A novel mechanism whereby BRCA1/1a/1b fine tunes the dynamic complex interplay between SUMO-dependent/independent activities of Ubc9 on E2-induced ERα activation/repression and degradation in breast cancer cells

International Journal of Oncology

Volumn 34, Issue 4, 2009, Pages 939-949

  Xu, J ^a   Watkins, T ^a   Reddy, A ^a   Reddy, E S P ^a   Rao, Veona N ^a  

^a MOREHOUSE SCHOOL OF MEDICINE   (United States)

Author keywords

BRCA1 1a 1b; Breast cancers; E3 ubiquitin ligase; Estrogenreceptor ; SUMO 1; Ubc9

Indexed keywords

BRCA1 PROTEIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; PROTEIN UBC9; SUMO PROTEIN; UBIQUITIN PROTEIN LIGASE E3;

ANIMAL CELL; ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MODIFICATION; WESTERN BLOTTING;

ANIMALS; BRCA1 PROTEIN; BREAST NEOPLASMS; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; ESTROGEN RECEPTOR ALPHA; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICROSCOPY, FLUORESCENCE; MODELS, GENETIC; MUTATION; SUMO-1 PROTEIN; UBIQUITIN-CONJUGATING ENZYMES; UBIQUITIN-PROTEIN LIGASES;

EID: 67649443799     PISSN: 10196439     EISSN: 17912423     Source Type: Journal    
DOI: 10.3892/ijo_00000220     Document Type: Article

References (43)

1. Miki Y, Swensen J, Shattuck-Eidens D, Futreal PA, Harshman K and Tavtigian S: A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266: 66-71, 1994.
2. Rowell S, Newman B, Boyd J and King MC: Inherited predisposition to breast and ovarian cancer. Am J Hum Genet 55: 861-865, 1994.
3. Gayther SA, Warren W, Mazoyer S, Russell PA, Harrington PA, Chiano M, et al: Germline mutations of the BRCA1 gene in breast and ovarian cancer families provide evidence for a genotype-phenotype correlation. Nat Genet 11: 428-433, 1995.
4. Orban TI and Olah E: Emerging roles of BRCA1 alternative splicing. Mol Pathol 56: 191-197, 2003.
5. Thakur S, Zhang HB, Peng Y, Le H, Carroll B, Ward T, et al: Localization of BRCA1 and a splice variant identifies the nuclear localization signal. Mol Cell Biol 17: 444-452, 1997.
6. Wilson CA, Payton MN, Elliott ES, Buaas FW, Cajulis EE, Grosshans D, et al: Differential subcellular localization, expression and biological toxicity of BRCA1 and the splice variant BRCA1-delta 11b. Oncogene 14: 1-16, 1997.
7. Cui JQ, Shao N, Chai Y, Wang H, Reddy ES and Rao VN: BRCAl splice variants BRCAla and BRCAlb associate with CBP co-activator. Oncol Rep 5: 591-595, 1998.
8. Wang H, Shao N, Ding OM, Cui J, Reddy ESP and Rao VN: BRCA1 proteins are transported to the nucleus in the absence of serum and splice variants BRCA1a, BRCA1b are tyrosine phosphoprotein that associate with E2F, cyclins and cyclin dependent kinases. Oncogene 15: 143-157, 1997.
9. Lu M, Conzen SD, Cole CN and Arrick B: Characterizations of functional messenger RNA splice variants of BRCA1 expressed in non malignant and tumor-derived breast cells. Cancer Res 56: 4578-4581, 1996.
10. Orban TI and Olah E: Expression profiles of BRCA1 splice variants in a synchronous and in G1/S synchronized tumor cell lines. Biochem Biophys Res Commun 280: 32-38, 2001.
11. Rosen EM, Fan S and Ma Y: BRCA1 regulation of transcription. Cancer Lett 236: 175-185, 2006.
12. Park MA, Seok Y, Jeong G and Lee J: SUMO1 negatively regulates BRCA1-medicated transcription, via modulation of promoter occupancy. Nucleic Acids Res 36: 263-283, 2008.
13. Foulkes WD, Metcalfe K, Sun P, Hanna WM, Lynch HT, Ghadirian P, et al: Estrogen receptor status in BRCA1-and BRCA2-related breast cancer: the influence of age, grade, and histological type. Clin Cancer Res 10: 2029-2034, 2004.
14. Morris GJ, Naidu S, Topham AK, Guiles F, Xu Y, McCue P, et al: Differences in breast carcinoma characteristics in newly diagnosed African-American and Caucasian patients: a single-institution compilation compared with the National Cancer Institute's Surveillance, Epidemiology, and End Results Database. Cancer 110: 876-884, 2007.
15. Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, et al: Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA 100: 8418-8423, 2003.
16. Turner NC and Reis-Filho JS: Basal-like breast cancer and the BRCA1 phenotype. Oncogene 25: 5846-5853, 2006.
17. Chai Y, Shao N, Lee L, Reddy V, Gabriela O, Rao R, et al: BRCA1a has antitumor activity in Triple-negative breast and ovarian and prostate cancer cells. Oncogene 26: 6031-6037, 2007.
18. Rebbeck TR, Levin AM, Eisen A, Snyder C, Watson P, Cannon-Albright L, et al: Breast cancer risk after bilateral prophylactic oophorectomy in BRCA1 mutation carriers. J Natl Cancer Inst 91: 1475-1479, 1999.
19. Ma YX, Tomita Y, Fan S, Wu K, Tong Y, Zhao Z, et al: Structural determinants of the BRCA1: estrogen receptor interaction. Oncogene 24: 1831-1846, 2005.
20. Song J, Zhang Z, Hu W and Chen Y: Small ubiquitin-like modifier (SUMO) recognition of a SUMO binding motif; a reversal of the bound orientation. J Biol Chem 280: 40122-40129, 2005.
21. Rodriguez, MS, Dargemont C and Hay RT: SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J Biol Chem 276: 12654-12659, 2001.
22. Sentis S, Romancer M L, Bianchin C, Rostan M and Corbo L: Sumoylation of the estrogen receptor. Hinge region regulates its transcriptional activity. Mol Endocr 19: 2671-2684, 2005.
23. Kobayashi S, Shibata H, Yokota K, Suda N, Murai A, Kurihara I, et al: FHL2, UBC9 and PIASI are novel estrogen receptor and interacting proteins. Endocr Res 30: 617-621, 2004.
24. Lonard DM, Nawaz Z, Smith CL and O'Malley BW: The 26S proteasome is required for estrogen receptor-α and coactivator turnover and for efficient estrogen receptor-α transactivation. Mol Cell 5: 939-948, 2000.
25. Koonin E, Altschul SF and Bork P: BRCA1 protein products functional motifs. Nat Genet 13: 266-268, 1996.
26. Bork P, Hofmann K. Bucher P, Neuwald AF, Altschul SF and Koonin EV: A super family of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. FASEB J 11: 68-76, 1997.
27. Nilsson S, Makela S, Treuter E, Tujague M, Thomsen J, Andersson G, et al: Mechanisms of estrogen action. Physiol Rev 81: 1535-1565, 2001.
28. Luo M, Koh M, Feng J, Wu Q and Melamed P: Cross talk in hormonally regulated gene transcription through induction of estrogen receptor ubiquitylation. Mol Cell Biol 25: 7386-7398, 2005.
29. Eakin CM, MacCoss MJ, Finney GL and Klevit RE: Estrogen receptor α is a putative substrare for the BRCA1 ubiquitin ligase. Proc Natl Acad Sci USA 104: 5794-5799, 2007.
30. Hashizume R, Fukuda M, Maeda I, Nishikawa H, Oyake D, Yabuki Y, et al: The RING heterodimer BRCA1-BARD1 is a ubiquitin ligase inactivated by a breast cancer derived mutation. J Biol Chem 276: 14537-14540, 2001.
31. Chai YL, Cui J, Chipitsyna G, Liao B, Lui S, Aysola K, et al: c-Fos oncogene regulator Elk-1 interacts with BRCA1 splice variants BRCA1a/1b and enhances BRCA1a/1b mediated growth suppression in breast cancer cells. Oncogene 20: 1357-1367, 2001.
32. Hay RT: SUMO: a history of modification. Mol Cell 18: 1-12, 2005.
33. Fan S, Ma YX, Wang C, Yuan RQ, Meng Q, Wang JA, et al: Role of direct interaction in BRCA1 inhibition of estrogen receptor activity. Oncogene 20: 77-87, 2001.
34. Fan S, Wang J, Yuan R, Ma Y, Meng Q, Erdos MR, et al: BRCA1 inhibition of estrogen receptor signaling in transfected cells. Science 284: 1354-1356, 1999.
35. Henttu P, Kalkhoven E and Parker G: AF-2 activity and recruitment of steroid receptor coactivator 1 to the estrogen receptor depend on a lysine residue conserved in nuclear receptors. Mol Cell Biol 17: 1832-1839, 1997.
36. Moschos SJ, Smith AP, Mandic M, Athanassiou C, Watson-Hurst K, Jukic DM, et al: SAGE and antibody array analysis of melanoma-infiltrated lymph nodes: identification of Ubc9 as an important molecule in advanced-stage melanomas. Oncogene 26: 4216-4225, 2007.
37. Ohta T and Fukuda M: Ubiquitin and breast cancer. Oncogene 23: 2079-2088, 2004.
38. Firestein R and Feuerstein N: Association of activating transcription factor 2 (ATF2) with the ubiquitin-conjugating enzyme hUBC9. Implication of the ubiquitin/proteasome pathway in regulation of ATF2 in T cells. J Biol Chem 273: 5892-5902, 1998.
39. Fang S, Lorick K, Jensen J and Weissman A: RING finger ubiquitin protein ligases: implications for tumorigenesis, metastasis and for molecular targets in cancer. Semin Cancer Biol 13: 1-14, 2002.
40. Tischkowitz MD and Foulkes WD: The basal phenotype of BRCA1-related breast cancer: past, present and future. Cell Cycle 5: 963-967, 2006.
41. Li W, Xiao C, Vonderhaar BK and Deng C-X: A role of estrogen/ERα signaling in BRCA1-associated tissue-specific tumor formation. Oncogene 26: 7204-7212, 2007.
42. Sun H, Leverson J and Hunter T: Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J 26: 4102-4112, 2007.
43. Uzunova K, Gottsche K, Miteva M, Weisshaar S, Glanemann C, Schnellhardt M, Niessen M, et al: Ubiquitin-dependent proteolytic control of SUMO conjugates. J Biol Chem 282: 34167-34175, 2007.