Cross talk in hormonally regulated gene transcription through induction of estrogen receptor ubiquitylation

Molecular and Cellular Biology

Volumn 25, Issue 16, 2005, Pages 7386-7398

  Luo, Min ^a   Koh, Mingshi ^a   Feng, Jiajun ^a   Wu, Qiang ^a   Melamed, Philippa ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; GONADORELIN; GONADOTROPIN; LUTEINIZING HORMONE BETA SUBUNIT; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PITX1; TRANSCRIPTION FACTOR SF 1; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ESTROGEN RESPONSIVE ELEMENT; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE INDUCTION; GENE OVEREXPRESSION; HORMONAL REGULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSACTIVATION; TRANSCRIPTION REGULATION; UBC4 GENE; UBIQUITINATION;

ANIMALS; BLOTTING, WESTERN; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; COS CELLS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GONADOTROPIN-RELEASING HORMONE; HOMEODOMAIN PROTEINS; HORMONES; IMMUNOPRECIPITATION; LIGANDS; MICE; MODELS, BIOLOGICAL; MODELS, GENETIC; NUCLEIC ACID HYBRIDIZATION; PAIRED BOX TRANSCRIPTION FACTORS; PLASMIDS; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECEPTORS, ESTROGEN; RESPONSE ELEMENTS; TIME FACTORS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; TWO-HYBRID SYSTEM TECHNIQUES; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES;

MAMMALIA;

EID: 23344441591     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.25.16.7386-7398.2005     Document Type: Article

References (64)

1. Anan, T., Y. Nagata, H. Koga, Y. Honda, N. Yabuki, C. Miyamoto, A. Kuwano, I. Matsudam, F. Endo, H. Saya, and M. Nakao. 1998. Human ubiquitin-protein ligase Nedd4: expression, subcellular localization and selective interaction with ubiquitin-conjugating enzymes. Genes Cells 3:751-763.
2. Brower, C. S., S. Sato, C. Tomomori-Sato, T. Kaniura, A. Pause, R. Stearman, R. D. Klausner, S. Malik, W. S. Lane, I. Sorokina, R. G. Roeder, J. W. Conaway, and R. C. Conaway. 2002. Mammalian mediator subunit mMED8 is an Elongin BC-interacting protein that can assemble with Cul2 and Rbx1 to reconstitute a ubiquitin ligase. Proc. Natl. Acad. Sci. USA 99:10353-10358.
3. Brown, P., and A. S. McNeilly. 1999. Transcriptional regulation of pituitary gonadolrophin subunit genes. Rev. Reprod. 4:117-124.
4. Colin, I. M., and J. L. Jameson. 1998. Estradiol sensitization of rat pituitary cells to gonadotropin-releasing hormone: involvement of protein kinase C- and calcium-dependent signaling pathways. Endocrinology 139:3796-3802.
5. Conaway, R. C., C, S. Brower, and J. W. Conaway. 2002. Gene expression-emerging roles of ubiquitin in transcription regulation. Science 296:1254-1258.
6. Cowley, M. A., C. Chen, and I, J. Clarke. 1999. Estrogen transiently increases delayed rectifier, voltage-dependent potassium currents in ovine gonadotropes. Neuroendocrinology 69:254-260.
7. Curtin, D., H. A. Ferris, M. Hakli, M. Gibson, O. A. Janne, J. J. Palvimo, and M. A. Shupnik. 2004. Small nuclear RING ringer protein stimulates the rat luteinizing hormone β promoter by interacting with Sp1 and steroidogenic factor-1 and protects from androgen suppression. Mol. Endocrinol. 18:1263-1276.
8. de Jager, T., T. Pelzer, S. Muller-Botz, A. Imam, J. Muck, and L. Neyses. 2001. Mechanisms of estrogen receptor action in the myocardium. Rapid gene activation via the ERK1/2 pathway and serum response elements. J. Biol. Chem. 276:27873-27880.
9. Demay, F., M. De Monti, C. Tiffoche, C. Vaillant, and M. L. Thieulant. 2001. Steroid-independent activation of ER by GnRH in gonadotrope pituitary cells. Endocrinology 142:3340-3347.
10. Di Fiore, P. P., S. Polo, and K. Hofmann. 2003. When ubiquitin meets ubiquitin receptors: a signalling connection. Nat. Rev. Mol. Cell Biol. 4:491-497.
11. Dorn, C., Q. L. Ou, J. Svaren, P. A. Crawford, and Y. Sadovsky. 1999. Activation of luteinizing hormone α gene by gonadotropin-releasing hormone requires the synergy of early growth response-1 and steroidogenic factor-1. J. Biol. Chem. 274:13870-13876.
12. Fan, M. Y., R. M. Bigsby, and K. P. Nephew. 2003. The NEDD8 pathway is required for proteasome-mediated degradation of human estrogen receptor (ER) α and essential for the anti proliferative activity of IC1 182,780 in ER α-positive breast cancer cells. Mol. Endocrinol. 17:356-365.
13. Fan, M. Y., H. Nakashatri, and K. P. Nephew. 2004. Inhibiting proteasomal proteolysis sustains estrogen receptor-α activation. Mol. Endocrinol. 18:2603-2615.
14. Ferdous, A., F. Gonzalez, L. P. Sun, T. Kodadek, and S. A. Johnston. 2001. The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. Mol. Cell 7:981-991.
15. Gharib, S. D., M. E. Wierman, M. A. Shupnik, and W. W. Chin. 1990. Molecular biology of the pituitary gonadotropins. Endocr. Rev. 11:177-199.
16. Gonzalez, F., A. Delahodde, T. Kodadek, and S. A. Johnston. 2002. Recruitment of a 19S proteasome subcomplex to an activated promoter. Science 296:548-550.
17. Grossman, S. R., M. E. Deato, C. Brignone, H. M. Chan, A. L. Kung, H. Taganii, Y. Nakatani, and D. M. Livingston. 2003. Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science 300:342-344.
18. Hakli, M., K. L. Lorick, A. M. Weissman, O. A. Janne, and J. H. Palvimo. 2004. Transcriptional coregulator SNURF (RNF4) possesses ubiquitin E3 ligasc activity. FEBS Lett. 560:56-62.
19. Hall, J. M., J. F. Couse, and K. S. Koraeh. 2001. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 276:36869-36872.
20. Halvorson, L. M., M. Ito, J. L. Jameson, and W. W. Chin. 1998. Steroidogenic factor-1 and early growth response protein 1 act through two composite DNA binding sites to regulate luteinizing hormone β-subunit gene expression. J. Biol Chem. 273:14712-14720.
21. Hicke, L. 2001. Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2:195-201.
22. Hirvonen-Santti, S. J., V. Sriraman, M. Anttonen, S. Savolainen, J. J. Palvimo, M. Heikinheimo, J. S. Richards, and O. A. Janne. 2004. Small nuclear RING finger protein expression during gonad development: regulation by gonadotropins and estrogen in the postnatal ovary. Endocrinology 145:2433-2444.
23. Jorgensen, J. S., and J. H. Nilson. 2001. AR suppresses transcription of the LHβ subunit by interacting with steroidogenic factor-1. Mol. Endocrinol. 15:1505-1516.
24. Kawakami, T., T. Chiba, T. Suzuki, K. Iwai, K. Yamanaka, N. Minato, H. Suzuki, N. Shimbara, Y. Hidaka, F. Osaka, M. Oniata, and K. Tanaka. 2001. NEDD8 recruits E2-ubiquitin to SCF E3 ligase. EMBO J. 20:4003-4012.
25. Keri, R. A., M. W. Wulfe, T. L. Saunders, I. Andersen, S. K. Kendall, T. Wagner, J. Yeung, J. Gorski, T. M. Nett, S. A. Camper, and J. H. Neilsun. 1994. The proximal promoter of the bovine luteinizing hormone β-subunit gene confers gonadotrope-specific expression and regulation by gonadotropin-releasing hormone, testosterone, and 17β-estradiol in transgenic mice. Mol. Endocrinol. 8:1807-1816.
26. Koegl, M., T. Hoppe, S. Schlenker, H. D. Ulrich, T. U. Mayer, and S. Jentsch. 1999. A novel ubiquitylation factor, E4, is involved in multiubiquitin chain assembly. Cell 96:635-644.
27. Le Dréan, Y., D. Liu, A. O. L. Wong, F. Xiong, and C. L. Hew. 1996. Steroidogenic factor 1 and estradiol receptor act in synergism to regulate the expression of the salmon gonadotropin IIβ subunit gene. Mol. Endocrinol. 10:217-229.
28. Le Dréan, Y., D. Liu, F, Xiong, and C. L. Hew. 1997. Presence of cis-acting elements on gonadotropin gene promoters in diverse species dictates the selective recruitment of different transcription factors by steroidogenic factor-1. Mol. Cell. Endocrinol. 135:31-40.
29. Li, M. Y., C. L. Brooks, F. Wu-Baer, D. L. Chen, R. Baer, and W. Gu. 2003. Mono- versus polyubiquitylation: differential control of p53 fate by Mdm2. Science 302:1972-1975.
30. Lipford, J. R., and R. J. Deshaies. 2003. Diverse roles for ubiquilin-dependent proteolysis in transcriptional activation. Nat. Cell Biol. 5:845-850.
31. Liu, D., F. Xiong, and C. L. Hew. 1995. Functional analysis of estrogen responsive elements in Chinook salmon (Oncorhynchus tschawytscha) gonadotropin IIβ subunit gene. Endocrinology 136:3486-3493.
32. Lonard, D. M., Z. Nawaz, C. L. Smith, and B. W. O'Malley. 2000. The 26S proteasome is required for estrogen receptor α and coactivator turnover and for efficient estrogen receptor α transactivation. Mol. Cell 5:939-948.
33. Lu, Q., H. Ebling, J. Mittler, W. E. Baur, and R. H. Karas. 2002. MAP kinase mediates growth factor-induced nuclear translocation of estrogen receptor α. FEBS Lett. 516:1-8.
34. Marsaud, V., A. Gougelet, S. Maillard, and J. M. Renoir. 2003. Various phosphorylation pathways, depending on agonist and antagonist binding to endogenous estrogen receptor α (ERα), differentially affect ERα extractability, proteasome-mediated stability, and transcriptional activity in human breast cancer cells. Mol. Endocrinol. 17:2013-2027.
35. Melamed, P., M. Koh, P. Preklathan, L. Bei, and C. L. Hew. 2002. Multiple mechanisms for Pitx-1 transactivation of a luteinizing hormone β subunit gene. J. Biol. Chem. 277:26200-26207.
36. Métivier, R., F. A. Gay, M. R. Hubner, G. Flouriot, G. Salbert, F. Gannon, O. Kah, and F. Pakdel. 2002. Formation of an hER α-COUP-TFI complex enhances hERα AF-1 through Ser118 phosphorylation by MAPK. EMBO J. 21:3443-3453.
37. Métivier, R., G. Penot, M. R. Hubner, G. Reid, H. Brand, M. Kos, and F. Gannon. 2003. Estrogen receptor α directs ordered, cyclical, and combinatorial recruitment of cofaetors on a natural target promoter. Cell 115:751-763.
38. Muratani, M., and W. R. Tansey. 2003. How the ubiquitin-proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4:192-201.
39. Naor, Z., O. Benard, and R. Seger. 2000. Activation of MAPK cascades by G-protein-coupled receptors: the ease of gonadotropin-releasing hormone receptor. Trends Endocrinol. Metab. 11:91-99.
40. Nawaz, Z., and B. W. O'Malley. 2004. Urban renewal in the nucleus: is protein turnover by proteasomes absolutely required for nuclear receptor-regulated transcription? Mol. Endocrinol. 18:493-499.
41. Nawaz, Z., D. M. Lonard, A. P. Dennis, C. L. Smith, and B. W. O'Malley. 1999. Proteasome-dependent degradation of the human estrogen receptor. Proc. Natl. Acad. Sci. USA 96:1858-1862.
42. Ortolan, T. G., P. Tongaonkar, D. Lambertson, L. Chen, C. Schauber, and K. Madura. 2000. The DNA repair protein Rad23 is a negative regulator of multi-ubiquitin chain assembly. Nat. Cell Biol. 2:601-608.
43. Ottosen, S., F. J. Herrera, and S. J. Triezenberg. 2002. Transcription: proteasome parts at gene promoters. Science 296:479-481.
44. Perissi, V., A. Aggarwal, C. K. Glass, D. W. Rose, and M. G. Rosenfeld. 2004. A corepressor/coactivator exchange complex required for transcriptional activation hy nuclear receptors and other regulated transcription factors. Cell 116:511-526.
45. Pratt, M. A. C., A. Satkunaratnam, and D. M. Novosad. 1998. Estrogen activates raf-1 kinase and induces expression of Egr-1 in MCF-7 breast cancer cells. Mol. Cell. Biochem. 189:119-125.
46. Quirk, C. C., K. L. Lozada, R. A. Keri, and J. H. Nilson. 2001. A single Pitx1 binding site is essential for activity of the LH beta promoter in transgenic mice. Mol. Endocrinol. 15:734-746.
47. Rajapurohitam, V., N. Bedard, and S. S. Wing. 2002. Control of ubiquitylation of proteins in rat tissues by ubiquitylation conjugating enzymes and isopeptidases. Am. J. Physiol. Endocrinol. Metab. 282:E739-E745.
48. Reid, G., M. R. Hubner, R. Métivier, H. Brand, S. Denger, D. Manu, J. Beaudouin, J. Ellenberg, and F. Gannon. 2003. Cyclin, proteasome mediated turnover of unliganded and liganded ERα on responsive promoters is an integral feature of estrogen signaling. Mol. Cell 11:695-707.
49. Salghetti, S. E., M. Muratani, H. Wijnen, B. Futcher, and W. P. Tansey. 2000. Functional overlap of sequences that activate transcription and signal ubiquitin-mediated proteolysis. Proc. Natl. Acad. Sci. USA 97:3118-3123.
50. Salghetti, S. E., A. A. Caudy, J. G. Chenoweth, and W. P. Tansey. 2001. Regulation of transcriptional activation domain function by ubiquitin. Science 293:1651-1653.
51. Seville, B., H. Poukka, M. Wormke, O. A. Janne, J. J. Palvimo, M. Stoner, I. Samudio, and S. Safe. 2002. Cooperative coactivation of estrogen receptor α in ZR-75 human breast cancer cells by SNURF and TATA-binding protein. J. Biol. Chem. 277:2485-2497.
52. Schnell, J. D., and E. Hicke. 2003. Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J. Biol. Chem. 278:35857-35860.
53. Schreihofer, D. A., E. M. Resnick, Y. Y. Ein, and M. A. Shupnik. 2001. Ligand-independent activation of pituitary ER: dependence on PKA-stimulated pathways. Endocrinology 142:3361-3368.
54. Shang, Y. F., X. Hu, J. DiRenzo, M. A. Lazar, and M. Brown. 2000. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103:843-852.
55. Shupnik, M. A., and B. A. Rosenzweig. 1991. Identification of an estrogen-responsive element in the rat LHβ gene-DNA-estrogen receptor interactions and functional analysis. J. Biol. Chem. 266:17084-17091.
56. Smith, C. L., D. G. DeVera, D. J. Lamb, Z. Nawaz, Y. H. Jiang, A. E. Beaudet, and B. W. O'Malley. 2002. Genetic ablation of the steroid receptor coactivator-ubiquitin ligase, E6-AP, results in tissue-selective steroid hormone resistance and defects in reproduction. Mol. Cell. Biol. 22:525-535.
57. Strack, P., M. Caligiuri, M. Pelletier, M. Boisclair, A. Theodoras, P. Beer-Romero, S. Glass, T. Parsons, R. A. Copeland, K. R. Auger, P. Benfield, L. Brizuela, and M. Rolfe. 2000. SCF beta-TRCP and phosphorylation dependent ubiquitylation of I kappa B alpha catalyzed by Ubc3 and Ubc4. Oncogene 19:3529-3536.
58. Tremblay, J. J., and J. Drouin. 1999. Egr-1 is a downstream effector of GnRH and synergizes by direct interaction with Ptx and Sf-1 to enhance luteinizing hormone β gene transcription. Mol. Cell. Biol. 19:2567-2576.
59. Tremblay, J. J., A. Marcil, Y. Gauthier, and J. Drouin. 1999 Ptx-1 regulates SF-1 activity by an interaction that mimics the role of the ligand-binding domain. EMBO J. 18:3431-3441.
60. Verma, S., A. Ishmail, X. Gao, G. Fu, X. Li, B. W. O'Malley, and Z. Nawaz. 2004. The ubiquitin-conjugating enzyme UBCH7 acts as a coactivator for steroid hormone receptors. Mol. Cell. Biol. 24:8716-8726.
61. Weissnian, A. M. 2001. Themes and variations on ubiquitylation. Nat. Rev. Mol. Cell Biol. 2:169-178.
62. Wijayaratne, A. L., and D. P. McDonnell. 2001. The human estrogen receptor α is a ubiquitinated protein whose stability is affected differentially by agonists, antagonists, and selective estrogen receptor modulators. J. Biol. Chem. 276:35684-35692.
63. Wojcikiewicz, R. J. H., Q. Xu, J. M. Webster, K. Alzayady, and C. Gao. 2003. Ubiquitylation and proteasomal degradation of endogenous and exogenous inositol 1,4,5-trisphosphate receptors in αT3-1 anterior pituitary cells. J. Biol. Chem. 278:940-947.
64. Xiong, F., D. Liu, H. P. Elsholtz, and C. L. Hew. 1994. The Chinook salmon gonadotropin IIβ gene contains a strong minimal promoter with a proximal negative element. Mol. Endocrinol. 8:771-781.