Coordinate regulation of estrogen receptor β degradation by Mdm2 and CREB-binding protein in response to growth signals

Oncogene

Volumn 32, Issue 1, 2013, Pages 117-126

  Sanchez, M ^a   Picard, N ^a   Sauve K ^a   Tremblay, A ^a,b  

^a UNIVERSITY OF MONTREAL   (Canada)

^b UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

26S proteasome ubiquitin system; breast cancer; CBP p300; ErbB2 Her 2 Neu; ErbB3; PI3 K Akt pathway

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; EPIDERMAL GROWTH FACTOR RECEPTOR 3; ESTROGEN RECEPTOR BETA; GROWTH FACTOR; HEREGULIN BETA; NEU DIFFERENTIATION FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; POLYUBIQUITIN; PROTEASOME; PROTEIN KINASE B; PROTEIN MDM2; SERINE; THREONINE; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; BREAST CANCER; CANCER CELL; CELL GROWTH; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVATION; GENE TARGETING; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; UBIQUITINATION;

AMINO ACID SEQUENCE; CREB-BINDING PROTEIN; ENZYME ACTIVATION; ESTROGEN RECEPTOR BETA; HUMANS; NEUREGULIN-1; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MDM2; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84871977882     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.19     Document Type: Article

References (44)

1. Heldring N, Pike A, Andersson S, Matthews J, Cheng G, Hartman J et al. Estrogen receptors: How do they signal and what are their targets. Physiol Rev 2007; 87: 905-931.
2. Weigel NL, Moore NL. Steroid receptor phosphorylation: A key modulator of multiple receptor functions. Mol Endocrinol 2007; 21: 2311-2319.
3. Sanchez M, Picard N, Sauvé K, Tremblay A. Challenging estrogen receptor beta with phosphorylation. Trends Endocrinol Metab 2010; 21: 104-110.
4. Sanchez M, Tremblay A. Growth factor signaling to estrogen receptors in hormone dependent cancers. Mol Genet Cancer 2005; 5: 149-185.
5. Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 1995; 270: 1491-1494.
6. Bunone G, Briand P-A, Miksicek RJ, Picard D. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J 1996; 15: 2174-2183.
7. Tremblay A, Giguere V. Contribution of steroid receptor coactivator-1 and CREB binding protein in ligand-independent activity of estrogen receptor beta. J Steroid Biochem Mol Biol 2001; 77: 19-27.
8. Tremblay A, Tremblay GB, Labrie F, Giguere V. Ligand-independent recruitment of SRC-1 to estrogen receptor b through phosphorylation of activation function AF-1. Mol Cell 1999; 3: 513-519.
9. St Laurent V, Sanchez M, Charbonneau C, Tremblay A. Selective hormonedependent repression of estrogen receptor beta by a p38-activated ErbB2/ErbB3 pathway. J Steroid Biochem Mol Biol 2005; 94: 23-37.
10. Sanchez M, Sauvé K, Picard N, Tremblay A. The hormonal response of estrogen receptor beta is decreased by the PI3K/Akt pathway via a phosphorylationdependent release of CREB-binding protein. J Biol Chem 2007; 282: 4830-4840.
11. Kalkhoven E. CBP and p300: HATs for different occasions. Biochem Pharmacol 2004; 68: 1145-1155.
12. Goodman RH, Smolik S. CBP/p300 in cell growth, transformation, and development. Genes Dev 2000; 14: 1553-1577.
13. Nawaz Z, Lonard DM, Dennis AP, Smith CL, O'Malley BW. Proteasome-dependent degradation of the human estrogen receptor. Proc Natl Acad Sci USA 1999; 96: 1858-1862.
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: 939-948.
15. Picard N, Charbonneau C, Sanchez M, Licznar A, Busson M, Lazennec G et al. Phosphorylation of activation function-1 regulates proteasome-dependent nuclear mobility and E6-AP ubiquitin ligase recruitment to the estrogen receptor beta. Mol Endocrinol 2008; 22: 317-330.
16. Meek DW, Hupp TR. The regulation of MDM2 by multisite phosphorylation- opportunities for molecular-based intervention to target tumours? Semin Cancer Biol 2010; 20: 19-28.
17. Mayo LD, Donner DB. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci USA 2001; 98: 11598-11603.
18. Feng J, Tamaskovic R, Yang Z, Brazil DP, Merlo A, Hess D et al. Stabilization of Mdm2 via decreased ubiquitination is mediated by protein kinase B/Aktdependent phosphorylation. J Biol Chem 2004; 279: 35510-35517.
19. Radhakrishnan I, Perez-Alvarado GC, Parker D, Dyson HJ, Montminy MR, Wright PE. Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: A model for activator:coactivator interactions. Cell 1997; 91: 741- 752.
20. Brekman A, Singh KE, Polotskaia A, Kundu N, Bargonetti J. A p53-independent role of Mdm2 in estrogen-mediated activation of breast cancer cell proliferation. Breast Cancer Res 2011; 13: R3.
21. Ma Y, Fan S, Hu C, Meng Q, Fuqua SA, Pestell RG et al. BRCA1 regulates acetylation and ubiquitination of estrogen receptor-alpha. Mol Endocrinol 2010; 24: 76-90.
22. Berry NB, Fan M, Nephew KP. Estrogen receptor-alpha hinge-region lysines 302 and 303 regulate receptor degradation by the proteasome. Mol Endocrinol 2008; 2: 1535-1551.
23. Subramanian K, Jia D, Kapoor-Vazirani P, Powell DR, Collins RE, Sharma D et al. Regulation of estrogen receptor alpha by the SET7 lysine methyltransferase. Mol Cell 2008; 30: 336-347.
24. Ariazi EA, Clark GM, Mertz JE. Estrogen-related receptor alpha and estrogenrelated receptor gamma associate with unfavorable and favorable biomarkers, respectively, in human breast cancer. Cancer Res 2002; 62: 6510-6518.
25. Shao W, Keeton EK, McDonnell DP, Brown M. Coactivator AIB1 links estrogen receptor transcriptional activity and stability. Proc Natl Acad Sci USA 2004; 101: 11599-11604.
26. Nawaz Z, Lonard DM, Smith CL, Lev-Lehman E, Tsai SY, Tsai MJ et al. The Angelman syndrome-associated protein, E6-AP, is a coactivator for the nuclear hormone receptor superfamily. Mol Cell Biol 1999; 19: 1182-1189.
27. Kim K, Burghardt R, Barhoumi R, Lee SO, Liu X, Safe S. MDM2 regulates estrogen receptor a and estrogen responsiveness in breast cancer cells. J Mol Endocrinol 2011; 46: 67-79.
28. Shi D, Pop MS, Kulikov R, Love IM, Kung AL, Grossman SR. CBP and p300 are cytoplasmic E4 polyubiquitin ligases for p53. Proc Natl Acad Sci USA 2009; 106: 16275-16280.
29. Marine JC, Lozano G. Mdm2-mediated ubiquitylation: P53 and beyond. Cell Death Differ 2010; 17: 93-102.
30. Grossman SR, Perez M, Kung AL, Joseph M, Mansur C, Xiao ZX et al. p300/MDM2 complexes participate in MDM2-mediated p53 degradation. Mol Cell 1998; 2: 405-415.
31. Arpino G, Wiechmann L, Osborne CK, Schiff R. Crosstalk between the estrogen receptor and the HER tyrosine kinase receptor family: Molecular mechanism and clinical implications for endocrine therapy resistance. Endocr Rev 2008; 29: 217-233.
32. Jordan VC, O'Malley BW. Selective estrogen-receptor modulators and antihormonal resistance in breast cancer. J Clin Oncol 2007; 25: 5815-5824.
33. Sakamoto G, Honma N. Estrogen receptor-beta status influences clinical outcome of triple-negative breast cancer. Breast Cancer 2009; 16: 281-282.
34. Lazennec G. Estrogen receptor beta, a possible tumor suppressor involved in ovarian carcinogenesis. Cancer Lett 2006; 231: 151-157.
35. Loda M, Kaelin Jr. WG Prostate cancer: Beta control your hormones. Cancer Cell 2010; 17: 311-312.
36. Roger P, Esslimani-Sahla M, Delfour C, Lazennec G, Rochefort H, Maudelonde T. Expression of estrogen receptors alpha and beta in early steps of human breast carcinogenesis. Adv Exp Med Biol 2008; 617: 139-148.
37. Leygue E, Dotzlaw H, Watson PH, Murphy LC. Altered estrogen receptor a and b messenger RNA expression during human breast tumorigenesis. Cancer Res 1998; 58: 3197-3201.
38. Lazennec G, Bresson D, Lucas A, Chauveau C, Vignon F. ER beta inhibits proliferation and invasion of breast cancer cells. Endocrinology 2001; 142: 4120 -4130.
39. Lindberg K, Strom A, Lock JG, Gustafsson JA, Haldosen LA, Helguero LA. Expression of estrogen receptor beta increases integrin alpha1 and integrin beta1 levels and enhances adhesion of breast cancer cells. J Cell Physiol 2010; 222: 156-167.
40. Treeck O, Lattrich C, Springwald A, Ortmann O. Estrogen receptor beta exerts growth-inhibitory effects on human mammary epithelial cells. Breast Cancer Res Treat 2010; 120: 557-565.
41. Nair HB, Kirma NB, Ganapathy M, Vadlamudi RK, Tekmal RR. Estrogen receptor-beta activation in combination with letrozole blocks the growth of breast cancer tumors resistant to letrozole therapy. Steroids 2011; 76:792-796.
42. Sauvé K, Lepage J, Sanchez M, Heveker N, Tremblay A. Positive Feedback Activation of Estrogen Receptors by the CXCL12-CXCR4 Pathway. Cancer Res 2009; 69: 5793-5800.
43. Demers A, Caron V, Rodrigue-Way A, Wahli W, Ong H, Tremblay A. A concerted kinase interplay identifies PPARc as a molecular target of ghrelin signaling in macrophages. PLoS ONE 2009; 4: E7728.
44. Avallone R, Demers A, Rodrigue-Way A, Bujold K, Harb D, Anghel S et al. A growth hormone-releasing peptide that binds scavenger receptor CD36 and ghrelin receptor upregulates ABC sterol transporters and cholesterol efflux in macrophages through a PPARc-dependent pathway. Mol Endocrinol 2006; 20: 3165-3178.