Class i lysine deacetylases facilitate glucocorticoid-induced transcription

Journal of Biological Chemistry

Volumn 288, Issue 40, 2013, Pages 28900-28912

  Kadiyala, Vineela ^a,b   Patrick, Nina M ^a   Mathieu, Wana ^a   Jaime Frias, Rosa ^a   Pookhao, Naruekamol ^a   An, Lingling ^a   Smith, Catharine L ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b University of Arizona   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR TARGETS; CLASS I; MMTV PROMOTERS; TARGET GENES; TRANSACTIVATION;

AMINO ACIDS; GENES;

TRANSCRIPTION;

GLUCOCORTICOID; HISTONE DEACETYLASE; LYSINE DEACETYLASE 1; LYSINE DEACETYLASE 2; UNCLASSIFIED DRUG; VALPROIC ACID;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME MECHANISM; GENE ACTIVATION; GENE EXPRESSION; GENE TARGETING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION INITIATION;

GENE TRANSCRIPTION; GLUCOCORTICOID RECEPTOR; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITORS; TRANSCRIPTION COACTIVATORS;

ACETYLATION; AMIDOHYDROLASES; ANIMALS; CELL LINE, TUMOR; DEXAMETHASONE; ENZYME INHIBITORS; GLUCOCORTICOIDS; HISTONES; HSP90 HEAT-SHOCK PROTEINS; HYDROXAMIC ACIDS; LYSINE; MICE; PEPTIDES, CYCLIC; PROTEIN BINDING; RECEPTORS, GLUCOCORTICOID; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION; VALPROIC ACID;

EID: 84885110227     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.505115     Document Type: Article

References (45)

1. Choudhary, C., Kumar, C., Gnad, F., Nielsen, M. L., Rehman, M., Walther, T. C., Olsen, J. V., and Mann, M. (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840
2. Kim, S. C., Sprung, R., Chen, Y., Xu, Y., Ball, H., Pei, J., Cheng, T., Kho, Y., Xiao, H., Xiao, L., Grishin, N. V., White, M., Yang, X. J., and Zhao, Y. (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 23, 607-618
3. Haberland, M., Montgomery, R. L., and Olson, E. N. (2009) The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10, 32-42
4. Lahm, A., Paolini, C., Pallaoro, M., Nardi, M. C., Jones, P., Neddermann, P., Sambucini, S., Bottomley, M. J., Lo Surdo, P., Carfí, A., Koch, U., De Francesco, R., Steinkühler, C., and Gallinari, P. (2007) Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc. Natl. Acad. Sci. U.S.A. 104, 17335-17340
5. Kovacs, J. J., Murphy, P. J., Gaillard, S., Zhao, X., Wu, J. T., Nicchitta, C. V., Yoshida, M., Toft, D. O., Pratt, W. B., and Yao, T. P. (2005) HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol. Cell 18, 601-607
6. Zhang, Y., Kwon, S., Yamaguchi, T., Cubizolles, F., Rousseaux, S., Kneissel, M., Cao, C., Li, N., Cheng, H. L., Chua, K., Lombard, D., Mizeracki, A., Matthias, G., Alt, F. W., Khochbin, S., and Matthias, P. (2008) Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally. Mol. Cell. Biol. 28, 1688-1701
7. Houtkooper, R. H., Pirinen, E., and Auwerx, J. (2012) Sirtuins as regulators of metabolism and healthspan. Nat. Rev. Mol. Cell Biol. 13, 225-238
8. Khan, N., Jeffers, M., Kumar, S., Hackett, C., Boldog, F., Khramtsov, N., Qian, X., Mills, E., Berghs, S. C., Carey, N., Finn, P. W., Collins, L. S., Tumber, A., Ritchie, J. W., Jensen, P. B., Lichenstein, H. S., and Sehested, M. (2008) Determination of the class and isoform selectivity of smallmolecule histone deacetylase inhibitors. Biochem. J. 409, 581-589
9. Bantscheff, M., Hopf, C., Savitski, M. M., Dittmann, A., Grandi, P., Michon, A. M., Schlegl, J., Abraham, Y., Becher, I., Bergamini, G., Boesche, M., Delling, M., Dümpelfeld, B., Eberhard, D., Huthmacher, C., Mathieson, T., Poeckel, D., Reader, V., Strunk, K., Sweetman, G., Kruse, U., Neubauer, G., Ramsden, N. G., and Drewes, G. (2011) Chemoproteomics profiling of HDAC inhibitors reveals selective targeting of HDAC complexes. Nat. Biotechnol. 29, 255-265
10. Spiegel, S., Milstien, S., and Grant, S. (2012) Endogenous modulators and pharmacological inhibitors of histone deacetylases in cancer therapy. Oncogene 31, 537-551
11. Chuang, D. M., Leng, Y., Marinova, Z., Kim, H. J., and Chiu, C. T. (2009) Multiple roles of HDAC inhibition in neurodegenerative conditions. Trends Neurosci. 32, 591-601
12. Isojärvi, J. I., Taubøll, E., and Herzog, A. G. (2005) Effect of antiepileptic drugs on reproductive endocrine function in individuals with epilepsy. CNS Drugs 19, 207-223
13. Luef, G., Rauchenzauner, M., Waldmann, M., Sturm, W., Sandhofer, A., Seppi, K., Trinka, E., Unterberger, I., Ebenbichler, C. F., Joannidis, M., Walser, G., Bauer, G., Hoppichler, F., and Lechleitner, M. (2009) Nonalcoholic fatty liver disease (NAFLD), insulin resistance and lipid profile in antiepileptic drug treatment. Epilepsy Res. 86, 42-47
14. Robyr, D., Wolffe, A. P., and Wahli, W. (2000) Nuclear hormone receptor coregulators in action: diversity for shared tasks. Mol. Endocrinol. 14, 329-347
15. Chen, J. D., and Li, H. (1998) Coactivation and corepression in transcriptional regulation by steroid/nuclear hormone receptors. Crit. Rev. Eukaryot. Gene Expr. 8, 169-190
16. Jackson, T. A., Richer, J. K., Bain, D. L., Takimoto, G. S., Tung, L., and Horwitz, K. B. (1997) The partial agonist activity of antagonist-occupied steroid receptors is controlled by a novel hinge domain-binding coactivator L7/SPA and the corepressors N-CoR or SMRT. Mol. Endocrinol. 11, 693-705
17. Wagner, B. L., Norris, J. D., Knotts, T. A., Weigel, N. L., and McDonnell, D. P. (1998) The nuclear corepressors NCoR and SMRT are key regulators of both ligand-and 8-bromo-cyclic AMP-dependent transcriptional activity of the human progesterone receptor. Mol. Cell. Biol. 18, 1369-1378
18. Lavinsky, R. M., Jepsen, K., Heinzel, T., Torchia, J., Mullen, T. M., Schiff, R., Del-Rio, A. L., Ricote, M., Ngo, S., Gemsch, J., Hilsenbeck, S. G., Osborne, C. K., Glass, C. K., Rosenfeld, M. G., and Rose, D. W. (1998) Diverse signaling pathways modulate nuclear receptor recruitment of N-CoR and SMRT complexes. Proc. Natl. Acad. Sci. U.S.A. 95, 2920-2925
19. Plesko, M. M., Hargrove, J. L., Granner, D. K., and Chalkley, R. (1983) Inhibition by sodium butyrate of enzyme induction by glucocorticoids and dibutyryl cyclic AMP. A role for the rapid form of histone acetylation. J. Biol. Chem. 258, 13738-13744
20. Bresnick, E. H., John, S., Berard, D. S., LeFebvre, P., and Hager, G. L. (1990) Glucocorticoid receptor-dependent disruption of a specific nucleosome on the mouse mammary tumor virus promoter is prevented by sodium butyrate. Proc. Natl. Acad. Sci. U.S.A. 87, 3977-3981
21. Tichonicky, L., Santana-Calderon, M. A., Defer, N., Giesen, E. M., Beck, G., and Kruh, J. (1981) Selective inhibition by sodium butyrate of glucocorticoid-induced tyrosine aminotransferase synthesis in hepatoma tissue-cultured cells. Eur. J. Biochem. 120, 427-433
22. Mulholland, N. M., Soeth, E., and Smith, C. L. (2003) Inhibition ofMMTV transcription byHDACinhibitors occurs independent of changes in chromatin remodeling and increased histone acetylation. Oncogene 22, 4807-4818
23. Sheldon, L. A., Becker, M., and Smith, C. L. (2001) Steroid hormone receptor-mediated histone deacetylation and transcription at the mouse mammary tumor virus promoter. J. Biol. Chem. 276, 32423-32426
24. Qiu, Y., Zhao, Y., Becker, M., John, S., Parekh, B. S., Huang, S., Hendarwanto, A., Martinez, E. D., Chen, Y., Lu, H., Adkins, N. L., Stavreva, D. A., Wiench, M., Georgel, P. T., Schiltz, R. L., and Hager, G. L. (2006) HDAC1 acetylation is linked to progressive modulation of steroid receptor-induced gene transcription. Mol. Cell 22, 669-679
25. Qiu, Y., Stavreva, D. A., Luo, Y., Indrawan, A., Chang, M., and Hager, G. L. (2011) Dynamic interaction of HDAC1 with a glucocorticoid receptorregulated gene is modulated by the activity state of the promoter. J. Biol. Chem. 286, 7641-7647
26. Lee, S. C., Magklara, A., and Smith, C. L. (2011) HDAC activity is required for efficient core promoter function at the mousemammarytumor virus promoter. J. Biomed. Biotechnol. 2011, 416905, dx.doi.org/10.1155/2011/ 416905
27. John, S., Johnson, T. A., Sung, M. H., Biddie, S. C., Trump, S., Koch-Paiz, C. A., Davis, S. R., Walker, R., Meltzer, P. S., and Hager, G. L. (2009) Kinetic complexity of the global response to glucocorticoid receptor action. Endocrinology 150, 1766-1774
28. Isojärvi, J. (2008) Disorders of reproduction in patients with epilepsy: antiepileptic drug related mechanisms. Seizure 17, 111-119
29. Pylvänen, V., Pakarinen, A., Knip, M., and Isojärvi, J. (2006) Insulin-related metabolic changes during treatment with valproate in patients with epilepsy. Epilepsy Behav. 8, 643-648
30. Murphy, P. J., Morishima, Y., Kovacs, J. J., Yao, T. P., and Pratt, W. B. (2005) Regulation of the dynamics of hsp90 action on the glucocorticoid receptor by acetylation/deacetylation of the chaperone. J. Biol. Chem. 280, 33792-33799
31. Terbach, N., and Williams, R. S. (2009) Structure-function studies for the panacea, valproic acid. Biochem. Soc. Trans. 37, 1126-1132
32. Clayton, A. L., Hazzalin, C. A., and Mahadevan, L. C. (2006) Enhanced histone acetylation and transcription: a dynamic perspective. Mol. Cell 23, 289-296
33. Wang, Z., Zang, C., Cui, K., Schones, D. E., Barski, A., Peng, W., and Zhao, K. (2009) Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138, 1019-1031
34. Kidder, B. L., and Palmer, S. (2012) HDAC1 regulates pluripotency and lineage specific transcriptional networks in embryonic and trophoblast stem cells. Nucleic Acids Res. 40, 2925-2939
35. Ram, O., Goren, A., Amit, I., Shoresh, N., Yosef, N., Ernst, J., Kellis, M., Gymrek, M., Issner, R., Coyne, M., Durham, T., Zhang, X., Donaghey, J., Epstein, C. B., Regev, A., and Bernstein, B. E. (2011) Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells. Cell 147, 1628-1639
36. Yang, X. J., and Seto, E. (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat. Rev. Mol. Cell Biol. 9, 206-218
37. Luo, Y., Jian, W., Stavreva, D., Fu, X., Hager, G., Bungert, J., Huang, S., and Qiu, Y. (2009) Trans-regulation of histone deacetylase activities through acetylation. J. Biol. Chem. 284, 34901-34910
38. Chng, K. R., Chang, C. W., Tan, S. K., Yang, C., Hong, S. Z., Sng, N. Y., and Cheung, E. (2012) A transcriptional repressor co-regulatory network governing androgen response in prostate cancers. EMBO J. 31, 2810-2823
39. Welsbie, D. S., Xu, J., Chen, Y., Borsu, L., Scher, H. I., Rosen, N., and Sawyers, C. L. (2009) Histone deacetylases are required for androgen receptor function in hormone-sensitive and castrate-resistant prostate cancer. Cancer Res. 69, 958-966
40. Lee, H. A., Lee, D. Y., Cho, H. M., Kim, S. Y., Iwasaki, Y., and Kim, I. (2013) Histone deacetylase inhibition attenuates transcriptional activity of mineralocorticoid receptor through its acetylation and prevents development of hypertension. Circ. Res. 112, 1004-1012
41. Rascle, A., Johnston, J. A., and Amati, B. (2003) Deacetylase activity is required for recruitment of the basal transcription machinery and transactivation by STAT5. Mol. Cell. Biol. 23, 4162-4173
42. Nader, N., Chrousos, G. P., and Kino, T. (2009) Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: potential physiological implications. FASEB J. 23, 1572-1583
43. Ito, K., Yamamura, S., Essilfie-Quaye, S., Cosio, B., Ito, M., Barnes, P. J., and Adcock, I. M. (2006) Histone deacetylase 2-mediated deacetylation of the glucocorticoid receptor enables NF-κB suppression. J. Exp. Med. 203, 7-13
44. Chen, H., Lin, R. J., Xie, W., Wilpitz, D., and Evans, R. M. (1999) Regulation of hormone-induced histone hyperacetylation and gene activation via acetylation of an acetylase. Cell 98, 675-686
45. Dinarello, C. A., Fossati, G., and Mascagni, P. (2011) Histone deacetylase inhibitors for treating a spectrum of diseases not related to cancer. Mol. Med. 17, 333-352