Transcriptional repression of estrogen receptor α Signaling by SENP2 in breast cancer cells

Molecular Endocrinology

Volumn 28, Issue 2, 2014, Pages 183-196

  Achour, Thiziri Nait ^a,c   Sentis, Stéphanie ^a,b,c   Teyssier, Catherine ^a,c   Philippat, Amandine ^a,b,c   Lucas, Annick ^a,c   Corbo, Laura ^a,b,c   Cavaillès, Vincent ^a,c   Jalaguier, Stéphan ^a,c  

^a INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

^b UNIVERSITÉ LYON 1   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GLUTATHIONE TRANSFERASE; HISTONE DEACETYLASE 3; PROTEINASE; SENTRIN SPECIFIC PROTEASE 2; SMALL INTERFERING RNA; SUMO 1 PROTEIN; UNCLASSIFIED DRUG; CYSTEINE PROTEINASE; ESTROGEN RECEPTOR ALPHA, HUMAN; HISTONE DEACETYLASE; PROTEIN BINDING; SENP2 PROTEIN, HUMAN;

AMINO TERMINAL SEQUENCE; ARTICLE; BREAST CANCER; CELL PROLIFERATION; CELL STRAIN COS7; CELL STRAIN MCF 7; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENE REPRESSION; HINGE REGION; HUMAN; HUMAN CELL; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SUMOYLATION; TRANSACTIVATION; TRANSCRIPTION INITIATION; TRANSIENT TRANSFECTION; BREAST TUMOR; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC TRANSCRIPTION; MCF 7 CELL LINE; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

BREAST NEOPLASMS; CELL PROLIFERATION; CYSTEINE ENDOPEPTIDASES; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HISTONE DEACETYLASES; HUMANS; MCF-7 CELLS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TRANSCRIPTION, GENETIC;

EID: 84892531183     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2013-1376     Document Type: Article

References (42)

1. Acconcia F, Kumar R. Signaling regulation of genomic and nongenomic functions of estrogen receptors. Cancer Lett. 2006;238:1-14.
2. Pearce ST, Jordan VC. The biological role of estrogen receptors α and β in cancer. Crit Rev Oncol Hematol. 2004;50:3-22.
3. Gronemeyer H, Gustafsson JA, Laudet V. Principles for modulation of the nuclear receptor superfamily. Nat Rev Drug Discov. 2004; 3:950-964.
4. Chen GG, Zeng Q, Tse GM. Estrogen and its receptors in cancer. Med Res Rev. 2008;28:954-974.
5. Carroll JS, Brown M. Estrogen receptor target gene: an evolving concept. Mol Endocrinol. 2006;20:1707-1714.
6. Le Romancer M, Poulard C, Cohen P, Sentis S, Renoir J-M, Corbo L. Cracking the estrogen receptor's posttranslational code in breast tumors. Endocr Rev. 2006;32:597-622.
7. Sentis S, Le Romancer M, Bianchin C, Rostan MC, Corbo L. Sumoylation of the estrogen receptor α hinge region regulates its transcriptional activity. Mol Endocrinol. 2005;19:2671-2684.
8. Hay RT. SUMO: a history of modification. Mol Cell. 2005;18:1-12.
9. Yeh ET, Gong L, Kamitani T. Ubiquitin-like proteins: new wines in new bottles. Gene. 2000;248:1-14.
10. Mukhopadhyay D, Ayaydin F, Kolli N, et al. SUSP1 antagonizes formation of highly SUMO2/3-conjugated species. J Cell Biol. 2006;174:939-949.
11. Chiu SY, Asai N, Costantini F, Hsu W. SUMO-specific protease 2 is essential for modulating p53-Mdm2 in development of trophoblast stem cell niches and lineages. PLoS Biol. 2008;6:e310.
12. Cheng J, Kang X, Zhang S, Yeh ET. SUMO-specific protease 1 is essential for stabilization of HIF1α during hypoxia. Cell. 2007;131: 584-595.
13. Jacques C, Baris O, Prunier-Mirebeau D, et al. Two-step differential expression analysis reveals a new set of genes involved in thyroid oncocytic tumors. J Clin Endocrinol Metab. 2005;90:2314-2320.
14. Cheng J, Bawa T, Lee P, Gong L, Yeh ET. Role of desumoylation in the development of prostate cancer. Neoplasia. 2006;8:667-676.
15. Chung SS, Ahn BY, Kim M, et al. Control of adipogenesis by the SUMO-specific protease SENP2. Mol Cell Biol. 2010;30:2135-2146.
16. Kim EY, Chen L, Ma Y, et al. Enhanced desumoylation in murine hearts by overexpressed SENP2 leads to congenital heart defects and cardiac dysfunction. J Mol Cell Cardiol. 2012;52:638-649.
17. Kaikkonen S, Jaaskelainen T, Karvonen U, et al. SUMO-specific protease 1 (SENP1) reverses the hormone-augmented SUMOylation of androgen receptor and modulates gene responses in prostate cancer cells. Mol Endocrinol. 2009;23:292-307.
18. Abdel-Hafiz HA, Horwitz KB. Control of progesterone receptor transcriptional synergy by SUMOylation and deSUMOylation. BMC Mol Biol. 2012;13:10.
19. Cavailles V, Dauvois S, Danielian PS, Parker MG. Interaction of proteins with transcriptionally active estrogen receptors. Proc Natl Acad Sci USA. 1994;91:10009-10013.
20. Le Romancer M, Treilleux I, Leconte N, et al. Regulation of estrogen rapid signaling through arginine methylation by PRMT1. Mol Cell. 2008;31:212-221.
21. Duong V, Boulle N, Daujat S, et al. Differential regulation of estrogen receptor α turnover and transactivation by Mdm2 and stressinducing agents. Cancer Res. 2007;67:5513-5521.
22. Docquier A, Harmand P-O, Fritsch S, Chanrion M, Darbon J-M, Cavaillès V. The transcriptional coregulator RIP140 represses E2F1 activity and discriminates breast cancer subtypes. Clin Cancer Res. 2010;16:2959-2970.
23. Hang J, Dasso M. Association of the human SUMO-1 protease SENP2 with the nuclear pore. J Biol Chem. 2002;277:19961-19966.
24. Best JL, Ganiatsas S, Agarwal S, et al. SUMO-1 protease-1 regulates gene transcription through PML. Mol Cell. 2002;10:843-855.
25. Cheng J, Wang D, Wang Z, Yeh ET. SENP1 enhances androgen receptor-dependent transcription through desumoylation of histone deacetylase 1. Mol Cell Biol. 2004;24:6021-6028.
26. Shuai K, Liu B. Regulation of gene-activation pathways by PIAS proteins in the immune system. Nat Rev Immunol. 2005;5:593-605.
27. Gross M, Yang R, Top I, Gasper C, Shuai K. PIASy-mediated repression of the androgen receptor is independent of sumoylation. Oncogene. 2004;23:3059-3066.
28. Schulz S, Chachami G, Kozaczkiewicz L, et al. Ubiquitin-specific protease-like 1 (USPL1) is a SUMO isopeptidase with essential, non-catalytic functions. EMBO Rep. 2012;13:930-938.
29. Liu X-F, Bagchi MK. Recruitment of distinct chromatin-modifying complexes by tamoxifen-complexed estrogen receptor at natural target gene promoters in vivo. J Biol Chem. 2004;279:15050-15058.
30. Suzuki A, Sanda N, Miyawaki Y, et al. Down-regulation of PROS1 gene expression by 17β-estradiol via estrogen receptor α (ERα)-Sp1 interaction recruiting receptor-interacting protein 140 and the corepressor-HDAC3 complex. J Biol Chem. 2010;285:13444-13453.
31. Guenther MG, Yu J, Kao GD, Yen TJ, Lazar MA. Assembly of the SMRT-histone deacetylase 3 repression complex requires the TCP-1 ring complex. Genes Dev. 2002;16:3130-3135.
32. Zhang J, Kalkum M, Chait BT, Roeder RG. The N-CoR-HDAC3 nuclear receptor corepressor complex inhibits the JNK pathway through the integral subunit GPS2. Mol Cell. 2002;9:611-623.
33. Gobinet J, Carascossa S, Cavaillès V, Vignon F, Nicolas JC, Jalaguier S. SHP represses transcriptional activity via recruitment of histone deacetylases. Biochemistry. 2005;44:6312-6320.
34. Park SW, Huang WH, Persaud SD, Wei LN. RIP140 in thyroid hormone-repression and chromatin remodeling of Crabp1 gene during adipocyte differentiation. Nucleic Acids Res. 2009;37: 7085-7094.
35. Hentschke M, Susens U, Borgmeyer U. Transcriptional ERRγ2-mediated activation is regulated by sentrin-specific proteases. Biochem J. 2009;419:167-176.
36. Gross M, Liu B, Tan J, French FS, Carey M, Shuai K. Distinct effects of PIAS proteins on androgen-mediated gene activation in prostate cancer cells. Oncogene. 2001;20:3880-3887.
37. Bawa-Khalfe T, Cheng J, Lin S-H, Ittmann MM, Yeh ETH. SENP1 induces prostatic intraepithelial neoplasia through multiple mechanisms. J Biol Chem. 2010;285:25859-25866.
38. Bawa-Khalfe T, Cheng J, Wang Z, Yeh ET. Induction of the SUMO-specific protease 1 transcription by the androgen receptor in prostate cancer cells. J Biol Chem. 2007;282:37341-37349.
39. Wang Q, Xia N, Li T, et al. SUMO-specific protease 1 promotes prostate cancer progression and metastasis. Oncogene. 2013;32(19):2493-2498.
40. Wang Q, Xia N, Li T, et al. SUMO-specific protease 1 promotes prostate cancer progression and metastasis. Oncogene. 2013;32: 2493-2498.
41. Han Y, Huang C, Sun X, et al. SENP3-mediated de-conjugation of SUMO2/3 from promyelocytic leukemia is correlated with accelerated cell proliferation under mild oxidative stress. J Biol Chem. 2010;285:12906-12915.
42. Mooney SM, Grande JP, Salisbury JL, Janknecht R. Sumoylation of p68 and p72 RNA helicases affects protein stability and transactivation potential. Biochemistry. 2010;49:1-10.