Inoculation of killed Leishmania major into immune mice rapidly disrupts immunity to a secondary challenge via IL-10-mediated process

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 33, 2009, Pages 13951-13956

  Okwor, Ifeoma ^a   Liu, Dong ^a   Beverley, Stephen M ^b   Uzonna, Jude E ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytokines; Memory; Parasitic protozoa; Regulatory T cells; Vaccination

Indexed keywords

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

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; DELAYED HYPERSENSITIVITY; FEMALE; IMMUNE RESPONSE; INFLAMMATION; INOCULATION; LEISHMANIA MAJOR; MOUSE; NONHUMAN; PARASITE VIRULENCE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; T LYMPHOCYTE; TRYPANOSOMA CONGOLENSE; VACCINATION;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; FORKHEAD TRANSCRIPTION FACTORS; IMMUNE SYSTEM; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; INTERLEUKIN-4; LEISHMANIA MAJOR; LEISHMANIASIS; LYMPH NODES; MICE; MICE, INBRED C57BL; RECEPTORS, INTERLEUKIN-10; TRYPANOSOMA CONGOLENSE;

LEISHMANIA MAJOR; MUS; PROTOZOA;

EID: 69549126593     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0905184106     Document Type: Article

References (33)

1. Reiner SL, Locksley RM (1995) The regulation of immunity to leishmania major. Annu Rev Immunol 13:151-177.
2. Handman E (2001) Leishmaniasis: Current status of vaccine development. Clin Microbiol Rev 14:229-243. (Pubitemid 32294669)
3. Afonso LC, et al. (1994) The adjuvant effect of interleukin-12 in a vaccine against leishmania major. Science 263:235-237.
4. Gurunathan S, Prussin C, Sacks DL, Seder RA (1998) Vaccine requirements for sustained cellular immunity to an intracellular parasitic infection. Nat Med 4:1409-1415. (Pubitemid 28553464)
5. Aebischer T, Moody SF, Handman E (1993) Persistence of virulent leishmania major in murine cutaneous leishmaniasis: A possible hazard for the host. Infect Immun 61:220-226. (Pubitemid 23015420)
6. Sacks D, Noben-Trauth N (2002) The immunology of susceptibility and resistance to leishmania major in mice. Nat Rev Immunol 2:845-858. (Pubitemid 37328707)
7. Sassi A, et al. (1999) Leishmanin skin test lymphoproliferative responses and cytokine production after symptomatic or asymptomatic leishmania major infection in tunisia. Clin Exp Immunol 116:127-132. (Pubitemid 29170015)
8. Muller I (1992) Role of T cell subsets during the recall of immunologic memory to leishmania major. Eur J Immunol 22:3063-3069.
9. Muller I, Kropf P, Etges RJ, Louis JA (1993) Gamma interferon response in secondary leishmania major infection: Role of CD8+ T cells. Infect Immun 61:3730-3738. (Pubitemid 23260044)
10. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL (2002) CD4+CD25+ regulatory T cells control leishmania major persistence and immunity. Nature 420:502-507.
11. Uzonna JE, Wei G, Yurkowski D, Bretscher P (2001) Immune elimination of leishmania major in mice: Implications for immune memory, vaccination, and reactivation disease. J Immunol 167:6967-6974. (Pubitemid 33144191)
12. Scott P (2005) Immunologic memory in cutaneous leishmaniasis. Cell Microbiol 7:1707-1713.
13. Ben Salah A, et al. (2005) The predictive validity of naturally acquired delayed-type hypersensitivity to leishmanin in resistance to leishmania major-associated cutaneous leishmaniasis. J Infect Dis 192:1981-1987. (Pubitemid 41681897)
14. Michel MY, et al. (2006) The adjuvant effects of IL-12 and BCG on autoclaved Leishmania major vaccine in experimental cutaneous leishmaniasis. J Egypt Soc Parasitol 36:159-176, following 76.
15. Momeni AZ, et al. (1999) A randomised, double-blind, controlled trial of a killed L. major vaccine plus BCG against zoonotic cutaneous leishmaniasis in Iran. Vaccine 17:466-472.
16. Mendez S, et al. (2003) Coinjection with CpG-containing immunostimulatory oligodeoxynucleotides reduces the pathogenicity of a live vaccine against cutaneous leishmaniasis but maintains its potency and durability. Infect Immun 71:5121-5129. (Pubitemid 37070755)
17. Rhee EG, et al. (2002) Vaccination with heat-killed leishmania antigen or recombinant leishmanial protein and CpG oligodeoxynucleotides induces long-term memory CD4+ and CD8+ T cell responses and protection against leishmania major infection. J Exp Med 195:1565-1573.
18. Mendez S, Reckling SK, Piccirillo CA, Sacks D, Belkaid Y (2004) Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J Exp Med 200:201-210. (Pubitemid 38982179)
19. Suffia IJ, Reckling SK, Piccirillo CA, Goldszmid RS, Belkaid Y (2006) Infected siterestricted Foxp3+ natural regulatory T cells are specific for microbial antigens. J Exp Med 203:777-788.
20. Belkaid Y (2003) The role of CD4(+)CD25(+) regulatory T cells in leishmania infection. Expert Opin Biol Ther 3:875-885. (Pubitemid 37093142)
21. Spath GF, et al. (2003) Persistence without pathology in phosphoglycan-deficient leishmania major. Science 301:1241-1243.
22. Titus RG, Gueiros-Filho FJ, de Freitas LA, Beverley SM (1995) Development of a safe live leishmania vaccine line by gene replacement. Proc Natl Acad Sci USA 92:10267-10271.
23. Okwor I, Liu D, Uzonna J (2009) Qualitative differences in the early immune response to live and killed leishmania major: Implications for vaccination strategies against leishmaniasis. Vaccine 27:2554-2562.
24. Anderson CF, Oukka M, Kuchroo VJ, Sacks D (2007) CD4(+)CD25(-)Foxp3(-) Th1 cells are the source of IL-10-mediated immune suppression in chronic cutaneous leishmaniasis. J Exp Med 204:285-297. (Pubitemid 46294545)
25. van Zandbergen G, et al. (2006) Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc Natl Acad Sci USA 103:13837-13842.
26. LaRosa DF, et al. (2007) CpG DNA inhibits CD4+CD25+ treg suppression through direct MyD88-dependent costimulation of effector CD4+ T cells. Immunol Lett 108:183-188.
27. Tiemessen MM, et al. (2007) CD4+CD25+Foxp3+ regulatory T cells induce alternative activation of human monocytes/macrophages. Proc Natl Acad Sci USA 104:19446-19451.
28. Sharifi I, et al. (1998) Randomised vaccine trial of single dose of killed leishmania major plus BCG against anthroponotic cutaneous leishmaniasis in bam, Iran. Lancet 351:1540-1543. (Pubitemid 28230888)
29. Gurunathan S, et al. (1997) Vaccination with DNA encoding the immunodominant LACK parasite antigen confers protective immunity to mice infected with leishmania major. J Exp Med 186:1137-1147. (Pubitemid 27441157)
30. Bousoffara T, Louzir H, Ben Salah A, Dellagi K (2004) Analysis of granzyme B activity as a surrogate marker of leishmania-specific cell-mediated cytotoxicity in zoonotic cutaneous leishmaniasis. J Infect Dis 189:1265-1273. (Pubitemid 38457252)
31. Campanelli AP, et al. (2006) CD4+CD25+ T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. J Infect Dis 193:1313-1322.
32. Zaph C, Uzonna J, Beverley SM, Scott P (2004) Central memory T cells mediate longterm immunity to leishmania major in the absence of persistent parasites. Nat Med 10:1104-1110. (Pubitemid 39424872)
33. Titus RG, Marchand M, Boon T, Louis JA (1985) A limiting dilution assay for quantifying leishmania major in tissues of infected mice. Parasite Immunol 7:545-555. (Pubitemid 16256170)