, M. Braun, I. Salmon, S. Van Meirvenne, K. Thielemans, M. Goldman, and V. Flamand. 2003. Dendritic cells overexpressing CD95 (Fas) ligand elicit vigorous allospecific T-cell responses in vivo. Blood 101: 1469-1476. (Pubitemid 36182522)
25. Woerly, G., K. Honda, M. Loyens, J. P. Papin, J. Auwerx, B. Staels, M. Capron, and D. Dombrowicz. 2003. Peroxisome proliferator-activated receptors alpha and gamma down-regulate allergic inflammation and eosinophil activation. J. Exp. Med. 198: 411-421.
26. Abramowicz, D., P. Vandervorst, C. Bruyns, J. M. Doutrelepont, P. Vandenabeele, and M. Goldman. 1990. Persistence of anti-donor allohelper T cells after neonatal induction of allotolerance in mice. Eur. J. Immunol. 20: 1647-1653.
27. Powell, T. J., Jr., and J. W. Streilein. 1990. Neonatal tolerance induction by class II alloantigens activates IL-4-secreting, tolerogen-responsive T cells. J. Immunol. 144: 854-859.
28. Schurmans, S., C. H. Heusser, H. Y. Qin, J. Merino, G. Brighouse, and P. H. Lambert. 1990. In vivo effects of anti-IL-4 monoclonal antibody on neonatal induction of tolerance and on an associated autoimmune syndrome. J. Immunol. 145: 2465-2473.
29. Donckier, V., M. Wissing, C. Bruyns, D. Abramowicz, M. Lybin, M.-L. Vanderhaeghen, and M. Goldman. 1995. Critical role of interleukin 4 in the induction of neonatal transplantation tolerance. Transplantation 59: 1571-1576.
30. Ridge, J. P., E. J. Fuchs, and P. Matzinger. 1996. Neonatal tolerance revisited: turning on newborn T cells with dendritic cells. Science 271: 1723-1726.
31. Lertmemongkolchai, G., G. Cai, C. A. Hunter, and G. J. Bancroft. 2001. Bystander activation of CD8+ T cells contributes to the rapid production of IFN-γ in response to bacterial pathogens. J. Immunol. 166: 1097-1105.
32. Karwot, R., J. H. Maxeiner, S. Schmitt, P. Scholtes, M. Hausding, H. A. Lehr, L. H. Glimcher, and S. Finotto. 2008. Protective role of nuclear factor of activated T cells 2 in CD8+ long-lived memory T cells in an allergy model. J. Allergy Clin. Immunol. 121: 992-999.e6.
33. Cohn, L., R. J. Homer, N. Niu, and K. Bottomly. 1999. T helper 1 cells and interferon gamma regulate allergic airway inflammation and mucus production. J. Exp. Med. 190: 1309-1318.
34. Trujillo-Vargas, C. M., K. D. Mayer, T. Bickert, A. Palmetshofer, S. Grunewald, J. R. Ramirez-Pineda, T. Polte, G. Hansen, G. Wohlleben, and K. J. Erb. 2005. Vaccinations with T-helper type 1 directing adjuvants have different suppressive effects on the development of allergen-induced T-helper type 2 responses. Clin. Exp. Allergy 35: 1003-1013.
35. Wells, J. W., C. J. Cowled, A. Giorgini, D. M. Kemeny, and A. Noble. 2007. Regulation of allergic airway inflammation by class I-restricted allergen presentation and CD8 T-cell infiltration. J. Allergy Clin. Immunol. 119: 226-234.
36. Kambayashi, T., E. Assarsson, A. E. Lukacher, H.-G. Ljunggren, and P. E. Jensen. 2003. Memory CD8+ T cells provide an early source of IFN-γ. J. Immunol. 170: 2399-2408.
37. Min, B., R. McHugh, G. D. Sempowski, C. Mackall, G. Foucras, and W. E. Paul. 2003. Neonates support lymphopenia-induced proliferation. Immunity 18: 131-140.
38. Schüler, T., G. J. Hämmerling, and B. Arnold. 2004. Cutting edge: IL-7-dependent homeostatic proliferation of CD8+ T cells in neonatal mice allows the generation of long-lived natural memory T cells. J. Immunol. 172: 15-19. (Pubitemid 38020449)
39. Cho, B. K., V. P. Rao, Q. Ge, H. N. Eisen, and J. Chen. 2000. Homeostasis-stimulated proliferation drives naive T cells to differentiate directly into memory T cells. J. Exp. Med. 192: 549-556.
40. + T cell memory. Science 297: 2060-2063.
41. Koschella, M., D. Voehringer, and H. Pircher. 2004. CD40 ligation in vivo induces bystander proliferation of memory phenotype CD8 T cells. J. Immunol. 172: 4804-4811. (Pubitemid 38456402)
42. + T cells. Curr. Opin. Immunol. 13: 465-470.
43. Andrassy, J., S. Kusaka, E. Jankowska-Gan, J. R. Torrealba, L. D. Haynes, B. R. Marthaler, R. C. Tam, B. M.-W. Illigens, N. Anosova, G. Benichou, and W. J. Burlingham. 2003. Tolerance to noninherited maternal MHC antigens in mice. J. Immunol. 171: 5554-5561.
44. Aoyama, K., M. Koyama, K. Matsuoka, D. Hashimoto, T. Ichinohe, M. Harada, K. Akashi, M. Tanimoto, and T. Teshima. 2009. Improved outcome of allogeneic bone marrow transplantation due to breastfeeding-induced tolerance to maternal antigens. Blood 113: 1829-1833.
45. Burlingham, W. J., A. P. Grailer, D. M. Heisey, F. H. Claas, D. Norman, T. Mohanakumar, D. C. Brennan, H. de Fijter, T. van Gelder, J. D. Pirsch, et al. 1998. The effect of tolerance to noninherited maternal HLA antigens on the survival of renal transplants from sibling donors. N. Engl. J. Med. 339: 1657-1664.
46. Opiela, S. J., R. B. Levy, and B. Adkins. 2008. Murine neonates develop vigorous in vivo cytotoxic and Th1/Th2 responses upon exposure to low doses of NIMA-like alloantigens. Blood 112: 1530-1538.
47. Mold, J. E., J. Michaëlsson, T. D. Burt, M. O. Muench, K. P. Beckerman, M. P. Busch, T.-H. Lee, D. F. Nixon, and J. M. McCune. 2008. Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero. Science 322: 1562-1565.