Advances in the understanding of the structure and function of ER-α36,a novel variant of human estrogen receptor-alpha

Journal of Steroid Biochemistry and Molecular Biology

Volumn 127, Issue 3-5, 2011, Pages 231-237

  Rao, Jun ^a   Jiang, Xiaomei ^a   Wang, Yang ^a   Chen, Bin ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Breast cancer; Endocrine therapy resistance; ER genomic nongenomic actions; ER 36; Estrogen receptor

Indexed keywords

CELL NUCLEUS RECEPTOR; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA36; ESTROGEN RECEPTOR ALPHA46; ESTROGEN RECEPTOR ALPHA66; FULVESTRANT; LETROZOLE; TAMOXIFEN; TRASTUZUMAB; UNCLASSIFIED DRUG;

BREAST CANCER; BREAST CARCINOGENESIS; CANCER GROWTH; CANCER HORMONE THERAPY; CHEMICAL STRUCTURE; HUMAN; LIGAND BINDING; MOLECULAR CLONING; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; REVIEW; SIGNAL TRANSDUCTION; TRANSACTIVATION; WILD TYPE;

EID: 81255207179     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2011.08.004     Document Type: Short Survey

References (73)

1. G.R. Cunha, A.A. Donjacour, P.S. Cooke, S. Mee, R.M. Bigsby, S.J. Higgins, and Y. Sugimura The endocrinology and developmental biology of the prostate Endocr. Rev. 8 3 1987 338 362
2. K. Dahlman-Wright, V. Cavailles, S.A. Fuqua, V.C. Jordan, J.A. Katzenellenbogen, K.S. Korach, A. Maggi, M. Muramatsu, M.G. Parker, and J.A. Gustafsson International Union of Pharmacology. LXIV. Estrogen receptors Pharmacol. Rev. 58 4 2006 773 781 (Pubitemid 44833745)
3. R.A. Jarred, B. Cancilla, G.S. Prins, K.A. Thayer, G.R. Cunha, and G.P. Risbridger Evidence that estrogens directly alter androgen-regulated prostate development Endocrinology 141 9 2000 3471 3477 (Pubitemid 32269037)
4. L.P. Menasce, G.R. White, C.J. Harrison, and J.M. Boyle Localization of the estrogen receptor locus (ESR) to chromosome 6q25.1 by FISH and a simple post-FISH banding technique Genomics 17 1 1993 263 265 (Pubitemid 23205095)
5. E. Enmark, M. Pelto-Huikko, K. Grandien, S. Lagercrantz, J. Lagercrantz, G. Fried, M. Nordenskjold, and J.A. Gustafsson Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern J. Clin. Endocrinol. Metab. 82 12 1997 4258 4265 (Pubitemid 27525550)
6. S. Ogawa, S. Inoue, T. Watanabe, H. Hiroi, A. Orimo, T. Hosoi, Y. Ouchi, and M. Muramatsu The complete primary structure of human estrogen receptor beta (hER beta) and its heterodimerization with ER alpha in vivo and in vitro Biochem. Biophys. Res. Commun. 243 1 1998 122 126 (Pubitemid 28414201)
7. A. Strom, J. Hartman, J.S. Foster, S. Kietz, J. Wimalasena, and J.A. Gustafsson Estrogen receptor beta inhibits 17beta-estradiol-stimulated proliferation of the breast cancer cell line T47D Proc. Natl. Acad. Sci. U.S.A. 101 6 2004 1566 1571 (Pubitemid 38236167)
8. Z. Weihua, S. Andersson, G. Cheng, E.R. Simpson, M. Warner, and J.A. Gustafsson Update on estrogen signaling FEBS Lett. 546 1 2003 17 24 (Pubitemid 36789762)
9. E.H. Kong, A.C. Pike, and R.E. Hubbard Structure and mechanism of the oestrogen receptor Biochem. Soc. Trans. 31 Pt 1 2003 56 59 (Pubitemid 36244928)
10. B.C. van der Eerden, J. Emons, S. Ahmed, H.W. van Essen, C.W. Lowik, J.M. Wit, and M. Karperien Evidence for genomic and nongenomic actions of estrogen in growth plate regulation in female and male rats at the onset of sexual maturation J. Endocrinol. 175 2 2002 277 288 (Pubitemid 35414376)
11. L. Bjornstrom, and M. Sjoberg Mechanisms of estrogen receptor signaling: convergence of genomic and nongenomic actions on target genes Mol. Endocrinol. 19 4 2005 833 842 (Pubitemid 40397050)
12. B.J. Cheskis, J.G. Greger, S. Nagpal, and L.P. Freedman Signaling by estrogens J. Cell Physiol. 213 3 2007 610 617 (Pubitemid 350058252)
13. D.J. Mangelsdorf, C. Thummel, M. Beato, P. Herrlich, G. Schutz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, and R.M. Evans The nuclear receptor superfamily: the second decade Cell 83 6 1995 835 839
14. J.M. Hall, J.F. Couse, and K.S. Korach The multifaceted mechanisms of estradiol and estrogen receptor signaling J. Biol. Chem. 276 40 2001 36869 36872
15. M. Wehling Specific, nongenomic actions of steroid hormones Annu. Rev. Physiol. 59 1997 365 393 (Pubitemid 27142447)
16. Z. Wang, X. Zhang, P. Shen, B.W. Loggie, Y. Chang, and T.F. Deuel Identification, cloning, and expression of human estrogen receptor-alpha36, a novel variant of human estrogen receptor-alpha66 Biochem. Biophys. Res. Commun. 336 4 2005 1023 1027 (Pubitemid 41383424)
17. G. Flouriot, H. Brand, S. Denger, R. Metivier, M. Kos, G. Reid, V. Sonntag-Buck, and F. Gannon Identification of a new isoform of the human estrogen receptor-alpha (hER-alpha) that is encoded by distinct transcripts and that is able to repress hER-alpha activation function 1 EMBO J. 19 17 2000 4688 4700
18. J.T. Moore, D.D. McKee, K. Slentz-Kesler, L.B. Moore, S.A. Jones, E.L. Horne, J.L. Su, S.A. Kliewer, J.M. Lehmann, and T.M. Willson Cloning and characterization of human estrogen receptor beta isoforms Biochem. Biophys. Res. Commun. 247 1 1998 75 78 (Pubitemid 28412528)
19. S.L. Lin, L.Y. Yan, X.T. Zhang, J. Yuan, M. Li, J. Qiao, Z.Y. Wang, and Q.Y. Sun ER-alpha36, a variant of ER-alpha, promotes tamoxifen agonist action in endometrial cancer cells via the MAPK/ERK and PI3K/Akt pathways PLoS One 5 2 2010 e9013
20. Z. Wang, X. Zhang, P. Shen, B.W. Loggie, Y. Chang, and T.F. Deuel A variant of estrogen receptor-{alpha}, hER-{alpha}36: transduction of estrogen- and antiestrogen-dependent membrane-initiated mitogenic signaling Proc. Natl. Acad. Sci. U.S.A. 103 24 2006 9063 9068 (Pubitemid 43902533)
21. L. Li, M.P. Haynes, and J.R. Bender Plasma membrane localization and function of the estrogen receptor alpha variant (ER46) in human endothelial cells Proc. Natl. Acad. Sci. U.S.A. 100 8 2003 4807 4812 (Pubitemid 36457810)
22. L.M. Lee, J. Cao, H. Deng, P. Chen, Z. Gatalica, and Z.Y. Wang ER-alpha36, a novel variant of ER-alpha, is expressed in ER-positive and -negative human breast carcinomas Anticancer Res. 28 1B 2008 479 483
23. H. Jiang, R. Teng, Q. Wang, X. Zhang, H. Wang, Z. Wang, J. Cao, and L. Teng Transcriptional analysis of estrogen receptor alpha variant mRNAs in colorectal cancers and their matched normal colorectal tissues J. Steroid Biochem. Mol. Biol. 112 1-3 2008 20 24
24. H. Deng, X. Huang, J. Fan, L. Wang, Q. Xia, X. Yang, Z. Wang, L. Liu, A variant of estrogen receptor-alpha, ER-alpha36 is expressed in human gastric cancer and is highly correlated with lymph node metastasis, Oncol. Rep. 24 (1) (2010) 171-176.
25. B.Z. Xu, S.L. Lin, M. Li, J.Q. Zhu, S. Li, Y.C. Ouyang, D.Y. Chen, and Q.Y. Sun Changes in estrogen receptor-alpha variant (ER-alpha36) expression during mouse ovary development and oocyte meiotic maturation Histochem. Cell Biol. 131 3 2009 347 354
26. L. Shi, B. Dong, Z. Li, Y. Lu, T. Ouyang, J. Li, T. Wang, Z. Fan, T. Fan, B. Lin, Z. Wang, and Y. Xie Expression of ER-{alpha}36, a novel variant of estrogen receptor {alpha}, and resistance to tamoxifen treatment in breast cancer J. Clin. Oncol. 27 21 2009 3423 3429
27. X.T Zhang, L.G. Kang, L. Ding, S. Vranic, Z. Gatalica, and Z.Y. Wang A positive feedback loop of ER-alpha36/EGFR promotes malignant growth of ER-negative breast cancer cells Oncogene 30 7 2011 770 780
28. S. Vranic, Z. Gatalica, H. Deng, S. Frkovic-Grazio, L.M. Lee, O. Gurjeva, and Z.Y. Wang ER-alpha36, a novel isoform of ER-alpha66, is commonly over-expressed in apocrine and adenoid cystic carcinomas of the breast J. Clin. Pathol. 64 1 2011 54 57
29. N. Roodi, L.R. Bailey, W.Y. Kao, C.S. Verrier, C.J. Yee, W.D. Dupont, and F.F. Parl Estrogen receptor gene analysis in estrogen receptor-positive and receptor-negative primary breast cancer J. Natl. Cancer Inst. 87 6 1995 446 451
30. Y. Zou, L. Ding, M. Coleman, and Z. Wang Estrogen receptor-alpha (ER-[alpha]) suppresses expression of its variant ER-[alpha]36 FEBS Lett. 583 8 2009 1368 1374
31. L. Kang, X. Zhang, Y. Xie, Y. Tu, D. Wang, Z. Liu, Z.Y. Wang, Involvement of estrogen receptor variant ER-alpha36, not GPR30, in nongenomic estrogen signaling, Mol. Endocrinol. 24 (4) (2010) 709-721.
32. R. Schiff, S.A. Massarweh, J. Shou, L. Bharwani, S.K. Mohsin, and C.K. Osborne Cross-talk between estrogen receptor and growth factor pathways as a molecular target for overcoming endocrine resistance Clin. Cancer Res. 10 1 Pt 2 2004 331S 336S (Pubitemid 38116639)
33. Y.L. Chung, M.L. Sheu, S.C. Yang, C.H. Lin, and S.H. Yen Resistance to tamoxifen-induced apoptosis is associated with direct interaction between Her2/neu and cell membrane estrogen receptor in breast cancer Int. J. Cancer 97 3 2002 306 312
34. S. Kahlert, S. Nuedling, M. van Eickels, H. Vetter, R. Meyer, and C. Grohe Estrogen receptor alpha rapidly activates the IGF-1 receptor pathway J. Biol. Chem. 275 24 2000 18447 18453 (Pubitemid 30414803)
35. C.W. Wong, C. McNally, E. Nickbarg, B.S. Komm, and B.J. Cheskis Estrogen receptor-interacting protein that modulates its nongenomic activity-crosstalk with Src/Erk phosphorylation cascade Proc. Natl. Acad. Sci. U.S.A. 99 23 2002 14783 14788 (Pubitemid 35334561)
36. M. Razandi, A. Pedram, S.T. Park, and E.R. Levin Proximal events in signaling by plasma membrane estrogen receptors J. Biol. Chem. 278 4 2003 2701 2712 (Pubitemid 36801351)
37. G.E. Stoica, T.F. Franke, A. Wellstein, E. Morgan, F. Czubayko, H.J. List, R. Reiter, M.B. Martin, and A. Stoica Heregulin-beta1 regulates the estrogen receptor-alpha gene expression and activity via the ErbB2/PI 3-K/Akt pathway Oncogene 22 14 2003 2073 2087 (Pubitemid 36539558)
38. M. Sun, J.E. Paciga, R.I. Feldman, Z. Yuan, D. Coppola, Y.Y. Lu, S.A. Shelley, S.V. Nicosia, and J.Q. Cheng Phosphatidylinositol-3-OH Kinase (PI3K)/AKT2, activated in breast cancer, regulates and is induced by estrogen receptor alpha (ERalpha) via interaction between ERalpha and PI3K Cancer Res. 61 16 2001 5985 5991 (Pubitemid 32762525)
39. C.A Lange-Carter, C.M. Pleiman, A.M. Gardner, K.J. Blumer, and G.L. Johnson A divergence in the MAP kinase regulatory network defined by MEK kinase and Raf Science 260 5106 1993 315 319 (Pubitemid 23160137)
40. W. Zhang, and H.T. Liu MAPK signal pathways in the regulation of cell proliferation in mammalian cells Cell Res. 12 1 2002 9 18 (Pubitemid 135708299)
41. I. Vivanco, and C.L. Sawyers The phosphatidylinositol 3-kinase AKT pathway in human cancer Nat. Rev. Cancer 2 7 2002 489 501 (Pubitemid 37328931)
42. C.G. Bologa, C.M. Revankar, S.M. Young, B.S. Edwards, J.B. Arterburn, A.S. Kiselyov, M.A. Parker, S.E. Tkachenko, N.P. Savchuck, L.A. Sklar, T.I. Oprea, and E.R. Prossnitz Virtual and biomolecular screening converge on a selective agonist for GPR30 Nat. Chem. Biol. 2 4 2006 207 212
43. T.M. Ahola, N. Alkio, T. Manninen, and T. Ylikomi Progestin and G protein-coupled receptor 30 inhibit mitogen-activated protein kinase activity in MCF-7 breast cancer cells Endocrinology 143 12 2002 4620 4626 (Pubitemid 35397603)
44. E. Filardo, J. Quinn, Y. Pang, C. Graeber, S. Shaw, J. Dong, and P. Thomas Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane Endocrinology 148 7 2007 3236 3245 (Pubitemid 46997004)
45. E.J. Filardo, J.A. Quinn, K.I. Bland, and A.R. Frackelton Jr. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF Mol. Endocrinol. 14 10 2000 1649 1660
46. Y. Jiang, Y.E. Liu, A. Lu, A. Gupta, I.D. Goldberg, J. Liu, and Y.E. Shi Stimulation of estrogen receptor signaling by gamma synuclein Cancer Res. 63 14 2003 3899 3903 (Pubitemid 36917902)
47. Y.E. Shi, Y. Chen, R. Dackour, L. Potters, S. Wang, Q. Ding, Z. Wang, and Y.E. Liu Synuclein gamma stimulates membrane-initiated estrogen signaling by chaperoning estrogen receptor (ER)-alpha36, a variant of ER-alpha Am. J. Pathol. 177 2 2010 964 973
48. Y. Zheng, J. Zhang, Z.Z. Xu, J.M. Sheng, X.C. Zhang, H.H. Wang, X.D. Teng, X.J. Liu, J. Cao, L.S. Teng, Quantitative profiles of the mRNAs of ER-alpha and its novel variant ER-alpha36 in breast cancers and matched normal tissues, J. Zhejiang Univ. Sci. B11 (2) (2010) 144-150.
49. C.M. Perou, T. Sorlie, M.B. Eisen, M. van de Rijn, S.S. Jeffrey, C.A. Rees, J.R. Pollack, D.T. Ross, H. Johnsen, L.A. Akslen, O. Fluge, A. Pergamenschikov, C. Williams, S.X. Zhu, P.E. Lonning, A.L. Borresen-Dale, P.O. Brown, and D. Botstein Molecular portraits of human breast tumours Nature 406 6797 2000 747 752
50. C. Sotiriou, S.Y. Neo, L.M. McShane, E.L. Korn, P.M. Long, A. Jazaeri, P. Martiat, S.B. Fox, A.L. Harris, and E.T. Liu Breast cancer classification and prognosis based on gene expression profiles from a population-based study Proc. Natl. Acad. Sci. U.S.A. 100 18 2003 10393 10398 (Pubitemid 37071889)
51. J.S. Ross, and J.A. Fletcher The HER-2/neu oncogene in breast cancer: prognostic factor, predictive factor, and target for therapy Oncologist 3 4 1998 237 252
52. C.L Vogel, M.A. Cobleigh, D. Tripathy, J.C. Gutheil, L.N. Harris, L. Fehrenbacher, D.J. Slamon, M. Murphy, W.F. Novotny, M. Burchmore, S. Shak, S.J. Stewart, and M. Press Efficacy and safety of trastuzumab as a single agent in first-line treatment of HER2-overexpressing metastatic breast cancer J. Clin. Oncol. 20 3 2002 719 726 (Pubitemid 34111379)
53. P. Carter, L. Presta, C.M. Gorman, J.B. Ridgway, D. Henner, W.L. Wong, A.M. Rowland, C. Kotts, M.E. Carver, and H.M. Shepard Humanization of an anti-p185HER2 antibody for human cancer therapy Proc. Natl. Acad. Sci. U.S.A. 89 10 1992 4285 4289
54. K.L. Cheung Endocrine therapy for breast cancer: an overview Breast 16 4 2007 327 343 (Pubitemid 47109203)
55. A. Goldhirsch, M. Colleoni, and R.D. Gelber Endocrine therapy of breast cancer Ann. Oncol. 13 Suppl. 4 2002 61 68 (Pubitemid 35369974)
56. K.I. Pritchard, A.H. Paterson, S. Fine, N.A. Paul, B. Zee, L.E. Shepherd, H. Abu-Zahra, J. Ragaz, M. Knowling, M.N. Levine, S. Verma, D. Perrault, P.L. Walde, V.H. Bramwell, M. Poljicak, N. Boyd, D. Warr, B.D. Norris, D. Bowman, G.R. Armitage, H. Weizel, and R.A. Buckman Randomized trial of cyclophosphamide, methotrexate, and fluorouracil chemotherapy added to tamoxifen as adjuvant therapy in postmenopausal women with node-positive estrogen and/or progesterone receptor-positive breast cancer: a report of the National Cancer Institute of Canada Clinical Trials Group Breast Cancer Site Group J. Clin. Oncol. 15 6 1997 2302 2311 (Pubitemid 27251132)
57. C. Gajdos, and V.C. Jordan Selective estrogen receptor modulators as a new therapeutic drug group: concept to reality in a decade Clin. Breast Cancer 2 4 2002 272 281 (Pubitemid 34196269)
58. V.C. Jordan New insights into the metabolism of tamoxifen and its role in the treatment and prevention of breast cancer Steroids 72 13 2007 829 842 (Pubitemid 47410069)
59. A. Howell Pure oestrogen antagonists for the treatment of advanced breast cancer Endocr. Relat. Cancer 13 3 2006 689 706 (Pubitemid 44763252)
60. K. Altundag, and N.K. Ibrahim Aromatase inhibitors in breast cancer: an overview Oncologist 11 6 2006 553 562 (Pubitemid 43967611)
61. A.U. Buzdar Aromatase inhibitors in breast cancer therapy Clin. Breast Cancer 4 Suppl. 2 2003 S84 S88
62. R.A. Madaio, G. Spalletta, L. Cravello, M. Ceci, L. Repetto, and G. Naso Overcoming endocrine resistance in breast cancer Curr. Cancer Drug Targets 10 5 2010 519 528
63. B.S. Katzenellenbogen, and J. Frasor Therapeutic targeting in the estrogen receptor hormonal pathway Semin. Oncol. 31 1 (Suppl. 3) 2004 28 38 (Pubitemid 38543938)
64. G. Arpino, L. Wiechmann, C.K. Osborne, and R. Schiff Crosstalk between the estrogen receptor and the HER tyrosine kinase receptor family: molecular mechanism and clinical implications for endocrine therapy resistance Endocr. Rev. 29 2 2008 217 233 (Pubitemid 351519691)
65. J. Shou, S. Massarweh, C.K. Osborne, A.E. Wakeling, S. Ali, H. Weiss, and R. Schiff Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer J. Natl. Cancer Inst. 96 12 2004 926 935 (Pubitemid 38868139)
66. C.K. Osborne, J. Shou, S. Massarweh, and R. Schiff Crosstalk between estrogen receptor and growth factor receptor pathways as a cause for endocrine therapy resistance in breast cancer Clin. Cancer Res. 11 2 Pt 2 2005 865s 870s (Pubitemid 40111098)
67. M. Dowsett, L.A. Martin, I. Smith, and S. Johnston Mechanisms of resistance to aromatase inhibitors J. Steroid Biochem. Mol. Biol. 95 1-5 2005 167 172 (Pubitemid 41137307)
68. M. Wang, J.Y. Pan, G.R. Song, H.B. Chen, L.J. An, and S.X. Qu Altered expression of estrogen receptor alpha and beta in advanced gastric adenocarcinoma: correlation with prothymosin alpha and clinicopathological parameters Eur. J. Surg. Oncol. 33 2 2007 195 201 (Pubitemid 46336548)
69. S.L. Lin, L.Y. Yan, X.W. Liang, Z.B. Wang, Z.Y. Wang, J. Qiao, H. Schatten, and Q.Y. Sun A novel variant of ER-alpha, ER-alpha36 mediates testosterone-stimulated ERK and Akt activation in endometrial cancer Hec1A cells Reprod. Biol. Endocrinol. 7 2009 102
70. B.B. Tu, S.L. Lin, L.Y. Yan, Z.Y. Wang, Q.Y. Sun, and J. Qiao ER-alpha36, a novel variant of estrogen receptor alpha, is involved in EGFR-related carcinogenesis in endometrial cancer Am. J. Obstet. Gynecol. 16 2011 16
71. J.S Tong, Q.H. Zhang, Z.B. Wang, S. Li, C.R. Yang, X.Q. Fu, Y. Hou, Z.Y. Wang, J. Sheng, and Q.Y. Sun ER-alpha36, a novel variant of ER-alpha, mediates estrogen-stimulated proliferation of endometrial carcinoma cells via the PKCdelta/ERK pathway PLoS One 5 11 2010
72. S. Jia, X. Zhang, D.Z. He, M. Segal, A. Berro, T.G. Gerson, Z. Wang, and T.B. Casale Expression and function of a novel variant of estrogen receptor-ER-{alpha}36 in mouse airway Am. J. Respir. Cell Mol. Biol. 3 2011 3 [Epub ahead of print]
73. H. Xie, M. Sun, X.B. Liao, L.Q. Yuan, Z.F. Sheng, J.C. Meng, D. Wang, Z.Y. Yu, L.Y. Zhang, H.D. Zhou, X.H. Luo, H. Li, X.P. Wu, Q.Y. Wei, S.Y. Tang, Z.Y. Wang, and E.Y. Liao Estrogen receptor alpha36 mediates a bone-sparing effect of 17beta-estrodiol in postmenopausal women J. Bone Miner. Res. 26 1 2011 156 168