Mechanisms of rapid induction of interleukin-22 in activated T cells and its modulation by cyclosporin A

Journal of Biological Chemistry

Volumn 287, Issue 7, 2012, Pages 4531-4543

  Rudloff, Ina ^a   Bachmann, Malte ^a   Pfeilschifter, Josef ^a   Muḧl, Heiko ^a  

^a UNIVERSITY HOSPITAL FRANKFURT   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOSPORIN A; CYTOKINES; GENE INDUCTION; IMMUNOSUPPRESSIVE DRUGS; JURKAT CELL; MOLECULAR MECHANISM; PATHOLOGICAL FUNCTIONS; PERIPHERAL BLOOD MONONUCLEAR CELLS; PROMOTER ANALYSIS; T CELLS; THERAPEUTIC EFFICACY;

CELLS; CYTOLOGY; GENE EXPRESSION;

MOLECULAR BIOLOGY;

CALCIMYCIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLOSPORIN A; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; I KAPPA B KINASE INHIBITOR; INTERLEUKIN 22; SMALL INTERFERING RNA; TACROLIMUS; TRANSCRIPTION FACTOR NFAT;

ARTICLE; BINDING SITE; CD3+ T LYMPHOCYTE; COMPLEX FORMATION; CONTROLLED STUDY; CYTOKINE RESPONSE; DRUG MECHANISM; GENE EXPRESSION REGULATION; GENE INDUCTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IL22 GENE; IMMUNE RESPONSE GENE; IMMUNOMODULATION; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; T LYMPHOCYTE ACTIVATION;

AUTOIMMUNE DISEASES; CALCIMYCIN; CALCIUM IONOPHORES; CARCINOGENS; CYCLOSPORINE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; I-KAPPA B KINASE; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKINS; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MALE; RESPONSE ELEMENTS; T-LYMPHOCYTES; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION FACTORS;

EID: 84856845712     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.286492     Document Type: Article

References (66)

1. Dumoutier, L., Van Roost, E., Colau, D., and Renauld, J. C. (2000) Human interleukin-10-related T cell-derived inducible factor. Molecular cloning and functional characterization as an hepatocyte-stimulating factor. Proc. Natl. Acad. Sci. U.S.A. 97, 10144-10149
2. Steinman, L. (2007) A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat. Med. 13, 139-145
3. Wolk, K., Witte, E., Witte, K., Warszawska, K., and Sabat, R. (2010) Biology of interleukin-22. Semin. Immunopathol. 32, 17-31
4. Blaschitz, C., and Raffatellu, M. (2010) Th17 cytokines and the gut mucosal barrier. J. Clin. Immunol. 30, 196-203
5. Duhen, T., Geiger, R., Jarrossay, D., Lanzavecchia, A., and Sallusto, F. (2009) Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat. Immunol. 10, 857-863
6. Trifari, S., Kaplan, C. D., Tran, E. H., Crellin, N. K., and Spits, H. (2009) Identification of a human helper T cell population that has abundant production of interleukin 22 and is distinct from T(H)-17, T(H)1, and T(H)2 cells. Nat. Immunol. 10, 864-871
7. Nograles, K. E., Zaba, L. C., Shemer, A., Fuentes-Duculan, J., Cardinale, I., Kikuchi, T., Ramon, M., Bergman, R., Krueger, J. G., and Guttman-Yassky, E. (2009) IL-22-producing "T22" T cells account for up-regulated IL-22 in atopic dermatitis despite reduced IL-17-producing TH17 T cells. J. Allergy Clin. Immunol. 123, 1244-1252.e2
8. Bachmann, M., Horn, K., Rudloff, I., Goren, I., Holdener, M., Christen, U., Darsow, N., Hunfeld, K. P., Koehl, U., Kind, P., Pfeilschifter, J., Kraiczy, P., and Mühl, H. (2010) Early production of IL-22 but not IL-17 by peripheral blood mononuclear cells exposed to live Borrelia burgdorferi. The role of monocytes and interleukin-1. PLoS Pathog. 6, e1001144
9. Res, P. C., Piskin, G., de Boer, O. J., van der Loos, C. M., Teeling, P., Bos, J. D., and Teunissen, M. B. (2010) Overrepresentation of IL-17A and IL-22 producing CD8 T cells in lesional skin suggests their involvement in the pathogenesis of psoriasis. PLoS One 5, e14108
10. Pickert, G., Neufert, C., Leppkes, M., Zheng, Y., Wittkopf, N., Warntjen, M., Lehr, H. A., Hirth, S., Weigmann, B., Wirtz, S., Ouyang, W., Neurath, M. F., and Becker, C. (2009) STAT3 links IL-22 signaling in intestinal epithelial cells to mucosal wound healing. J. Exp. Med. 206, 1465-1472
11. Sonnenberg, G. F., Fouser, L. A., and Artis, D. (2011) Border patrol. Regulation of immunity, inflammation, and tissue homeostasis at barrier surfaces by IL-22. Nat. Immunol. 12, 383-390
12. Radaeva, S., Sun, R., Pan, H. N., Hong, F., and Gao, B. (2004) Interleukin 22 (IL-22) plays a protective role in T cell-mediated murine hepatitis. IL-22 is a survival factor for hepatocytes via STAT3 activation. Hepatology 39, 1332-1342 (Pubitemid 38569055)
13. Sugimoto, K., Ogawa, A., Mizoguchi, E., Shimomura, Y., Andoh, A., Bhan, A. K., Blumberg, R. S., Xavier, R. J., and Mizoguchi, A. (2008) IL-22 ameliorates intestinal inflammation in a mouse model of ulcerative colitis. J. Clin. Invest. 118, 534-544 (Pubitemid 351206544)
14. Wolk, K., Kunz, S., Witte, E., Friedrich, M., Asadullah, K., and Sabat, R. (2004) IL-22 increases the innate immunity of tissues. Immunity 21, 241-254 (Pubitemid 39094053)
15. Aujla, S. J., Chan, Y. R., Zheng, M., Fei, M., Askew, D. J., Pociask, D. A., Reinhart, T. A., McAllister, F., Edeal, J., Gaus, K., Husain, S., Kreindler, J. L., Dubin, P. J., Pilewski, J. M., Myerburg, M. M., Mason, C. A., Iwakura, Y., and Kolls, J. K. (2008) IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat. Med. 14, 275-281 (Pubitemid 351347908)
16. Hoegl, S., Bachmann, M., Scheiermann, P., Goren, I., Hofstetter, C., Pfeilschifter, J., Zwissler, B., and Muhl, H. (2011) Protective properties of inhaled IL-22 in a model of ventilator-induced lung injury. Am. J. Respir. Cell Mol. Biol. 44, 369-376
17. Brand, S., Beigel, F., Olszak, T., Zitzmann, K., Eichhorst, S. T., Otte, J. M., Diepolder, H., Marquardt, A., Jagla, W., Popp, A., Leclair, S., Herrmann, K., Seiderer, J., Ochsenkühn, T., Göke, B., Auernhammer, C. J., and Dambacher, J. (2006) IL-22 is increased in active Crohn disease and promotes proinflammatory gene expression and intestinal epithelial cell migration. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G827-838
18. Boniface, K., Bernard, F. X., Garcia, M., Gurney, A. L., Lecron, J. C., and Morel, F. (2005) IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J. Immunol. 174, 3695-3702 (Pubitemid 40354080)
19. Ziesché, E., Bachmann, M., Kleinert, H., Pfeilschifter, J., and Mühl, H. (2007) The interleukin-22/STAT3 pathway potentiates expression of inducible nitric-oxide synthase in human colon carcinoma cells. J. Biol. Chem. 282, 16006-16015
20. Zheng, Y., Valdez, P. A., Danilenko, D. M., Hu, Y., Sa, S. M., Gong, Q., Abbas, A. R., Modrusan, Z., Ghilardi, N., de Sauvage, F. J., and Ouyang, W. (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14, 282-289 (Pubitemid 351347912)
21. Geboes, L., Dumoutier, L., Kelchtermans, H., Schurgers, E., Mitera, T., Renauld, J. C., and Matthys, P. (2009) Proinflammatory role of the Th17 cytokine interleukin-22 in collagen-induced arthritis in C57BL/6 mice. Arthritis Rheum. 60, 390-395
22. Ma, H. L., Liang, S., Li, J., Napierata, L., Brown, T., Benoit, S., Senices, M., Gill, D., Dunussi-Joannopoulos, K., Collins, M., Nickerson-Nutter, C., Fouser, L. A., and Young, D. A. (2008) IL-22 is required for Th17 cell-mediated pathology in a mouse model of psoriasis-like skin inflammation. J. Clin. Invest. 118, 597-607 (Pubitemid 351206549)
23. Miossec, P., Korn, T., and Kuchroo, V. K. (2009) Interleukin-17 and type 17 helper T cells. N. Engl. J. Med. 361, 888-898
24. Louten, J., Boniface, K., and de Waal Malefyt, R. (2009) Development and function of TH17 cells in health and disease. J. Allergy Clin. Immunol. 123, 1004-1011
25. O'Connor, W., Jr., Zenewicz, L. A., and Flavell, R. A. (2010) The dual nature of T(H)17 cells. Shifting the focus to function. Nat. Immunol. 11, 471-476
26. Macian, F. (2005) NFAT proteins. Key regulators of T-cell development and function. Nat. Rev. Immunol. 5, 472-484
27. Müller, M. R., and Rao, A. (2010) NFAT, immunity and cancer. A transcription factor comes of age. Nat. Rev. Immunol. 10, 645-656
28. Al-Daraji, W. I., Grant, K. R., Ryan, K., Saxton, A., and Reynolds, N. J. (2002) Localization of calcineurin/NFAT in human skin and psoriasis and inhibition of calcineurin/NFAT activation in human keratinocytes by cyclosporin A. J. Invest. Dermatol. 118, 779-788 (Pubitemid 34526539)
29. Mühl, H., Kunz, D., Rob, P., and Pfeilschifter, J. (1993) Cyclosporin derivatives inhibit interleukin 1β induction of nitric-oxide synthase in renal mesangial cells. Eur. J. Pharmacol. 249, 95-100 (Pubitemid 23326914)
30. Hämäläinen, M., Korhonen, R., and Moilanen, E. (2009) Calcineurin inhibitors down-regulate iNOS expression by destabilizing mRNA. Int. Immunopharmacol. 9, 159-167
31. Maza, A., Montaudié, H., Sbidian, E., Gallini, A., Aractingi, S., Aubin, F., Bachelez, H., Cribier, B., Joly, P., Jullien, D., Le Maître, M., Misery, L., Richard, M. A., Ortonne, J. P., and Paul, C. (2011) J. Eur. Acad. Dermatol. Venereol. 25, Suppl. 2, 19-27
32. Dumoutier, L., Van Roost, E., Ameye, G., Michaux, L., and Renauld, J. C. (2000) IL-TIF/IL-22. Genomic organization and mapping of the human and mouse genes. Genes Immun. 1, 488-494
33. Sadik, C. D., Bachmann, M., Pfeilschifter, J., and Mühl, H. (2009) Nucleic Acids Res. 37, 5041-5056
34. Frantz, B., Nordby, E. C., Bren, G., Steffan, N., Paya, C. V., Kincaid, R. L., Tocci, M. J., O'Keefe, S. J., and O'Neill, E. A. (1994) Calcineurin acts in synergy with PMA to inactivate IκB/MAD3, an inhibitor of NF-κB.EMBO J. 13, 861-870
35. Trushin, S. A., Pennington, K. N., Algeciras-Schimnich, A., and Paya, C. V. (1999) Protein kinase C and calcineurin synergize to activate IκB kinase and NF-κB in T lymphocytes. J. Biol. Chem. 274, 22923-22931
36. Ledbetter, J. A., Gentry, L. E., June, C. H., Rabinovitch, P. S., and Purchio, A. F. (1987) Mol. Cell. Biol. 7, 650-656
37. 2+-dependent phosphatase calcineurin controls the formation of the Carma1-Bcl10-Malt1 complex during T cell receptor-induced NF-κB activation. J. Biol. Chem. 286, 7522-7534
38. Whitehurst, C. E., and Geppert, T. D. (1996) MEK1 and the extracellular signal-regulated kinases are required for the stimulation of IL-2 gene transcription in T cells. J. Immunol. 156, 1020-1029 (Pubitemid 26048095)
39. Park, J. H., and Levitt, L. (1993) Overexpression of mitogen-activated protein kinase (ERK1) enhances T-cell cytokine gene expression. Role of AP1, NF-AT, and NF-KB. Blood 82, 2470-2477
40. Veldhoen, M., Hirota, K., Westendorf, A. M., Buer, J., Dumoutier, L., Renauld, J. C., and Stockinger, B. (2008) The aryl hydrocarbon receptor links TH17 cell-mediated autoimmunity to environmental toxins. Nature 453, 106-109 (Pubitemid 351630329)
41. Ramirez, J. M., Brembilla, N. C., Sorg, O., Chicheportiche, R., Matthes, T., Dayer, J. M., Saurat, J. H., Roosnek, E., and Chizzolini, C. (2010) Activation of the aryl hydrocarbon receptor reveals distinct requirements for IL-22 and IL-17 production by human T helper cells. Eur. J. Immunol. 40, 2450-2459
42. Ziesché, E. (2009) Untersuchungen zur Bildung und Funktion von IL-21 bei entzündungsbedingter Immunaktivierung. Ph.D. Dissertation, Goethe-University Frankfurt, Frankfurt, Germany
43. + T cells specific for Candida albicans are present in humans. Eur. J. Immunol. 39, 1472-1479
44. Rao, A., Luo, C., and Hogan, P. G. (1997) Transcription factors of the NFAT family. Regulation and function. Annu. Rev. Immunol. 15, 707-747 (Pubitemid 27169297)
45. Ruan, Q., Kameswaran, V., Tone, Y., Li, L., Liou, H. C., Greene, M. I., Tone, M., and Chen, Y. H. (2009) Development of Foxp3(+) regulatory T cells is driven by the c-Rel enhanceosome. Immunity 31, 932-940
46. Wen, A. Y., Sakamoto, K. M., and Miller, L. S. (2010) The role of the transcription factor CREB in immune function. J. Immunol. 185, 6413-6419
47. Granelli-Piperno, A., and Nolan, P. (1991) Nuclear transcription factors that bind to elements of the IL-2 promoter. Induction requirements in primary human T cells. J. Immunol. 147, 2734-2739
48. Bamberger, A. M., Erdmann, I., Bamberger, C. M., Jenatschke, S. S., and Schulte, H. M. (1997) Transcriptional regulation of the human "leukemia inhibitory factor" gene. Modulation by glucocorticoids and estradiol. Mol. Cell. Endocrinol. 127, 71-79 (Pubitemid 27144084)
49. Mosenden, R., and Taskén, K. (2011) Cyclic AMP-mediated immune regulation. Overview of mechanisms of action in T cells. Cell Signal. 23, 1009-1016
50. Yadav, M., Rosenbaum, J., and Goetzl, E. J. (2008) Cutting edge. Vasoactive intestinal peptide (VIP) induces differentiation of Th17 cells with a distinctive cytokine profile. J. Immunol. 180, 2772-2776
51. Ma, C. S., Chew, G. Y., Simpson, N., Priyadarshi, A., Wong, M., Grimbacher, B., Fulcher, D. A., Tangye, S. G., and Cook, M. C. (2008) Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J. Exp. Med. 205, 1551-1557 (Pubitemid 351962018)
52. Xiao, G., Cvijic, M. E., Fong, A., Harhaj, E. W., Uhlik, M. T., Waterfield, M., and Sun, S. C. (2001) Retroviral oncoprotein Tax induces processing of NF-κB2/p100 in T cells. Evidence for the involvement of IKKα. EMBO J. 20, 6805-6815 (Pubitemid 33134210)
53. Li, L., Ruan, Q., Hilliard, B., Devirgiliis, J., Karin, M., and Chen, Y. H. (2011) Transcriptional regulation of the Th17 immune response by IKK(α). J. Exp. Med. 208, 787-796
54. Israël A. (2010) The IKK complex.Acentral regulator of NF-κB activation. Cold Spring Harb. Perspect. Biol. 2, a000158
55. Wang, X., Zhang, F., Chen, F., Liu, D., Zheng, Y., Zhang, Y., Dong, C., and Su, B. (2011) MEKK3 regulates IFN-γ production in T cells through the Rac1/2-dependent MAPK cascades. J. Immunol. 186, 5791-5800
56. Kempiak, S. J., Hiura, T. S., and Nel, A. E. (1999) The Jun kinase cascade is responsible for activating the CD28 response element of the IL-2 promoter. Proof of cross-talk with the IκB kinase cascade. J. Immunol. 162, 3176-3187 (Pubitemid 29313563)
57. Liu, X. K., Lin, X., and Gaffen, S. L. (2004) Crucial role for nuclear factor of activated T cells in T cell receptor-mediated regulation of human interleukin-17. J. Biol. Chem. 279, 52762-52771 (Pubitemid 39656652)
58. Mühl, H., Bachmann, M., and Pfeilschifter, J. (2011) Inducible NO synthase and antibacterial host defence in times of Th17/Th22/T22 immunity. Cell Microbiol. 13, 340-348
59. Gaffen, S. L. (2008) An overview of IL-17 function and signaling. Cytokine 43, 402-407
60. Schön, M. P., and Boehncke, W. H. (2005) Psoriasis. N. Engl. J. Med. 352, 1899-1912 (Pubitemid 40627816)
61. Sabat, R., and Wolk, K. (2011) Research in practice: IL-22 and IL-20: significance for epithelial homeostasis and psoriasis pathogenesis. J. Dtsch. Dermatol. Ges. 9, 518-523
62. Wolk, K., Witte, E., Wallace, E., Döcke, W. D., Kunz, S., Asadullah, K., Volk, H. D., Sterry, W., and Sabat, R. (2006) IL-22 regulates the expression of genes responsible for antimicrobial defense, cellular differentiation, and mobility in keratinocytes.Apotential role in psoriasis. Eur. J. Immunol. 36, 1309-1323
63. Boniface, K., Guignouard, E., Pedretti, N., Garcia, M., Delwail, A., Bernard, F. X., Nau, F., Guillet, G., Dagregorio, G., Yssel, H., Lecron, J. C., and Morel, F. (2007) A role for T cell-derived interleukin 22 in psoriatic skin inflammation. Clin. Exp. Immunol. 150, 407-415 (Pubitemid 350098734)
64. Nograles, K. E., Zaba, L. C., Guttman-Yassky, E., Fuentes-Duculan, J., Suárez-Fariñas, M., Cardinale, I., Khatcherian, A., Gonzalez, J., Pierson, K. C., White, T. R., Pensabene, C., Coats, I., Novitskaya, I., Lowes, M. A., and Krueger, J. G. (2008) Th17 cytokines interleukin (IL)-17 and IL-22 modulate distinct inflammatory and keratinocyte-response pathways. Br. J. Dermatol. 159, 1092-1102
65. Wolk, K., Witte, E., Warszawska, K., Schulze-Tanzil, G., Witte, K., Philipp, S., Kunz, S., Döcke, W. D., Asadullah, K., Volk, H. D., Sterry, W., and Sabat, R. (2009) The Th17 cytokine IL-22 induces IL-20 production in keratinocytes. A novel immunological cascade with potential relevance in psoriasis. Eur. J. Immunol. 39, 3570-3581
66. Haider, A. S., Lowes, M. A., Suárez-Fariñas, M., Zaba, L. C., Cardinale, I., Khatcherian, A., Novitskaya, I., Wittkowski, K. M., and Krueger, J. G. (2008) Identification of cellular pathways of "type 1," Th17 T cells, and TNF and inducible nitric-oxide synthase-producing dendritic cells in autoimmune inflammation through pharmacogenomic study of cyclosporine A in psoriasis. J. Immunol. 180, 1913-1920