Acetylation of histone deacetylase 1 regulates NuRD corepressor complex activity

Journal of Biological Chemistry

Volumn 287, Issue 48, 2012, Pages 40279-40291

  Yang, Tao ^a,b   Jian, Wei ^a   Luo, Yi ^a   Fu, Xueqi ^b   Noguchi, Constance ^c   Bungert, Jörg ^a   Huang, Suming ^a   Qiu, Yi ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b JILIN UNIVERSITY   (China)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COACTIVATORS; COREPRESSOR COMPLEXES; DEACETYLASE ACTIVITY; ERYTHROID DIFFERENTIATION; GENE ACTIVATION; HISTONE DEACETYLASES; OVER-EXPRESSION; REMODELING ACTIVITY;

ACETYLATION; CELL PROLIFERATION; CHEMICAL ACTIVATION; GENES;

TRANSCRIPTION;

E1A ASSOCIATED P300 PROTEIN; HEMOGLOBIN BETA CHAIN; HISTONE DEACETYLASE 1; NUCLEAR RECEPTOR COREPRESSOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOG 1; TRANSCRIPTION FACTOR GATA 1; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME REPRESSION; ERYTHROPOIESIS; GENE SILENCING; GENETIC TRANSCRIPTION; HISTONE ACETYLATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; UPREGULATION;

ACETYLATION; ANIMALS; CELL DIFFERENTIATION; CELL LINE; CO-REPRESSOR PROTEINS; ERYTHROID CELLS; GATA1 TRANSCRIPTION FACTOR; HISTONE DEACETYLASE 1; HUMANS; MI-2 NUCLEOSOME REMODELING AND DEACETYLASE COMPLEX; MICE; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; TRANSCRIPTIONAL ACTIVATION;

EID: 84870023777     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.349704     Document Type: Article

References (71)

1. Cress, W. D., and Seto, E. (2000) Histone deacetylases, transcriptional control, and cancer. J. Cell. Physiol. 184, 1-16 (Pubitemid 30349623)
2. Cho, Y., Griswold, A., Campbell, C., and Min, K. T. (2005) Individual histone deacetylases in Drosophila modulate transcription of distinct genes. Genomics 86, 606-617 (Pubitemid 41416792)
3. Foglietti, C., Filocamo, G., Cundari, E., De Rinaldis, E., Lahm, A., Cortese, R., and Steinkühler, C. (2006) Dissecting the biological functions of Drosophila histone deacetylases by RNA interference and transcriptional profiling. J. Biol. Chem. 281, 17968-17976 (Pubitemid 44035596)
4. Glozak, M. A., and Seto, E. (2007) Histone deacetylases and cancer. Oncogene 26, 5420-5432 (Pubitemid 47255924)
5. Glaser, K. B., Li, J., Staver, M. J., Wei, R. Q., Albert, D. H., and Davidsen, S. K. (2003) Role of class I and class II histone deacetylases in carcinoma cells using siRNA. Biochem. Biophys. Res. Commun. 310, 529-536 (Pubitemid 37163696)
6. Haberland, M., Johnson, A., Mokalled, M. H., Montgomery, R. L., and Olson, E. N. (2009) Genetic dissection of histone deacetylase requirement in tumor cells. Proc. Natl. Acad. Sci. U.S.A. 106, 7751-7755
7. Inoue, S., Mai, A., Dyer, M. J., and Cohen, G. M. (2006) Inhibition of histone deacetylase class I but not class II is critical for the sensitization of leukemic cells to tumor necrosis factor-related apoptosis-inducing ligandinduced apoptosis. Cancer Res. 66, 6785-6792 (Pubitemid 44085638)
8. Lagger, G., Doetzlhofer, A., Schuettengruber, B., Haidweger, E., Simboeck, E., Tischler, J., Chiocca, S., Suske, G., Rotheneder, H., Wintersberger, E., and Seiser, C. (2003) The tumor suppressor p53 and histone deacetylase 1 are antagonistic regulators of the cyclin-dependent kinase inhibitor p21/WAF1/CIP1 gene. Mol. Cell. Biol. 23, 2669-2679 (Pubitemid 36403069)
9. Siegel, D., Hussein, M., Belani, C., Robert, F., Galanis, E., Richon, V. M., Garcia-Vargas, J., Sanz-Rodriguez, C., and Rizvi, S. (2009) Vorinostat in solid and hematologic malignancies. J. Hematol. Oncol. 2, 31
10. Zhang, Y., LeRoy, G., Seelig, H. P., Lane, W. S., and Reinberg, D. (1998) The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 95, 279-289 (Pubitemid 28473788)
11. Wade, P. A., Jones, P. L., Vermaak, D., and Wolffe, A. P. (1998) A multiple subunit Mi-2 histone deacetylase from Xenopus laevis cofractionates with an associated Snf2 superfamily ATPase. Curr. Biol. 8, 843-846 (Pubitemid 28324541)
12. Fatemi, M., and Wade, P. A. (2006) MBD family proteins: reading the epigenetic code. J. Cell Sci. 119, 3033-3037 (Pubitemid 44322117)
13. Feng, Q., Cao, R., Xia, L., Erdjument-Bromage, H., Tempst, P., and Zhang, Y. (2002) Identification and functional characterization of the p66/p68 components of the MeCP1 complex. Mol. Cell. Biol. 22, 536-546 (Pubitemid 34027498)
14. Feng, Q., and Zhang, Y. (2001) The MeCP1 complex represses transcription through preferential binding, remodeling, and deacetylating methylated nucleosomes. Genes Dev. 15, 827-832 (Pubitemid 32295063)
15. Ng, H. H., Zhang, Y., Hendrich, B., Johnson, C. A., Turner, B. M., Erdjument-Bromage, H., Tempst, P., Reinberg, D., and Bird, A. (1999) MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat. Genet. 23, 58-61 (Pubitemid 29418788)
16. Ahringer, J. (2000) NuRD and SIN3 histone deacetylase complexes in development. Trends Genet. 16, 351-356
17. Hutchins, A. S., Mullen, A. C., Lee, H. W., Sykes, K. J., High, F. A., Hendrich, B. D., Bird, A. P., and Reiner, S. L. (2002) Gene silencing quantitatively controls the function of a developmental trans-activator. Mol. Cell 10, 81-91 (Pubitemid 34876564)
18. Kehle, J., Beuchle, D., Treuheit, S., Christen, B., Kennison, J. A., Bienz, M., and Müller, J. (1998) dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282, 1897-1900 (Pubitemid 28555270)
19. Williams, C. J., Naito, T., Arco, P. G., Seavitt, J. R., Cashman, S. M., De Souza, B., Qi, X., Keables, P., Von Andrian, U. H., and Georgopoulos, K. (2004) The chromatin remodeler Mi-2β is required for CD4 expression and T cell development. Immunity 20, 719-733 (Pubitemid 38757442)
20. Brunmeir, R., Lagger, S., and Seiser, C. (2009) Histone deacetylase HDAC1/HDAC2-controlled embryonic development and cell differentiation. Int. J. Dev. Biol. 53, 275-289
21. Oh, Y. M., Kwon, Y. E., Kim, J. M., Bae, S. J., Lee, B. K., Yoo, S. J., Chung, C. H., Deshaies, R. J., and Seol, J. H. (2009) Chfr is linked to tumour metastasis through the down-regulation of HDAC1. Nat. Cell Biol. 11, 295-302
22. 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 (Pubitemid 43817601)
23. Qiu, Y., Stavreva, D. A., Luo, Y., Indrawan, A., Chang, M., and Hager, G. L. (2011) Dynamic interaction of HDAC1 with a glucocorticoid receptor-regulated gene is modulated by the activity state of the promoter. J. Biol. Chem. 286, 7641-7647
24. 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
25. Crispino, J. D. (2005) GATA1 in normal and malignant hematopoiesis. Semin. Cell Dev. Biol. 16, 137-147
26. Weiss, M. J., and Orkin, S. H. (1995) GATA transcription factors: key regulators of hematopoiesis. Exp. Hematol. 23, 99-107
27. Migliaccio, A. R., Rana, R. A., Vannucchi, A. M., and Manzoli, F. A. (2005) Role of GATA-1 in normal and neoplastic hemopoiesis. Ann. N.Y. Acad. Sci. 1044, 142-158 (Pubitemid 40967605)
28. Fujiwara, T., O'Geen, H., Keles, S., Blahnik, K., Linnemann, A. K., Kang, Y. A., Choi, K., Farnham, P. J., and Bresnick, E. H. (2009) Discovering hematopoietic mechanisms through genome-wide analysis of GATA factor chromatin occupancy. Mol. Cell 36, 667-681
29. Yu, M., Riva, L., Xie, H., Schindler, Y., Moran, T. B., Cheng, Y., Yu, D., Hardison, R., Weiss, M. J., Orkin, S. H., Bernstein, B. E., Fraenkel, E., and Cantor, A. B. (2009) Insights into GATA-1-mediated gene activation versus repression via genome-wide chromatin occupancy analysis. Mol. Cell 36, 682-695
30. Wu, W., Cheng, Y., Keller, C. A., Ernst, J., Kumar, S. A., Mishra, T., Morrissey, C., Dorman, C. M., Chen, K. B., Drautz, D., Giardine, B., Shibata, Y., Song, L., Pimkin, M., Crawford, G. E., Furey, T. S., Kellis, M., Miller, W., Taylor, J., Schuster, S. C., Zhang, Y., Chiaromonte, F., Blobel, G. A., Weiss, M. J., and Hardison, R. C. (2011) Dynamics of the epigenetic landscape during erythroid differentiation after GATA1 restoration. Genome Res. 21, 1659-1671
31. Evans, T., and Felsenfeld, G. (1989) The erythroid-specific transcription factor Eryf1: a new finger protein. Cell 58, 877-885 (Pubitemid 19227897)
32. Horak, C. E., Mahajan, M. C., Luscombe, N. M., Gerstein, M., Weissman, S. M., and Snyder, M. (2002) GATA-1 binding sites mapped in the β-globin locus by using mammalian chIp-chip analysis. Proc. Natl. Acad. Sci. U.S.A. 99, 2924-2929 (Pubitemid 34240562)
33. Welch, J. J., Watts, J. A., Vakoc, C. R., Yao, Y., Wang, H., Hardison, R. C., Blobel, G. A., Chodosh, L. A., and Weiss, M. J. (2004) Global regulation of erythroid gene expression by transcription factor GATA-1. Blood 104, 3136-3147 (Pubitemid 39507127)
34. Blobel, G. A., Nakajima, T., Eckner, R., Montminy, M., and Orkin, S. H. (1998) CREB-binding protein cooperates with transcription factor GATA-1 and is required for erythroid differentiation. Proc. Natl. Acad. Sci. U.S.A. 95, 2061-2066 (Pubitemid 28145894)
35. Cantor, A. B., and Orkin, S. H. (2002) Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 21, 3368-3376 (Pubitemid 34587709)
36. Hong, W., Nakazawa, M., Chen, Y. Y., Kori, R., Vakoc, C. R., Rakowski, C., and Blobel, G. A. (2005) FOG-1 recruits the NuRD repressor complex to mediate transcriptional repression by GATA-1. EMBO J. 24, 2367-2378 (Pubitemid 41032588)
37. Rodriguez, P., Bonte, E., Krijgsveld, J., Kolodziej, K. E., Guyot, B., Heck, A. J., Vyas, P., de Boer, E., Grosveld, F., and Strouboulis, J. (2005) GATA-1 forms distinct activating and repressive complexes in erythroid cells. EMBO J. 24, 2354-2366 (Pubitemid 41032587)
38. Harju-Baker, S., Costa, F. C., Fedosyuk, H., Neades, R., and Peterson, K. R. (2008) Silencing of Aγ-globin gene expression during adult definitive erythropoiesis mediated by GATA-1-FOG-1-Mi2 complex binding at the -566 GATA site. Mol. Cell. Biol. 28, 3101-3113 (Pubitemid 351657077)
39. Snow, J. W., and Orkin, S. H. (2009) Translational isoforms of FOG1 regulate GATA1-interacting complexes. J. Biol. Chem. 284, 29310-29319
40. Crispino, J. D., Lodish, M. B., MacKay, J. P., and Orkin, S. H. (1999) Use of altered specificity mutants to probe a specific protein-protein interaction in differentiation: the GATA-1:FOG complex. Mol. Cell 3, 219-228 (Pubitemid 29292622)
41. Grass, J. A., Boyer, M. E., Pal, S., Wu, J., Weiss, M. J., and Bresnick, E. H. (2003) GATA-1-dependent transcriptional repression of GATA-2 via disruption of positive autoregulation and domain-wide chromatin remodeling. Proc. Natl. Acad. Sci. U.S.A. 100, 8811-8816 (Pubitemid 36899180)
42. Rylski, M., Welch, J. J., Chen, Y. Y., Letting, D. L., Diehl, J. A., Chodosh, L. A., Blobel, G. A., and Weiss, M. J. (2003) GATA-1-mediated proliferation arrest during erythroid maturation. Mol. Cell. Biol. 23, 5031-5042 (Pubitemid 36793347)
43. Miccio, A., Wang, Y., Hong, W., Gregory, G. D., Wang, H., Yu, X., Choi, J. K., Shelat, S., Tong, W., Poncz, M., and Blobel, G. A. (2010) NuRD mediates activating and repressive functions of GATA-1 and FOG-1 during blood development. EMBO J. 29, 442-456
44. Letting, D. L., Chen, Y. Y., Rakowski, C., Reedy, S., and Blobel, G. A. (2004) Context-dependent regulation of GATA-1 by friend of GATA-1. Proc. Natl. Acad. Sci. U.S.A. 101, 476-481 (Pubitemid 38084661)
45. Huang, S., and Brandt, S. J. (2000) mSin3A regulates murine erythroleukemia cell differentiation through association with the TAL1 (or SCL) transcription factor. Mol. Cell. Biol. 20, 2248-2259 (Pubitemid 30123840)
46. Weiss, M. J., Yu, C., and Orkin, S. H. (1997) Erythroid-cell-specific properties of transcription factor GATA-1 revealed by phenotypic rescue of a gene-targeted cell line. Mol. Cell. Biol. 17, 1642-1651 (Pubitemid 27097393)
47. Gregory, T., Yu, C., Ma, A., Orkin, S. H., Blobel, G. A., and Weiss, M. J. (1999) GATA-1 and erythropoietin cooperate to promote erythroid cell survival by regulating bcl-xL expression. Blood 94, 87-96 (Pubitemid 29300137)
48. Pal, S., Cantor, A. B., Johnson, K. D., Moran, T. B., Boyer, M. E., Orkin, S. H., and Bresnick, E. H. (2004) Coregulator-dependent facilitation of chromatin occupancy by GATA-1. Proc. Natl. Acad. Sci. U.S.A. 101, 980-985 (Pubitemid 38160570)
49. Hu, X., Li, X., Valverde, K., Fu, X., Noguchi, C., Qiu, Y., and Huang, S. (2009) LSD1-mediated epigenetic modification is required for TAL1 function and hematopoiesis. Proc. Natl. Acad. Sci. U.S.A. 106, 10141-10146
50. Huang, S., Qiu, Y., Shi, Y., Xu, Z., and Brandt, S. J. (2000) P/CAF-mediated acetylation regulates the function of the basic helix-loop-helix transcription factor TAL1/SCL. EMBO J. 19, 6792-6803 (Pubitemid 32011672)
51. Hamiche, A., and Xiao, H. (2004) Methods for analysis of nucleosome sliding by Drosophila NURF. Methods Enzymol. 377, 353-363 (Pubitemid 38166827)
52. Kuendgen, A., and Gattermann, N. (2007) Valproic acid for the treatment of myeloid malignancies. Cancer 110, 943-954 (Pubitemid 47312858)
53. Friend, C., Scher, W., Holland, J. G., and Sato, T. (1971) Hemoglobin synthesis in murine virus-induced leukemic cells in vitro: stimulation of erythroid differentiation by dimethyl sulfoxide. Proc. Natl. Acad. Sci. U.S.A. 68, 378-382
54. Sawado, T., Igarashi, K., and Groudine, M. (2001) Activation of β-major globin gene transcription is associated with recruitment of NF-E2 to the β-globin LCR and gene promoter. Proc. Natl. Acad. Sci. U.S.A. 98, 10226-10231 (Pubitemid 32803002)
55. Tsiftsoglou, A. S., and Wong, W. (1985) Molecular and cellular mechanisms of leukemic hemopoietic cell differentiation: an analysis of the Friend system. Anticancer Res. 5, 81-99
56. Letting, D. L., Rakowski, C., Weiss, M. J., and Blobel, G. A. (2003) Formation of a tissue-specific histone acetylation pattern by the hematopoietic transcription factor GATA-1. Mol. Cell. Biol. 23, 1334-1340 (Pubitemid 36177041)
57. Nakatani, Y., and Ogryzko, V. (2003) Immunoaffinity purification of mammalian protein complexes. Methods Enzymol. 370, 430-444 (Pubitemid 37542800)
58. Humphrey, G. W., Wang, Y., Russanova, V. R., Hirai, T., Qin, J., Nakatani, Y., and Howard, B. H. (2001) Stable histone deacetylase complexes distinguished by the presence of SANT domain proteins CoREST/kiaa0071 and Mta-L1. J. Biol. Chem. 276, 6817-6824
59. Kobayashi, M., and Yamamoto, M. (2007) Regulation of GATA1 gene expression. J. Biochem. 142, 1-10 (Pubitemid 351455375)
60. Tsai, S. F., Strauss, E., and Orkin, S. H. (1991) Functional analysis and in vivo footprinting implicate the erythroid transcription factor GATA-1 as a positive regulator of its own promoter. Genes Dev. 5, 919-931 (Pubitemid 21906007)
61. Valverde-Garduno, V., Guyot, B., Anguita, E., Hamlett, I., Porcher, C., and Vyas, P. (2004) Differences in the chromatin structure and cis-element organization of the human and mouse GATA1 loci: implications for ciselement identification. Blood 104, 3106-3116 (Pubitemid 39507125)
62. Mahajan, M. C., Karmakar, S., and Weissman, S. M. (2007) Control of β-globin genes. J. Cell. Biochem. 102, 801-810
63. Kim, S. I., and Bresnick, E. H. (2007) Transcriptional control of erythropoiesis: emerging mechanisms and principles. Oncogene 26, 6777-6794
64. Grass, J. A., Jing, H., Kim, S. I., Martowicz, M. L., Pal, S., Blobel, G. A., and Bresnick, E. H. (2006) Distinct functions of dispersed GATA factor complexes at an endogenous gene locus. Mol. Cell. Biol. 26, 7056-7067 (Pubitemid 44477685)
65. Martowicz, M. L., Grass, J. A., Boyer, M. E., Guend, H., and Bresnick, E. H. (2005) Dynamic GATA factor interplay at a multicomponent regulatory region of the GATA-2 locus. J. Biol. Chem. 280, 1724-1732
66. Lee, H. Y., Johnson, K. D., Fujiwara, T., Boyer, M. E., Kim, S. I., and Bresnick, E. H. (2009) Controlling hematopoiesis through sumoylationdependent regulation of a GATA factor. Mol. Cell 36, 984-995
67. 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
68. Kransdorf, E. P., Wang, S. Z., Zhu, S. Z., Langston, T. B., Rupon, J. W., and Ginder, G. D. (2006) MBD2 is a critical component of a methyl cytosine-binding protein complex isolated from primary erythroid cells. Blood 108, 2836-2845
69. Kim, S. I., Bultman, S. J., Jing, H., Blobel, G. A., and Bresnick, E. H. (2007) Dissecting molecular steps in chromatin domain activation during hematopoietic differentiation. Mol. Cell. Biol. 27, 4551-4565 (Pubitemid 46906576)
70. Kim, S. I., Bultman, S. J., Kiefer, C. M., Dean, A., and Bresnick, E. H. (2009) BRG1 requirement for long-range interaction of a locus control region with a downstream promoter. Proc. Natl. Acad. Sci. U.S.A. 106, 2259-2264
71. Mahajan, M. C., Narlikar, G. J., Boyapaty, G., Kingston, R. E., and Weissman, S. M. (2005) Heterogeneous nuclear ribonucleoprotein C1/C2, MeCP1, and SWI/SNF form a chromatin remodeling complex at the β-globin locus control region. Proc. Natl. Acad. Sci. U.S.A. 102, 15012-15017 (Pubitemid 41513326)