Distinctive actions of membrane-targeted versus nuclear localized estrogen receptors in breast cancer cells

Molecular Endocrinology

Volumn 19, Issue 6, 2005, Pages 1606-1617

  Rai, Deshanie ^a,c   Frolova, Antonina ^a   Frasor, Jonna ^a   Carpenter, Anne E ^b,d   Katzenellenbogen, Benita S ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c BRISTOL MYERS SQUIBB   (United States)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIESTROGEN; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; RECEPTOR SUBUNIT;

ACETYLATION; ARTICLE; CANCER CELL CULTURE; CELL LINE; CELL MEMBRANE; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOPLASM; DNA FLANKING REGION; DNA SEQUENCE; DOWN REGULATION; GENE EXPRESSION REGULATION; HORMONE ACTION; HORMONE BINDING; HUMAN; HUMAN CELL; MYRISTYLATION; NUCLEAR LOCALIZATION SIGNAL; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN FUNCTION; RECEPTOR AFFINITY; SERUM; TRANSCRIPTION INITIATION; UPREGULATION;

BLOTTING, WESTERN; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MEMBRANE; CELL NUCLEUS; CELL PROLIFERATION; CYTOPLASM; DNA; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; ESTROGENS; HUMANS; IMMUNOHISTOCHEMISTRY; KINETICS; MICROSCOPY, FLUORESCENCE; MYRISTIC ACID; NUCLEAR LOCALIZATION SIGNALS; PALMITIC ACID; PHOSPHORYLATION; PLASMIDS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ESTROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SERUM RESPONSE ELEMENT; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTION, GENETIC; TRANSFECTION; UP-REGULATION;

EID: 22344449234     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2004-0468     Document Type: Article

References (60)

1. Osborne CK 1998 Tamoxifen in the treatment of breast cancer. N Engl J Med 339:1609-1618
2. Katzenellenbogen BS, Frasor J 2004 Therapeutic targeting in the estrogen receptor hormonal pathway. Semin Oncol 31:28-38
3. Hall JM, Couse JF, Korach KS 2001 The multifaceted mechanisms of estradiol and estrogen receptor signaling. J Biol Chem 276:36869-36872
4. Katzenellenbogen BS, Katzenellenbogen JA 2000 Estrogen receptor transcription and transactivation: estrogen receptor and estrogen receptor β: regulation by selective estrogen receptor modulators and importance in breast cancer. Breast Cancer Res 2:335-344
5. Weisz A, Rosales R 1990 Identification of an estrogen response element upstream of the human c-fos gene that binds the estrogen receptor and the AP-1 transcription factor. Nucleic Acids Res 18:5097-5106
6. Pfahl M 1993 Nuclear receptor/AP-1 interaction. Endocr Rev 14:651-658
7. Duan R, Porter W, Safe S 1998 Estrogen-induced c-fos protooncogene expression in MCF-7 human breast cancer cells: role of estrogen receptor Sp1 complex formation. Endocrinology 139:1981-1990
8. Edwards DP 2005 Regulation of signal transduction pathways by estrogen and progesterone. Annu Rev Physiol 67:23.1-23.42
9. Pietras RJ, Szego CM 1975 Endometrial cell calcium and oestrogen action. Nature 253:357-359
10. Pappas TC, Gametchu B, Watson CS 1995 Membrane estrogen receptors identified by multiple antibody labeling and impeded-ligand binding. FASEB J 9:404-410
11. Razandi M, Pedram A, Greene GL, Levin ER 1999 Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: Studies of ER and ER expressed in Chinese hamster ovary cells. Mol Endocrinol 13:307-319
12. Pietras RJ, Szego CM 1979 Metabolic and proliferative responses to estrogen by hepatocytes selected for plasma membrane binding-sites specific for estradiol-17β. J Cell Physiol 98:145-159
13. Migliaccio A, Di Domenico M, Castoria G, de Flaco A, Bontempo P, Nola E, Auricchio F 1996 Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells. EMBO J 15:1292-1300
14. Vasudevan N, Kow LM, Pfaff DW 2001 Early membrane estrogenic effects required for full expression of slower genomic actions in a nerve cell line. Proc Natl Acad Sci USA 98:12267-12271
15. Le Mellay V, Grosse B, Lieberherr M 1997 Phospholipase Cβ and membrane action of calcitriol and estradiol. J Biol Chem 272:11902-11907
16. Levin ER 1999 Cellular functions of the plasma membrane estrogen receptor. Trends Endocrinol Metab 10: 374-377
17. Pietras RJ, Szego CM 1977 Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature 265:69-72
18. Pietras RJ, Szego CM 1980 Partial purification and characterization of oestrogen receptors in subfractions of hepatocyte plasma membranes. Biochem J 191:743-760
19. Razandi M, Oh P, Pedram A, Schnitzer J, Levin ER 2002 ERs associate with and regulate the production of caveolin: implications for signaling and cellular actions. Mol Endocrinol 16:100-115
20. Haynes MP, Sinha D, Russell KS, Collinge M, Fulton D, Morales-Ruiz M, Sessa WC, Bender JR 2000 Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ Res 87:677-682
21. Chambliss KL, Yuhanna IS, Mineo C, Liu P, German Z, Sherman TS, Mendelsohn ME, Anderson RG, Shaul PW 2000 Estrogen receptor α and endothelial nitric oxide synthase are organized into a functional signaling module in caveolae. Circ Res 87:E44-E52
22. Russell KS, Haynes MP, Sinha D, Clerisme E, Bender JR 2000 Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling. Proc Natl Acad Sci USA 97: 5930-5935
23. Razandi M, Pedram A, Park ST, Levin ER 2003 Proximal events in signaling by plasma membrane estrogen receptors. J Biol Chem 278:2701-2712
24. van't Hof W, Resh MD 1997 Rapid plasma membrane anchoring of newly synthesized p59fyn: selective requirement for NH2-terminal myristoylation and palmitoylation at cysteine-3. J Cell Biol 136:1023-1035
25. Berthiaume L, Resh MD 1995 Biochemical characterization of a palmitoyl acyltransferase activity that palmitoylates myristoylated proteins. J Biol Chem 270: 22399-22405
26. McCabe JB, Berthiaume LG 1999 Functional roles for fatty acylated amino-terminal domains in subcellular localization. Mol Biol Cell 10:3771-3786
27. Ediger TR, Kraus WL, Weinman EJ, Katzenellenbogen BS 1999 Estrogen receptor regulation of the Na+/H+ exchanger regulatory factor. Endocrinology 140:2976-2982
28. Stauffer SR, Coletta CJ, Tedesco R, Nishiguchi G, Carlson K, Sun J, Katzenellenbogen BS, Katzenellenbogen JA 2000 Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-α- selective agonists. J Med Chem 43:4934-4947
29. Harris HA, Katzenellenbogen JA, Katzenellenbogen BS 2002 Characterization of the biological roles of the estrogen receptors, ERα and ERβ, in estrogen target tissues in vivo through the use of an ERα-selective ligand. Endocrinology 143:4172-4177
30. Muthyala RS, Ju YH, Sheng S, Williams LD, Doerge DR, Katzenellenbogen BS, Helferich WG, Katzenellenbogen JA 2004 Equol, a natural estrogenic metabolite from soy isoflavones: convenient preparation and resolution of Rand S-equols and their differing binding and biological activity through estrogen receptors α and β. Bioorg Med Chem 12:1559-1567
31. Lazennec G, Katzenellenbogen BS 1999 Expression of human estrogen receptor using an efficient adenoviral gene delivery system is able to restore hormone-dependent features to estrogen receptor-negative breast carcinoma cells. Mol Cell Endocrinol 149:93-105
32. Lazennec G, Alcorn JL, Katzenellenbogen BS 1999 Adenovirus-mediated delivery of a dominant negative estrogen receptor gene abrogates estrogen-stimulated gene expression and breast cancer cell proliferation. Mol Endocrinol 13:969-980
33. Frasor J, Danes JM, Komm B, Chang KC, Lyttle CR, Katzenellenbogen BS 2003 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 144:4562-4574
34. Yang NN, Venugopalan M, Hardikar S, Glasebrook A 1996 Identification of an estrogen response element activated by metabolites of 17-β-estradiol and raloxifene. Science 273:1222-1225
35. Yang NN, Venugopalan M, Hardikar S, Glasebrook A 1997 Correction: raloxifene response needs more than an element. Science 275:1249
36. Duan R, Xie W, Burghardt RC, Safe S 2001 Estrogen receptor-mediated activation of the serum response element in MCF-7 cells through MAPK-dependent phosphorylation of Elk-1. J Biol Chem 276:11590-11598
37. Martin MB, Franke TF, Stoica GE, Chambon P, Katzenellenbogen BS, Stoica BA, McLemore MS, Olivo SE, Stoica A 2000 A role for Akt in mediating the estrogenic functions of epidermal growth factor and insulin-like growth factor I. Endocrinology 141:4503-4511
38. Jiang SY, Jordan VC 1992 Growth regulation of estrogen receptor-negative breast cancer cells transfected with complementary DNAs for estrogen receptor. J Natl Cancer Inst 84:580-591
39. Song RX, McPherson RA, Adam L, Bao Y, Shupnik M, Kumar R, Santen RJ 2002 Linkage of rapid estrogen action to MAPK activation by ERα-Shc association and Shc pathway activation. Mol Endocrinol 16:116-127
40. Kousteni S, Bellido T, Plotkin LI, O'Brien CA, Bodenner DL, Han L, Han K, DiGregorio GB, Katzenellenbogen JA, Katzenellenbogen BS, Roberson PK, Weinstein RS, Jilka RL, Manolagas SC 2001 Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104: 719-730
41. Kousteni S, Chen JR, Bellido T, Han L, Ali AA, O'Brien CA, Plotkin L, Fu Q, Mancino AT, Wen Y, Vertino AM, Powers CC, Stewart SA, Ebert R, Parfitt AM, Weinstein RS, Jilka RL, Manolagas SC 2002 Reversal of bone loss in mice by nongenotropic signaling of sex steroids. Science 298:843-846
42. Razandi M, Alton G, Pedram A, Ghonshani S, Webb P, Levin ER 2003 Identification of a structural determinant necessary for the localization and function of estrogen receptor α at the plasma membrane. Mol Cell Biol 23: 1633-1646
43. Wyckoff MH, Chambliss KL, Mineo C, Yuhanna IS, Mendelsohn ME, Mumby SM, Shaul PW 2001 Plasma membrane estrogen receptors are coupled to endothelial nitric-oxide synthase through Gα(i). J Biol Chem 276: 27071-27076
44. Kelly MJ, Wagner EJ 1999 Estrogen modulation of Gprotein-coupled receptors. Trends Endocrinol Metab 10: 369-374
45. Simoncini T, Hafezi-Moghadam A, Brazil DP, Ley K, Chin WW, Liao JK 2000 Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407:538-541
46. Liu Y, Fisher DA, Storm DR 1993 Analysis of the palmitoylation and membrane targeting domain of neuromodulin (GAP-43) by site-specific mutagenesis. Biochemistry 32:10714-10719
47. Zhang Z, Maier B, Santen RJ, Song RX 2002 Membrane association of estrogen receptor α mediates estrogen effect on MAPK activation. Biochem Biophys Res Commun 294:926-933
48. Dauvois S, Danielian PS, White R, Parker MG 1992 Antiestrogen ICI164,384 reduces cellular estrogen receptor content by increasing its turnover. Proc Natl Acad Sci USA 89:4037-4041
49. Montano MM, Ekena K, Krueger KD, Keller AL, Katzenellenbogen BS 1996 Human estrogen receptor ligand activity inversion mutants: receptors that interpret antiestrogens as estrogens and estrogens as antiestrogens and discriminate among different antiestrogens. Mol Endocrinol 10:230-242
50. Kumar R, Wang RA, Mazumdar A, Talukder AH, Mandal M, Yang Z, Bagheri-Yarmand R, Sahin A, Hortobagyi G, Adam L, Barnes CJ, Vadlamudi RK 2002 A naturally occurring MTA1 variant sequesters oestrogen receptor-α in the cytoplasm. Nature 418:654-657
51. Barletta F, Wong CW, McNally C, Komm BS, Katzenellenbogen B, Cheskis BJ 2004 Characterization of the interactions of estrogen receptor and MNAR in the activation of cSrc. Mol Endocrinol 18:1096-1108
52. Li L, Haynes MP, Bender JR 2003 Plasma membrane localization and function of the estrogen receptor α variant (ER46) in human endothelial cells. Proc Natl Acad Sci USA 100:4807-4812
53. Acconcia F, Ascenzi P, Fabozzi G, Visca P, Marino M 2004 S-palmitoylation modulates human estrogen receptor-α functions. Biochem Biophys Res Commun 316: 878-883
54. Pakdel F, Katzenellenbogen BS 1992 Human estrogen receptor mutants with altered estrogen and antiestrogen ligand discrimination. J Biol Chem 267:3429-3437
55. Sun J, Meyers MJ, Fink BE, Rajendran R, Katzenellenbogen JA, Katzenellenbogen BS 1999 Novel ligands that function as selective estrogens or antiestrogens for es-trogen receptor-or estrogen receptor-β. Endocrinology 140:800-804
56. Schodin DJ, Zhuang Y, Shapiro DJ, Katzenellenbogen BS 1995 Analysis of mechanisms that determine dominant negative estrogen receptor effectiveness. J Biol Chem 270:31163-31171
57. Stossi F, Barnett DH, Frasor J, Komm B, Lyttle CR, Katzenellenbogen BS 2004 Transcriptional profiling of estrogen-regulated gene expression via estrogen receptor (ER)α or ER β in human osteosarcoma cells: Distinct and common target genes for these receptors. Endocrinology 145:3473-3486
58. Nye AC, Rajendran R, Stenoien D, Mancini M, Katzenellenbogen BS, Belmont AS 2002 Alteration of large-scale chromatin structure by estrogen receptor. Mol Cell Biol 22:3437-3449
59. 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
60. Laborda J 1991 36B4 cDNA used as an estradiolindependent mRNA control is the cDNA for human acidic ribosomal phosphoprotein PO. Nucleic Acids Res 19:3998