CD4+CD25-Foxp3- Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis

Journal of Experimental Medicine

Volumn 204, Issue 2, 2007, Pages 285-297

  Anderson, Charles F ^a   Oukka, Mohammed ^b   Kuchroo, Vijay J ^b   Sacks, David ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ CD25- T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL POLARITY; CONTROLLED STUDY; FEEDBACK SYSTEM; IMMUNE RESPONSE; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; INNATE IMMUNITY; LEISHMANIA MAJOR; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SKIN DEFECT; SKIN LEISHMANIASIS; T CELL DEPLETION; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

ANIMALS; DNA-BINDING PROTEINS; FLOW CYTOMETRY; IMMUNOBLOTTING; INTERFERON TYPE II; INTERLEUKIN-10; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, REGULATORY; TH1 CELLS;

EID: 33847163271     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20061886     Document Type: Article

References (62)

1. Sacks, D., and N. Noben-Trauth. 2002. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2:845-858.
2. Melby, P.C., F.J. Andrade-Narvaez, B.J. Darnell, G. Valencia-Pacheco, V.V. Tryon, and A. Palomo-Cetina. 1994. Increased expression of proinflammatory cytokines in chronic lesions of human cutaneous leishmaniasis. Infect. Immun. 62:837-842.
3. Louzir, H., P.C. Melby, A. Ben Salah, H. Marrakchi, K. Aoun, R. Ben Ismail, and K. Dellagi. 1998. Immunologic determinants of disease evolution in localized cutaneous leishmaniasis due to Leishmania major. J. Infect. Dis. 177:1687-1695.
4. Gasim, S., A.M. Elhassan, E.A. Khalil, A. Ismail, A.M. Kadaru, A. Kharazmi, and T.G. Theander. 1998. High levels of plasma IL-10 and expression of IL-10 by keratinocytes during visceral leishmaniasis predict subsequent development of post-kala-azar dermal leishmaniasis. Clin. Exp. Immunol. 111:64-69. (published erratum appears in Clin. Exp. Immunol. 1998. 112:547)
5. Ismail, A., A.M. El Hassan, K. Kemp, S. Gasim, A.E. Kadaru, T. Moller, A. Kharazmi, and T.G. Theander. 1999. Immunopathology of post kala-azar dermal leishmaniasis (PKDL): T-cell phenotypes and cytokine profile. J. Pathol. 189:615-622.
6. Ghalib, H.W., M.R. Piuvezam, Y.A. Skeiky, M. Siddig, F.A. Hashim, A.M. el-Hassan, D.M. Russo, and S.G. Reed. 1993. Interleukin 10 production correlates with pathology in human Leishmania donovani infections. J. Clin. Invest. 92:324-329.
7. Karp, C.L., S.H. el-Safi, T.A. Wynn, M.M. Satti, A.M. Kordofani, F.A. Hashim, M. Hag-Ali, F.A. Neva, T.B. Nutman, and D.L. Sacks. 1993. In vivo cytokine profiles in patients with kala-azar. Marked elevation of both interleukin-10 and interferon-gamma. J. Clin. Invest. 91:1644-1648.
8. Kenney, R.T., D.L. Sacks, A.A. Gam, H.W. Murray, and S. Sundar. 1998. Splenic cytokine responses in Indian kala-azar before and after treatment. J. Infect. Dis. 177:815-818.
9. Murray, H.W., C.M. Lu, S. Mauze, S. Freeman, A.L. Moreira, G. Kaplan, and R.L. Coffman. 2002. Interleukin-10 (IL-10) in experimental visceral leishmaniasis and IL-10 receptor blockade as immunotherapy. Infect. Immun. 70:6284-6293.
10. Murphy, M.L., U. Wille, E.N. Villegas, C.A. Hunter, and J.P. Farrell. 2001. IL-10 mediates susceptibility to Leishmania donovani infection. Eur. J. Immunol. 31:2848-2856.
11. Buxbaum, L.U., and P. Scott. 2005. Interleukin 10- and Fcgamma receptor-deficient mice resolve Leishmania mexicana lesions. Infect. Immun. 73:2101-2108.
12. Noben-Trauth, N., R. Lira, H. Nagase, W.E. Paul, and D.L. Sacks. 2003. The relative contribution of IL-4 receptor signaling and IL-10 to susceptibility to Leishmania major. J. Immunol. 170:5152-5158.
13. Anderson, C.F., S. Mendez, and D.L. Sacks. 2005. Nonhealing infection despite Th1 polarization produced by a strain of Leishmania major in C57BL/6 mice. J. Immunol. 174:2934-2941.
14. Moore, K.W., R. de Waal Malefyt, R.L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19:683-765.
15. Kane, M.M., and D.M. Mosser. 2001. The role of IL-10 in promoting disease progression in leishmaniasis. J. Immunol. 166:1141-1147.
16. Miles, S.A., S.M. Conrad, R.G. Alves, S.M. Jeronimo, and D.M. Mosser. 2005. A role for IgG immune complexes during infection with the intracellular pathogen Leishmania. J. Exp. Med. 201:747-754.
17. Groux, H., F. Cottrez, M. Rouleau, S. Mauze, S. Antonenko, S. Hurst, T. McNeil, M. Bigler, M.G. Roncarolo, and R.L. Coffman. 1999. A transgenic model to analyze the immunoregulatory role of IL-10 secreted by antigen-presenting cells. J. Immunol. 162:1723-1729.
18. Stager, S., A. Maroof, S. Zubairi, S.L. Sanos, M. Kopf, and P.M. Kaye. 2006. Distinct roles for IL-6 and IL-12p40 in mediating protection against Leishmania donovani and the expansion of IL-10(+) CD4(+) T cells. Eur. J. Immunol. 36:1764-1771.
19. Belkaid, Y., C.A. Piccirillo, S. Mendez, E.M. Shevach, and D.L. Sacks. 2002. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature. 420:502-507.
20. Belkaid, Y., and B.T. Rouse. 2005. Natural regulatory T cells in infectious disease. Nat. Immunol. 6:353-360.
21. Sakaguchi, S. 2004. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22:531-562.
22. Mills, K.H., and P. McGuirk. 2004. Antigen-specific regulatory T cells-their induction and role in infection. Semin. Immunol. 16:107-117.
23. O'Garra, A., P.L. Vieira, P. Vieira, and A.E. Goldfeld. 2004. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J. Clin. Invest. 114:1372-1378.
24. + T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196:505-515.
25. McGuirk, P., C. McCann, and K.H. Mills. 2002. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J. Exp. Med. 195:221-231.
26. Boussiotis, V.A., E.Y. Tsai, E.J. Yunis, S. Thim, J.C. Delgado, C.C. Dascher, A. Berezovskaya, D. Rousset, J.M. Reynes, and A.E. Goldfeld. 2000. IL-10-producing T cells suppress immune responses in anergic tuberculosis patients. J. Clin. Invest. 105:1317-1325.
27. Satoguina, J., M. Mempel, J. Larbi, M. Badusche, C. Loliger, O. Adjei, G. Gachelin, B. Fleischer, and A. Hoerauf. 2002. Antigen-specific T regulatory-1 cells are associated with immunosuppression in a chronic helminth infection (onchocerciasis). Microbes Infect. 4:1291-1300.
28. Noble, A., A. Giorgini, and J.A. Leggat. 2006. Cytokine-induced IL-10-secreting CD8 T cells represent a phenotypically distinct suppressor T-cell lineage. Blood. 107:4475-4483.
29. Suffia, I., S.K. Reckling, G. Salay, and Y. Belkaid. 2005. A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection. J. Immunol. 174:5444-5455.
30. Padigel, U.M., and J.P. Farrell. 2005. Control of infection with Leishmania major in susceptible BALB/c mice lacking the common gamma-chain for FcR is associated with reduced production of IL-10 and TGF-beta by parasitized cells. J. Immunol. 174:6340-6345.
31. Apostolou, I., A. Sarukhan, L. Klein, and H. von Boehmer. 2002. Origin of regulatory T cells with known specificity for antigen. Nat. Immunol. 3:756-763.
32. Zelenay, S., T. Lopes-Carvalho, I. Caramalho, M.F. Moraes-Fontes, M. Rebelo, and J. Demengeot. 2005. Foxp3+ CD25? CD4 T cells constitute a reservoir of committed regulatory cells that regain CD25 expression upon homeostatic expansion. Proc. Natl. Acad. Sci. USA. 102:4091-4096.
33. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T.B. Strom, M. Oukka, H.L. Weiner, and V.K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 441:235-238.
34. Asseman, C., S. Mauze, M.W. Leach, R.L. Coffman, and F. Powrie. 1999. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190:995-1004.
35. Liu, H., B. Hu, D. Xu, and F.Y. Liew. 2003. CD4+CD25+ regulatory T cells cure murine colitis: the role of IL-10, TGF-beta, and CTLA4. J. Immunol. 171:5012-5017.
36. Sacks, D., and C. Anderson. 2004. Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Immunol. Rev. 201:225-238.
37. Belkaid, Y., S. Mendez, R. Lira, N. Kadambi, G. Milon, and D. Sacks. 2000. A natural model of Leishmania major infection reveals a prolonged "silent" phase of parasite amplification in the skin before the onset of lesion formation and immunity. J. Immunol. 165:969-977.
38. + T cells during initiation of infection. J. Exp. Med. 179:447-456.
39. Ji, J., J. Masterson, J. Sun, and L. Soong. 2005. CD4+CD25+ regulatory T cells restrain pathogenic responses during Leishmania amazonensis infection. J. Immunol. 174:7147-7153.
40. Aseffa, A., A. Gumy, P. Launois, H.R. MacDonald, J.A. Louis, and F. Tacchini-Cottier. 2002. The early IL-4 response to Leishmania major and the resulting Th2 cell maturation steering progressive disease in BALB/c mice are subject to the control of regulatory CD4+CD25+ T cells. J. Immunol. 169:3232-3241.
41. Xu, D., H. Liu, M. Komai-Koma, C. Campbell, C. McSharry, J. Alexander, and F.Y. Liew. 2003. CD4+CD25+ regulatory T cells suppress differentiation and functions of Th1 and Th2 cells, Leishmania major infection, and colitis in mice. J. Immunol. 170:394-399.
42. Bluestone, J.A., and A.K. Abbas. 2003. Natural versus adaptive regulatory T cells. Nat. Rev. Immunol. 3:253-257.
43. Plebanski, M., K.L. Flanagan, E.A. Lee, W.H. Reece, K. Hart, C. Gelder, G. Gillespie, M. Pinder, and A.V. Hill. 1999. Interleukin 10-mediated immunosuppression by a variant CD4 T cell epitope of Plasmodium falciparum. Immunity. 10:651-660.
44. + T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2-inducing cytokines. J. Exp. Med. 195:603-616.
45. Groux, H., A. O'Garra, M. Bigler, M. Rouleau, S. Antonenko, J.E. de Vries, and M.G. Roncarolo. 1997. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 389:737-742.
46. + T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J. Exp. Med. 192:1213-1222.
47. Levings, M.K., S. Gregori, E. Tresoldi, S. Cazzaniga, C. Bonini, and M.G. Roncarolo. 2005. Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells. Blood. 105:1162-1169.
48. Battaglia, M., S. Gregori, R. Bacchetta, and M.G. Roncarolo. 2006. Tr1 cells: from discovery to their clinical application. Semin. Immunol. 18:120-127.
49. Trinchieri, G. 2001. Regulatory role of T cells producing both interferon γ and interleukin 10 in persistent infection. J. Exp. Med. 194:F53-F57.
50. Gerosa, F., C. Nisii, S. Righetti, R. Micciolo, M. Marchesini, A. Cazzadori, and G. Trinchieri. 1999. CD4(+) T cell clones producing both interferon-gamma and interleukin-10 predominate in bronchoalveolar lavages of active pulmonary tuberculosis patients. Clin. Immunol. 92:224-234.
51. Pohl-Koppe, A., K.E. Balashov, A.C. Steere, E.L. Logigian, and D.A. Hafler. 1998. Identification of a T cell subset capable of both IFNgamma and IL-10 secretion in patients with chronic Borrelia burgdorferi infection. J. Immunol. 160:1804-1810.
52. Winkler, S., M. Willheim, K. Baier, D. Schmid, A. Aichelburg, W. Graninger, and P.G. Kremsner. 1998. Reciprocal regulation of Th1- and Th2-cytokine-producing T cells during clearance of parasitemia in Plasmodium falciparum malaria. Infect. Immun. 66:6040-6044.
53. Jankovic, D., M.C. Kullberg, S. Hieny, P. Caspar, C.M. Collazo, and A. Sher. 2002. In the absence of IL-12, CD4(+) T cell responses to intracellular pathogens fail to default to a Th2 pattern and are host protective in an IL-10(?/?) setting. Immunity. 16:429-439.
54. Sarawar, S.R., and P.C. Doherty. 1994. Concurrent production of interleukin-2, interleukin-10, and gamma interferon in the regional lymph nodes of mice with influenza pneumonia. J. Virol. 68:3112-3119.
55. Svetic, A., Y.C. Jian, P. Lu, F.D. Finkelman, and W.C. Gause. 1993. Brucella abortus induces a novel cytokine gene expression pattern characterized by elevated IL-10 and IFN-gamma in CD4+ T cells. Int. Immunol. 5:877-883.
56. Gerosa, F., C. Paganin, D. Peritt, F. Paiola, M.T. Scupoli, M. Aste-Amezaga, I. Frank, and G. Trinchieri. 1996. Interleukin-12 primes human CD4 and CD8 T cell clones for high production of both interferon-gamma and interleukin-10. J. Exp. Med. 183:2559-2569.
57. Meyaard, L., E. Hovenkamp, S.A. Otto, and F. Miedema. 1996. IL-12-induced IL-10 production by human T cells as a negative feedback for IL-12-induced immune responses. J. Immunol. 156:2776-2782.
58. Shaw, M.H., G.J. Freeman, M.F. Scott, B.A. Fox, D.J. Bzik, Y. Belkaid, and G.S. Yap. 2006. Tyk2 negatively regulates adaptive Th1 immunity by mediating IL-10 signaling and promoting IFN-gamma-dependent IL-10 reactivation. J. Immunol. 176:7263-7271.
59. - Th1 cells are the major source of host-protective regulatory IL-10 during intracellular protozoan infection. J. Exp. Med. 204:273-283.
60. Stager, S., A. Maroof, S. Zubairi, S.L. Sanos, M. Kopf, and P.M. Kaye. 2006. Distinct roles for IL-6 and IL-12p40 in mediating protection against Leishmania donovani and the expansion of IL-10+ CD4+ T cells. Eur. J. Immunol. 36:1764-1771.
61. Assenmacher, M., M. Lohning, A. Scheffold, R.A. Manz, J. Schmitz, and A. Radbruch. 1998. Sequential production of IL-2, IFN-gamma and IL-10 by individual staphylococcal enterotoxin B-activated T helper lymphocytes. Eur. J. Immunol. 28:1534-1543.
62. Spath, G.F., and S.M. Beverley. 2001. A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Exp. Parasitol. 99:97-103.