IL-23 enhances the inflammatory cell response in Cryptococcus neoformans infection and induces a cytokine pattern distinct from IL-12

Journal of Immunology

Volumn 176, Issue 2, 2006, Pages 1098-1106

  Kleinschek, Melanie A ^a   Muller, Uwe ^a   Brodie, Scott J ^b   Stenzel, Werner ^c   Kohler, Gabriele ^d   Blumenschein, Wendy M ^b   Straubinger, Reinhard K ^a   McClanahan, Terril ^b   Kastelein, Robert A ^b   Alber, Gottfried ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b MERCK RESEARCH LABORATORIES   (United States)

^c UNIVERSITY OF COLOGNE   (Germany)

^d UNIVERSITY HOSPITAL MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 23; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN P19; PROTEIN P35; PROTEIN P40; PROTEIN SUBUNIT; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 23; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; CHRONIC INFLAMMATION; CONTROLLED STUDY; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION; HISTOPATHOLOGY; HOST RESISTANCE; IMMUNE RESPONSE; IMMUNOREGULATION; INFLAMMATORY CELL; INTERFERON PRODUCTION; LIVER GRANULOMA; MICROGLIA; MONONUCLEAR CELL; MORTALITY; MOUSE; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; SURVIVAL TIME; WILD TYPE;

EID: 30744434833     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.176.2.1098     Document Type: Article

References (43)

1. Oppmann, B., R. Lesley, B. Blom, J. C. Timans, Y. Xu, B. Hunte, F. Vega, N. Yu, J. Wang, K. Singh, et al. 2000. Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 13: 715-725.
2. Brombacher, F., R. A. Kastelein, and G. Alber. 2003. Novel IL-12 family members shed light on the orchestration of Th1 responses. Trends Immunol. 24: 207-212.
3. Trinchieri, G., S. Pflanz, and R. A. Kastelein. 2003. The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 19: 641-644.
4. Presky, D. H., H. Yang, L. J. Minetti, A. O. Chua, N. Nabavi, C. Y. Wu, M. K. Gately, and U. Gubler. 1996. A functional interleukin 12 receptor complex is composed of two β-type cytokine receptor subunits. Proc. Natl. Acad. Sci. USA 93: 14002-14007.
5. Parham, C., M. Chirica, J. Timans, E. Vaisberg, M. Travis, J. Cheung, S. Pflanz, R. Zhang, K. P. Singh, F. Vega, et al. 2002. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rβ1 and a novel cytokine receptor subunit, IL-23R. J. Immunol. 168: 5699-5708.
6. Trinchieri, G. 2003. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat. Rev. Immunol. 3: 133-146.
7. Langrish, C. L., B. S. McKenzie, N. J. Wilson, M. R. de Waal, R. A. Kastelein, and D. J. Cua. 2004. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol. Rev. 202: 96-105.
8. Hunter, C. A. 2005. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat. Rev. Immunol. 5: 521-531.
9. Cua, D. J., J. Sherlock, Y. Chen, C. A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421: 744-748.
10. Murphy, C. A., C. L. Langrish, Y. Chen, W. Blumenschein, T. McClanahan, R. A. Kastelein, J. D. Sedgwick, and D. J. Cua. 2003. Divergent pro- and anti-inflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J. Exp. Med. 198: 1951-1957.
11. Langrish, C. L., Y. Chen, W. M. Blumenschein, J. Mattson, B. Basham, J. D. Sedgwick, T. McClanahan, R. A. Kastelein, and D. J. Cua. 2005. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201: 233-240.
12. Aggarwal, S., N. Ghilardi, M. H. Xie, F. J. De Sauvage, and A. L. Gurney. 2003. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278: 1910-1914.
13. Aggarwal, S., and A. L. Gurney. 2002. IL-17: prototype member of an emerging cytokine family. J. Leukocyte Biol. 71: 1-8.
14. Kolls, J. K., and A. Linden. 2004. Interleukin-17 family members and inflammation. Immunity 21: 467-476.
15. Ghilardi, N., N. Kljavin, Q. Chen, S. Lucas, A. L. Gurney, and F. J. De Sauvage. 2004. Compromised humoral and delayed-type hypersensitivity responses in IL-23-deficient mice. J. Immunol. 172: 2827-2833.
16. Nakae, S., Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, I. Homma, K. Sekikawa, M. Asano, and Y. Iwakura. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17: 375-387.
17. Stark, M. A., Y. Huo, T. L. Burcin, M. A. Morris, T. S. Olson, and K. Ley. 2005. Phagocytosis of apoptotic neutrophils regulates granulopoiesis via IL-23 and IL-17. Immunity 22: 285-294.
18. Decken, K., G. Kohler, K. Palmer-Lehmann, A. Wunderlin, F. Manner, 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.
19. Elkins, K. L., A. Cooper, S. M. Colombini, S. C. Cowley, and T. L. Kieffer. 2002. In vivo clearance of an intracellular bacterium, Francisella tularensis LVS, is dependent on the p40 subunit of interleukin-12 (IL-12) but not on IL-12 p70. Infect. Immun. 70: 1936-1948.
20. Holscher, C., R. A. Atkinson, B. Arendse, N. Brown, E. Myburgh, G. Alber, and F. Brombacher. 2001. A protective and agonistic function of IL-12p40 in mycobacterial infection. J. Immunol. 167: 6957-6966.
21. Lehmann, J., S. Bellmann, C. Werner, R. Schroder, N. Schutze, and G. Alber. 2001. IL-12p40-dependent agonistic effects on the development of protective innate and adaptive immunity against Salmonella enteritidis. J. Immunol. 167: 5304-5315.
22. Lieberman, L. A., F. Cardillo, A. M. Owyang, D. M. Rennick, D. J. Cua, R. A. Kastelein, and C. A. Hunter. 2004. IL-23 provides a limited mechanism of resistance to acute toxoplasmosis in the absence of IL-12. J. Immunol. 173: 1887-1893.
23. Casadevall, A., and J. R. Perfect. 1998. Cryptococcus neoformans. ASM Press, Washington, DC.
24. Chen, G. H., R. A. McDonald, J. C. Wells, G. B. Huffnagle, N. W. Lukacs, and G. B. Toews. 2005. The γ interferon receptor is required for the protective pulmonary inflammatory response to Cryptococcus neoformans. Infect. Immun. 73: 1788-1796.
25. Hoag, K. A., M. F. Lipscomb, A. A. Izzo, and N. E. Street. 1997. IL-12 and IFN-γ are required for initiating the protective Th 1 response to pulmonary cryptococcosis in resistant C.B-17 mice. Am. J. Respir. Cell Mol. Biol. 17: 733-739.
26. Huffnagle, G. B., G. B. Toews, M. D. Burdick, M. B. Boyd, K. S. McAllister, R. A. McDonald, S. L. Kunkel, and R. M. Strieter. 1996. Afferent phase production of TNF-α is required for the development of protective T cell immunity to Cryptococcus neoformans. J. Immunol. 157: 4529-4536.
27. Kawakami, K., M. Tohyama, X. Qifeng, and A. Saito. 1997. Expression of cytokines and inducible nitric oxide synthase mRNA in the lungs of mice infected with Cryptococcus neoformans: effects of interleukin-12. Infect. Immun. 65: 1307-1312.
28. Magram, J., S. E. Connaughton, R. R. Warner, 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. Mattner, F., J. Magram, J. Ferrante, P. Launois, P. K. Di, R. Behin, M. K. Gately, J. A. Louis, and G. Alber. 1996. Genetically resistant mice lacking interleukin-12 are susceptible to infection with Leishmania major and mount a polarized Th2 cell response. Eur. J. Immunol 26: 1553-1559.
30. Stenzel, W., S. Soltek, H. Miletic, M. M. Hermann, H. Korner, J. D. Sedgwick, D. Schluter, and M. Deckert. 2005. An essential role for tumor necrosis factor in the formation of experimental murine Staphylococcus aureus-introduced brain abscess and clearance. J. Neuropathol. Exp. Neurol. 64: 27-36.
31. Biondo, C., A. Midiri, L. Messina, F. Tomasello, G. Garufi, M. R. Catania, M. Bombaci, C. Beninati, G. Teti, and G. Mancuso. 2005. MyD88 and TLR2, but not TLR4, are required for host defense against Cryptococcus neoformans. Eur. J. Immunol 35: 870-878.
32. Nichols, K. L., S. K. Bauman, F. B. Schafer, and J. W. Murphy. 2002. Differences in components at delayed-type hypersensitivity reaction sites in mice immunized with either a protective or a nonprotective immunogen of Cryptococcus neoformans. Infect. Immun. 70: 591-600.
33. D'Andrea, A., M. Rengaraju, N. M. Valiante, J. Chehimi, M. Kubin, M. Aste, S. H. Chan, M. Kobayashi, D. Young, E. Nickbarg, et al. 1992. Production of natural killer cell stimulatory factor (interleukin 12) by peripheral blood mononuclear cells. J. Exp. Med. 176: 1387-1398.
34. Khader, S. A., J. E. Pearl, K. Sakamoto, L. Gilmartin, G. K. Bell, D. M. Jelley-Gibbs, N. Ghilardi, F. Desauvage, and A. M. Cooper. 2005. IL-23 Compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-γ responses if IL-12p70 is available. J. Immunol. 175: 788-795.
35. Feng, C. G., D. Jankovic, M. Kullberg, A. Cheever, C. A. Scanga, S. Hieny, P. Caspar, G. S. Yap, and A. Sher. 2005. Maintenance of pulmonary Th1 effector function in chronic tuberculosis requires persistent IL-12 production. J. Immunol. 174: 4185-4192.
36. Lu, B., B. J. Rutledge, L. Gu, J. Fiorillo, N. W. Lukacs, S. L. Kunkel, R. North, C. Gerard, and B. J. Rollins. 1998. Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J. Exp. Med. 187: 601-608.
37. + T cells during a pulmonary Cryptococcus neoformans infection. J. Immunol. 155: 4790-4797.
38. Uicker, W. C., H. A. Doyle, J. P. McCracken, M. Langlois, and K. L. Buchanan. 2005. Cytokine and chemokine expression in the central nervous system associated with protective cell-mediated immunity against Cryptococcus neoformans. Med. Mycol. 43: 27-38.
39. Kopp, T., P. Lenz, C. Bello-Fernandez, R. A. Kastelein, T. S. Kupper, and G. Stingl. 2003. IL-23 production by cosecretion of endogenous p19 and transgenic p40 in keratin 14/p40 transgenic mice: evidence for enhanced cutaneous immunity. J. Immunol. 170: 5438-5444.
40. Belladonna, M. L., J. C. Renauld, R. Bianchi, C. Vacca, F. Fallarino, C. Orabona, M. C. Fioretti, V. Grohmann, and P. Puccetti. 2002. IL-23 and IL-12 have overlapping, but distinct, effects on murine dendritic cells. J. Immunol. 168: 5448-5454.
41. Jovanovic, D. V., J. A. Di Battista, J. Martel-Pelletier, F. C. Jolicoeur, Y. He, M. Zhang, F. Mineau, and J. P. Pelletier. 1998. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-β and TNF-α, by human macrophages. J. Immunol. 160: 3513-3521.
42. Happel, K. I., M. Zheng, E. Young, L. J. Quinton, E. Lockhart, A. J. Ramsay, J. E. Shellito, J. R. Schurr, G. J. Bagby, S. Nelson, and J. K. Kolls. 2003. Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 expression in response to Klebsiella pneumoniae infection. J. Immunol. 170: 4432-4436.
43. Ye, P., F. H. Rodriguez, S. Kanaly, K. L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194: 519-527.