Role for CD4+ CD25+ regulatory T cells in reactivation of persistent Leishmaniasis and control of concomitant immunity

Journal of Experimental Medicine

Volumn 200, Issue 2, 2004, Pages 201-210

  Mendez, Susana ^a,c   Reckling, Stacie K ^b   Piccirillo, Ciriacco A ^a,d   Sacks, David ^a   Belkaid, Yasmine ^b  

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

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^c GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

CD4+ CD25+; Chronicity; Leishmania; Memory; Reactivation; Regulatory T cells

Indexed keywords

CD4 ANTIGEN; INTERLEUKIN 2 RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNITY; IMMUNOLOGICAL MEMORY; IMMUNOREGULATION; LEISHMANIA; LEISHMANIASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PURIFICATION; SUPERINFECTION; T LYMPHOCYTE;

ANIMALS; ANTIGENS, CD4; CD4-POSITIVE T-LYMPHOCYTES; CELL MOVEMENT; CYTOKINES; IMMUNOLOGIC MEMORY; IMMUNOSUPPRESSION; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; LYMPHOCYTE ACTIVATION; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; RECEPTORS, INTERLEUKIN-2; SKIN; T-LYMPHOCYTES; TIME FACTORS;

EID: 3242787209     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20040298     Document Type: Article

References (50)

1. Stenger, S., N. Donhauser, H. Thuring, M. Rollinghoff, and C. Bogdan. 1996. Reactivation of latent leishmaniasis by inhibition of inducible nitric oxide synthase. J. Exp. Med. 183: 1501-1514.
2. Vardy, D.A., A. Cohen, L. Kachko, A. Zvulunov, and S. Frankenburg. 1999. Relapse of cutaneous leishmaniasis in a patient with an infected subcutaneous rheumatoid nodule. Br. J. Dermatol. 141:914-917.
3. Alvar, J., C. Canavate, B. Gutierrez-Solar, M. Jimenez, F. Laguna, R. Lopez-Velez, R. Molina, and J. Moreno. 1997. Leishmania and human immunodeficiency virus coinfection: the first 10 years. Clin. Microbiol. Rev. 10:298-319.
4. el Hassan, A.M., H.W. Ghalib, E.E. Zijlstra, I.A. Eltoum, M. Satti, M.S. Ali, and H.M. Ali. 1992. Post kala-azar dermal leishmaniasis in the Sudan: clinical features, pathology and treatment. Trans. R. Soc. Trop. Med. Hyg. 86:245-248.
5. Choi, C.M., and E.A. Lerner. 2001. Leishmaniasis as an emerging infection. J. Invest. Dermatol. 6:175-182.
6. Saravia, N.G., A.F. Holguin, D. McMahon-Pratt, and A. D'Alessandro. 1985. Mucocutaneous leishmaniasis in Colombia: Leishmania braziliensis subspecies diversity. Am. J. Trop. Med. Hyg. 34:714-720.
7. Da-Cruz, A.M., D.V. Filgueiras, Z. Coutinho, W. Mayrink, G. Grimaldi, Jr., P.M. De Luca, S.C. Mendonca, and S.G. Coutinho. 1999. Atypical mucocutaneous leishmaniasis caused by Leishmania braziliensis in an acquired immunodeficiency syndrome patient: T-cell responses and remission of lesions associated with antigen immunotherapy. Mem. Inst. Oswaldo Cruz. 94:537-542.
8. Reiner, S.L., and R.M. Locksley. 1995, The regulation of immunity to Leishmania major. Annu. Rev. Immunol. 13:151-177.
9. Belkaid, Y., S. Kamhawi, G. Modi, J. Valenzuela, N. Noben-Trauth, E. Rowton, J. Ribeiro, and D.L. Sacks. 1998. Development of a natural model of cutaneous leishmaniasis: powerful effects of vector saliva and saliva preexposure on the long-term outcome of Leishmania major infection in the mouse ear dermis. J. Exp. Med. 188:1941-1953.
10. Nicolas, L., S. Sidjanski, J.H. Colle, and G. Milon. 2000. Leishmania major reaches distant cutaneous sites where it persists transiently while persisting durably in the primary dermal site and its draining lymph node: a study with laboratory mice. Infect. Immun. 68:6561-6566.
11. Aebischer, T., S.F. Moody, and E. Handman. 1993. Persistence of virulent Leishmania major in murine cutaneous leishmaniasis: a possible hazard for the host. Infect. Immun. 61: 220-226.
12. Ramirez, J.L., and P. Guevara. 1997. Persistent infections by Leishmania (Viannia) braziliensis. Mem. Inst. Oswaldo Cruz. 92: 333-338.
13. Shevach, E.M. 2002. CD4+ CD25+ suppressor T cells: more questions than answers. Nat. Rev. Immunol. 2:389-400.
14. Gavin, M.A., S.R. Clarke, E. Negrou, A. Gallegos, and A. Rudensky. 2002. Homeostasis and anergy of CD4(+) CD25(+) suppressor T cells in vivo. Nat. Immunol. 3:33-41.
15. Maloy, K.J., and F. Powrie. 2001. Regulatory T cells in the control of immune pathology. Nat. Immunol. 2:816-822.
16. Asseman, C., and M. von Herrath. 2002. About CD4pos CD25pos regulatory cells. Autoimmun. Rev. 1:190-197.
17. Belkaid, Y., A.C. Piccirilo, S. Mendez, E. Shevack, and D.L. Sacks. 2002. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature. 420:502-507.
18. Belkaid, Y., E. Von Stebut, S. Mendez, R. Lira, E. Caler, S. Bertholet, M.C. Udey, and D. Sacks. 2002. CD8(+) T cells are required for primary immunity in C57BL/6 mice following low-dose, intradermal challenge with Leishmania major. J. Immunol. 168:3992-4000.
19. Belkaid, Y., K.F. Hoffmann, S. Mendez, S. Kamhawi, M.C. Udey, T.A. Wynn, and D.L. Sacks. 2001. The role of interleukin (IL)-10 in the persistence of Leishmania major in the skin after healing and the therapeutic potential of anti-IL-10 receptor antibody for sterile cure. J. Exp. Med. 194:1497-1506.
20. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J. Exp. Med. 188:287-296.
21. 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.
22. Muller, I., and J.A. Louis. 1989. Immunity to experimental infection with Leishmania major: generation of protective L3T4+ T cell clones recognizing antigen(s) associated with live parasites. Eur. J. Immunol. 19:865-871.
23. Stobie, L., S. Gurunathan, C. Prussin, D.L. Sacks, N. Glaichenhaus, C.Y. Wu, and R.A. Seder. 2000. The role of antigen and IL-12 in sustaining Th1 memory cells in vivo: IL-12 is required to maintain memory/effector Th1 cells sufficient to mediate protection to an infectious parasite challenge. Proc. Natl. Acad. Sci. USA. 97:8427-8432.
24. Preston, P.M., and D.C. Dumonde. 1976. Experimental cutaneous leishmaniasis. V. Protective immunity in subclinical and self-healing infection in the mouse. Clin. Exp. Immunol. 23:126-138.
25. Muller, I. 1992. Role of T cell subsets during the recall of immunologic memory to Leishmania major. Eur. J. Immunol. 22:3063-3069.
26. 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.
27. Hori, S., T.L. Carvalho, and J. Demengeot. 2002. CD25+ CD4+ regulatory T cells suppress CD4+ T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice. Eur. J. Immunol. 32:1282-1291.
28. Xu, D., L.H. Komai-Koma, M. Campbell, C. Mc, C. Sharry, 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.
29. + T cell responses. J. Exp. Med. 198:889-901.
30. Hisaeda, H., Y. Maekawa, D. Iwakawa, H. Okada, K. Himeno, K. Kishihara, S. Tsukumo, and K. Yasutomo. 2004. Escape of malaria parasites from host immunity requires CD4(+)CD25(+) regulatory T cells. Nat. Med. 10:29-30.
31. Sacks, D., and N. Noben-Trauth. 2002. The immunology of susceptibility and resistance to Leishmania major in mice. Nat. Rev. Immunol. 2:845-858.
32. Qi, H., J. Ji, N. Wanasen, and L. Soong. 2004. Enhanced replication of Leishmania amazonensis amastigotes in gamma interferon-stimulated murine macrophages: implications for the pathogenesis of cutaneous leishmaniasis. Infect. Immun. 72:988-995.
33. Bystry, R.S., V. Aluvihare, K.A. Welch, M. Kallikourdis, and A.G. Betz. 2001. B cells and professional APCs recruit regulatory T cells via CCL4. Nat. Immunol. 2:1126-1132.
34. + regulatory T cells. J. Exp. Med. 194:847-853.
35. Szanya, V., J. Ermann, C. Taylor, C. Holness, and C.G. Fathman. 2002. The subpopulation of CD4+CD25+ splenocytes that delays adoptive transfer of diabetes expresses L-selectin and high levels of CCR7. J. Immunol. 169:2461-2465.
36. Pasare, C., and R. Medzhitov. 2003. Toll pathway-dependent blockade of CD4+ CD25+ T cell-mediated suppression by dendritic cells. Science. 299:1033-1036.
37. Serra, P., A. Amrani, J. Yamanouchi, B. Han, S. Thiessen, T. Utsugi, J. Verdaguer, and P. Santamaria. 2003. CD40 ligation releases immature dendritic cells from the control of regulatory CD4+CD25+ T cells. Immunity. 19:877-889.
38. Choi, B.K., J.S. Bae, E.M. Choi, W.J. Kang, S. Sakaguchi, D.S. Vinay, and B.S. Kwon. 2003. 4-1BB-dependent inhibition of immunosuppression by activated CD4+CD25+ T cells. J. Leukoc. Biol. 75:785-791.
39. Malek, T.R. 2003. The main function of IL-2 is to promote the development of T regulatory cells. J. Leukoc. Biol. 74: 961-965.
40. Thornton, A., C. Piccirillo, and E. Shevach. 2004. Activation requirements for the induction of CD4+CD25+ T cell suppressor function. Eur. J. Immunol. 34:366-376.
41. 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.
42. Kane, M.M., and D.M. Mosser. 2001. The role of IL-10 in promoting disease progression in leishmaniasis. J. Immunol. 166:1141-1147.
43. Yamakami, K., S. Akao, T. Tadakuma, Y. Nitta, J. Miyazaki, and N. Yoshizawa. 2002. Administration of plasmids expressing interleukin-4 and interleukin-10 causes BALB/c mice to induce a T helper 2-type response despite the expected T helper 1-type response with a low-dose infection of Leishmania major. Immunology. 105:515-523.
44. 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.
45. Gazzinelli, R.T., I.P. Oswald, S.L. James, and A. Sher. 1992. IL-10 inhibits parasite killing and nitrogen oxide production by IFN-gamma-activated macrophages. J. Immunol. 148: 1792-1796.
46. Schopf, L.R., K.F. Hoffmann, AW. Cheever, J.F. Urban, Jr., and T.A. Wynn. 2002. IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. J. Immunol. 168:2383-2392.
47. 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.
48. Murray, H.W., A.L. Moreira, C.M. Lu, J.L. DeVecchio, M. Matsuhashi, X. Ma, and F.P. Heinzel. 2003. Determinants of response to interleukin-10 receptor blockade immunotherapy in experimental visceral leishmaniasis. J. Infect. Dis. 188:458-464.
49. Rajagopalan, S. 2001. Tuberculosis and aging: a global health problem. Clin. Infect. Dis. 33:1034-1039.
50. Gane, E., and H. Pilmore. 2002. Management of chronic viral hepatitis before and after renal transplantation. Transplantation. 74:427-437.