Systems level-based RNAi screening by high content analysis identifies UBR5 as a regulator of estrogen receptor- protein levels and activity

Oncogene

Volumn 34, Issue 2, 2015, Pages 154-164

  Bolt, M J ^a   Stossi, F ^a   Callison, A M ^a   Mancini, M G ^a   Dandekar, R ^a   Mancini, M A ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

estrogen receptor; high content screening; high throughput microscopy; ubiquitin ligase; UBR5

Indexed keywords

ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA, HUMAN; NUCLEAR PROTEIN; SUPT5H PROTEIN, HUMAN; TRANSCRIPTION ELONGATION FACTOR; UBIQUITIN PROTEIN LIGASE; UBR5 PROTEIN, HUMAN;

BREAST TUMOR; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HELA CELL LINE; HUMAN; MCF 7 CELL LINE; METABOLISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

BREAST NEOPLASMS; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE KNOCKDOWN TECHNIQUES; HELA CELLS; HUMANS; MCF-7 CELLS; NUCLEAR PROTEINS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ELONGATION FACTORS; UBIQUITIN-PROTEIN LIGASES;

EID: 85027932158     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2013.550     Document Type: Article

References (61)

1. Dickson RB, Lippman ME. Control of human breast cancer by estrogen, growth factors, and oncogenes. Cancer Treat Res 1988; 40: 119-165.
2. Jacquemier JD, Hassoun J, Torrente M, Martin PM. Distribution of estrogen and progesterone receptors in healthy tissue adjacent to breast lesions at various stages-immunohistochemical study of 107 cases. Breast Cancer Res Treat 1990; 15: 109-117.
3. Frasor J, Danes JM, Komm B, Chang KC, Lyttle CR, Katzenellenbogen BS. Profiling of estrogen up-and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 2003; 144: 4562-4574.
4. Dubik D, Shiu RP. Mechanism of estrogen activation of c-myc oncogene expression. Oncogene 1992; 7: 1587-1594.
5. Ali S, Coombes RC. Endocrine-responsive breast cancer and strategies for combating resistance. Nat Rev 2002; 2: 101-112.
6. Esslimani-Sahla M, Simony-Lafontaine J, Kramar A, Lavaill R, Mollevi C, Warner M et al. Estrogen receptor beta (ER beta) level but not its ER beta cx variant helps to predict tamoxifen resistance in breast cancer. Clin Cancer Res 2004; 10: 5769-5776.
7. Bernardo GM, Lozada KL, Miedler JD, Harburg G, Hewitt SC, Mosley JD et al. FOXA1 is an essential determinant of ERalpha expression and mammary ductal morphogenesis. Development (Cambridge, England) 2010; 137: 2045-2054.
8. Li XF, Wang SJ, Jiang LS, Dai LY. Stage specific effect of leptin on the expressions of estrogen receptor and extracellular matrix in a model of chondrocyte differentiation. Cytokine 2013; 61: 876-884.
9. Ellison-Zelski SJ, Solodin NM, Alarid ET. Repression of ESR1 through actions of estrogen receptor alpha and Sin3A at the proximal promoter. Mol Cell Biol 2009; 29: 4949-4958.
10. Sun J, Zhou W, Kaliappan K, Nawaz Z, Slingerland JM. ERalpha phosphorylation at Y537 by Src triggers E6-AP-ERalpha binding, ERalpha ubiquitylation, promoter occupancy, and target gene expression. Mol Endocrinol (Baltimore, Md) 2012; 26: 1567-1577.
11. Bhatt S, Xiao Z, Meng Z, Katzenellenbogen BS. Phosphorylation by p38 mitogenactivated protein kinase promotes estrogen receptor alpha turnover and functional activity via the SCF(Skp2) proteasomal complex. Mol Cell Biol 2012; 32: 1928-1943.
12. Fan M, Park A, Nephew KP. CHIP (carboxyl terminus of Hsc70-interacting protein) promotes basal and geldanamycin-induced degradation of estrogen receptoralpha. Mol Endocrinol (Baltimore, Md) 2005; 19: 2901-2914.
13. Giamas G, Filipovic A, Jacob J, Messier W, Zhang H, Yang D et al. Kinome screening for regulators of the estrogen receptor identifies LMTK3 as a new therapeutic target in breast cancer. Nat Med 2011; 17: 715-719.
14. Fox EM, Miller TW, Balko JM, Kuba MG, Sanchez V, Smith RA et al. A kinome-wide screen identifies the insulin/IGF-I receptor pathway as a mechanism of escape from hormone dependence in breast cancer. Cancer Res 2011; 71: 6773-6784.
15. Mendes-Pereira AM, Sims D, Dexter T, Fenwick K, Assiotis I, Kozarewa I et al. Genome-wide functional screen identifies a compendium of genes affecting sensitivity to tamoxifen. Proc Natl Acad Sci USA 2012; 109: 2730-2735.
16. Sharp ZD, Mancini MG, Hinojos CA, Dai F, Berno V, Szafran AT et al. Estrogenreceptor-alpha exchange and chromatin dynamics are ligand-and domaindependent. J Cell Sci 2006; 119(Pt 19): 4101-4116.
17. Ashcroft FJ, Newberg JY, Jones ED, Mikic I, Mancini MA. High content imagingbased assay to classify estrogen receptor-alpha ligands based on defined mechanistic outcomes. Gene 2011; 477: 42-52.
18. Berno V, Amazit L, Hinojos C, Zhong J, Mancini MG, Sharp ZD et al. Activation of estrogen receptor-alpha by E2 or EGF induces temporally distinct patterns of large-scale chromatin modification and mRNA transcription. PLoS One 2008; 3: e2286.
19. Zwart W, de Leeuw R, Rondaij M, Neefjes J, Mancini MA, Michalides R. The hinge region of the human estrogen receptor determines functional synergy between AF-1 and AF-2 in the quantitative response to estradiol and tamoxifen. J Cell Sci 2010; 123(Pt 8): 1253-1261.
20. Bolt MJ, Stossi F, Newberg JY, Orjalo A, Johansson HE, Mancini MA. Coactivators enable glucocorticoid receptor recruitment to fine-tune estrogen receptor transcriptional responses. Nucleic Acids Res 2013; 41: 4036-4048.
21. Tcherepanova I, Puigserver P, Norris JD, Spiegelman BM, McDonnell DP. Modulation of estrogen receptor-alpha transcriptional activity by the coactivator PGC-1. J Biol Chem 2000; 275: 16302-16308.
22. Wu Q, Burghardt R, Safe S. Vitamin D-interacting protein 205 (DRIP205) coactivation of estrogen receptor alpha (ERalpha) involves multiple domains of both proteins. J Biol Chem 2004; 279: 53602-53612.
23. Mook OR, Baas F, de Wissel MB, Fluiter K. Allele-specific cancer cell killing in vitro and in vivo targeting a single-nucleotide polymorphism in POLR2A. Cancer Gene Ther 2009; 16: 532-538.
24. Karmakar S, Foster EA, Smith CL. Unique roles of p160 coactivators for regulation of breast cancer cell proliferation and estrogen receptor-alpha transcriptional activity. Endocrinology 2009; 150: 1588-1596.
25. Dong J, Tsai-Morris CH, Dufau ML. A novel estradiol/estrogen receptor alphadependent transcriptional mechanism controls expression of the human prolactin receptor. J Biol Chem 2006; 281: 18825-18836.
26. Schaufele F. Regulation of estrogen receptor activation of the prolactin enhancer/promoter by antagonistic activation function-2-interacting proteins. Mol Endocrinol (Baltimore, Md) 1999; 13: 935-945.
27. Zhang X, Krutchinsky A, Fukuda A, Chen W, Yamamura S, Chait BT et al. MED1/TRAP220 exists predominantly in a TRAP/Mediator subpopulation enriched in RNA polymerase II and is required for ER-mediated transcription. Mol Cell 2005; 19: 89-100.
28. Ansari SA, Morse RH. Mechanisms of Mediator complex action in transcriptional activation. Cell Mol Life Sci 2013; 70: 2743-2756.
29. Toth-Petroczy A, Oldfield CJ, Simon I, Takagi Y, Dunker AK, Uversky VN et al. Malleable machines in transcription regulation: the mediator complex. PLoS Comput Biol 2008; 4: e1000243.
30. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 2007; 130: 77-88.
31. Hirose Y, Ohkuma Y. Phosphorylation of the C-terminal domain of RNA polymerase II plays central roles in the integrated events of eukaryotic gene expression. J Biochem 2007; 141: 601-608.
32. Gonzalez-Arenas A, Hansberg-Pastor V, Hernandez-Hernandez OT, Gonzalez-Garcia TK, Henderson-Villalpando J, Lemus-Hernandez D et al. Estradiol increases cell growth in human astrocytoma cell lines through ERalpha activation and its interaction with SRC-1 and SRC-3 coactivators. Biochim Biophys Acta 2012; 1823: 379-386.
33. Prapapanich V, Chen S, Nair SC, Rimerman RA, Smith DF. Molecular cloning of human p48, a transient component of progesterone receptor complexes and an Hsp70-binding protein. Mol Endocrinol (Baltimore, Md.) 1996; 10: 420-431.
34. Snow BE, Erdmann N, Cruickshank J, Goldman H, Gill RM, Robinson MO et al. Functional conservation of the telomerase protein Est1p in humans. Curr Biol 2003; 13: 698-704.
35. Stanlie A, Begum NA, Akiyama H, Honjo T. The DSIF subunits Spt4 and Spt5 have distinct roles at various phases of immunoglobulin class switch recombination. PLoS Genet 2012; 8: e1002675.
36. Jiang W, Wang S, Xiao M, Lin Y, Zhou L, Lei Q et al. Acetylation regulates gluconeogenesis by promoting PEPCK1 degradation via recruiting the UBR5 ubiquitin ligase. Mol Cell 2011; 43: 33-44.
37. Gudjonsson T, Altmeyer M, Savic V, Toledo L, Dinant C, Grofte M et al. TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 2012; 150: 697-709.
38. Henderson MJ, Russell AJ, Hird S, Munoz M, Clancy JL, Lehrbach GM et al. EDD, the human hyperplastic discs protein, has a role in progesterone receptor coactivation and potential involvement in DNA damage response. J Biol Chem 2002; 277: 26468-26478.
39. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012; 2: 401-404.
40. Comprehensive molecular portraits of human breast tumours. Nature 2012; 490: 61-70.
41. Horner-Glister E, Maleki-Dizaji M, Guerin CJ, Johnson SM, Styles J, White IN. Influence of oestradiol and tamoxifen on oestrogen receptors-alpha and-beta protein degradation and non-genomic signalling pathways in uterine and breast carcinoma cells. J Mol Endocrinol 2005; 35: 421-432.
42. Rudnik V, Sanyal A, Syed FA, Monroe DG, Spelsberg TC, Oursler MJ et al. Loss of ERE binding activity by estrogen receptor-alpha alters basal and estrogen-stimulated bone-related gene expression by osteoblastic cells. J Cell Biochem 2008; 103: 896-907.
43. Burandt E, Jens G, Holst F, Janicke F, Muller V, Quaas A et al. Prognostic relevance of AIB1 (NCoA3) amplification and overexpression in breast cancer. Breast Cancer Res Treat 2013; 137: 745-753.
44. Gururaj AE, Peng S, Vadlamudi RK, Kumar R. Estrogen induces expression of BCAS3, a novel estrogen receptor-alpha coactivator, through proline-, glutamic acid-, and leucine-rich protein-1 (PELP1). Mol Endocrinol (Baltimore, Md) 2007; 21: 1847-1860.
45. Garcia-Becerra R, Berno V, Ordaz-Rosado D, Sharp ZD, Cooney AJ, Mancini MA et al. Ligand-induced large-scale chromatin dynamics as a biosensor for the detection of estrogen receptor subtype selective ligands. Gene 2010; 458: 37-44.
46. Bourdoncle A, Labesse G, Margueron R, Castet A, Cavailles V, Royer CA. The nuclear receptor coactivator PGC-1alpha exhibits modes of interaction with the estrogen receptor distinct from those of SRC-1. J Mol Biol 2005; 347: 921-934.
47. Chen YJ, Lee MT, Yao HC, Hsiao PW, Ke FC, Hwang JJ. Crucial role of estrogen receptor-alpha interaction with transcription coregulators in follicle-stimulating hormone and transforming growth factor beta1 up-regulation of steroidogenesis in rat ovarian granulosa cells. Endocrinology 2008; 149: 4658-4668.
48. Stokes K, Alston-Mills B, Teng C. Estrogen response element and the promoter context of the human and mouse lactoferrin genes influence estrogen receptor alpha-mediated transactivation activity in mammary gland cells. J Mol Endocrinol 2004; 33: 315-334.
49. Lai F, Orom UA, Cesaroni M, Beringer M, Taatjes DJ, Blobel GA et al. Activating RNAs associate with Mediator to enhance chromatin architecture and transcription. Nature 2013; 494: 497-501.
50. Willis IM, Chua G, Tong AH, Brost RL, Hughes TR, Boone C et al. Genetic interactions of MAF1 identify a role for Med20 in transcriptional repression of ribosomal protein genes. PLoS Genet 2008; 4: e1000112.
51. Smits VA. EDD induces cell cycle arrest by increasing p53 levels. Cell Cycle (Georgetown, Tex) 2012; 11: 715-720.
52. Cojocaru M, Bouchard A, Cloutier P, Cooper JJ, Varzavand K, Price DH et al. Transcription factor IIS cooperates with the E3 ligase UBR5 to ubiquitinate the CDK9 subunit of the positive transcription elongation factor B. J Biol Chem 2011; 286: 5012-5022.
53. Bernassola F, Karin M, Ciechanover A, Melino G. The HECT family of E3 ubiquitin ligases: multiple players in cancer development. Cancer Cell 2008; 14: 10-21.
54. La Rosa P, Pesiri V, Marino M, Acconcia F. 17beta-Estradiol-induced cell proliferation requires estrogen receptor (ER) alpha monoubiquitination. Cell Signal 2011; 23: 1128-1135.
55. Metivier R, Penot G, Hubner MR, Reid G, Brand H, Kos M et al. Estrogen receptoralpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003; 115: 751-763.
56. Reid G, Hubner MR, Metivier R, Brand H, Denger S, Manu D 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.
57. Long X, Nephew KP. Fulvestrant (ICI 182,780)-dependent interacting proteins mediate immobilization and degradation of estrogen receptor-alpha. J Biol Chem 2006; 281: 9607-9615.
58. Chin SF, Teschendorff AE, Marioni JC, Wang Y, Barbosa-Morais NL, Thorne NP et al. High-resolution aCGH and expression profiling identifies a novel genomic subtype of ER negative breast cancer. Genome Biol 2007; 8: R215.
59. Clancy JL, Henderson MJ, Russell AJ, Anderson DW, Bova RJ, Campbell IG et al. EDD, the human orthologue of the hyperplastic discs tumour suppressor gene, is amplified and overexpressed in cancer. Oncogene 2003; 22: 5070-5081.
60. de Hoon MJ, Imoto S, Nolan J, Miyano S. Open source clustering software. Bioinformatics (Oxford, England) 2004; 20: 1453-1454.
61. Saldanha AJ. Java Treeview-extensible visualization of microarray data. Bioinformatics (Oxford, England) 2004; 20: 3246-3248.