Differential regulation of estrogen receptor α turnover and transactivation by Mdm2 and stress-inducing agents

Cancer Research

Volumn 67, Issue 11, 2007, Pages 5513-5521

  Duong, Vanessa ^a,b   Boulle, Nathalie ^a,b   Daujat, Sylvain ^c,d   Chauvet, Jérôme ^a,b   Bonnet, Sandrine ^a,b   Neel, Henry ^c   Cavaillès, Vincent ^a,b  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

^c INSTITUT DE GÉNÉTIQUE MOLÉCULAIRE DE MONTPELLIER   (France)

^d MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; PROTEASOME; PROTEIN MDM2; PROTEIN P53; UBIQUITIN PROTEIN LIGASE;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL STRAIN MCF 7; CONTROLLED STUDY; DATA ANALYSIS; ENZYME ACTIVITY; ENZYME STABILITY; ESTROGEN RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INTERACTION; TRANSCRIPTION INITIATION; ULTRAVIOLET IRRADIATION; WESTERN BLOTTING;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; DNA-BINDING PROTEINS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; LEUPEPTINS; NEOPLASM PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TUMOR SUPPRESSOR PROTEIN P53; ULTRAVIOLET RAYS;

EID: 34347262483     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-0967     Document Type: Article

References (57)

1. Nilsson S, Makela S, Treuter E, et al. Mechanisms of estrogen action. Physiol Rev 2001;81:1535-65.
2. McKenna NJ, Xu J, Nawaz Z, et al. Nuclear receptor coactivators: multiple enzymes, multiple complexes, multiple functions. J Steroid Biochem Mol Biol 1999;69:3-12.
3. Nawaz Z, Lonard DM, Dennis AP, Smith CL, O'Malley BW. Proteasome-dependent degradation of the human estrogen receptor. Proc Natl Acad Sci U S A 1999;96:1858-62.
4. Perissi V, Aggar wal A, Glass CK, Rose DW, Rosenfeld MG. A corepressor/coactivator exchange complex required for transcriptional activation by nuclear receptors and other regulated transcription factors. Cell 2004;116:511-26.
5. Imhof MO, M cDonnell DP. Yeast RSP5 and its human homolog hRPF1 potentiate hormone-dependent activation of transcription by human progesterone and glucocorticoid receptors. Mol Cell Biol 1996;16:2594-605.
6. Nawaz Z, Lonard DM, Smith CL, et al. The Angelman syndrome-associated protein, E6-AP, is a coactivator for the nuclear hormone receptor superfamily. Mol Cell Biol 1999;19:1182-9.
7. Lee JW, Ryan F, Swaffield JC, Johnston SA, Moore DD. Interaction of thyroid-hormone receptor with a conserved transcriptional mediator. Nature 1995;374:91-4.
8. Ishizuka T, Satoh T, Monden T, et al. Human immunodeficiency virus type 1 Tat binding protein-1 is a transcriptional coactivator specific for TR. Mol Endocrinol 2001;15:1329-43.
9. Jensen EV, De Sombre ER. Oestrogen-receptor interaction in target tissues. Biochem J 1969;115:28-9P.
10. Wijayaratne AL, McDonnell DP. The human estrogen receptor-alpha is a ubiquitinated protein whose stability is affected differentially by agonists, anta gonists, and selective estrogen receptor modulators. J Biol Chem 2001;276:35684-92.
11. Alarid ET, Bakopoulos N, Solodin N. Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation. Mol Endocrinol 1999;13:1522-34.
12. El Khissiin A, Leclercq G. Implication of proteasome in estrogen receptor degradation. FEBS Lett 1999;448:160-6.
13. Dauvois S, Danielian PS, White R, Parker MG. Antiestrogen ICI 164,384 reduces cellular estrogen receptor content by increasing its turnover. Proc Natl Acad Sci U S A 1992;89:4037-41.
14. Lonard DM, Nawaz Z, Smith CL, O'Malley BW. The 26S proteasome is required for estrogen receptor-alpha and coactivator turnover and for efficient estrogen receptor-alpha transactivation. Mol Cell 2000;5:939-48.
15. Stenoien DL, Patel K, Mancini MG, et al. FRAP reveals that mobility of oestrogen receptor-alpha is ligand- and proteasome-dependent. Nat Cell Biol 2001;3:15-23.
16. Momand J, Jung D, Wilczynski S, Niland J. The MDM2 gene amplification database. Nucleic Acids Res 1998;26:3453-9.
17. Honda R, Tanaka H, Yasuda H. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 1997;420:25-7.
18. Haupt Y, Maya R, Kazaz A, Oren M. Mdm2 promotes the rapid degradation of p53. Nature 1997;387:296-9.
19. Michael D, Oren M. The p53-2 module and the ubiquitin system. Semin Cancer Biol 2003;13:49-58.
20. Saji S, Okumura N, Eguchi H, et al. MDM2 enhances the function of estrogen receptor alpha in human breast cancer cells. Biochem Biophys Res Commun 2001;281:259-65.
21. Liu G, Schwartz JA, Brooks SC. Estrogen receptor protects p53 from deactivation by human double minute-2. Cancer Res 2000;60:1810-4.
22. Cavailles V, Dauvois S, Danielian PS, Parker MG. Interaction of proteins with transcriptionally active estrogen receptors. Proc Natl Acad Sci U S A 1994;91:10009-13.
23. Teyssier C, Belguise K, Galtier F, Cavailles V, Chalbos D. Receptor-interacting protein 140 binds c-Jun and inhibits estradiol-induced activator protein-1 activity by reversing glucocorticoid receptor-interacting protein 1 effect. Mol Endocrinol 2003;17:287-99.
24. Balaguer P, Francois F, Comunale F, et al. Reporter cell lines to study the estrogenic effects of xenoestrogens. Sci Total Environ 1999;233:47-56.
25. Lassus P, Roux P, Zugasti O, et al. Extinction of rac1 and Cdc42Hs signalling defines a novel p53-dependent apoptotic pathway. Oncogene 2000;19:2377-85.
26. Neel H, Weil D, Giansante C, Dautry F. In vivo cooperation between introns during pre-mRNA processing. Genes Dev 1993;7:2194-205.
27. Sadowski I, Ptashne M. A vector for expressing GAL4(1-147) fusions in mammalian cells. Nucleic Acids Res 1989;17:7539.
28. Castet A, Boulahtouf A, Versini G, et al. Multiple domains of the receptor-interacting protein 140 contribute to transcription inhibition. Nucleic Acids Res 2004;32:1957-66.
29. Balaguer P, Boussioux AM, Demirpence E, Nicolas JC. Reporter cell lines are useful tools for monitoring biological activity of nuclear receptor ligands. Luminescence 2001;16:153-8.
30. McMasters KM, Montes de Oca LR, Pena JR, Lozano G. mdm2 deletion does not alter growth characteristics of p53-deficient embryo fibroblasts. Oncogene 1996;13:1731-6.
31. Duong V, Licznar A, Margueron R, et al. ERalpha and ERbeta expression and transcriptional activity are differentially regulated by HDAC inhibitors. Oncogene 2006;25:1799-806.
32. Montes de Oca LR, Wagner DS, Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature 1995;378:203-6.
33. Honda R, Yasuda H. Activity of MDM2, a ubiquitin ligase, toward p53 or itself is dependent on the RING finger domain of the ligase. Oncogene 2000;19:1473-6.
34. Issaeva N, Bozko P, Enge M, et al. Small molecule RITA binds to p53, block s p53-HDM-2 interaction and activates p53 function in tumors. Nat Med 2004;10:1321-8.
35. Sengupta S, Wasylyk B. Ligand-dependent interaction of the glucocorticoid receptor with p53 enhances their degradation by Hdm2. Genes Dev 2001;15:2367-80.
36. Lin HK, Wang L, Hu YC, Altuwaijri S, Chang C. Phosphorylation-dependent ubiquitylation and degradation of androgen receptor by Akt require Mdm2 E3 ligase. EMBO J 2002;21:4037-48.
37. Reid G, Hubner MR, Metivier R, et al. Cyclic, proteasome-mediated turnover of unliganded and liganded ERalpha on responsive promoters is an integral feature of estrogen signaling. Mol Cell 2003;11:695-707.
38. Valley CC, Metivier R, Solodin NM, et al. Differential regulation of estrogen-inducible proteolysis and transcription by the estrogen receptor alpha N terminus. Mol Cell Biol 2005;25:5417-28.
39. Kinyamu HK, Archer TK. Estrogen receptor-dependent proteasomal degradation of the glucocorticoid receptor is coupled to an increase in mdm2 protein expression. Mol Cell Biol 2003;23:5867-81.
40. Lee SK, Kim HJ, Kim JW, Lee JW. Steroid receptor coactivator-1 and its family members differentially regulate transactivation by the tumor suppressor protein p53. Mol Endocrinol 1999;13:1924-33.
41. Shao W, Keeton EK, McDonnell DP, Brown M. Coactivator AIB1 links estrogen receptor transcriptional activity and stability. Proc Natl Acad Sci U S A 2004;101:11599-604.
42. Bautista S, Valles H, Walker RL, et al. In breast cancer, amplification of the steroid receptor coactivator gene AIB1 is correlated with estrogen and progesterone receptor positivity. Clin Cancer Res 1998;4:2925-9.
43. Yan F, Gao X, Lonard DM, Nawaz Z. Specific ubiquitin-conjugating enzymes promote degradation of specific nuclear receptor coactivators. Mol Endocrinol 2003;17:1315-31.
44. Alarid ET, Preisler-Mashek MT, Solodin NM. Thyroid hormone is an inhibitor of estrogen-induced degradation of estrogen receptor-alpha protein: estrogendependent proteolysis is not essential for receptor transactivation function in the pituitary. Endocrinology 2003;144:3469-76.
45. Fan M, Bigsby RM, Nephew KP. The NEDD8 pathway is required for proteasome-mediated degradation of human estrogen receptor (ER)-alpha and essential for the antiproliferative activity of ICI 182,780 in ERalpha-positive breast cancer cells. Mol Endocrinol 2003;17:356-65.
46. Callige M, Kieffer I, Richard-Foy H. CSN5/Jab1 is involved in ligand-dependent degradation of estrogen receptor {alpha} by the proteasome. Mol Cell Biol 2005;25:4349-58.
47. Tateishi Y, Kawabe Y, Chiba T, et al. Ligand-dependent switching of ubiquitin-proteasome pathways for estrogen receptor. EMBO J 2004;23:4813-23.
48. Li L, Li Z, Howley PM, Sacks DB. E6AP and calmodulin reciprocally regulate estrogen receptor stability. J Biol Chem 2006;281:1978-85.
49. Meek DW. p53 Induction: phosphorylation sites cooperate in regulating. Cancer Biol Ther 2002;1:284-6.
50. Lange CA, Shen T, Horwitz KB. Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. Proc Natl Acad Sci U S A 2000;97:1032-7.
51. Gianni M, Bauer A, Garattini E, Chambon P, Rochette-Egly C. Phosphorylation by p38MAPK and recruitment of SUG-1 are required for RA-induced RAR gamma degradation and transactivation. EMBO J 2002;21:3760-9.
52. Henrich LM, Smith JA, Kitt D, et al. Extracellular signal-regulated kinase 7, a regulator of hormone-dependent estrogen receptor destruction. Mol Cell Biol 2003;23:5979-88.
53. Marsaud V, Gougelet A, Maillard S, Renoir JM. Various phosphorylation pathways, depend ing on agonist and antagonist binding to endogenous estrogen receptor alpha (ERalpha), differentially affect ERalpha extractability, proteasome- mediated stability, and transcriptional activity in human breast cancer cells. Mol Endocrinol 2003;17:2013-27.
54. Fan M, Nakshatri H, Nephew KP. Inhibiting proteasomal proteolysis sustains estrogen receptor-alpha activation. Mol Endocrinol 2004;18:2603-15.
55. Sengupta S, Wasylyk B. Physiological and pathological consequences of the interactions of the p53 tumor suppressor with the glucocorticoid, androgen, and estrogen receptors. Ann N Y Acad Sci 2004;1024:54-71.
56. Turbin DA, Cheang MC, Bajdik CD, et al. MDM2 protein expression is a negative prognostic marker in breast carcinoma. Mod Pathol 2006;19:69-74.
57. Platet N, Cunat S, Chalbos D, Rochefort H, Garcia M. Unliganded and liganded estrogen receptors protect against cancer invasion via different mechanisms. Mol Endocrinol 2000;14:999-1009.