The histone demethylase JARID1A regulates progesterone receptor expression

FEBS Journal

Volumn 278, Issue 9, 2011, Pages 1458-1469

  Stratmann, Antje ^a,b   Haendler, Bernard ^a  

^a BAYER PHARMA AG   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

ChIP; estrogen; histone demethylation; JARID1; progesterone receptor

Indexed keywords

ENZYME; ESTROGEN; ESTROGEN RECEPTOR ALPHA; HISTONE; HISTONE DEMETHYLASE; MUTANT PROTEIN; PROGESTERONE RECEPTOR; RETINOBLASTOMA BINDING PROTEIN 2; RNA POLYMERASE II;

ARTICLE; CELL STRAIN MCF 7; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA MODIFICATION; ENHANCER REGION; ESTROGEN RESPONSIVE ELEMENT; GENE CONSTRUCT; GENE EXPRESSION; GENE OVEREXPRESSION; GENE REPRESSION; HUMAN; HUMAN CELL; LIGAND BINDING; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RECEPTOR BINDING; RECEPTOR GENE; REPORTER GENE; TRANSCRIPTION REGULATION;

CELL LINE, TUMOR; DNA METHYLATION; HUMANS; PROMOTER REGIONS, GENETIC; RECEPTORS, PROGESTERONE; RETINOBLASTOMA-BINDING PROTEIN 2;

EID: 79955050920     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08058.x     Document Type: Article

References (54)

1. Ismail PM, Amato P, Soyal SM, DeMayo FJ, Conneely OM, O'Malley BW, &, Lydon JP, (2003) Progesterone involvement in breast development and tumorigenesis-as revealed by progesterone receptor 'knockout' and 'knockin' mouse models. Steroids 68, 779-787. (Pubitemid 37532400)
2. Gadkar-Sable S, Shah C, Rosario G, Sachdeva G, &, Puri C, (2005) Progesterone receptors: various forms and functions in reproductive tissues. Front Biosci 10, 2118-2130. (Pubitemid 40905287)
3. Kastner P, Krust A, Turcotte B, Stropp U, Tora L, Gronemeyer H, &, Chambon P, (1990) Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 9, 1603-1614.
4. Graham JD, Roman SD, McGowan E, Sutherland RL, &, Clarke CL, (1995) Preferential stimulation of human progesterone receptor B expression by estrogen in T-47D human breast cancer cells. J Biol Chem 270, 30693-30700. (Pubitemid 26005135)
5. Flototto T, Niederacher D, Hohmann D, Heimerzheim T, Dall P, Djahansouzi S, Bender HG, &, Hanstein B, (2004) Molecular mechanism of estrogen receptor (ER)alpha-specific, estradiol-dependent expression of the progesterone receptor (PR) B-isoform. J Steroid Biochem Mol Biol 88, 131-142. (Pubitemid 38488853)
6. Petz LN, Ziegler YS, Schultz JR, Kim H, Kemper JK, &, Nardulli AM, (2004) Differential regulation of the human progesterone receptor gene through an estrogen response element half site and Sp1 sites. J Steroid Biochem Mol Biol 88, 113-122. (Pubitemid 38482029)
7. Petz LN, Ziegler YS, Loven MA, &, Nardulli AM, (2002) Estrogen receptor alpha and activating protein-1 mediate estrogen responsiveness of the progesterone receptor gene in MCF-7 breast cancer cells. Endocrinology 143, 4583-4591. (Pubitemid 35397599)
8. Daniel AR, Knutson TP, &, Lange CA, (2009) Signaling inputs to progesterone receptor gene regulation and promoter selectivity. Mol Cell Endocrinol 308, 47-52.
9. Conneely OM, Mulac-Jericevic B, &, Arnett-Mansfield R, (2007) Progesterone signaling in mammary gland development. Ernst Schering Found Symp Proc 2007/1, 45-54.
10. Lange CA, Sartorius CA, Abdel-Hafiz H, Spillman MA, Horwitz KB, &, Jacobsen BM, (2008) Progesterone receptor action: translating studies in breast cancer models to clinical insights. Adv Exp Med Biol 630, 94-111.
11. Mote PA, Bartow S, Tran N, &, Clarke CL, (2002) Loss of co-ordinate expression of progesterone receptors A and B is an early event in breast carcinogenesis. Breast Cancer Res Treat 72, 163-172. (Pubitemid 34407211)
12. Klinge CM, Jernigan SC, Mattingly KA, Risinger KE, &, Zhang J, (2004) Estrogen response element-dependent regulation of transcriptional activation of estrogen receptors alpha and beta by coactivators and corepressors. J Mol Endocrinol 33, 387-410. (Pubitemid 39429565)
13. Kim H, Heo K, Kim JH, Kim K, Choi J, &, An W, (2009) Requirement of histone methyltransferase SMYD3 for estrogen receptor-mediated transcription. J Biol Chem 284, 19867-19877.
14. Hamamoto R, Silva FP, Tsuge M, Nishidate T, Katagiri T, Nakamura Y, &, Furukawa Y, (2006) Enhanced SMYD3 expression is essential for the growth of breast cancer cells. Cancer Sci 97, 113-118. (Pubitemid 43379478)
15. Mo R, Rao SM, &, Zhu YJ, (2006) Identification of the MLL2 complex as a coactivator for estrogen receptor alpha. J Biol Chem 281, 15714-15720. (Pubitemid 43848459)
16. Lee DY, Northrop JP, Kuo MH, &, Stallcup MR, (2006) Histone H3 lysine 9 methyltransferase G9a is a transcriptional coactivator for nuclear receptors. J Biol Chem 281, 8476-8485. (Pubitemid 43847950)
17. Carling T, Kim KC, Yang XH, Gu J, Zhang XK, &, Huang S, (2004) A histone methyltransferase is required for maximal response to female sex hormones. Mol Cell Biol 24, 7032-7042. (Pubitemid 39014431)
18. Shi B, Liang J, Yang X, Wang Y, Zhao Y, Wu H, Sun L, Zhang Y, Chen Y, Li R, et al. (2007) Integration of estrogen and Wnt signaling circuits by the polycomb group protein EZH2 in breast cancer cells. Mol Cell Biol 27, 5105-5119. (Pubitemid 47068285)
19. Huang N, vom Baur E, Garnier JM, Lerouge T, Vonesch JL, Lutz Y, Chambon P, &, Losson R, (1998) Two distinct nuclear receptor interaction domains in NSD1, a novel SET protein that exhibits characteristics of both corepressors and coactivators. EMBO J 17, 3398-3412. (Pubitemid 28279513)
20. Garcia-Bassets I, Kwon YS, Telese F, Prefontaine GG, Hutt KR, Cheng CS, Ju BG, Ohgi KA, Wang J, Escoubet-Lozach L, et al. (2007) Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell 128, 505-518. (Pubitemid 46198894)
21. Benevolenskaya EV, (2007) Histone H3K4 demethylases are essential in development and differentiation. Biochem Cell Biol 85, 435-443. (Pubitemid 47518039)
22. Klose RJ, &, Zhang Y, (2007) Regulation of histone methylation by demethylimination and demethylation. Nat Rev Mol Cell Biol 8, 307-318. (Pubitemid 46474659)
23. Fattaey AR, Helin K, Dembski MS, Dyson N, Harlow E, Vuocolo GA, Hanobik MG, Haskell KM, Oliff A, Defeo-Jones D, et al. (1993) Characterization of the retinoblastoma binding proteins RBP1 and RBP2. Oncogene 8, 3149-3156. (Pubitemid 23312922)
24. Klose RJ, Yan Q, Tothova Z, Yamane K, Erdjument-Bromage H, Tempst P, Gilliland DG, Zhang Y, &, Kaelin WG Jr, (2007) The retinoblastoma binding protein RBP2 is an H3K4 demethylase. Cell 128, 889-900. (Pubitemid 46341416)
25. Christensen J, Agger K, Cloos PA, Pasini D, Rose S, Sennels L, Rappsilber J, Hansen KH, Salcini AE, &, Helin K, (2007) RBP2 belongs to a family of demethylases, specific for tri- and dimethylated lysine 4 on histone 3. Cell 128, 1063-1076. (Pubitemid 46427869)
26. Tu S, Teng YC, Yuan C, Wu YT, Chan MY, Cheng AN, Lin PH, Juan LJ, &, Tsai MD, (2008) The ARID domain of the H3K4 demethylase RBP2 binds to a DNA CCGCCC motif. Nat Struct Mol Biol 15, 419-421. (Pubitemid 351483392)
27. Lopez-Bigas N, Kisiel TA, Dewaal DC, Holmes KB, Volkert TL, Gupta S, Love J, Murray HL, Young RA, &, Benevolenskaya EV, (2008) Genome-wide analysis of the H3K4 histone demethylase RBP2 reveals a transcriptional program controlling differentiation. Mol Cell 31, 520-530.
28. Sharma SV, Lee DY, Li B, Quinlan MP, Takahashi F, Maheswaran S, McDermott U, Azizian N, Zou L, Fischbach MA, et al. (2010) A chromatin-mediated reversible drug-tolerant state in cancer cell subpopulations. Cell 141, 69-80.
29. Lu PJ, Sundquist K, Baeckstrom D, Poulsom R, Hanby A, Meier-Ewert S, Jones T, Mitchell M, Pitha-Rowe P, Freemont P, et al. (1999) A novel gene (PLU-1) containing highly conserved putative DNA/chromatin binding motifs is specifically up-regulated in breast cancer. J Biol Chem 274, 15633-15645.
30. Xiang Y, Zhu Z, Han G, Ye X, Xu B, Peng Z, Ma Y, Yu Y, Lin H, Chen AP, et al. (2007) JARID1B is a histone H3 lysine 4 demethylase up-regulated in prostate cancer. Proc Natl Acad Sci USA 104, 19226-19231.
31. Scibetta AG, Santangelo S, Coleman J, Hall D, Chaplin T, Copier J, Catchpole S, Burchell J, &, Taylor-Papadimitriou J, (2007) Functional analysis of the transcription repressor PLU-1/JARID1B. Mol Cell Biol 27, 7220-7235. (Pubitemid 47549757)
32. Tahiliani M, Mei P, Fang R, Leonor T, Rutenberg M, Shimizu F, Li J, Rao A, &, Shi Y, (2007) The histone H3K4 demethylase SMCX links REST target genes to X-linked mental retardation. Nature 447, 601-605. (Pubitemid 46868038)
33. Akimoto C, Kitagawa H, Matsumoto T, &, Kato S, (2008) Spermatogenesis-specific association of SMCY and MSH5. Genes Cells 13, 623-633. (Pubitemid 351761778)
34. Fritah A, Saucier C, Mester J, Redeuilh G, &, Sabbah M, (2005) p21WAF1/CIP1 selectively controls the transcriptional activity of estrogen receptor alpha. Mol Cell Biol 25, 2419-2430. (Pubitemid 40354635)
35. Yamane K, Tateishi K, Klose RJ, Fang J, Fabrizio LA, Erdjument-Bromage H, Taylor-Papadimitriou J, Tempst P, &, Zhang Y, (2007) PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol Cell 25, 801-812. (Pubitemid 46436533)
36. Welboren WJ, Sweep FC, Span PN, &, Stunnenberg HG, (2009) Genomic actions of estrogen receptor alpha: what are the targets and how are they regulated? Endocr Relat Cancer 16, 1073-1089.
37. Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH, et al. (2009) An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 462, 58-64.
38. Kwon YS, Garcia-Bassets I, Hutt KR, Cheng CS, Jin M, Liu D, Benner C, Wang D, Ye Z, Bibikova M, et al. (2007) Sensitive ChIP-DSL technology reveals an extensive estrogen receptor alpha-binding program on human gene promoters. Proc Natl Acad Sci USA 104, 4852-4857. (Pubitemid 47186140)
39. Lin CY, Vega VB, Thomsen JS, Zhang T, Kong SL, Xie M, Chiu KP, Lipovich L, Barnett DH, Stossi F, et al. (2007) Whole-genome cartography of estrogen receptor alpha binding sites. PLoS Genet 3, e87.
40. Vega VB, Lin CY, Lai KS, Kong SL, Xie M, Su X, Teh HF, Thomsen JS, Yeo AL, Sung WK, et al. (2006) Multiplatform genome-wide identification and modeling of functional human estrogen receptor binding sites. Genome Biol 7, R82.
41. Kraus WL, Montano MM, &, Katzenellenbogen BS, (1994) Identification of multiple, widely spaced estrogen-responsive regions in the rat progesterone receptor gene. Mol Endocrinol 8, 952-969. (Pubitemid 24254004)
42. Carroll JS, Meyer CA, Song J, Li W, Geistlinger TR, Eeckhoute J, Brodsky AS, Keeton EK, Fertuck KC, Hall GF, et al. (2006) Genome-wide analysis of estrogen receptor binding sites. Nat Genet 38, 1289-1297. (Pubitemid 44646291)
43. Petz LN, &, Nardulli AM, (2000) Sp1 binding sites and an estrogen response element half-site are involved in regulation of the human progesterone receptor A promoter. Mol Endocrinol 14, 972-985. (Pubitemid 32250515)
44. Ferguson AT, Lapidus RG, &, Davidson NE, (1998) Demethylation of the progesterone receptor CpG island is not required for progesterone receptor gene expression. Oncogene 17, 577-583. (Pubitemid 28401026)
45. Sims RJ III, Millhouse S, Chen CF, Lewis BA, Erdjument-Bromage H, Tempst P, Manley JL, &, Reinberg D, (2007) Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell 28, 665-676. (Pubitemid 350137805)
46. Hublitz P, Albert M, &, Peters AH, (2009) Mechanisms of transcriptional repression by histone lysine methylation. Int J Dev Biol 53, 335-354.
47. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108-112.
48. Boney-Montoya J, Ziegler YS, Curtis CD, Montoya JA, &, Nardulli AM, (2010) Long-range transcriptional control of progesterone receptor gene expression. Mol Endocrinol, 24, 346-358.
49. Patsialou A, Wilsker D, &, Moran E, (2005) DNA-binding properties of ARID family proteins. Nucleic Acids Res 33, 66-80. (Pubitemid 40276929)
50. Pan YF, Wansa KD, Liu MH, Zhao B, Hong SZ, Tan PY, Lim KS, Bourque G, Liu ET, &, Cheung E, (2008) Regulation of estrogen receptor-mediated long range transcription via evolutionarily conserved distal response elements. J Biol Chem 283, 32977-32988.
51. Parisi F, Sonderegger B, Wirapati P, Delorenzi M, &, Naef F, (2009) Relationship between estrogen receptor alpha location and gene induction reveals the importance of downstream sites and cofactors. BMC Genomics 10, 381.
52. Okitsu CY, &, Hsieh CL, (2007) DNA methylation dictates histone H3K4 methylation. Mol Cell Biol 27, 2746-2757. (Pubitemid 46581362)
53. Otani J, Nankumo T, Arita K, Inamoto S, Ariyoshi M, &, Shirakawa M, (2009) Structural basis for recognition of H3K4 methylation status by the DNA methyltransferase 3A ATRX-DNMT3-DNMT3L domain. EMBO Rep 10, 1235-1241.
54. Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, Chang HY, Simon MD, Kutateladze TG, &, Gozani O, (2009) ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Mol Cell 33, 248-256.