Inhibiting proteasomal proteolysis sustains estrogen receptor-α activation

Molecular Endocrinology

Volumn 18, Issue 11, 2004, Pages 2603-2615

  Fan, Meiyun ^a   Nakshatri, Harikrishna ^b,c   Nephew, Kenneth P ^a,b,c  

^a Indiana University School of Medicine   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIESTROGEN; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BETA GALACTOSIDASE; CATHEPSIN D; CHLORAMPHENICOL ACETYLTRANSFERASE; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; HYDROXYTAMOXIFEN; LUCIFERASE; PROGESTERONE RECEPTOR; PROTEASOME; PROTEIN PS2; UBIQUITIN;

ARTICLE; CELL STRAIN MCF 7; CONTROLLED STUDY; DOSE RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; ESTROGEN RESPONSIVE ELEMENT; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HELA CELL; HORMONE SENSITIVITY; HUMAN; HUMAN CELL; LIGAND BINDING; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; RECEPTOR UPREGULATION; REPORTER GENE; UBIQUITINATION;

CATHEPSIN D; CELL LINE, TUMOR; CYSTEINE PROTEINASE INHIBITORS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION REGULATION; HUMANS; LEUPEPTINS; MEMBRANE PROTEINS; PRESENILIN-2; PROMOTER REGIONS (GENETICS); PROTEASOME ENDOPEPTIDASE COMPLEX; RECEPTORS, PROGESTERONE; TAMOXIFEN; UBIQUITINS;

MINK CELL FOCUS-FORMING VIRUS;

EID: 8344241132     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2004-0164     Document Type: Article

References (71)

1. McKenna NJ, O'Malley BW 2001 Nuclear receptors, coregulators, ligands, and selective receptor modulators: making sense of the patchwork quilt. Ann NY Acad Sci 949:3-5
2. Webb P, Lopez GN, Greene GL, Baxter JD, Kushner PJ 1992 The limits of the cellular capacity to mediate an estrogen response. Mol Endocrinol 6:157-167
3. Klinge CM 2000 Estrogen receptor interaction with co-activators and co-repressors. Steroids 65:227-251
4. Saceda M, Lippman ME, Chambon P, Lindsey RL, Ponglikitmongkol M, Puente M, Martin MB 1988 Regulation of the estrogen receptor in MCF-7 cells by estradiol. Mol Endocrinol 2:1157-1162
5. Pink JJ, Jordan VC 1996 Models of estrogen receptor regulation by estrogens and antiestrogens in breast cancer cell lines. Cancer Res 56:2321-2330
6. Nephew KP, Long X, Osborne E, Burke KA, Ahluwalia A, Bigsby RM 2000 Effect of estradiol on estrogen receptor expression in rat uterine cell types. Biol Reprod 62: 168-177
7. Lonard DM, Nawaz Z, Smith CL, O'Malley BW 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
8. Nawaz Z, Lonard DM, Dennis AP, Smith CL, O'Malley BW 1999 Proteasome-dependent degradation of the human estrogen receptor. Proc Natl Acad Sci USA 96: 1858-1862
9. Alarid ET, Bakopoulos N, Solodin N 1999 Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation. Mol Endocrinol 13:1522-1534
10. El Khissiin A, Leclercq G 1999 Implication of proteasome in estrogen receptor degradation. FEBS Lett 448: 160-166
11. Wijayaratne AL, McDonnell DP 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
12. Muratani M, Tansey WP 2003 How the ubiquitin-proteasome system controls transcription. Nat Rev Mol Cell Biol 4:192-201
13. Conaway RC, Brower CS, Conaway JW 2002 Emerging roles of ubiquitin in transcription regulation. Science 296: 1254-1258
14. Tansey WP 2001 Transcriptional activation: risky business. Genes Dev 15:1045-1050
15. Salghetti SE, Muratani M, Wijnen H, Futcher B, Tansey WP 2000 Functional overlap of sequences that activate transcription and signal ubiquitin-mediated proteolysis. Proc Natl Acad Sci USA 97:3118-3123
16. Salghetti SE, Caudy AA, Chenoweth JG, Tansey WP 2001 Regulation of transcriptional activation domain function by ubiquitin. Science 293:1651-1653
17. Wallace AD, Cidlowski JA 2001 Proteasome-mediated glucocorticoid receptor degradation restricts transcriptional signaling by glucocorticoids. J Biol Chem 276: 42714-42721
18. Pollenz RS 2002 The mechanism of AH receptor protein down-regulation (degradation) and its impact on AH receptor-mediated gene regulation. Chem Biol Interact 141:41-61
19. Blanquart C, Barbier O, Fruchart JC, Staels B, Glineur C 2002 Peroxisome proliferator-activated receptor α (PPARα) turnover by the ubiquitin-proteasome system controls the ligand-induced expression level of its target genes. J Biol Chem 277:37254-37259
20. Boudjelal M, Voorhees JJ, Fisher GJ 2002 Retinoid signaling is attenuated by proteasome-mediated degradation of retinoid receptors in human keratinocyte HaCaT cells. Exp Cell Res 274:130-137
21. 3 receptors by blocking ubiquitin/proteasome-mediated degradation in human skin. Mol Endocrinol 13:1686-1694
22. Kang Z, Pirskanen A, Janne OA, Palvimo JJ 2002 Involvement of proteasome in the dynamic assembly of the androgen receptor transcription complex. J Biol Chem 277:48366-48371
23. Lin HK, Altuwaijri S, Lin WJ, Kan PY, Collins LL, Chang C 2002 Proteasome activity is required for androgen receptor transcriptional activity via regulation of androgen receptor nuclear translocation and interaction with coregulators in prostate cancer cells. J Biol Chem 277: 36570-36576
24. Stavreva DA, Muller WG, Hager GL, Smith CL, McNally JG 2004 Rapid glucocorticoid receptor exchange at a promoter is coupled to transcription and regulated by chaperones and proteasomes. Mol Cell Biol 24: 2682-2697
25. Ciechanover A, Orian A, Schwartz AL 2000 Ubiquitin-mediated proteolysis: biological regulation via destruction. Bioessays 22:442-451
26. Molinari E, Gilman M, Natesan S 1999 Proteasome-mediated degradation of transcriptional activators correlates with activation domain potency in vivo. EMBO J 18:6439-6447
27. Nawaz Z, Lonard DM, Smith CL, Lev-Lehman E, Tsai SY, Tsai MJ, O'Malley BW 1999 The Angelman syndrome-associated protein, E6-AP, is a coactivator for the nuclear hormone receptor superfamily. Mol Cell Biol 19: 1182-1189
28. Grossman SR, Deato ME, Brignone C, Chan HM, Kung AL, Tagami H, Nakatani Y, Livingston DM 2003 Polyubiquitination of p53 by a ubiquitin ligase activity of p300. Science 300:342-344
29. Hanstein B, Eckner R, DiRenzo J, Halachmi S, Liu H, Searcy B, Kurokawa R, Brown M 1996 p300 is a component of an estrogen receptor coactivator complex. Proc Natl Acad Sci USA 93:11540-11545
30. Ruffner H, Joazeiro CA, Hemmati D, Hunter T, Verma IM 2001 Cancer-predisposing mutations within the RING domain of BRCA1: loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. Proc Natl Acad Sci USA 98:5134-5139
31. Fan S, Wang J, Yuan R, Ma Y, Meng Q, Erdos MR, Pestell RG, Yuan F, Auborn KJ, Goldberg ID, Rosen EM 1999 BRCA1 inhibition of estrogen receptor signaling in transfected cells. Science 284:1354-1356
32. Fraser RA, Rossignol M, Heard DJ, Egly JM, Chambon P 1997 SUG1, a putative transcriptional mediator and subunit of the PA700 proteasome regulatory complex, is a DNA helicase. J Biol Chem 272:7122-7126
33. Saji S, Okumura N, Eguchi H, Nakashima S, Suzuki A, Toi M, Nozawa Y, Hayashi S 2001 MDM2 enhances the function of estrogen receptor α in human breast cancer cells. Biochem Biophys Res Commun 281:259-265
34. Masuyama H, Hiramatsu Y 2004 Involvement of suppressor for Gal 1 in the ubiquitin/proteasome-mediated degradation of estrogen receptors. J Biol Chem 279: 12020-12026
35. Reid G, Hubner MR, Metivier R, Brand H, Denger S, Manu D, Beaudouin J, Ellenberg J, Gannon F 2003 Cyclic, proteasome-mediated turnover of unliganded and liganded ERα on responsive promoters is an integral feature of estrogen signaling. Mol Cell 11:695-707
36. Deroo BJ, Archer TK 2002 Proteasome inhibitors reduce luciferase and β-galactosidase activity in tissue culture cells. J Biol Chem 277:20120-20123
37. Laios I, Journe F, Laurent G, Nonclercq D, Toillon RA, Seo HS, Leclercq G 2003 Mechanisms governing the accumulation of estrogen receptor α in MCF-7 breast cancer cells treated with hydroxytamoxifen and related antiestrogens. J Steroid Biochem Mol Biol 87:207-221
38. Frasor J, Stossi F, Danes JM, Komm B, Lyttle CR, Katzenellenbogen BS 2004 Selective estrogen receptor modulators: discrimination of agonistic versus antagonistic activities by gene expression profiling in breast cancer cells. Cancer Res 64:1522-1533
39. Alarid ET, Preisler-Mashek MT, Solodin NM 2003 Thyroid hormone is an inhibitor of estrogen-induced degradation of estrogen receptor-α protein: estrogen-dependent proteolysis is not essential for receptor transactivation function in the pituitary. Endocrinology 144:3469-3476
40. Schreihofer DA, Resnick EM, Un VY, Shupnik MA 2001 Ligand-independent activation of pituitary ER: dependence on PKA-stimulated pathways. Endocrinology 142: 3361-3368
41. Wada H, Yeh ET, Kamitani T 2000 A dominant-negative UBC12 mutant sequesters NEDD8 and inhibits NEDD8 conjugation in vivo. J Biol Chem 275:17008-17015
42. Fan M, Bigsby RM, Nephew KP 2003 The NEDD8 pathway is required for proteasome-mediated degradation of human estrogen receptor (ER)-α and essential for the antiproliferative activity of ICI 182,780 in ERα-positive breast cancer cells. Mol Endocrinol 17:356-365
43. Bloom J, Amador V, Bartolini F, DeMartino G, Pagano M 2003 Proteasome-mediated degradation of p21 via N-terminal ubiquitinylation. Cell 115:71-82
44. Thompson JF, Hayes LS, Lloyd DB 1991 Modulation of firefly luciferase stability and impact on studies of gene regulation. Gene 103:171-177
45. Berry M, Nunez AM, Chambon P 1989 Estrogen-responsive element of the human pS2 gene is an imperfectly palindromic sequence. Proc Natl Acad Sci USA 86: 1218-1222
46. Brown AM, Jeltsch JM, Roberts M, Chambon P 1984 Activation of pS2 gene transcription is a primary response to estrogen in the human breast cancer cell line MCF-7. Proc Natl Acad Sci USA 81:6344-6348
47. Lipson KE, Baserga R 1989 Transcriptional activity of the human thymidine kinase gene determined by a method using the polymerase chain reaction and an intron-specific probe. Proc Natl Acad Sci USA 86:9774-9777
48. Tian Y, Ke S, Thomas T, Meeker RJ, Gallo MA 1998 Transcriptional suppression of estrogen receptor gene expression by 2,3,7,8-tetrachlorodibenzo- p-dioxin (TCDD). J Steroid Biochem Mol Biol 67:17-24
49. Elferink CJ, Reiners Jr JJ 1996 Quantitative RT-PCR on CYP1A1 heterogeneous nuclear RNA: a surrogate for the in vitro transcription run-on assay. Biotechniques 20: 470-477
50. Delany AM 2001 Measuring transcription of metalloproteinase genes. Nuclear run-off assay vs analysis of hnRNA. Methods Mol Biol 151:321-333
51. Anzai Y, Holinka CF, Kuramoto H, Gurpide E 1989 Stimulatory effects of 4-hydroxytamoxifen on proliferation of human endometrial adenocarcinoma cells (Ishikawa line). Cancer Res 49:2362-2365
52. Jamil A, Croxtall JD, White JO 1991 The effect of anti-oestrogens on cell growth and progesterone receptor concentration in human endometrial cancer cells (Ishikawa). J Mol Endocrinol 6:215-221
53. Shang Y, Brown M 2002 Molecular determinants for the tissue specificity of SERMs. Science 295:2465-2468
54. Barkhem T, Haldosen LA, Gustafsson JA, Nilsson S 2002 pS2 Gene expression in HepG2 cells: complex regulation through crosstalk between the estrogen receptor a, an estrogen-responsive element, and the activator protein 1 response element. Mol Pharmacol 61:1273-1283
55. Lee YJ, Gorski J 1996 Estrogen-induced transcription of the progesterone receptor gene does not parallel estrogen receptor occupancy. Proc Natl Acad Sci USA 93: 15180-15184
56. Makino Y, Yogosawa S, Kayukawa K, Coin F, Egly JM, Wang Z, Roeder RG, Yamamoto K, Muramatsu M, Tamura T 1999 TATA-binding protein-interacting protein 120, TIP120, stimulates three classes of eukaryotic transcription via a unique mechanism. Mol Cell Biol 19: 7951-7960
57. Russell SJ, Johnston SA 2001 Evidence that proteolysis of Gal4 cannot explain the transcriptional effects of proteasome ATPase mutations. J Biol Chem 276:9825-9831
58. Ferdous A, Gonzalez F, Sun L, Kodadek T, Johnston SA 2001 The 19S regulatory particle of the proteasome is required for efficient transcription elongation by RNA polymerase II. Mol Cell 7:981-991
59. Gonzalez F, Delahodde A, Kodadek T, Johnston SA 2002 Recruitment of a 19S proteasome subcomplex to an activated promoter. Science 296:548-550
60. Ferdous A, Kodadek T, Johnston SA 2002 A nonproteolytic function of the 19S regulatory subunit of the 26S proteasome is required for efficient activated transcription by human RNA polymerase II. Biochemistry 41: 12798-12805
61. Van F, Gao X, Lonard DM, Nawaz Z 2003 Specific ubiquitin-conjugating enzymes promote degradation of specific nuclear receptor coactivators. Mol Endocrinol 17: 1315-1331
62. Katzenellenbogen BS, Kendra KL, Norman MJ, Berthois Y 1987 Proliferation, hormonal responsiveness, and estrogen receptor content of MCF-7 human breast cancer cells grown in the short-term and long-term absence of estrogens. Cancer Res 47:4355-4360
63. Panno ML, Salerno M, Pezzi V, Sisci D, Maggiolini M, Mauro L, Morrone EG, Ando S 1996 Effect of oestradiol and insulin on the proliferative pattern and on oestrogen and progesterone receptor contents in MCF-7 cells. J Cancer Res Clin Oncol 122:745-749
64. Clarke RB, Howell A, Potten CS, Anderson E 1997 Dissociation between steroid receptor expression and cell proliferation in the human breast. Cancer Res 57: 4987-4991
65. Shoker BS, Jarvis C, Clarke RB, Anderson E, Hewlett J, Davies MP, Sibson DR, Sloane JP 1999 Estrogen receptor-positive proliferating cells in the normal and precancerous breast. Am J Pathol 155:1811-1815
66. Shoker BS, Jarvis C, Clarke RB, Anderson E, Munro C, Davies MP, Sibson DR, Sloane JP 2000 Abnormal regulation of the oestrogen receptor in benign breast lesions. J Clin Pathol 53:778-783
67. Fan M, Long X, Bailey JA, Reed CA, Osborne E, Gize EA, Kirk EA, Bigsby RM, Nephew KP 2002 The activating enzyme of NEDD8 inhibits steroid receptor function. Mol Endocrinol 16:315-330
68. Klein-Hitpass L, Tsai SY, Greene GL, Clark JH, Tsai MJ, O'Malley BW 1989 Specific binding of estrogen receptor to the estrogen response element. Mol Cell Biol 9:43-49
69. Rajendran RR, Nye AC, Frasor J, Balsara RD, Martini PG, Katzenellenbogen BS 2003 Regulation of nuclear receptor transcriptional activity by a novel DEAD box RNA helicase (DP97). J Biol Chem 278:4628-4638
70. Aerts JL, Christiaens MR, Vandekerckhove P 2002 Evaluation of progesterone receptor expression in eosinophils using real-time quantitative PCR. Biochim Biophys Acta 1571:167-172
71. Augereau P, Miralles F, Cavailles V, Gaudelet C, Parker M, Rochefort H 1994 Characterization of the proximal estrogen-responsive element of human cathepsin D gene. Mol Endocrinol 8:693-703