IL-12 is required for induction but not maintenance of protective, memory responses to Blastomyces dermatitidis: Implications for vaccine development in immune-deficient hosts

Journal of Immunology

Volumn 175, Issue 8, 2005, Pages 5288-5297

  Wüthrich, Marcel ^a,c   Warner, Tom ^a   Klein, Bruce S ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c University of Wisconsin Health   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLASTOMYCES DERMATITIDIS VACCINE; CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; FUNGUS VACCINE; INTERLEUKIN 12; RECOMBINANT INTERLEUKIN 12; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLASTOMYCES DERMATITIDIS; BLASTOMYCOSIS; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENETIC ENGINEERING; IMMUNE DEFICIENCY; IMMUNOLOGICAL MEMORY; KNOCKOUT MOUSE; LUNG INFECTION; LYMPHOCYTE DIFFERENTIATION; MALE; MEMORY CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; T LYMPHOCYTE; VACCINATION; VACCINE PRODUCTION;

EID: 26844539942     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.8.5288     Document Type: Article

References (52)

1. Cozad, G. C. 1992. Experimental blastomycosis. In Blastomycosis. Y. Al-Doorey and A. F. DiSalvo, eds. Plenum Publishing Corporation, New York, p. 221-236.
2. Cozad, G. C., and C. T. Chang. 1980. Cell-mediated immunoprotection in blastomycosis. Infect. Immun. 28: 398-403.
3. Wüthrich, M., H. I. Filutowicz, and B. S. Klein. 2000. Mutation of the WI-1 gene yields an attenuated Blastomyces dermatitidis strain that induces host resistance. J. Clin. Invest. 106: 1381-1389.
4. Wüthrich, M., H. I. Filutowicz, T. Warner, and B. S. Klein. 2002. Requisite elements in vaccine immunity to Blastomyces dermatitidis: plasticity uncovers vaccine potential in immune-deficient hosts. J. Immunol. 169: 6969-6976.
5. + T cells: implications for vaccine development in immune-deficient hosts. J. Exp. Med. 197: 1405-1416.
6. Chan, S. H., B. Perussia, J. W. Gupta, M. Kobayashi, M. Pospisil, H. A. Young, S. F. Wolf, D. Young, S. C. Clark, and G. Trinchieri. 1991. Induction of interferon γ production by natural killer cell stimulatory factor: characterization of the responder cells and synergy with other inducers. J. Exp. Med. 173: 869-879.
7. Kobayashi, M., L. Fitz, M. Ryan, R. M. Hewick, S. C. Clark, S. Chan, R. Loudon, F. Sherman, B. Perussia, and G. Trinchieri. 1989. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J. Exp. Med. 170: 827-845.
8. + T cells through IL-12 produced by Listeria-induced macrophages. Science 260: 547-549.
9. Manetti, R., F. Gerosa, M. G. Giudizi, R. Biagiotti, P. Parronchi, M. P. Piccinni, S. Sampognaro, E. Maggi, S. Romagnani, G. Trinchieri, et al. 1994. Interleukin 12 induces stable priming for interferon γ (IFN-γ) production during differentiation of human T helper (Th) cells and transient IFN-γ production in established Th2 cell clones. J. Exp. Med. 179: 1273-1283.
10. Wu, C. Y., C. Demeure, M. Kiniwa, M. Gately, and G. Delespesse. 1993. IL-12 induces the production of IFN-γ by neonatal human CD4 T cells. J. Immunol. 151: 1938-1949.
11. + T cells to enhance priming for interferon γ production and diminishes interleukin 4 inhibition of such priming. Proc. Nat. Acad. Sci. USA 90: 10188-10192.
12. Yap, G., M. Pesin, and A. Sher. 2000. Cutting edge: IL-12 is required for the maintenance of IFN-γ production in T cells mediating chronic resistance to the intracellular pathogen, Toxoplasma gondii. J. Immunol. 165: 628-631.
13. Park, A. Y., B. D. Hondowicz, and P. Scott. 2000. IL-12 is required to maintain a Th1 response during Leishmania major infection. J. Immunol. 165: 896-902.
14. Stern, A. S., F. J. Podlaski, J. D. Hulmes, Y. C. Pan, P. M. Quinn, A. G. Wolitzky, P. C. Familletti, D. L. Stremlo, T. Truitt, R. Chizzonite, et al. 1990. Purification to homogeneity and partial characterization of cytotoxic lymphocyte maturation factor from human B-lymphoblastoid cells. Proc. Natl. Acad. Sci. USA 87: 6808-6812.
15. Constantinescu, C. S., B. D. Hondowicz, M. M. Elloso, M. Wysocka, G. Trinchieri, and P. Scott. 1998. The role of IL-12 in the maintenance of an established Th1 immune response in experimental leishmaniasis. Eur. J. Immunol. 28: 2227-2233.
16. Gazzinelli, R. T., M. Wysocka, S. Hayashi, E. Y. Denkers, S. Hieny, P. Caspar, G. Trinchieri, and A. Sher. 1994. Parasite-induced IL-12 stimulates early IFN-γ synthesis and resistance during acute infection with Toxoplasma gondii. J. Immunol. 153: 2533-2543.
17. Tripp, C. S., O. Kanagawa, and E. R. Unanue. 1995. Secondary response to Listeria infection requires IFN-γ but is partially independent of IL-12. J. Immunol. 155: 3427-3432.
18. Seder, R. A., B. L. Kelsall, and D. Jankovic. 1996. Differential roles for IL-12 in the maintenance of immune responses in infectious versus autoimmune disease. J. Immunol. 157: 2745-2748.
19. Zhou, P., G. Miller, and R. A. Seder. 1998. Factors involved in regulating primary and secondary immunity to infection with Histoplasma capsulatum: TNF-α plays a critical role in maintaining secondary immunity in the absence of IFN-γ. J. Immunol. 160: 1359-1368.
20. Park, A. Y., B. Hondowicz, M. Kopf, and P. Scott. 2002. The role of IL-12 in maintaining resistance to Leishmania major. J. Immunol. 168: 5771-5777.
21. 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.
22. + T cells. J. Exp. Med. 189: 1355-1360.
23. Harrison, T. S., and S. M. Levitz. 1996. Role of IL-12 in peripheral blood mononuclear cell responses to fungi in persons with and without HIV infection. J. Immunol. 156: 4492-4497.
24. Harrison, T. S., and S. M. Levitz. 1997. Priming with IFN-γ restores deficient IL-12 production by peripheral blood mononuclear cells from HIV-seropositive donors. J. Immunol. 158: 459-463.
25. Harvey, R. P., E. S. Schmid, C. C. Carrington, and D. A. Stevens. 1978. Mouse model of pulmonary blastomycosis: utility, simplicity, and quantitative parameters. Am. Rev. Respir. Dis. 117: 695-703.
26. Brandhorst, T. T., M. Wüthrich, T. Warner, and B. Klein. 1999. Targeted gene disruption reveals an adhesin indispensable for pathogenicity of Blastomyces dermatitidis. J. Exp. Med. 189: 1207-1216.
27. Fabien, N., I. Bergerot, V. Maguer-Satta, J. Orgiazzi, and C. Thivolet. 1995. Pancreatic lymph nodes are early targets of T cells during adoptive transfer of diabetes in NOD mice. J. Autoimmun. 8: 323-334.
28. Magram, J., S. E. Connaughton, R. R. Warrier, D. M. Carvajal, C. Y. Wu, J. Ferrante, C. Stewart, U. Sarmiento, D. A. Faherty, and M. K. Gately. 1996. IL-12-deficient mice are defective in IFN-γ production and type 1 cytokine responses. Immunity 4: 471-481.
29. Johnson, M. R., K. Wang, J. B. Smith, M. J. Heslin, and R. B. Diasio. 2000. Quantitation of dihydropyrimidine dehydrogenase expression by real-time reverse transcription polymerase chain reaction. Anal Biochem. 278: 175-184.
30. Altare, F., A. Durandy, D. Lammas, J. F. Emile, S. Lamhamedi, F. Le Deist, P. Drysdale, E. Jouanguy, R. Doffinger, F. Bernaudin, et al. 1998. Impairment of mycobacterial immunity in human interleukin-12 receptor deficiency. Science 280: 1432-1435.
31. Fisher, L. D., and G. van Belle. 1993. Biostatistics: A Methodology for the Health Sciences. John Wiley & Sons, New York.
32. Mantel, N., and W. Haenszel. 1959. Statistical aspects of the analysis of data from retrospective studies of disease. J. Natl. Cancer Inst. 22: 719-748.
33. Afonso, L. C., T. M. Scharton, L. Q. Vieira, M. Wysocka, G. Trinchieri, and P. Scott. 1994. The adjuvant effect of interleukin-12 in a vaccine against Leishmania major. Science 263: 235-237.
34. Heinzel, F. P., D. S. Schoenhaut, R. M. Rerko, L. E. Rosser, and M. K. Gately. 1993. Recombinant interleukin 12 cures mice infected with Leishmania major. J. Exp. Med. 177: 1505-1509.
35. Sypek, J. P., C. L. Chung, S. E. Mayor, J. M. Subramanyam, S. J. Goldman, D. S. Sieburth, S. F. Wolf, and R. G. Schaub. 1993. Resolution of cutaneous leishmaniasis: interleukin 12 initiates a protective T helper type 1 immune response. J. Exp. Med. 177: 1797-1802.
36. Decken, K., G. Kohler, K. Palmer-Lehmann, A. Wunderlin, F. Mattner, J. Magram, M. K. Gately, and G. Alber. 1998. Interleukin-12 is essential for a protective Th1 response in mice infected with Cryptococcus neoformans. Infect. Immun. 66: 4994-5000.
37. Zhou, P., M. C. Sieve, J. Bennett, K. J. Kwon-Chung, R. P. Tewari, R. T. Gazzinelli, A. Sher, and R. A. Seder. 1995. IL-12 prevents mortality in mice infected with Histoplasma capsulatum through induction of IFN-γ. J. Immunol. 155: 785-795.
38. Oxenius, A., U. Karrer, R. M. Zinkemagel, and H. Hengartner. 1999. IL-12 is not required for induction of type 1 cytokine responses in viral infections. J. Immunol. 162:965-973.
39. Schijns, V. E., B. L. Haagmans, C. M. Wierda, B. Kruithof, I. A. Heijnen, G. Alber, and M. C. Horzinek. 1998. Mice lacking IL-12 develop polarized Th1 cells during viral infection. J. Immunol 160: 3958-3964.
40. Sallusto, F., D. Lenig, R. Forster, M. Lipp, and A. Lanzavecchia. 1999. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401: 708-712.
41. Reinhardt, R. L., A. Khoruts, R. Merica, T. Zell, and M. K. Jenkins. 2001. Visualizing the generation of memory CD4 T cells in the whole body. Nature 410: 101-105.
42. Ahmadzadeh, M., S. F. Hussain, and D. L. Farber. 2001. Heterogeneity of the memory CD4 T cell response: persisting effectors and resting memory T cells. J. Immunol. 166: 926-935.
43. + T cells during a Th2 response in Leishmania major-infected mice. Eur. J. Immunol. 30: 2007-2014.
44. Mocci, S., and R. L. Coffman. 1995. Induction of a Th2 population from a polarized Leishmania-specific Th1 population by in vitro culture with IL-4. J. Immunol. 154: 3779-3787.
45. + T cells are important for the balance between protective and pathogenic cell-mediated immunity. J. Exp. Med. 179: 589-600.
46. + T cells from human immunodeficiency virus-infected persons. J. Exp. Med. 182: 1759-1767.
47. Marth, T., M. Zeitz, B. R. Ludviksson, W. Strober, and B. L. Kelsall. 1999. Extinction of IL-12 signaling promotes Fas-mediated apoptosis of antigen-specific T cells. J. Immunol. 162: 7233-7240.
48. Palmer, E. M., L. Farrokh-Siar, J. Maguire van Seventer, and G. A. van Seventer. 2001. IL-12 decreases activation-induced cell death in human naive Th cells costimulated by intercellular adhesion molecule-1. I. IL-12 alters caspase processing and inhibits enzyme function. J. Immunol. 167: 749-758.
49. Sallusto, F., J. Geginat, and A. Lanzavecchia. 2004. Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22: 745-763.
50. Zaph, C., J. Uzonna, S. M. Beverley, and P. Scott. 2004. Central memory T cells mediate long-term immunity to Leishmania major in the absence of persistent parasites. Nat. Med. 10: 1104-1110.
51. Roman, E., E. Miller, A. Harmsen, J. Wiley, U. H. Von Andrian, G. Huston, and S. L. Swain. 2002. CD4 effector T cell subsets in the response to influenza: heterogeneity, migration, and function. J. Exp. Med. 196: 957-968.
52. Pasare, C., and R. Medzhitov. 2004. Toll-dependent control mechanisms of CD4 T cell activation. Immunity 21: 733-741.