STAT3-dependent effects of IL-22 in human keratinocytes are counterregulated by sirtuin 1 through a direct inhibition of STAT3 acetylation

FASEB Journal

Volumn 25, Issue 3, 2011, Pages 916-927

  Sestito, Rosanna ^a,b   Madonna, Stefania ^a   Scarponi, Claudia ^a   Cianfarani, Francesca ^a   Failla, Cristina M ^a   Cavani, Andrea ^a   Girolomoni, Giampiero ^b   Albanesi, Cristina ^a  

^a LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

Author keywords

Class III histone deacetylase (HDAC); IFN ; Post translational modification; Psoriasis; Skin inflammation

Indexed keywords

ACYLTRANSFERASE; DEACETYLASE; GAMMA INTERFERON; INTERLEUKIN 22; LYMPHOKINE; SIRTUIN 1; STAT3 PROTEIN; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PSORIASIS;

ACETYLATION; ADULT; CELL DIVISION; CELL MOVEMENT; CELLS, CULTURED; DERMATITIS; HISTONE DEACETYLASES; HUMANS; INTERFERON-GAMMA; INTERLEUKINS; KERATINOCYTES; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PSORIASIS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SIRTUIN 1; STAT3 TRANSCRIPTION FACTOR;

EID: 79954569231     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.10-172288     Document Type: Article

References (35)

1. Ouyang, W., Kolls, J. K., and Zheng, Y. (2008) The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28, 454-467 (Pubitemid 351471762)
2. Spolski, R., and Leonard, W. J. (2009) Cytokine mediators of Th17 function. Eur. J. Immunol. 39, 658-661
3. 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
4. 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
5. Eyerich, S., Eyerich, K., Pennino, D., Carbone, T., Nasorri, F., Pallotta, S., Cianfarani, F., Odorisio, T., Traidl-Hoffmann, C., Behrendt, H., Durham, S. R., Schmidt-Weber, C. B., and Cavani, A. (2009) Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodelling. J. Clin. Invest. 119, 3573-3585
6. Kotenko, S. V., Izotova, L. S., Mirochnitchenko, O. V., Esterova, E., Dickensheets, H., Donnelly, R. P., and Pestka, S. (2001) Identification of the functional interleukin-22 (IL-22) receptor complex: the IL-10R2 chain (IL-10Rbeta) is a common chain of both the IL-10 and IL-22 (IL-10-related T cell-derived inducible factor, IL-TIF) receptor complexes. J. Biol. Chem. 276, 2725-2732
7. Wolk, K., and Sabat, R. (2006) Interleukin-22: a novel T and NK cell-derived cytokine that regulates the biology of tissue cells. Cytok. Growth Factor Rev. 17, 367-380 (Pubitemid 44572879)
8. 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)
9. 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: a potential role in psoriasis. Eur. J. Immunol. 36, 1309-1323
10. 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)
11. Zheng, Y., Danilenko, D. M., Valdez, P., Kasman, I., Eastham-Anderson, J., Wu, J., and Ouyang, W. (2007) Interleukin-22, a T (H) 17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 445, 648-651 (Pubitemid 46232884)
12. Sano, S., Chan, K. S., Carbajal, S., Clifford, J., Peavey, M., Kiguchi, K., Itami, S., Nickoloff, B. J., and DiGiovanni, J. (2005) Stat3 links activated keratinocytes and immunocytes required for development of psoriasis in a novel transgenic mouse model. Nat. Med. 11, 43-49 (Pubitemid 40215836)
13. Wen, Z., Zhong, Z., and Darnell, J. E. J. (1995) Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82, 241-250
14. Zhu, B. M., Ishida, Y., Robinson, G. W., Pacher-Zavisin, M., Yoshimura, A., Murphy, P. M., and Hennighausen, L. (2008) SOCS3 negatively regulates the gp130-STAT3 pathway in mouse skin wound healing. J. Invest. Dermatol. 128, 1821-1829 (Pubitemid 351847364)
15. Yuan, Z. L., Guan, Y. J., Chatterjee, D., and Chin, Y. E. (2005) Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 307, 269-273 (Pubitemid 40116244)
16. Nie, Y., Erion, D. M., Yuan, Z., Dietrich, M., Shulman, G. I., Horvath, T. L., and Gao, Q. (2009) STAT3 inhibition of gluconeogenesis is downregulated by SirT1. Nat. Cell Biol. 11, 492-500
17. Blander, G., Bhimavarapu, A., Mammone, T., Maes, D., Elliston, K., Reich, C., Matsui, M. S., Guarente, L., and Loureiro, J. J. (2009) SIRT1 promotes differentiation of normal human keratinocytes. J. Invest. Dermatol. 129, 41-49
18. Picard, F., Kurtev, M., Chung, N., Topark-Ngarm, A., Senawong, T., Machado De Oliveira, R., Leid, M., McBurney, M. W., and Guarente, L. (2004) Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature 429, 771-776 (Pubitemid 38833129)
19. Fulco, M., Schiltz, R. L., Iezzi, S., King, M. T., Zhao, P., Kashiwaya, Y., Hoffman, E., Veech, R. L., and Sartorelli, V. (2003) Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol. Cell 12, 51-62 (Pubitemid 36945036)
20. Madonna, S., Scarponi, C., De Pità, O., and Albanesi, C. (2008) Suppressor of cytokine signaling 1 inhibits IFN-gamma inflammatory signaling in human keratinocytes by sustaining ERK1/2 activation. FASEB J. 22, 3287-3297
21. Pennino, D., Eyerich, K., Scarponi, C., Carbone, T., Eyerich, S., Nasorri, F., Garcovich, S., Traidl-Hoffmann, C., Albanesi, C., and Cavani, A. (2010) IL-17 amplifies human contact hypersensitivity by licensing hapten nonspecific Th1 cells to kill autologous keratinocytes. J. Immunol. 184, 4880-4888
22. Ong, P. Y., Ohtake, T., Brandt, C., Strickland, I., Boguniewicz, M., Ganz, T., Gallo, R. L., and Leung, D. Y. M. (2002) Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N. Engl. J. Med. 347, 1151-1160
23. 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)
24. 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
25. Genovese, C., Trani, D., Caputi, M., and Claudio, P. P. (2006) Cell cycle control and beyond: emerging roles for the retinoblastoma gene family. Oncogene 25, 5201-5209 (Pubitemid 44299078)
26. Hancock, G. E., Kaplan, G., and Cohn, Z. A. (1988) Keratinocyte growth regulation by the products of immune cells. J. Exp. Med. 168, 1395-1402 (Pubitemid 18264873)
27. Sano, S., Chan, K. S., and Di Giovanni, J. (2008) Impact of Stat3 activation upon skin biology: a dichotomy of its role between homeostasis and diseases. J. Dermatol. Sci. 50, 1-14 (Pubitemid 351249893)
28. Lejeune, D., Dumoutier, L., Constantinescu, S., Kruijer, W., Schuringa, J. J., and Renauld, J. C. (2002) Interleukin-22 (IL-22) activates the JAK/STAT, ERK, JNK, and p38 MAP kinase pathways in a rat hepatoma cell line. J. Biol. Chem. 277, 33676-33682
29. Fierlbeck, G., Rassner, G., and Müller, C. (1990) Psoriasis induced at the injection site of recombinant interferon gamma. Results of immunohistologic investigations. Arch. Dermatol 126, 351-355 (Pubitemid 20094675)
30. Scheynius, A., Fransson, J., Johansson, C., Hammar, H., Baker, B., Fry, L., and Valdimarsson, H. (1992) Expression of interferon-gamma receptors in normal and psoriatic skin. J. Invest. Dermatol. 98, 255-258
31. Feige, J. N., and Auwerx, J. (2008) Transcriptional targets of sirtuins in the coordination of mammalian physiology. Curr. Opin. Cell Biol. 20, 303-309
32. Bata-Csorgo, Z., Hammerberg, C., Voorhees, J. J., and Cooper, K. D. (1993) Flow cytometric identification of proliferative subpopulations within normal human epidermis and the localization of the primary hyperproliferative population in psoriasis. J. Exp. Med. 178, 1271-1281 (Pubitemid 23277360)
33. Guilloteau, K., Paris, I., Pedretti, N., Boniface, K., Juchaux, F., Huguier, V., Guillet, G., Bernard, F. X., Lecron, J. C., and Morel, F. (2010) Skin inflammation induced by the synergistic action of IL-17A, IL-22, oncostatin M., IL-1α, and TNF-α recapitulates some features of psoriasis. J. Immunol. 184, 5263-5270
34. Chan, K. S., Carbajal, S., Kiguchi, K., Clifford, J., Sano, S., DiGiovanni, J. (2004) Epidermal growth factor receptor-mediated activation of Stat3 during multistage skin carcinogenesis. Cancer Res. 64, 2382-2389 (Pubitemid 38523890)
35. Miyoshi, K., Takaishi, M., Nakajima, K., Ikeda, M., Kanda, T., Tarutani, M., Iiyama, T., Asao, N., Digiovanni, J., and Sano, S. (2010) Stat3 as a therapeutic target for the treatment of psoriasis: a clinical feasibility study with STA-21, a Stat3 inhibitor. [E-pub ahead of print] J. Invest. Dermatol. doi:10.1038/jid.2010.255