Involvement of estrogen receptor β5 in the progression of glioma

Brain Research

Volumn 1503, Issue , 2013, Pages 97-107

  Li, Wenjun ^a   Winters, Ali ^a   Poteet, Ethan ^a   Ryou, Myoung Gwi ^a   Lin, Song ^b   Hao, Shuyu ^b   Wu, Zhen ^b   Yuan, Fang ^b   Hatanpaa, Kimmo J ^c   Simpkins, James W ^a   Yang, Shao Hua ^a,b  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

Estrogen receptor ; Glioblastoma multiforme; Hypoxia inducible factor; PTEN

Indexed keywords

ESTROGEN RECEPTOR BETA; ESTROGEN RECEPTOR BETA1; ESTROGEN RECEPTOR BETA2; ESTROGEN RECEPTOR BETA5; HYPOXIA INDUCIBLE FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ARTICLE; BRAIN TISSUE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; GLIOMA; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPOXIA; IMMUNOHISTOCHEMISTRY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANALYSIS OF VARIANCE; BRAIN NEOPLASMS; CELL CYCLE; CELL HYPOXIA; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE PROGRESSION; ESTROGEN RECEPTOR BETA; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIAL FIBRILLARY ACIDIC PROTEIN; GLIOMA; HUMANS; OXYGEN CONSUMPTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 84875222587     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.02.004     Document Type: Article

References (51)

1. A. Bardin, N. Boulle, G. Lazennec, F. Vignon, and P. Pujol Loss of ERbeta expression as a common step in estrogen-dependent tumor progression Endocr. Relat. Cancer 11 2004 537 551
2. A. Batistatou, P.A. Kyzas, A. Goussia, E. Arkoumani, S. Voulgaris, K. Polyzoidis, N.J. Agnantis, and D. Stefanou Estrogen receptor beta (ERbeta) protein expression correlates with BAG-1 and prognosis in brain glial tumours J. Neurooncol. 77 2006 17 23
3. S.M. Belcher, X. Ma, and H.H. Le Blockade of estrogen receptor signaling inhibits growth and migration of medulloblastoma Endocrinology 150 2009 1112 1121
4. K.A. Burns, and K.S. Korach Estrogen receptors and human disease: an update Arch. Toxicol. 86 2012 1491 1504
5. W.T. Couldwell, D.R. Hinton, A.A. Surnock, C.M. DeGiorgio, L.P. Weiner, M.L. Apuzzo, L. Masri, R.E. Law, and M.H. Weiss Treatment of recurrent malignant gliomas with chronic oral high-dose tamoxifen Clin. Cancer Res. 2 1996 619 622
6. G.S. Cruickshank, R.P. Rampling, and W. Cowans Direct measurement of the PO2 distribution in human malignant brain tumours Adv. Exp. Med. Biol. 345 1994 465 470
7. M.P. Davies, P.A. O'Neill, H. Innes, D.R. Sibson, W. Prime, C. Holcombe, and C.S. Foster Correlation of mRNA for oestrogen receptor beta splice variants ERbeta1, ERbeta2/ERbetacx and ERbeta5 with outcome in endocrine-treated breast cancer J. Mol. Endocrinol. 33 2004 773 782
8. E.M. Dioum, S.L. Clarke, K. Ding, J.J. Repa, and J.A. Garcia HIF-2alpha-haploinsufficient mice have blunted retinal neovascularization due to impaired expression of a proangiogenic gene battery Invest. Ophthalmol. Vis. Sci. 49 2008 2714 2720
9. M. Esslimani-Sahla, J. Simony-Lafontaine, A. Kramar, R. Lavaill, C. Mollevi, M. Warner, J.A. Gustafsson, and H. Rochefort Estrogen receptor beta (ER beta) level but not its ER beta cx variant helps to predict tamoxifen resistance in breast cancer Clin. Cancer Res. 10 2004 5769 5776
10. S.M. Evans, K.D. Judy, I. Dunphy, W.T. Jenkins, P.T. Nelson, R. Collins, E.P. Wileyto, K. Jenkins, S.M. Hahn, C.W. Stevens, A.R. Judkins, P. Phillips, B. Geoerger, and C.J. Koch Comparative measurements of hypoxia in human brain tumors using needle electrodes and EF5 binding Cancer Res. 64 2004 1886 1892
11. J. Fields, J. Gardner-Mercer, K. Borgmann, I. Clark, and A. Ghorpade CCAAT/enhancer binding protein beta expression is increased in the brain during HIV-1-infection and contributes to regulation of astrocyte tissue inhibitor of metalloproteinase-1 J. Neurochem. 118 2011 93 104
12. F.B. Furnari, H. Lin, H.S. Huang, and W.K. Cavenee Growth suppression of glioma cells by PTEN requires a functional phosphatase catalytic domain Proc. Nat. Acad. Sci. U.S.A. 94 1997 12479 12484
13. I. Garcia-Cao, M.S. Song, R.M. Hobbs, G. Laurent, C. Giorgi, V.C. de Boer, D. Anastasiou, K. Ito, A.T. Sasaki, L. Rameh, A. Carracedo, M.G. Vander Heiden, L.C. Cantley, P. Pinton, M.C. Haigis, and P.P. Pandolfi Systemic elevation of PTEN induces a tumor-suppressive metabolic state Cell 149 2012 49 62
14. C. Guido, S. Panza, M. Santoro, P. Avena, M.L. Panno, I. Perrotta, F. Giordano, I. Casaburi, S. Catalano, F. De Amicis, F. Sotgia, M.P. Lisanti, S. Ando, and S. Aquila Estrogen receptor beta (ERbeta) produces autophagy and necroptosis in human seminoma cell line through the binding of the Sp1 on the phosphatase and tensin homolog deleted from chromosome 10 (PTEN) promoter gene Cell Cycle 11 2012 2911 2921
15. J.M. Hall, and D.P. McDonnell The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens Endocrinology 140 1999 5566 5578
16. J. Hartman, K. Edvardsson, K. Lindberg, C. Zhao, C. Williams, A. Strom, and J.A. Gustafsson Tumor repressive functions of estrogen receptor beta in SW480 colon cancer cells Cancer Res. 69 2009 6100 6106
17. J.M. Harvey, G.M. Clark, C.K. Osborne, and D.C. Allred Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer J. Clin. Oncol. 17 1999 1474 1481
18. A. Heyer, M. Hasselblatt, N. von Ahsen, H. Hafner, A.L. Siren, and H. Ehrenreich In vitro gender differences in neuronal survival on hypoxia and in 17beta-estradiol-mediated neuroprotection J. Cereb. Blood Flow Metab. 25 2005 427 430
19. S. Hirata, T. Shoda, J. Kato, and K. Hoshi The multiple untranslated first exons system of the human estrogen receptor beta (ER beta) gene J. Steroid Biochem. Mol. Biol. 78 2001 33 40
20. N. Honma, R. Horii, T. Iwase, S. Saji, M. Younes, K. Takubo, M. Matsuura, Y. Ito, F. Akiyama, and G. Sakamoto Clinical importance of estrogen receptor-beta evaluation in breast cancer patients treated with adjuvant tamoxifen therapy J. Clin. Oncol. 26 2008 3727 3734
21. T.A. Hopp, H.L. Weiss, I.S. Parra, Y. Cui, C.K. Osborne, and S.A. Fuqua Low levels of estrogen receptor beta protein predict resistance to tamoxifen therapy in breast cancer Clin. Cancer Res. 10 2004 7490 7499
22. T.A. Jarvinen, M. Pelto-Huikko, K. Holli, and J. Isola Estrogen receptor beta is coexpressed with ERalpha and PR and associated with nodal status, grade, and proliferation rate in breast cancer Am. J. Pathol. 156 2000 29 35
23. S. Kamalakaran, S.K. Radhakrishnan, and W.T. Beck Identification of estrogen-responsive genes using a genome-wide analysis of promoter elements for transcription factor binding sites J. Biol. Chem. 280 2005 21491 21497
24. G. Lazennec, D. Bresson, A. Lucas, C. Chauveau, and F. Vignon ER beta inhibits proliferation and invasion of breast cancer cells Endocrinology 142 2001 4120 4130
25. Y.K. Leung, P. Mak, S. Hassan, and S.M. Ho Estrogen receptor (ER)-beta isoforms: a key to understanding ER-beta signaling Proc. Nat. Acad. Sci. U.S.A. 103 2006 13162 13167
26. Y.K. Leung, H.M. Lam, S. Wu, D. Song, L. Levin, L. Cheng, C.L. Wu, and S.M. Ho Estrogen receptor beta2 and beta5 are associated with poor prognosis in prostate cancer, and promote cancer cell migration and invasion Endocr. Relat. Cancer 17 2010 675 689
27. E. Leygue, H. Dotzlaw, P.H. Watson, and L.C. Murphy Expression of estrogen receptor beta1, beta2, and beta5 messenger RNAs in human breast tissue Cancer Res. 59 1999 1175 1179
28. L.C. Li, C.C. Yeh, D. Nojima, and R. Dahiya Cloning and characterization of human estrogen receptor beta promoter Biochem. Biophys. Res. Commun. 275 2000 682 689
29. W. Li, E. Poteet, L. Xie, R. Liu, Y. Wen, and S.H. Yang Regulation of matrix metalloproteinase 2 by oligomeric amyloid beta protein Brain Res. 1387 2011 141 148
30. W. Lim, Y. Park, J. Cho, C. Park, J. Park, Y.K. Park, H. Park, and Y. Lee Estrogen receptor beta inhibits transcriptional activity of hypoxia inducible factor-1 through the downregulation of arylhydrocarbon receptor nuclear translocator Breast Cancer Res. 13 2011 R32
31. K. Lindberg, L.A. Helguero, Y. Omoto, J.A. Gustafsson, and L.A. Haldosen Estrogen receptor beta represses Akt signaling in breast cancer cells via downregulation of HER2/HER3 and upregulation of PTEN: implications for tamoxifen sensitivity Breast Cancer Res. 13 2011 R43
32. M.M. Liu, C. Albanese, C.M. Anderson, K. Hilty, P. Webb, R.M. Uht, R.H. Price Jr., R.G. Pestell, and P.J. Kushner Opposing action of estrogen receptors alpha and beta on cyclin D1 gene expression J. Biol. Chem. 277 2002 24353 24360
33. 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 1998 75 78
34. L.C. Murphy, and E. Leygue The role of estrogen receptor-beta in breast cancer Semin. Reprod. Med. 30 2012 5 13
35. D. Nojima, L.C. Li, A. Dharia, G. Perinchery, L. Ribeiro-Filho, T.S. Yen, and R. Dahiya CpG hypermethylation of the promoter region inactivates the estrogen receptor-beta gene in patients with prostate carcinoma Cancer 92 2001 2076 2083
36. Y. Omoto, H. Eguchi, Y. Yamamoto-Yamaguchi, and S. Hayashi Estrogen receptor (ER) beta1 and ERbetacx/beta2 inhibit ERalpha function differently in breast cancer cell line MCF7 Oncogene 22 2003 5011 5020
37. S. Paruthiyil, H. Parmar, V. Kerekatte, G.R. Cunha, G.L. Firestone, and D.C. Leitman Estrogen receptor beta inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest Cancer Res. 64 2004 423 428
38. S. Patel, S. DiBiase, B. Meisenberg, T. Flannery, A. Patel, A. Dhople, S. Cheston, and P. Amin Phase I clinical trial assessing temozolomide and tamoxifen with concomitant radiotherapy for treatment of high-grade glioma Int. J. Radiat. Oncol. Biol. Phys. 82 2012 739 742
39. I. Poola, J. Abraham, K. Baldwin, A. Saunders, and R. Bhatnagar Estrogen receptors beta4 and beta5 are full length functionally distinct ERbeta isoforms: cloning from human ovary and functional characterization Endocrine 27 2005 227 238
40. A. Rody, U. Holtrich, C. Solbach, K. Kourtis, G. von Minckwitz, K. Engels, S. Kissler, R. Gatje, T. Karn, and M. Kaufmann Methylation of estrogen receptor beta promoter correlates with loss of ER-beta expression in mammary carcinoma and is an early indication marker in premalignant lesions Endocr. Relat. Cancer 12 2005 903 916
41. G.R. Sareddy, B.C. Nair, V.K. Gonugunta, Q.G. Zhang, A. Brenner, D.W. Brann, R.R. Tekmal, and R.K. Vadlamudi Therapeutic significance of estrogen receptor beta agonists in gliomas Mol. Cancer Ther. 11 2012 1174 1182
42. A.M. Shaaban, A.R. Green, S. Karthik, Y. Alizadeh, T.A. Hughes, L. Harkins, I.O. Ellis, J.F. Robertson, E.C. Paish, P.T. Saunders, N.P. Groome, and V. Speirs Nuclear and cytoplasmic expression of ERbeta1, ERbeta2, and ERbeta5 identifies distinct prognostic outcome for breast cancer patients Clin. Cancer Res. 14 2008 5228 5235
43. B.G. Skov, B.M. Fischer, and H. Pappot Oestrogen receptor beta over expression in males with non-small cell lung cancer is associated with better survival Lung Cancer 59 2008 88 94
44. 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. Nat. Acad. Sci. U.S.A. 101 2004 1566 1571
45. F. Suzuki, J. Akahira, I. Miura, T. Suzuki, K. Ito, S. Hayashi, H. Sasano, and N. Yaegashi Loss of estrogen receptor beta isoform expression and its correlation with aberrant DNA methylation of the 5′-untranslated region in human epithelial ovarian carcinoma Cancer Sci. 99 2008 2365 2372
46. S.I. Wang, J. Puc, J. Li, J.N. Bruce, P. Cairns, D. Sidransky, and R. Parsons Somatic mutations of PTEN in glioblastoma multiforme Cancer Res. 57 1997 4183 4186
47. N.S. Wickramasinghe, T.T. Manavalan, S.M. Dougherty, K.A. Riggs, Y. Li, and C.M. Klinge Estradiol downregulates miR-21 expression and increases miR-21 target gene expression in MCF-7 breast cancer cells Nucleic Acids Res. 37 2009 2584 2595
48. X. Wu, M. Subramaniam, S.B. Grygo, Z. Sun, V. Negron, W.L. Lingle, M.P. Goetz, J.N. Ingle, T.C. Spelsberg, and J.R. Hawse Estrogen receptor-beta sensitizes breast cancer cells to the anti-estrogenic actions of endoxifen Breast Cancer Res. 13 2011 R27
49. Yang, L., Wang, Y., Chen, P., Hu, J., Xiong, Y., Feng, D., Liu, H., Zhang, H., Yang, H., He, J., Na(+)/H(+) exchanger regulatory factor 1 (NHERF1) is required for the estradiol-dependent increase of phosphatase and tensin homolog (PTEN) protein expression. Endocrinology. 152, 4537-4549.
50. P.M. Yuet-Kin Leung, Leena Singh, Xuegong Zhu, Irwin Leav, and Shuk-Mei Ho Transcriptional regulation of novel and known estrogen receptor-beta isoforms during prostate carcinogenesis Proc. Am. Assoc. Cancer Res. 46 2005 749
51. C. Zhao, E.W. Lam, A. Sunters, E. Enmark, M.T. De Bella, R.C. Coombes, J.A. Gustafsson, and K. Dahlman-Wright Expression of estrogen receptor beta isoforms in normal breast epithelial cells and breast cancer: regulation by methylation Oncogene 22 2003 7600 7606