Estrogen activation of the mitogen-activated protein kinase is mediated by ER-α36 in ER-positive breast cancer cells

Journal of Steroid Biochemistry and Molecular Biology

Volumn 143, Issue , 2014, Pages 434-443

  Zhang, Xintian ^a   Deng, Hao ^a   Wang, Zhao Yi ^a  

^a CREIGHTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Amphiregulin; EGFR; ER 36; ERK1 2; HB EGF; HER2; IGF IR; Rapid estrogen signaling

Indexed keywords

3 BROMO 5 TERT BUTYL 4 HYDROXYBENZYLIDENEMALONONITRILE; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; 4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; 5 (2 BENZOTHIAZOLYL)THIOMETHYL 4 HYDROXY 3 METHOXYBENZYLIDENECYANOACETAMIDE; AMPHIREGULIN; EPIDERMAL GROWTH FACTOR RECEPTOR; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR ALPHA36; HEPARIN BINDING EPIDERMAL GROWTH FACTOR; ILOMASTAT; LAPATINIB; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; NEUTRALIZING ANTIBODY; SHORT HAIRPIN RNA; SOMATOMEDIN C RECEPTOR; UNCLASSIFIED DRUG; ESTROGEN RECEPTOR ALPHA, HUMAN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE;

3' UNTRANSLATED REGION; ARTICLE; BREAST CANCER CELL LINE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; EXPRESSION VECTOR; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; STABLE TRANSFECTION; STEADY STATE; UPREGULATION; WESTERN BLOTTING; APOPTOSIS; BREAST NEOPLASMS; CELL CYCLE; CELL PROLIFERATION; DRUG EFFECTS; FEMALE; FLOW CYTOMETRY; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL CULTURE;

APOPTOSIS; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL CYCLE; CELL PROLIFERATION; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; FLOW CYTOMETRY; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, ERBB-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 84903825131     PISSN: 09600760     EISSN: 18791220     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2014.06.009     Document Type: Article

References (40)

1. S. Nilsson, S. Mäkelä, E. Treuter, M. Tujague, J. Thomsen, G. Andersson, E. Enmark, K. Pettersson, M. Warner, and J.A. Gustafsson Mechanisms of estrogen action Physiol. Rev. 81 4 2001 1535 1565 (Pubitemid 32951806)
2. B.W. O'Malley, and R. Kumar Nuclear receptor coregulators in cancer biology Cancer Res. 69 21 2009 8217 8222
3. N. Heldring, A. Pike, S. Andersson, J. Matthews, G. Cheng, J. Hartrman, M. Tujague, A. Ström, E. Treuter, and M. Wanter et al. Estrogen receptors: how do they signal and what are their targets Physiol. Rev. 87 3 2007 905 931 (Pubitemid 47084672)
4. M.J. Kelly, and E.R. Levin Rapid actions of plasma membrane estrogen receptors Trends Endocrinol. Metab. 12 4 2001 152 156 (Pubitemid 33713555)
5. E.R. Levin Plasma membrane estrogen receptors Trends Endocrinol. Metab. 20 10 2009 477 482
6. F. Acconcial, and M. Marino The effects of 17β-estradiol in cancer are mediated by estrogen receptor signaling at the plasma membrane Front. Physiol. 2 30 2011 1 8
7. R.J. Pietras, and C.M. Szego Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells Nature 265 5589 1977 69 72 (Pubitemid 8004314)
8. Y. Berthois, N. Pourreau-Schneider, P. Gandilhon, H. Mittrea, N. Tubiana, and P.M. Martina Estrodiol membrane binding sites on human breast cancer cell lines. Use of a fluorescent estradiol conjugate to demonstrate plasma membrane binding systems J. Steroid Biochem. 25 6 1986 963 972 (Pubitemid 17206014)
9. M. Razandi, A. Pedram, G.L. Greene, and E.R. Levin Cell membrane and nuclear estrogen recptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells Mol. Endocrinol. 13 2 1999 307 319 (Pubitemid 29068005)
10. A. Pedram, M. Razandi, and E.R. Levin Nature of functional estrogen receptors at the plasma membrane Mol. Endocrinol. 20 9 2006 1996 2009 (Pubitemid 44286700)
11. S.R. Hammes, and E.R. Levin Extranuclear steroid receptors: nature and actions Endocr. Rev. 28 7 2007 726 741 (Pubitemid 350294293)
12. M. Marino, and P. Ascenzi Membrane association of estrogen receptor alpha and beta influences 17beta-estradiol-mediated cancer cell proliferation Steroids 73 9-10 2008 853 858
13. Z. Chen, I.S. Yuhanna, Z. Galcheva-Gargova, R.H. Karas, M.E. Mendelsohn, and P.W. Shaul Estrogen receptor α mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen J. Clin. Investig. 103 103 1999 401 406 (Pubitemid 29069990)
14. K.S. Russell, M.P. Haynes, D. Sinha, E. Clerisme, and J.R. Bender Human vascular endothelial cells contain membrane binding sites for estradiol, which mediate rapid intracellular signaling Proc. Natl. Acad. Sci. U. S. A. 97 11 2000 5930 5935 (Pubitemid 30367501)
15. J.J. Watters, J.S. Campbell, M.J. Cunningham, E.G. Krebs, and D.M. Dorsa Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signaling cascade and c-fos immediate early gene transcription Endocrinology 138 9 1997 4030 4033 (Pubitemid 27351961)
16. Q. Gu, K.S. Korach, and R.L. Moss Rapid action of 17beta-estradiol on kainite-induced currents in hippocampal reurons lacking intracellular estrogen receptor Endocrinology 140 2 1999 660 666 (Pubitemid 29058198)
17. E.J. Filardo, J.A. Qiunn, 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 transactivation of the epidermal growth factor receptor through release of HB-EGF Mol. Endocrinol. 14 10 2001 1649 1660
18. C.M. Revankar, D.F. Cimino, L.A. Sklar, J.B. Arterburn, and E.R. Prossnitz A transmembrane intracellular estrogen receptor mediates rapid cell signaling Science 307 5715 2005 1625 1630 (Pubitemid 40354745)
19. S. Caristi, J.L. Galera, F. Matarese, M. Imai, S. Caporali, M. Cancemi, L. Altucci, L. Cicatiello, D. Teti, and F. Bresciani et al. Estrogens do not modify MAP kinase-dependent nuclear signaling during stimulation of early G (1) progression in human breast cancer cells Cancer Res. 61 17 2001 6360 6366 (Pubitemid 32783238)
20. S.L. Brower, J.R. Roberts, J.M. Antonini, and M.R. Miller Difficulty demonstrating estradiol-mediated Erk1/2 phosphorylation in MCF-7 cells J. Steroid Biochem. Mol. Biol. 96 5 2005 375 385 (Pubitemid 41384139)
21. E.K. Lobenhofer, and J.R. Marks Estrogen-induced mitogenesis of MCF-7 cells does not require the induction of mitogen-activated protein kinase activity J. Steroid Biochem. Mol. Biol. 75 1 2000 11 20 (Pubitemid 32155419)
22. E.K. Lobenhofer, G. Huper, J.D. Iglehart, and J.R. Marks Inhibition of mitogen-activated protein kinase and phosphatidylinositol 3-kinase activity in MCF-7 cells prevents estrogen-induced mitogenesis Cell Growth Differ. 11 2 2000 99 110 (Pubitemid 30131490)
23. Z.Y. Wang, X.T. 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)
24. Z.Y. Wang, X.T. 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)
25. 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
26. 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-α36, a novel variant of ER-α, mediates estrogen-stimulated proliferation of endometrial carcinoma cells via the PKCδ/ERK pathway PLoS One 5 11 2010 e15408
27. X.T. Zhang, and Z.Y. Wang Estrogen receptor-α variant, ER-α36, is involved in tamoxifen resistance and estrogen hypersensitivity Endocrinology 154 6 2013 1990 1998
28. Z. Nawaz, D.M. Lonard, A.P. Dennis, C.L. Smith, and B.W. O'Malley Proteasome-dependent degradation of the human estrogen receptor Proc. Natl. Acad. Sci. U. S. A. 96 5 1999 1858 1862 (Pubitemid 29117832)
29. C. Mathilde, and H. Richard-Foy Ligand-induced estrogen receptor α degradation by the proteasome: new actors? Nucl. Recept. Signal. 4 2006 e004
30. X.T. Zhang, L.G. Kang, L. Ding, S. Vranic, Z. Gatalic, and Z.Y. Wang A positive feedback loop of ER-α36/EGFR promotes malignant growth of ER-negative breast cancer cells Oncogene 30 6 2011 770 780
31. L.G. Kang, Y.M. Guo, X.T. Zhang, J. Meng, and Z.Y. Wang A positive cross-regulation of HER2 and ER-α36 controls ALDH1 positive breast cancer cells J. Steroid Biochem. Mol. Biol. 127 3 2011 262 268
32. Y. Zou, L. Ding, M. Coleman, and Z.Y. Wang Estrogen receptor-alpha (ER-alpha) suppresses expression of its variant ER-alpha36 FEBS Lett. 583 8 2009 1368 1374
33. 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)
34. R.X. Song, Z. Zhang, Y. Chen, Y. Bao, and R.J. Santen Estrogen signaling via a linear pathway involving insulin-like growth factor I receptor, matrix metalloproteinases, and epidermal growth factor receptor to activate mitogen-activated protein kinase in MCF-7 breast cancer cells Endocrinology 148 8 2007 4091 4101 (Pubitemid 47105855)
35. G.L. Li, J. Zhang, K.T. Jin, K.F. He, Y. Zheng, X. Xu, H.H. Wang, H.Y. Wang, Z.Q. Li, X.F. Yu, X.T. Teng, J. Cao, and L.S. Teng Estrogen receptor-a36 is involved in development of acquired tamoxifen resistance via regulating the growth status switch in breast cancer cells Mol. Oncol. 7 2013 611 624
36. A. Migliaccio, M. Di Domenico, G. Castoria, A. de Falco, P. Bontempo, E. Nola, and F. Auricchio Tyrosine kinase/p21ras/MAP-kinase pathway activation by estradiol-receptor complex in MCF-7 cells EMBO J. 15 6 1996 1292 1300
37. C.B. Wade, S. Robinson, R.A. Shapiro, and D.M. Dorsa Estrogen receptor (ER) alpha and ERbeta exhibit unique pharmacologic properties when coupled to activation of the mitogen-activated protein kinase pathway Endocrinology 142 6 2001 2336 2342 (Pubitemid 32473088)
38. I.S. Nethrapalli, A.A. Tinnikov, V. Krishnan, C.D. Lei, and C.D. Toran-Allerand Estrogen activates mitogen-activated protein kinase in native, nontransfected CHO-K1, COS-7, and RAT2 fibroblast cell lines Endocrinology 146 1 2005 56 63 (Pubitemid 40051723)
39. I. Martínez-Lacaci, M. Saceda, G.D. Plowman, G.R. Johnson, N. Normanno, D.S. Salomon, and R.B. Dickson Estrogen and phorbol esters regulate amphiregulin expression by two separate mechanisms in human breast cancer cell lines Endocrinology 136 9 1995 3983 3992
40. A. Migliaccio, G. Castoria, M. Di Domenico, A. de Falco, A. Bilancio, M. Lombardi, D. Bottero, L. Varricchio, M. Nanayakkara, and A. Rotondi et al. Sex steroid hormones act as growth factors J. Steroid Biochem. Mol. Biol. 83 1-5 2002 31 35 (Pubitemid 37040639)