Disruption of histone modification and CARM1 recruitment by arsenic represses transcription at glucocorticoid receptor-regulated promoters

PLoS ONE

Volumn 4, Issue 8, 2009, Pages

  Barr, Fiona D ^a   Krohmer, Lori J ^a,b   Hamilton, Joshua W ^a,c   Sheldon, Lynn A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b Marine Biological Laboratory ^*

^c MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARSENIC; COACTIVATOR ASSOCIATED ARGININE METHYLTRANSFERASE 1; GLUCOCORTICOID RECEPTOR; HISTONE ACETYLTRANSFERASE PCAF; HISTONE H3; HISTONE H4; PROTEIN METHYLTRANSFERASE; PROTEIN P160; UNCLASSIFIED DRUG; CHLORAMPHENICOL ACETYLTRANSFERASE; COACTIVATOR-ASSOCIATED ARGININE METHYLTRANSFERASE 1; HISTONE; PROTEIN ARGININE METHYLTRANSFERASE;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA MODIFICATION; GENE DISRUPTION; GENE INTERACTION; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC REGULATION; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PROMOTER REGION; ANIMAL; DRUG EFFECT; GEL MOBILITY SHIFT ASSAY; GENETICS; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

MOUSE MAMMARY TUMOR VIRUS;

ANIMALS; ARSENIC; CELL LINE, TUMOR; CHLORAMPHENICOL O-ACETYLTRANSFERASE; CHROMATIN IMMUNOPRECIPITATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HISTONES; MICE; POLYMERASE CHAIN REACTION; PROMOTER REGIONS, GENETIC; PROTEIN-ARGININE N-METHYLTRANSFERASES; RECEPTORS, GLUCOCORTICOID; TRANSCRIPTION, GENETIC;

EID: 69849115076     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006766     Document Type: Article

References (74)

1. Smith AH, Lopipero PA, Bates MN, Steinmaus CM (2002) Public health. Arsenic epidemiology and drinking water standards. Science 296: 2145-2146.
2. NRC (2001) Arsenic in Drinking Water-2001 Update. Washington, DC: National Academies Press.
3. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, et al. (2007) Estrogen receptors: how do they signal and what are their targets. Physiological reviews 87: 905-931.
4. Vegiopoulos A, Herzig S (2007) Glucocorticoids, metabolism and metabolic diseases. Mol Cell Endocrinol 275: 43-61.
5. Jacobsen BM, Schittone SA, Richer JK, Horwitz KB (2005) Progesterone-independent effects of human progesterone receptors (PRs) in estrogen receptor-positive breast cancer: PR isoform-specific gene regulation and tumor biology. Mol Endocrinol 19: 574-587.
6. Balk SP, Knudsen KE (2008) AR, the cell cycle, and prostate cancer. Nuclear receptor signaling 6: e001.
7. Kaltreider RC, Davis AM, Lariviere JP, Hamilton JW (2001) Arsenic alters the function of the glucocorticoid receptor as a transcription factor. Environ Health Perspect 109: 245-251.
8. Davey JC, Bodwell JE, Gosse JA, Hamilton JW (2007) Arsenic as an endocrine disruptor: effects of arsenic on estrogen receptor-mediated gene expression in vivo and in cell culture. Toxicol Sci 98: 75-86.
9. Bodwell JE, Kingsley LA, Hamilton JW (2004) Arsenic at very low concentrations alters glucocorticoid receptor (GR)-mediated gene activation but not GR-mediated gene repression: complex dose-response effects are closely correlated with levels of activated GR and require a functional GR DNA binding domain. Chemical research in toxicology 17: 1064-1076.
10. Davey JC, Nomikos AP, Wungjiranirun M, Sherman JR, Ingram L, et al. (2008) Arsenic as an endocrine disruptor: arsenic disrupts retinoic acid receptor-and thyroid hormone receptor-mediated gene regulation and thyroid hormone-mediated amphibian tail metamorphosis. Environ Health Perspect 116: 165-172.
11. Tsai M-J, O'Malley BW (1994) Molecular Mechanisms of Action of Steroid/ Thyroid Receptor Superfamily Members. Ann Rev Biochem 63: 451-486.
12. Aoyagi S, Archer TK (2008) Dynamics of coactivator recruitment and chromatin modifications during nuclear receptor mediated transcription. Mol Cell Endocrinol 280: 1-5.
13. Li J, Gorospe M, Barnes J, Liu Y (2003) Tumor promoter arsenite stimulates histone H3 phosphoacetylation of proto-oncogenes c-fos and c-jun Chromatin in huiman diploid fibroblasts. J Biol Chem 278: 13183-13191.
14. Zhou X, Sun H, Ellen TP, Chen H, Costa M (2008) Arsenite alters global histone H3 methylation. Carcinogenesis.
15. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45.
16. Lonard DM, O'Malley B W (2007) Nuclear receptor coregulators: judges, juries, and executioners of cellular regulation. Mol Cell 27: 691-700.
17. Schurter BT, Koh SP, Chen D, Bunick gJ, Harp JM, et al. (2001) Methylation of Histone H3 by coactivator-associated arginine methyltransferase 1. Biochem 40: 5747-5756.
18. Kouzarides T (2007) Chromatin modifications and their function. Cell 128: 693-705.
19. Daujat S, Bauer U-M, Shah V, Turner BM, Berger SL, et al. (2002) Crosstalk between CARM1 Methylation and CBP Acetylation on Histone H3. Curr Biology 12: 2090-2097.
20. Ma H, Baumann CT, Li H, Strahl BD, Rice R, et al. (2001) Hormone-dependent, CARM1-directed, arginine-specific methylation of histone H3 on a steroid-regulated promoter. Curr Biol 11: 1981-1985.
21. Chen D, Huang SM, Stallcup MR (2000) Synergistic, p160 coactivator-dependent enhancement of estrogen receptor function by CARM1 and p300. J Biol Chem 275: 40810-40816.
22. Richard-Foy H, Hager G (1987) Sequence-specific positioning of nucleosomes over the steroid-inducible MMTV promoter. EMBO 6: 2321-2328.
23. Fragoso G, Pennie WD, John S, Hager GL (1998) The Position and Length of the Steroid-Dependent Hypersensitive Region in the Mouse Mammary Tumor Virus Long Terminal Repeat Are Invariant Despite Multiple Nucleosome B Frames. Mol Cell Biol 18: 3633-3644.
24. Picard D, Yamamoto K (1987) Two signals mediate hormone-dependent nuclear localization of the glucocorticoid receptor. EMBO J 6: 3333-3340.
25. Evans RM (1988) The Steroid and Thyroid Hormone Receptor Superfamily. Science 240: 889-895.
26. Sheldon LA, Becker M, Smith CL (2001) Steroid Hormone Receptor-mediated histone deacetylation and transcription at the mouse mammary tumor virus promoter. Jour Biol Chem 276: 32423-32426.
27. Li X, Wong J, Sophia TY, Tsai M-J, O'Malley BW (2003) Progesterone and glucocorticoid receptors recruit distinct coactivator complexes and promote distinct patterns of local chromatin modification. Mol Cell Biol 23: 3763-3773.
28. Aoyagi S, Archer TK (2007) Dynamic histone acetylation/deacetylation with progesterone receptor-mediated transcription. Mol Endocrinol 21: 843-856.
29. Metivier R, Penot G, Hubner MR, Reid G, Brand H, et al. (2003) Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115: 751-763.
30. Lambert JR, Nordeen SK (2003) CBP Recruitment and histone acetylation in differential gene induction by glucocorticoids and progestins. Mol Endocrinology 17: 1085-1094.
31. Chen H, JLR, Xie W, Wilpitz D, Evans RM (1999) Regulation of Hormone-Induced histone Hyperacetylation and Gene activation via Acetylation of an Acetylase. Cell 98: 675-686.
32. Rosenfeld MG, Lunyak VV, Glass CK (2006) Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev 20: 1405-1428.
33. Chen D, Ma H, Hong H, Koh SS, Huang S-M, et al. (1999) Regulation of Transcription by a Protein Methyltransferase. Science 284: 2174-2177.
34. Fletcher TM, Xiao N, Mautino G, Baumann CT, Wolford R, et al. (2002) ATP-dependent mobilization of the glucocorticoid receptor during chromatin remodeling. Mol Cell Biol 22: 3255-3263.
35. Johnson TA, Elbi C, Parekh BS, Hager GL, John S (2008) Chromatin remodeling complexes interact dynamically with a glucocorticoid receptor-regulated promoter. Molecular biology of the cell 19: 3308-3322.
36. Fryer CJ, Archer T, K (1998) Chromatin remodelling by the glucocorticoid receptor requires the BRG1 complex. Nature 393: 88-91.
37. DiRenzo J, Shang Y, Phelan M, Sif S, Meyers M, et al. (2000) BRG-1 is recruited to estrogen-responsive promoters and cooperates with factors involved in histone acetylation. Mol Cell Biol 20: 7541-7549.
38. Xu W, Cho H, Kadam S, Banayo EM, Anderson S, et al. (2004) A methylation-mediator complex in hormone signaling. Genes Dev 18: 144-156.
39. Dacwag CS, Bedford MT, Sif S, Imbalzano AN (2009) Distinct protein arginine methyltransferases promote ATP-dependent chromatin remodeling function at different stages of skeletal muscle differentiation. Mol Cell Biol.
40. Wu RC, Feng Q, Lonard DM, O'Malley BW (2007) SRC-3 coactivator functional lifetime is regulated by a phospho-dependent ubiquitin time clock. Cell 129: 1125-1140.
41. Yi P, Feng Q, Amazit L, Lonard DM, Tsai SY, et al. (2008) Atypical protein kinase C regulates dual pathways for degradation of the oncogenic coactivator SRC-3/AIB1. Mol Cell 29: 465-476.
42. Baumann CT, Ma H, Wolford R, Reyes JC, Maruvada P, et al. (2001) The glucocorticoid receptor interacting protein 1 (GRIP1) localizes in discrete nuclear foci that associate with ND10 bodies and are enriched in components of the 26S proteasome. Mol Endocrinol 15: 485-500.
43. Lonard DM, Nawaz Z, Smith CL, O'Malley BW (2000) The 26S proteasome is required for estrogen receptor-alpha and coactivator turnover and for efficient estrogen receptor-alpha transactivation. Mol Cell 5: 939-948.
44. Hong H, Kohli K, Trivedi A, Johnson DL, Stallcup MR (1996) GRIP-1, a novel mouse protein that serves as a transcriptional coactivator in yeast for the hormone binding domains of steroid receptors. Proc Natl Acad Sci USA 93: 4948-4952.
45. Teyssier C, Chen D, Stallcup MR (2002) Requirement for multiple domains of the protein arginine methyltransferase CARM1 in its transcriptional coactivator function. J Biol Chem 277: 46066-46072.
46. Naeem H, Cheng D, Zhao Q, Underhill C, Tini M, et al. (2007) The activity and stability of the transcriptional coactivator p/CIP/SRC-3 are regulated by CARM1-dependent methylation. Mol Cell Biol 27: 120-134.
47. Feng Q, Yi P, Wong J, O'Malley BW (2006) Signaling within a coactivator complex: methylation of SRC-3/AIB1 is a molecular switch for complex disassembly. Mol Cell Biol 26: 7846-7857.
48. Oh AS, Lahusen JT, Chien CD, Fereshteh MP, Zhang X, et al. (2008) Tyrosine phosphorylation of the nuclear receptor coactivator AIB1/SRC-3 is enhanced by Abl kinase and is required for its activity in cancer cells. Mol Cell Biol 28: 6580-6593.
49. Frigo DE, Basu A, Nierth-Simpson EN, Weldon CB, Dugan CM, et al. (2006) p38 mitogen-activated protein kinase stimulates estrogen-mediated transcription and proliferation through the phosphorylation and potentiation of the p160 coactivator glucocorticoid receptor-interacting protein 1. Mol Endocrinol 20: 971-983.
50. Verma A, Mohindru M, Deb DK, Sassano A, Kambhampati S, et al. (2002) Activation of Rac1 and the p38 mitogen-activated protein kinase pathway in response to arsenic trioxide. J Biol Chem 277: 44988-44995.
51. Bode AM, Dong Z (2005) Signal transduction pathways in cancer development and as targets for cancer prevention. Progress in nucleic acid research and molecular biology 79: 237-297.
52. Kannan-Thulasiraman P, Katsoulidis E, Tallman MS, Arthur JS, Platanias LC (2006) Activation of the mitogen- and stress-activated kinase 1 by arsenic trioxide. J Biol Chem 281: 22446-22452.
53. Higashimoto K, Kuhn P, Desai D, Cheng X, Xu W (2007) Phosphorylation-mediated inactivation of coactivator-associated arginine methyltransferase 1. Proc Natl Acad Sci U S A 104: 12318-12323.
54. Li S, Shang Y (2007) Regulation of SRC family coactivators by post-translational modifications. Cellular signalling 19: 1101-1112.
55. Teyssier C, Ou CY, Khetchoumian K, Losson R, Stallcup MR (2006) Transcriptional intermediary factor 1alpha mediates physical interaction and functional synergy between the coactivator-associated arginine methyltransferase 1 and glucocorticoid receptor-interacting protein 1 nuclear receptor coactivators. Mol Endocrinol 20: 1276-1286.
56. Vo N, Goodman RH (2001) CREB-binding protein and p300 in transcriptional regulation. J Biol Chem 276: 13505-13508.
57. Chen H, Ke Q, Kluz T, Yan Y, Costa M (2006) Nickel ions increase histone H3 lysine 9 dimethylation and induce transgene silencing. Mol Cell Biol 26: 3728-3737.
58. Schnekenburger M, Talaska G, Puga A (2007) Chromium cross-links HDAC1·DNMT1 complexes to chromatin inhibiting histone remodeling marks critical for transcriptional activation. Mol Cell Biol.
59. Golebiowski F, Kasprzak KS (2005) Inhibition of core histones acetylation by carcinogenic nickel(II). Mol Cell Biochem 279: 133-139.
60. Georgel PT, Fletcher TM, Hager GL, Hansen JC (2003) Formation of higher-order secondary and tertiary chromatin structures by genomic mouse mammary tumor virus promoters. Genes Dev 17: 1617-1629.
61. Bodwell JE, Holbrook NJ, Munck A (1984) Evidence for distinct sulfhydryl groups associated with steroid- and DNA-binding domains of rat thymus glucocorticoid receptors. Biochemistry 23: 4237-4242.
62. Simons SS Jr, Chakraborti PK, Cavanaugh AH (1990) Arsenite and cadmium(II) as probes of glucocorticoid receptor structure and function. J Biol Chem 265: 1938-1945.
63. Rosenblatt AE, Burnstein KL (2009) Inhibition of Androgen Receptor Transcriptional Activity as a Novel Mechanism of Action of Arsenic. Mol Endocrinol.
64. An W, Kim J, Roeder RG (2004) Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117: 735-748.
65. Nasr R, Guillemin MC, Ferhi O, Soilihi H, Peres L, et al. (2008) Eradication of acute promyelocytic leukemia-initiating cells through PML-RARA degradation. Nature medicine 14: 1333-1342.
66. Hong SH, Yang Z, Privalsky ML (2001) Arsenic trioxide is a potent inhibitor of the interaction of SMRT corepressor with Its transcription factor partners, including the PML-retinoic acid receptor alpha oncoprotein found in human acute promyelocytic leukemia. Mol Cell Biol 21: 7172-7182.
67. Li C, Wu RC, Amazit L, Tsai SY, Tsai MJ, et al. (2007) Specific amino acid residues in the basic helix-loop-helix domain of SRC-3 are essential for its nuclear localization and proteasome-dependent turnover. Mol Cell Biol 27: 1296-1308.
68. Anzick SL, Kononen J, Walker RL, Azorsa DO, Tanner MM, et al. (1997) AIB1, a Steroid Receptor Coactivator amplified in Breast and Ovarian Cancer. Science 277: 965-968.
69. Charron J, Richard-Foy H, Berard DS, Hager GL, Drouin J (1989) Independent Glucocorticoid Induction and Repression of Two Contiguous Responsive Genes. Molec Cell Biol 9: 3127-3131.
70. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
71. Lee KA, Bindereif A, Green MR (1988) A small-scale procedure for preparation of nuclear extracts that support efficicient transcription and pre-mRNA splicing. Gene Anal Techn 5: 22-31.
72. Fletcher TM, Ryu B-W, Baumann CT, Warren BS, Fragoso G, et al. (2000) Structure and Dynamic Properties of a Glucocorticoid Receptor-Induced Chromatin Transition. Mol Cell Biol 20: 6466-6475.
73. Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, et al. (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370: 223-226.
74. Impey S, Fong AL, Wang Y, Cardinaux JR, Fass DM, et al. (2002) Phosphorylation of CBP mediates transcriptional activation by neural activity and CaM kinase IV. Neuron 34: 235-244.