IL-10 production differentially influences the magnitude, quality, and protective capacity of Th1 responses depending on the vaccine platform

Journal of Experimental Medicine

Volumn 207, Issue 7, 2010, Pages 1421-1433

  Darrah, Patricia A ^a   Hegde, Sonia T ^a   Patel, Dipti T ^a   Lindsay, Ross W B ^a   Chen, Linda ^a   Roederer, Mario ^a   Seder, Robert A ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 2; MML PROTEIN; RECOMBINANT PROTEIN; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; VACCINE;

ADENOVIRUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; IMMUNE RESPONSE; IMMUNIZATION; INNATE IMMUNITY; INTERFERON PRODUCTION; LEISHMANIA MAJOR; LEISHMANIASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL;

ADENOVIRIDAE; ANIMALS; FEMALE; FLOW CYTOMETRY; IMMUNITY, INNATE; IMMUNIZATION; INTERLEUKIN-10; INTERLEUKIN-12; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED C57BL; OLIGODEOXYRIBONUCLEOTIDES; PROTOZOAN PROTEINS; PROTOZOAN VACCINES; SIGNAL TRANSDUCTION; TH1 CELLS;

EID: 77954412167     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20092532     Document Type: Article

References (35)

1. 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.
2. - Th1 cells are the source of IL10- mediated immune suppression in chronic cutaneous leishmaniasis. J. Exp. Med. 204:285-297. doi:10.1084/jem.20061886
3. 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.
4. 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-IL10 receptor antibody for sterile cure. J. Exp. Med. 194:1497-1506. doi:10.1084/jem.194.10.1497
5. 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. doi:10.1038/nature01152
6. Boonstra, A., R. Rajsbaum, M. Holman, R. Marques, C. AsselinPaturel, J.P. Pereira, E.E. Bates, S. Akira, P. Vieira, Y.J. Liu, et al. 2006. Macrophages and myeloid dendritic cells, but not plasmacytoid dendritic cells, produce IL10 in response to MyD88- and TRIF-dependent TLR signals, and TLR-independent signals. J. Immunol. 177:7551-7558.
7. Castro, A.G., M. Neighbors, S.D. Hurst, F. Zonin, R.A. Silva, E. Murphy, Y.J. Liu, and A. O'Garra. 2000. Anti-interleukin 10 receptor monoclonal antibody is an adjuvant for T helper cell type 1 responses to soluble antigen only in the presence of lipopolysaccharide. J. Exp. Med. 192:1529-1534. doi:10.1084/jem.192.10.1529
8. Chu, R.S., O.S. Targoni, A.M. Krieg, P.V. Lehmann, and C.V. Harding. 1997. CpG oligodeoxynucleotides act as adjuvants that switch on T helper 1 (Th1) immunity. J. Exp. Med. 186:1623-1631. doi:10.1084/ jem.186.10.1623
9. Coler, R.N., and S.G. Reed. 2005. Secondgeneration vaccines against leishmaniasis. Trends Parasitol. 21:244-249. doi:10.1016/j.pt.2005.03.006
10. Coler, R.N., D. Carter, M. Friede, and S.G. Reed. 2009. Adjuvants for malaria vaccines. Parasite Immunol. 31:520-528. doi:10.1111/j.13653024.2009. 01142.x
11. Darrah, P.A., D.T. Patel, P.M. De Luca, R.W. Lindsay, D.F. Davey, B.J. Flynn, S.T. Hoff, P. Andersen, S.G. Reed, S.L. Morris, et al. 2007. Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat. Med. 13:843-850. doi:10.1038/ nm1592
12. Forbes, E.K., C. Sander, E.O. Ronan, H. McShane, A.V. Hill, P.C. Beverley, and E.Z. Tchilian. 2008. Multifunctional, high-level cytokine-producing Th1 cells in the lung, but not spleen, correlate with protection against Mycobacterium tuberculosis aerosol challenge in mice. J. Immunol. 181:4955-4964.
13. Gérard, C., C. Bruyns, A. Marchant, D. Abramowicz, P. Vandenabeele, A. Delvaux, W. Fiers, M. Goldman, and T. Velu. 1993. Interleukin 10 reduces the release of tumor necrosis factor and prevents lethality in experimental endotoxemia. J. Exp. Med. 177:547-550. doi:10.1084/jem.177.2.547
14. 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. doi:10.1038/39614
15. Howard, M., T. Muchamuel, S. Andrade, and S. Menon. 1993. Interleukin 10 protects mice from lethal endotoxemia. J. Exp. Med. 177:1205-1208. doi:10.1084/jem.177.4.1205 (Pubitemid 23097411)
16. Jankovic, D., M.C. Kullberg, S. Hieny, P. Caspar, C.M. Collazo, and A. Sher. 2002. In the absence of IL12, CD4(+) T cell responses to intracellular pathogens fail to default to a Th2 pattern and are host protective in an IL10(-/-) setting. Immunity. 16:429-439. doi:10.1016/S1074-7613 (02)00278-9
17. - Th1 cells are the major source of host-protective regulatory IL10 during intracellular protozoan infection. J. Exp. Med. 204:273-283. doi:10.1084/jem.20062175
18. Jarnicki, A.G., H. Conroy, C. Brereton, G. Donnelly, D. Toomey, K. Walsh, C. Sweeney, O. Leavy, J. Fletcher, E.C. Lavelle, et al. 2008. Attenuating regulatory T cell induction by TLR agonists through inhibition of p38 MAPK signaling in dendritic cells enhances their efficacy as vaccine adjuvants and cancer immunotherapeutics. J. Immunol. 180:3797-3806.
19. Kimblin, N., N. Peters, A. Debrabant, N. Secundino, J. Egen, P. Lawyer, M.P. Fay, S. Kamhawi, and D. Sacks. 2008. Quantification of the infectious dose of Leishmania major transmitted to the skin by single sand flies. Proc. Natl. Acad. Sci. USA. 105:10125-10130. doi:10.1073/ pnas.0802331105
20. Lindenstrøm, T., E.M. Agger, K.S. Korsholm, P.A. Darrah, C. Aagaard, R.A. Seder, I. Rosenkrands, and P. Andersen. 2009. Tuberculosis subunit vaccination provides long-term protective immunity characterized by multifunctional CD4 memory T cells. J. Immunol. 182:8047-8055. doi:10.4049/jimmunol.0801592
21. 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. doi:10.1146/annurev.immunol.19.1.683
22. Perfetto, S.P., P.K. Chattopadhyay, L. Lamoreaux, R. Nguyen, D. Ambrozak, R.A. Koup, and M. Roederer. 2006. Amine reactive dyes: an effective tool to discriminate live and dead cells in polychromatic flow cytometry. J. Immunol. Methods. 313:199-208. doi:10.1016/ j.jim.2006.04.007
23. Roestenberg, M., M. McCall, J. Hopman, J. Wiersma, A.J. Luty, G.J. van Gemert, M. van de Vegte-Bolmer, B. van Schaijk, K. Teelen, T. Arens, et al. 2009. Protection against a malaria challenge by sporozoite inoculation. N. Engl. J. Med. 361:468-477. doi:10.1056/NEJMoa0805832
24. Roman, M., E. Martin-Orozco, J.S. Goodman, M.D. Nguyen, Y. Sato, A. Ronaghy, R.S. Kornbluth, D.D. Richman, D.A. Carson, and E. Raz. 1997. Immunostimulatory DNA sequences function as T helper-1-promoting adjuvants. Nat. Med. 3:849-854. doi:10.1038/ nm0897-849
25. 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. doi:10.1111/j.0105-2896.2004.00185.x
26. Samarasinghe, R., P. Tailor, T. Tamura, T. Kaisho, S. Akira, and K. Ozato. 2006. Induction of an anti-inflammatory cytokine, IL10, in dendritic cells after toll-like receptor signaling. J. Interferon Cytokine Res. 26:893-900. doi:10.1089/jir.2006.26.893
27. Seder, R.A., P.A. Darrah, and M. Roederer. 2008. T-cell quality in memory and protection: implications for vaccine design. Nat. Rev. Immunol. 8:247-258. doi:10.1038/nri2274
28. Skeiky, Y.A., and J.C. Sadoff. 2006. Advances in tuberculosis vaccine strategies. Nat. Rev. Microbiol. 4:469-476. doi:10.1038/nrmicro1419
29. Skeiky, Y.A., R.N. Coler, M. Brannon, E. Stromberg, K. Greeson, R.T. Crane, J.R. Webb, A. Campos-Neto, and S.G. Reed. 2002. Protective efficacy of a tandemly linked, multi-subunit recombinant leishmanial vaccine (Leish111f) formulated in MPL adjuvant. Vaccine. 20:3292-3303. doi:10.1016/S0264410X(02) 00302X
30. Stober, C.B., U.G. Lange, M.T. Roberts, A. Alcami, and J.M. Blackwell. 2005. IL-10 from regulatory T cells determines vaccine efficacy in murine Leishmania major infection. J. Immunol. 175:2517-2524.
31. Sun, J., R. Madan, C.L. Karp, and T.J. Braciale. 2009. Effector T cells control lung inflammation during acute influenza virus infection by producing IL-10. Nat. Med. 15:277-284. doi:10.1038/nm.1929
32. Thorner, A.R., A.A. Lemckert, J. Goudsmit, D.M. Lynch, B.A. Ewald, M. Denholtz, M.J. Havenga, and D.H. Barouch. 2006. Immunogenicity of heterologous recombinant adenovirus prime-boost vaccine regimens is enhanced by circumventing vector cross-reactivity. J. Virol. 80:12009-12016. doi:10.1128/JVI.0174906
33. Trinchieri, G. 2001. Regulatory role of T cells producing both interferon γ and interleukin 10 in persistent infection. J. Exp. Med. 194:F53-F57. doi:10.1084/jem.194.10.f53 (Pubitemid 33081514)
34. Trumpfheller, C., M. Caskey, G. Nchinda, M.P. Longhi, O. Mizenina, Y. Huang, S.J. Schlesinger, M. Colonna, and R.M. Steinman. 2008. The microbial mimic poly IC induces durable and protective CD4+ T cell immunity together with a dendritic cell targeted vaccine. Proc. Natl. Acad. Sci. USA. 105:2574-2579. doi:10.1073/pnas.0711976105
35. Wu, C.Y., J.R. Kirman, M.J. Rotte, D.F. Davey, S.P. Perfetto, E.G. Rhee, B.L. Freidag, B.J. Hill, D.C. Douek, and R.A. Seder. 2002. Distinct lineages of T(H)1 cells have differential capacities for memory cell generation in vivo. Nat. Immunol. 3:852-858. doi:10.1038/ni832