Evaluation of T cell responses in healing and nonhealing leishmaniasis reveals differences in T helper cell polarization ex vivo and in vitro

Parasite Immunology

Volumn 31, Issue 4, 2009, Pages 199-209

  Choi, B S ^a   Kropf, P ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Cell proliferation; T cells; Th1 Th2 cells

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BAGG ALBINO MOUSE; CBA MOUSE; CD4+ T LYMPHOCYTE; CELL POLARITY; CELLULAR IMMUNITY; CONTROLLED STUDY; EFFECTOR CELL; EXPERIMENTAL INFECTION; FEMALE; HEALING; LEISHMANIASIS; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-4; LEISHMANIASIS, CUTANEOUS; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED CBA; REGENERATION;

LEISHMANIA MAJOR; MUS;

EID: 62149148446     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2009.01094.x     Document Type: Article

References (43)

1. Etges R Müller I. Progressive disease or protective immunity to Leishmania major infection: the result of a network of stimulatory and inhibitory interactions. J Mol Med 1998 76 : 372 390.
2. Sacks DL Noben-Trauth N. The immunology of susceptibility and resistance to Leishmania major in mice. Nature Rev Immunol 2002 2 : 845 858.
3. Alexander J Bryson K. T helper (h) 1/Th2 and Leishmania: paradox rather than paradigm. Immunol Lett 2005 99 : 17 23.
4. Wei X, Charles IG, Smith A, et al. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 1995 375 : 408 411.
5. Munder M, Eichmann K Modolell M. Alternative metabolic states in murine macrophages reflected by the nitric oxide synthase/arginase balance: competitive regulation by CD4+ T cells correlates with Th1/Th2 phenotype. J Immunol 1998 160 : 5347 5354.
6. Iniesta V, Gomez-Nieto LC Corraliza I. The inhibition of Arginase by Nw-Hydroxy-L-Arginine controls the growths of Leishmania inside macrophages. J Exp Med 2001 193 : 777 783.
7. Kropf P, Fuentes JM, Fahnrich E, et al. Arginase and polyamine synthesis are key factors in the regulation of experimental leishmaniasis in vivo. FASEB J 2005 19 : 1000 1002.
8. Mosmann TR Moore KW. The role of IL-10 in crossregulation of TH1 and TH2 responses. Immunol Today 1991 12 : A49 A53.
9. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM Sacks DL. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 2002 420 : 502 507.
10. Anderson CF, Oukka M, Kuchroo VJ Sacks D. CD4(+)CD25(-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J Exp Med 2007 204 : 285 297.
11. Kropf P., Brunson K, Etges R Müller I. The Leishmaniasis Model. In Kaufmann Kabeliz (eds) : Immunology of Infection, Vol 25 San Diego, Academic Press, 1998 : 419 458.
12. Herath S, Kropf P Müller I. Cross-talk between CD8+ and CD4+ T cells in experimental cutaneous leishmaniasis: CD8+ T cells are required for optimal IFN-γ production by CD4+ T cells. Parasite Immunol 2003 25 : 559 567.
13. Kropf P, Herath S, Tewari R, Syed N, Klemenz R Müller I. Identification of two distinct subpopulations of Leishmania major specific T helper 2 cells. Infect Immun 2002 70 : 5512 5520.
14. Darrah PA, Patel DT, De Luca PM, et al. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 2007 13 : 843 850.
15. Kropf P, Bickle Q, Klemenz R Müller I. Organ-specific distribution of CD4+T1/ST2+Th2 cells in Leishmania major infection. Eur J Immunol 2002 32 : 2450 2459.
16. Nylen S Sacks D. Interleukin-10 and the pathogenesis of human visceral leishmaniasis. Trends Immunol 2007 28 : 378 384.
17. Wang Z-E, Reiner SL, Zheng S, Dalton DK Locksley RM. CD4+ effector cells default to the Th2 pathway in interferon g deficient mice infected with Leishmania major. J Exp Med 1994 179 : 1367 1371.
18. Swihart K, Fruth U, Messmer N, et al. Mice from a genetically resistant background lacking the Interferon-g receptor are susceptible to infection with Leishmania major but mount a polarized T helper cell 1-type CD4+ T cell response. J Exp Med 1995 181 : 961 971.
19. Mattner F, Magram J, Ferrante J, et al. Genetically resistant mice lacking interleukin-12 are susceptible to infection with Leishmania major and mount a polarized Th2 cell response. Eur J Immunol 1996 26 : 1553 1559.
20. Noben-Trauth N, Kropf P Müller I. Susceptibility to Leishmania major infection in interleukin-4 deficient mice. Science 1996 271 : 987 990.
21. Noben-Trauth N, Paul WE Sacks DL. IL-4 and IL-4 receptor-deficient BALB/c mice reveal differences in susceptibility to Leishmania major parasite substrains. In J Immunol 1999 162 : 6132 6140.
22. Dent AL, Doherty TM, Paul WE, Sher A Staudt LM. BCL-6-deficient mice reveal an IL-4 independent STAT6 dependent pathway that controls susceptibility to infection by Leishmania major. In J Immunol 1999; 163 : 2098 2103.
23. Heinzel FP Maier RA. Interleukin-4-independent acceleration of cutaneous leishmaniasis in susceptible BALB/c mice following treatment with anti-CTLA4 antibody. Infect Immun 1999 67 : 6454 6460.
24. Anderson CF, Mendez S Sacks DL. Nonhealing infection despite Th1 polarization produced by a strain of Leishmania major in C57BL/6 mice. J Immunol 2005 174 : 2934 2941.
25. Carter KC, Gallagher G, Baillie AJ Alexander J. The induction of protective immunity to Leishmania major in the BALB/c mouse by interleukin 4 treatment. Eur J Immunol 1989 19 : 779 782.
26. Biedermann T, Zimmermann S, Himmelrich H, et al. IL-4 instructs TH1 responses and resistance to Leishmania major in susceptible BALB/c mice. Nature Immunol 2001 2 : 1054 1060.
27. Sadick MD, Heinzel FP, Holaday BJ, Pu RT, Dawkins RS Locksley RM. Cure of murine leishmaniasis with anti-interleukin-4 monoclonal antibody. Evidence for a T-cell-dependent, interferon-g-independent mechanism. J Exp Med 1990 171 : 115 127.
28. Kenney RT, Sacks DL, Gam AA, Murray HW Sundar S. Splenic cytokine responses in Indian Kala-Azar before and after treatment. J Infect Dis 1998 177 : 815 819.
29. Nylen S, Maurya R, Eidsmo L, Manandhar KD, Sundar S Sacks D. Splenic accumulation of IL-10 mRNA in T cells distinct from CD4+CD25+ (Foxp3) regulatory T cells in human visceral leishmaniasis. J Exp Med 2007 204 : 805 817.
30. Kurkjian KM, Mahmutovic AJ, Kellar KL, Haque R, Bern C Secor WE. Multiplex analysis of circulating cytokines in the sera of patients with different clinical forms of visceral leishmaniasis. Cytometry A 2006 69 : 353 358.
31. Ansari NA, Saluja S Salotra P. Elevated levels of interferon-gamma, interleukin-10, and interleukin-6 during active disease in Indian kala azar. Clin Immunol 2006 119 : 339 345.
32. Reiner SL, Zheng S, Wang Z-E, Stowring L Locksley RM. Leishmania promastigotes evade interleukin 12 (IL-12) induction by macrophages and stimulate a broad range of cytokines from CD4+ T cells during initiation of infection. J Exp Med 1994 179 : 447 456.
33. Heinzel FP, Sadick MD, Mutha SS Locksley RM. Production of interferon g, interleukin 2, interleukin 4, and interleukin 10 by CD4+ lymphocytes in vivo during healing and progressive murine leishmaniasis. Proc Natl Acad Sci USA 1991 88 : 7011 7015.
34. Nicolas L, Sidjanski S, Colle J-H Milon G. 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 2002 68 : 6561 6566.
35. Oswald IP, Gazzinelli RT, Sher A James SL. IL-10 synergizes with IL-4 and transforming growth factor-b to inhibit macrophage cytotoxic activity. J Immunol 1992 148 : 3578 3582.
36. Peters N Sacks D. Immune privilege in sites of chronic infection: Leishmania and regulatory T cells. Immunol Rev 2006 213 : 159 179.
37. Noben-Trauth N, Lira R, Nagase H, Paul WE Sacks DL. The relative contribution of IL-4 receptor signaling and IL-10 to susceptibility to Leishmania major. J Immunol 2003 170 : 5152 5158.
38. Kane MM Mosser DM. The role of IL-10 in promoting disease progression in leishmaniasis. J Immunol 2001 166 : 1141 1147.
39. Belkaid Y, Kamhawi S, Modi G, et al. 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 1998 188 : 1941 1953.
40. Rogers ME, Ilg T, Nikolaev AV, Ferguson MAJ Bates PA. Transmission of cutaneous leishmaniasis by sandflies is enhanced by regurgitation of fPPG. Nature 2004 430 : 463 467.
41. Kimblin N, Peters N, Debrabant A, et al. Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proc Natl Acad Sci USA 2008 105 : 10125 10130.
42. Nabors GS, Nolan T, Croop W, Li J Farrell JP. The influence of the site of parasite inoculation on the development of Th1 and Th2 type responses in (BALB/cxC57BL/6), F1 mice infected with Leishmania major. Parasite Immunol 17 : 1995 : 569 579.
43. Titus RG Ribeiro JM. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 1988 239 : 1306 1308.