Opposed regulation of type I IFN-induced STAT3 and ISGF3 transcriptional activities by histone deacetylases (HDACS) 1 and 2

FASEB Journal

Volumn 26, Issue 1, 2012, Pages 240-249

  Icardi, Laura ^a,b   Lievens, Sam ^a,b   Mori, Raffaele ^a,b   Piessevaux, Julie ^a,b   De Cauwer, Lode ^a,b   De Bosscher, Karolien ^a,b   Tavernier, Jan ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b GHENT UNIVERSITY   (Belgium)

Author keywords

Interferon signaling; Interferon stimulated genes; Trichostatin A; TSA

Indexed keywords

ALPHA2 INTERFERON; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; INTERFERON; INTERFERON STIMULATED GENE FACTOR 3; PROTEIN C FOS; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRICHOSTATIN A;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ENZYME ACTIVITY; GENE EXPRESSION; GENE INDUCTION; GENE SILENCING; GENE TRANSLOCATION; GENETIC REGULATION; GENETIC TRANSCRIPTION; HISTONE PHOSPHORYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; REPORTER GENE;

CELL NUCLEUS; HEK293 CELLS; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; HYDROXAMIC ACIDS; INTERFERON TYPE I; INTERFERON-ALPHA; INTERFERON-STIMULATED GENE FACTOR 3, GAMMA SUBUNIT; PHOSPHORYLATION; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTIONAL ACTIVATION;

EID: 84855373185     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-191122     Document Type: Article

References (41)

1. Muller, U., Steinhoff, U., Reis, L. F., Hemmi, S., Pavlovic, J., Zinkernagel, R. M., and Aguet, M. (1994) Functional role of type I and type II interferons in antiviral defense. Science 264, 1918-1921 (Pubitemid 24245635)
2. Gutterman, J. U. (1994) Cytokine therapeutics: lessons from interferon alpha. Proc. Natl. Acad. Sci. U. S. A. 91, 1198-1205
3. Schindler, C., Levy, D. E., and Decker, T. (2007) JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 282, 20059-20063 (Pubitemid 47099977)
4. Van Boxel-Dezaire, A. H., Rani, M. R., and Stark, G. R. (2006) Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 25, 361-372 (Pubitemid 44354225)
5. Bromberg, J. F. (2001) Activation of STAT proteins and growth control. Bioessays. 23, 161-169
6. Levy, D. E., and Darnell, J. E., Jr. (2002) Stats: transcriptional control and biological impact. Nat. Rev. Mol. Cell. Biol. 3, 651-662 (Pubitemid 34987786)
7. Wen, Z., Zhong, Z., and Darnell, J. E., Jr. (1995) Maximal activation of transcription by Stat1 and Stat3 requires both tyrosine and serine phosphorylation. Cell 82, 241-250
8. Hou, T., Ray, S., Lee, C., and Brasier, A. R. (2008) The STAT3 NH2-terminal domain stabilizes enhanceosome assembly by interacting with the p300 bromodomain. J. Biol. Chem. 283, 30725-30734
9. 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)
10. Ray, S., Lee, C., Hou, T., Boldogh, I., and Brasier, A. R. (2008) Requirement of histone deacetylase1 (HDAC1) in signal transducer and activator of transcription 3 (STAT3) nucleocytoplasmic distribution. Nucleic Acids Res. 36, 4510-4520
11. Togi, S., Kamitani, S., Kawakami, S., Ikeda, O., Muromoto, R., Nanbo, A., and Matsuda, T. (2009) HDAC3 influences phosphorylation of STAT3 at serine 727 by interacting with PP2A. Biochem. Biophys. Res. Commun. 379, 616-620
12. Bromberg, J. (2002) Stat proteins and oncogenesis. J. Clin. Invest. 109, 1139-1142
13. Bromberg, J. F., Wrzeszczynska, M. H., Devgan, G., Zhao, Y., Pestell, R. G., Albanese, C., and Darnell, J. E., Jr. (1999) Stat3 as an oncogene. Cell 98, 295-303 (Pubitemid 29380565)
14. Nusinzon, I., and Horvath, C. M. (2003) Interferon-stimulated transcription and innate antiviral immunity require deacetylase activity and histone deacetylase 1. Proc. Natl. Acad. Sci. U. S. A. 100, 14742-14747 (Pubitemid 37517961)
15. Eyckerman, S., Verhee, A., der Heyden, J. V., Lemmens, I., Ostade, X. V., Vandekerckhove, J., and Tavernier, J. (2001) Design and application of a cytokine-receptor-based interaction trap. Nat. Cell Biol. 3, 1114-1119 (Pubitemid 33130462)
16. Van Schoubroeck, B., Van Acker, K., Dams, G., Jochmans, D., Clayton, R., Berke, J. M., Lievens, S., Van der Heyden, J., and Tavernier, J. (2012) MAPPIT as a high-throughput screening assay for modulators of protein-protein interactions in HIV and HCV. Methods Mol. Biol. 812 In press
17. Graham, F. L., and van der Eb, A. J. (1973) A new technique for the assay of infectivity of human adenovirus 5 DNA. Virology 52, 456-467
18. Witcher, M., Ross, D. T., Rousseau, C., Deluca, L., and Miller, W. H., Jr. (2003) Synergy between all-trans retinoic acid and tumor necrosis factor pathways in acute leukemia cells. Blood 102, 237-245 (Pubitemid 36759660)
19. Pierreux, C. E., Nicolas, F. J., and Hill, C. S. (2000) Transforming growth factor beta-independent shuttling of Smad4 between the cytoplasm and nucleus. Mol. Cell. Biol. 20, 9041-9054 (Pubitemid 32245933)
20. Hirano, T., Ishihara, K., and Hibi, M. (2000) Roles of STAT3 in mediating the cell growth, differentiation and survival signals relayed through the IL-6 family of cytokine receptors. Oncogene 19, 2548-2556 (Pubitemid 30339210)
21. 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
22. Taplick, J., Kurtev, V., Kroboth, K., Posch, M., Lechner, T., and Seiser, C. (2001) Homo-oligomerisation and nuclear localisation of mouse histone deacetylase 1. J. Mol. Biol. 308, 27-38 (Pubitemid 33027624)
23. Yang, W. M., Tsai, S. C., Wen, Y. D., Fejer, G., and Seto, E. (2002) Functional domains of histone deacetylase-3. J. Biol. Chem. 277, 9447-9454
24. Senese, S., Zaragoza, K., Minardi, S., Muradore, I., Ronzoni, S., Passafaro, A., Bernard, L., Draetta, G. F., Alcalay, M., Seiser, C., and Chiocca, S. (2007) Role for histone deacetylase 1 in human tumor cell proliferation. Mol. Cell. Biol. 27, 4784-4795 (Pubitemid 47016131)
25. Meraz, M. A., White, J. M., Sheehan, K. C., Bach, E. A., Rodig, S. J., Dighe, A. S., Kaplan, D. H., Riley, J. K., Greenlund, A. C., Campbell, D., Carver-Moore, K., DuBois, R. N., Clark, R., Aguet, M., and Schreiber, R. D. (1996) Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84, 431-442 (Pubitemid 26058568)
26. Wang, R., Cherukuri, P., and Luo, J. (2005) Activation of Stat3 sequence-specific DNA binding and transcription by p300/CREBbinding protein-mediated acetylation. J. Biol. Chem. 280, 11528-11534 (Pubitemid 40418464)
27. Ohbayashi, N., Ikeda, O., Taira, N., Yamamoto, Y., Muromoto, R., Sekine, Y., Sugiyama, K., Honjoh, T., and Matsuda, T. (2007) LIF- and IL-6-induced acetylation of STAT3 at Lys-685 through PI3K/Akt activation. Biol. Pharm. Bull. 30, 1860-1864 (Pubitemid 47607769)
28. Ray, S., Boldogh, I., and Brasier, A. R. (2005) STAT3 NH2- terminal acetylation is activated by the hepatic acute-phase response and required for IL-6 induction of angiotensinogen. Gastroenterology 129, 1616-1632 (Pubitemid 41597401)
29. Melnick, A., and Licht, J. D. (2002) Histone deacetylases as therapeutic targets in hematologic malignancies. Curr. Opin. Hematol. 9, 322-332 (Pubitemid 34596877)
30. Segre, C. V., and Chiocca, S. (2011) Regulating the regulators: the post-translational code of class I HDAC1 and HDAC2. J. Biomed. Biotechnol. 2011:690848
31. Tang, X., Gao, J. S., Guan, Y. J., McLane, K. E., Yuan, Z. L., Ramratnam, B., and Chin, Y. E. (2007) Acetylation-dependent signal transduction for type I interferon receptor. Cell 131, 93-105 (Pubitemid 47498527)
32. Chang, H. M., Paulson, M., Holko, M., Rice, C. M., Williams, B. R., Marie, I., and Levy, D. E. (2004) Induction of interferon-stimulated gene expression and antiviral responses require protein deacetylase activity. Proc. Natl. Acad. Sci. U. S. A. 101, 9578-9583 (Pubitemid 38869278)
33. Nusinzon, I., and Horvath, C. M. (2006) Positive and negative regulation of the innate antiviral response and beta interferon gene expression by deacetylation. Mol. Cell. Biol. 26, 3106-3113
34. Sakamoto, S., Potla, R., and Larner, A. C. (2004) Histone deacetylase activity is required to recruit RNA polymerase II to the promoters of selected interferon-stimulated early response genes. J. Biol. Chem. 279, 40362-40367 (Pubitemid 39287623)
35. Ho, H. H., and Ivashkiv, L. B. (2006) Role of STAT3 in type I interferon responses. Negative regulation of STAT1-dependent inflammatory gene activation. J. Biol. Chem. 281, 14111-14118 (Pubitemid 43848338)
36. Regis, G., Pensa, S., Boselli, D., Novelli, F., and Poli, V. (2008) Ups and downs: the STAT1:STAT3 seesaw of interferon and gp130 receptor signalling. Semin. Cell Dev. Biol. 19, 351-359
37. Costa-Pereira, A. P., Tininini, S., Strobl, B., Alonzi, T., Schlaak, J. F., Is'harc, H., Gesualdo, I., Newman, S. J., Kerr, I. M., and Poli, V. (2002) Mutational switch of an IL-6 response to an interferon-gamma-like response. Proc. Natl. Acad. Sci. U. S. A. 99, 8043-8047 (Pubitemid 34651002)
38. Qing, Y., and Stark, G. R. (2004) Alternative activation of STAT1 and STAT3 in response to interferon-gamma. J. Biol. Chem. 279, 41679-41685 (Pubitemid 39313613)
39. Regis, G., Icardi, L., Conti, L., Chiarle, R., Piva, R., Giovarelli, M., Poli, V., and Novelli, F. (2009) IL-6, but not IFN-gamma, triggers apoptosis and inhibits in vivo growth of human malignant T cells on STAT3 silencing. Leukemia 23, 2102-2108
40. Tanabe, Y., Nishibori, T., Su, L., Arduini, R. M., Baker, D. P., and David, M. (2005) Cutting edge: role of STAT1, STAT3, and STAT5 in IFN-alpha beta responses in T lymphocytes. J. Immunol. 174, 609-613 (Pubitemid 40094251)
41. Gamero, A. M., Potla, R., Wegrzyn, J., Szelag, M., Edling, A. E., Shimoda, K., Link, D. C., Dulak, J., Baker, D. P., Tanabe, Y., Grayson, J. M., and Larner, A. C. (2006) Activation of Tyk2 and Stat3 is required for the apoptotic actions of interferon-beta in primary pro-B cells. J. Biol. Chem. 281, 16238-16244