Cellular targets of estrogen signaling in regeneration of inner ear sensory epithelia

Hearing Research

Volumn 252, Issue 1-2, 2009, Pages 61-70

  McCullar, Jennifer S ^a   Oesterle, Elizabeth C ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

Cochlea; EGF; Estrogen; Regeneration; Review; TGF ; TGF

Indexed keywords

EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; AUDITORY SYSTEM; CELL INTERACTION; CELL PROLIFERATION; CELL REGENERATION; EMBRYONIC STEM CELL; HUMAN; HUMAN CELL; INNER EAR; MOUSE; NEUROEPITHELIUM; NONHUMAN; PRIORITY JOURNAL; SIGNAL PROCESSING; VESTIBULAR SYSTEM;

ANIMALS; CELL PROLIFERATION; EAR, INNER; EMBRYONIC STEM CELLS; EPIDERMAL GROWTH FACTOR; ESTROGENS; FEMALE; HUMANS; MALE; MODELS, BIOLOGICAL; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, ESTROGEN; REGENERATION; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA;

EID: 67349183981     PISSN: 03785955     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.heares.2009.01.012     Document Type: Article

References (179)

1. Adler H.J., and Raphael Y. New hair cells arise from supporting cell conversion in the acoustically damaged chick inner ear. Neurosci. Lett. 205 1 (1996) 17-20
2. Al-Dhaheri M.H., and Rowan B.G. Protein kinase A exhibits selective modulation of estradiol-dependent transcription in breast cancer cells that is associated with decreased ligand binding, altered estrogen receptor alpha promoter interaction, and changes in receptor phosphorylation. Mol. Endocrinol. 21 2 (2007) 439-456
3. Alonso-Magdalena P., Ropero A.B., Carrera M.P., Cederroth C.R., Baquie M., Gauthier B.R., Nef S., Stefani E., and Nadal A. Pancreatic insulin content regulation by the estrogen receptor ER alpha. PLoS ONE 3 4 (2008) e2069
4. Asarian L. Membrane estrogen receptors and energy homeostasis. J. Neurosci. 26 44 (2006) 11255-11256
5. Ashcroft G.S., Dodsworth J., van Boxtel E., Tarnuzzer R.W., Horan M.A., Schultz G.S., and Ferguson M.W. Estrogen accelerates cutaneous wound healing associated with an increase in TGF-beta1 levels. Nat. Med. 3 11 (1997) 1209-1215
6. Ashcroft G.S., Mills S.J., Flanders K.C., Lyakh L.A., Anzano M.A., Gilliver S.C., and Roberts A.B. Role of Smad3 in the hormonal modulation of in vivo wound healing responses. Wound Repair Regen. 11 6 (2003) 468-473
7. Auger A.P. Ligand-independent activation of progestin receptors: relevance for female sexual behaviour. Reproduction 122 6 (2001) 847-855
8. Baraldi Gdos S., de Almeida L.C., and Borges A.C. Hearing loss in aging. Rev. Bras. Otorrinolaringol. (Engl. Ed.) 73 1 (2007) 58-64
9. Barkhem T., Nilsson S., and Gustafsson J.A. Molecular mechanisms, physiological consequences and pharmacological implications of estrogen receptor action. Am. J. Pharmacogenomics 4 1 (2004) 19-28
10. Barros R.P.A., Machado U.F., and Gustafsson J.-A. Estrogen receptors: new players in diabetes mellitus. Trends Mol. Med. 12 9 (2006) 425-431
11. Berno V., Amazit L., Hinojos C., Zhong J., Mancini M.G., Sharp Z.D., and Mancini M.A. Activation of estrogen receptor-alpha by E2 or EGF induces temporally distinct patterns of large-scale chromatin modification and mRNA transcription. PLoS ONE 3 5 (2008) e2286
12. Blaustein J.D. Minireview: neuronal steroid hormone receptors: they are not just for hormones anymore. Endocrinology 145 3 (2004) 1075-1081
13. Bodo C., and Rissman E.F. New roles for estrogen receptor beta in behavior and neuroendocrinology. Front Neuroendocrinol. 27 2 (2006) 217-232
14. Brannvall K., Korhonen L., and Lindholm D. Estrogen-receptor-dependent regulation of neural stem cell proliferation and differentiation. Mol. Cell. Neurosci. 21 3 (2002) 512-520
15. Buck M., and Knabbe C. TGF-beta signaling in breast cancer. Ann. NY Acad. Sci. 1089 (2006) 119-126
16. Bunone G., Briand P.A., Miksicek R.J., and Picard D. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J. 15 9 (1996) 2174-2183
17. Burdette J.E., and Woodruff T.K. Activin and estrogen crosstalk regulates transcription in human breast cancer cells. Endocr. Relat. Cancer 14 3 (2007) 679-689
18. Cafaro J., Lee G.S., and Stone J.S. Atoh1 expression defines activated progenitors and differentiating hair cells during avian hair cell regeneration. Dev. Dyn. 236 1 (2007) 156-170
19. Cano D.A., Rulifson I.C., Heiser P.W., Swigart L.B., Pelengaris S., German M., Evan G.I., Bluestone J.A., and Hebrok M. Regulated beta-cell regeneration in the adult mouse pancreas. Diabetes 57 4 (2008) 958-966
20. Cao A., and Zhang C. Sex-specific effects of androgen and estrogen on proliferation of the embryonic chicken hypothalamic neurons. Endocrine 31 2 (2007) 161-166
21. Carmeci C., Thompson D.A., Ring H.Z., Francke U., and Weigel R.J. Identification of a gene (GPR30) with homology to the G-protein-coupled receptor superfamily associated with estrogen receptor expression in breast cancer. Genomics 45 3 (1997) 607-617
22. Carraway K.L., and Burden S.J. Neuregulins and their receptors. Curr. Opin. Neurobiol. 5 5 (1995) 606-612
23. Chardin S., and Romand R. Regeneration and mammalian auditory hair cells. Science 267 5198 (1995) 707-711
24. Chen D., Pace P.E., Coombes R.C., and Ali S. Phosphorylation of human estrogen receptor alpha by protein kinase A regulates dimerization. Mol. Cell. Biol. 19 2 (1999) 1002-1015
25. Chen P., and Segil N. P27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126 8 (1999) 1581-1590
26. Chen S., Ye J., Kijima I., Kinoshita Y., and Zhou D. Positive and negative transcriptional regulation of aromatase expression in human breast cancer tissue. J. Steroid Biochem. Mol. Biol. 95 1-5 (2005) 17-23
27. Cherlet T., and Murphy L.C. Estrogen receptors inhibit Smad3 transcriptional activity through Ap-1 transcription factors. Mol. Cell. Biochem. 306 1-2 (2007) 33-42
28. Cheskis B.J., Greger J.G., Nagpal S., and Freedman L.P. Signaling by estrogens. J. Cell. Physiol. 213 3 (2007) 610-617
29. Ciana P., Ghisletti S., Mussi P., Eberini I., Vegeto E., and Maggi A. Estrogen Receptor {alpha}, a Molecular Switch Converting Transforming Growth Factor-{alpha}-mediated Proliferation into Differentiation in Neuroblastoma Cells. J. Biol. Chem. 278 34 (2003) 31737-31744
30. Clarke C.H., Norfleet A.M., Clarke M.S., Watson C.S., Cunningham K.A., and Thomas M.L. Perimembrane localization of the estrogen receptor alpha protein in neuronal processes of cultured hippocampal neurons. Neuroendocrinology 71 1 (2000) 34-42
31. Coleman K.M., and Smith C.L. Intracellular signaling pathways: nongenomic actions of estrogens and ligand-independent activation of estrogen receptors. Front Biosci. 6 (2001) D1379-D1391
32. Collado M.S., Burns J.C., Hu Z., and Corwin J.T. Recent advances in hair cell regeneration research. Curr. Opin. Otolaryngol. Head Neck Surg. 16 5 (2008) 465-471
33. Concina P., Sordello S., Barbacanne M.A., Elhage R., Pieraggi M.T., Fournial G., Plouet J., Bayard F., and Arnal J.F. The mitogenic effect of 17beta-estradiol on in vitro endothelial cell proliferation and on in vivo reendothelialization are both dependent on vascular endothelial growth factor. J. Vasc. Res. 37 3 (2000) 202-208
34. Cornil C.A., Ball G.F., and Balthazart J. Functional significance of the rapid regulation of brain estrogen action: where do the estrogens come from?. Brain Res 1126 1 (2006) 2-26
35. Corwin J., and Cotanche D. Regeneration of sensory hair cells after acoustic trauma. Science 240 4860 (1988) 1772-1774
36. Corwin J., Warchol M., Saffer L., Finley J., Gu R., and Lamber P. Growth factors as potential drugs for the sensory epithelia of the ear. Ciba Found Symp. 196 (1996) 167-182 (discussion 182-187)
37. Cvoro A., Tzagarakis-Foster C., Tatomer D., Paruthiyil S., Fox M.S., and Leitman D.C. Distinct roles of unliganded and liganded estrogen receptors in transcriptional repression. Mol. Cell. 21 4 (2006) 555-564
38. de Caestecker M. The transforming growth factor-beta superfamily of receptors. Cytokine Growth Factor Rev. 15 1 (2004) 1-11
39. Demay F., De Monti M., Tiffoche C., Vaillant C., and Thieulant M.L. Steroid-independent activation of er by gnrh in gonadotrope pituitary cells. Endocrinology 142 8 (2001) 3340-3347
40. Ding J., and Zhu B.T. Unique effect of the pregnancy hormone estriol on antigen-induced production of specific antibodies in female BALB/c mice. Steroids 73 3 (2008) 289-298
41. Dreisbach L.E., Kramer S.J., Cobos S., and Cowart K. Racial and gender effects on pure-tone thresholds and distortion-product otoacoustic emissions (DPOAEs) in normal-hearing young adults. Int. J. Audiol. 46 8 (2007) 419-426
42. El-Tanani M.K., and Green C.D. Two separate mechanisms for ligand-independent activation of the estrogen receptor. Mol. Endocrinol. 11 7 (1997) 928-937
43. Elliot S.J., Karl M., Berho M., Xia X., Pereria-Simon S., Espinosa-Heidmann D., and Striker G.E. Smoking induces glomerulosclerosis in aging estrogen-deficient mice through cross-talk between TGF-beta1 and IGF-I signaling pathways. J. Am. Soc. Nephrol. 17 12 (2006) 3315-3324
44. Filardo E., Quinn J., Pang Y., Graeber C., Shaw S., Dong J., and Thomas P. Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane. Endocrinology 148 7 (2007) 3236-3245
45. Filardo E.J. Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J. Steroid Biochem. Mol. Biol. 80 2 (2002) 231-238
46. Filardo E.J., Quinn J.A., Bland K.I., and Frackelton Jr. A.R. 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
47. Filardo E.J., Quinn J.A., Frackelton Jr. A.R., and Bland K.I. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol. Endocrinol. 16 1 (2002) 70-84
48. Filardo E.J., Quinn J.A., and Sabo E. Association of the membrane estrogen receptor, GPR30, with breast tumor metastasis and transactivation of the epidermal growth factor receptor. Steroids 73 9-10 (2008) 870-873
49. Filardo E.J., and Thomas P. GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol. Metab. 16 8 (2005) 362-367
50. Flint A.P., Sheldrick E.L., and Fisher P.A. Ligand-independent activation of steroid receptors. Domest Anim. Endocrinol. 23 1-2 (2002) 13-24
51. Gandrillon O., Schmidt U., Beug H., and Samarut J. TGF-beta cooperates with TGF-alpha to induce the self-renewal of normal erythrocytic progenitors: evidence for an autocrine mechanism. EMBO J. 18 10 (1999) 2764-2781
52. Gargett C.E., Chan R.W., and Schwab K.E. Hormone and growth factor signaling in endometrial renewal: Role of stem/progenitor cells. Mol. Cell. Endocrinol 288 1-2 (2008) 22-29
53. Gilliver S.C., Ashworth J.J., and Ashcroft G.S. The hormonal regulation of cutaneous wound healing. Clin. Dermatol. 25 1 (2007) 56-62
54. Girod D., Duckert L., and Rubel E. Possible precursors of regenerated hair cells in the avian cochlea following acoustic trauma. Hear Res. 42 2-3 (1989) 175-194
55. Gottfried-Blackmore A., Croft G., Clark J., McEwen B.S., Jellinck P.H., and Bulloch K. Characterization of a cerebellar granule progenitor cell line, EtC.1, and its responsiveness to 17-beta-estradiol. Brain Res. 1186 (2007) 29-40
56. Gu R., Montcouquiol M., Marchionni M., and Corwin J.T. Proliferative responses to growth factors decline rapidly during postnatal maturation of mammalian hair cell epithelia. Eur. J. Neurosci. 25 5 (2007) 1363-1372
57. Guimaraes P., Frisina S.T., Mapes F., Tadros S.F., Frisina D.R., and Frisina R.D. Progestin negatively affects hearing in aged women. Proc. Natl. Acad. Sci. USA 103 38 (2006) 14246-14249
58. Guimaraes P., Zhu X., Cannon T., Kim S., and Frisina R.D. Sex differences in distortion product otoacoustic emissions as a function of age in CBA mice. Hear Res. 192 1-2 (2004) 83-89
59. Hall J.M., Couse J.F., and Korach K.S. The multifaceted mechanisms of estradiol and estrogen receptor signaling. J. Biol. Chem. 276 40 (2001) 36869-36872
60. Han H.J., Heo J.S., and Lee Y.J. Estradiol-17beta stimulates proliferation of mouse embryonic stem cells: involvement of MAPKs and CDKs as well as protooncogenes. Am. J. Physiol. Cell. Physiol. 290 4 (2006) C1067-C1075
61. Hanna G.S. Sudden deafness and the contraceptive pill. J. Laryngol. Otol. 100 6 (1986) 701-706
62. Hart L.L., and Davie J.R. The estrogen receptor: more than the average transcription factor. Biochem. Cell. Biol. 80 3 (2002) 335-341
63. Hawkins R.D., Bashiardes S., Powder K.E., Sajan S.A., Bhonagiri V., Alvarado D.M., Speck J., Warchol M.E., and Lovett M. Large scale gene expression profiles of regenerating inner ear sensory epithelia. PLoS ONE 2 (2007) e525
64. Hederstierna C., Hultcrantz M., Collins A., and Rosenhall U. Hearing in women at menopause. Prevalence of hearing loss, audiometric configuration and relation to hormone replacement therapy. Acta Otolaryngol. 127 2 (2007) 149-155
65. Heldring N., Pike A., Andersson S., Matthews J., Cheng G., Hartman J., Tujague M., Strom A., Treuter E., Warner M., and Gustafsson J.-A. Estrogen receptors: how do they signal and what are their targets. Physiol. Rev. 87 3 (2007) 905-931
66. Hewitt S.C., Collins J., Grissom S., Deroo B., and Korach K.S. Global uterine genomics in vivo: microarray evaluation of the estrogen receptor alpha-growth factor cross-talk mechanism. Mol. Endocrinol. 19 3 (2005) 657-668
67. Hong L., Colpan A., and Peptan I.A. Modulations of 17-beta estradiol on osteogenic and adipogenic differentiations of human mesenchymal stem cells. Tissue Eng. 12 10 (2006) 2747-2753
68. Hong L., Colpan A., Peptan I.A., Daw J., George A., and Evans C.A. 17-Beta estradiol enhances osteogenic and adipogenic differentiation of human adipose-derived stromal cells. Tissue Eng. 13 6 (2007) 1197-1203
69. Horner K.C., Cazals Y., Guieu R., Lenoir M., and Sauze N. Experimental estrogen-induced hyperprolactinemia results in bone-related hearing loss in the guinea pig. Am. J. Physiol. Endocrinol. Metab. 293 5 (2007) E1224-E1232
70. Hultcrantz M., Simonoska R., and Stenberg A. Estrogen and hearing: a summary of recent investigations. Acta Otolaryngol. 126 1 (2006) 10-14
71. Hume C., Kirkegaard M., and Oesterle E. ErbB expression: the mouse inner ear and maturation of the mitogenic response to heregulin. J. Assoc. Res. Otolaryngol. 4 3 (2003) 422-443
72. Imamov O., Shim G.J., Warner M., and Gustafsson J.A. Estrogen receptor beta in health and disease. Biol. Reprod. 73 5 (2005) 866-871
73. Izumikawa M., Minoda R., Kawamoto K., Abrashkin K.A., Swiderski D.L., Dolan D.F., Brough D.E., and Raphael Y. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat. Med. 11 3 (2005) 271-276
74. Jonsson R., Rosenhall U., Gause-Nilsson I., and Steen B. Auditory function in 70- and 75-year-olds of four age cohorts. A cross-sectional and time-lag study of presbyacusis. Scand. Audiol. 27 2 (1998) 81-93
75. Junier M.-P. What role(s) for TGF[alpha] in the central nervous system?. Prog. Neurobiol. 62 5 (2000) 443-473
76. Kanda N., and Watanabe S. Regulatory roles of sex hormones in cutaneous biology and immunology. J. Dermatol. Sci. 38 1 (2005) 1-7
77. Kato S., Endoh H., Masuhiro Y., Kitamoto T., Uchiyama S., Sasaki H., Masushige S., Gotoh Y., Nishida E., Kawashima H., Metzger D., and Chambon P. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270 5241 (1995) 1491-1494
78. Kawase Y., Yanagi Y., Takato T., Fujimoto M., and Okochi H. Characterization of multipotent adult stem cells from the skin: transforming growth factor-beta (TGF-beta) facilitates cell growth. Exp. Cell Res. 295 1 (2004) 194-203
79. Kelly M.J., and Levin E.R. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol. Metab. 12 4 (2001) 152-156
80. Kilicdag E.B., Yavuz H., Bagis T., Tarim E., Erkan A.N., and Kazanci F. Effects of estrogen therapy on hearing in postmenopausal women. Am. J. Obstet. Gynecol. 190 1 (2004) 77-82
81. Kim J.K., and Levin E.R. Estrogen signaling in the cardiovascular system. Nucl. Recept. Signal 4 (2006) e013
82. Kim S.H., Chae H.D., Kang B.M., and Kim C.H. The association between serum estradiol level and hearing sensitivity in postmenopausal women. Obstet. Gynecol. 99 5 Pt 1 (2002) 726-730
83. Kipp J.L., Kilen S.M., Bristol-Gould S., Woodruff T.K., and Mayo K.E. Neonatal exposure to estrogens suppresses activin expression and signaling in the mouse ovary. Endocrinology 148 5 (2007) 1968-1976
84. Kipp J.L., Kilen S.M., Woodruff T.K., and Mayo K.E. Activin regulates estrogen receptor gene expression in the mouse ovary. J. Biol. Chem. 282 50 (2007) 36755-36765
85. Kleuser B., Malek D., Gust R., Pertz H.H., and Potteck H. 17-{beta}-Estradiol inhibits Transforming Growth Factor-{beta} signalling and function in breast cancer cells via activation of Extracellular Signal-Regulated Kinase through the G protein coupled receptor 30. Mol. Pharmacol. 74 6 (2008) 1533-1543
86. Korach K.S. Insights from the study of animals lacking functional estrogen receptor. Science 266 5190 (1994) 1524-1527
87. Kuiper G.G., Carlsson B., Grandien K., Enmark E., Haggblad J., Nilsson S., and Gustafsson J.A. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology 138 3 (1997) 863-870
88. Kuntz A., and Oesterle E. Transforming growth factor alpha with insulin stimulates cell proliferation in vivo in adult rat vestibular sensory epithelium. J. Comp. Neurol. 399 3 (1998) 413-423
89. Kusumegi T., Tanaka J., Kawano M., Yonemoto J., Tohyama C., and Sone H. BMP7/ActRIIB regulates estrogen-dependent apoptosis: new biomarkers for environmental estrogens. J. Biochem. Mol. Toxicol. 18 1 (2004) 1-11
90. Lambard S., Silandre D., Delalande C., Denis-Galeraud I., Bourguiba S., and Carreau S. Aromatase in testis: expression and role in male reproduction. J. Steroid Biochem. Mol. Biol. 95 1-5 (2005) 63-69
91. Lambert P.R. Inner ear hair cell regeneration in a mammal: identification of a triggering factor. Laryngoscope 104 6 Pt 1 (1994) 701-718
92. Lau K.H., Kapur S., Kesavan C., and Baylink D.J. Up-regulation of the Wnt, estrogen receptor, insulin-like growth factor-I, and bone morphogenetic protein pathways in C57BL/6J osteoblasts as opposed to C3H/HeJ osteoblasts in part contributes to the differential anabolic response to fluid shear. J. Biol. Chem. 281 14 (2006) 9576-9588
93. Leary A., and Dowsett M. Combination therapy with aromatase inhibitors: the next era of breast cancer treatment?. Br. J. Cancer 95 6 (2006) 661-666
94. Lecanda J., Parekh T., Gama P., Lin K., Liarski V., Uretsky S., Mittal K., and Gold L. Transforming growth factor-beta, estrogen, and progesterone converge on the regulation of p27Kip1 in the normal and malignant endometrium. Cancer Res. 67 3 (2007) 1007-1018
95. Leung Y.K., Mak P., Hassan S., and Ho S.M. Estrogen receptor (ER)-beta isoforms: a key to understanding ER-beta signaling. Proc. Natl. Acad. Sci. USA 103 35 (2006) 13162-13167
96. Levin E.R. Cellular functions of the plasma membrane estrogen receptor. Trends Endocrinol. Metab. 10 9 (1999) 374-377
97. Li H., Liu H., and Heller S. Pluripotent stem cells from the adult mouse inner ear. Nat. Med. 9 10 (2003) 1293-1299
98. Li L., and Forge A. Morphological evidence for supporting cell to hair cell conversion in the mammalian utricular macula. Int. J. Dev. Neurosci. 15 4-5 (1997) 433-446
99. Li Q., Karam S.M., Coerver K.A., Matzuk M.M., and Gordon J.I. Stimulation of activin receptor II signaling pathways inhibits differentiation of multiple gastric epithelial lineages. Mol. Endocrinol. 12 2 (1998) 181-192
100. Linggi B., and Carpenter G. ErbB receptors: new insights on mechanisms and biology. Trends Cell Biol. 16 12 (2006) 649-656
101. Liu X.Z., and Yan D. Ageing and hearing loss. J. Pathol. 211 2 (2007) 188-197
102. Longo M., Peruzzi B., Fortunati D., De Luca V., Denger S., Caselli G., Migliaccio S., and Teti A. Modulation of human estrogen receptor alpha F promoter by a protein kinase C/c-Src-dependent mechanism in osteoblast-like cells. J. Mol. Endocrinol. 37 3 (2006) 489-502
103. Lowenheim H., Furness D.N., Kil J., Zinn C., Gultig K., Fero M.L., Frost D., Gummer A.W., Roberts J.M., Rubel E.W., Hackney C.M., and Zenner H.P. Gene disruption of p27(Kip1) allows cell proliferation in the postnatal and adult organ of corti. Proc. Natl. Acad. Sci. USA 96 7 (1999) 4084-4088
104. Ma Y., Hu C., Riegel A.T., Fan S., and Rosen E.M. Growth factor signaling pathways modulate BRCA1 repression of estrogen receptor-alpha activity. Mol. Endocrinol. 21 8 (2007) 1905-1923
105. Malek D., Gust R., and Kleuser B. 17-Beta-estradiol inhibits transforming-growth-factor-beta-induced MCF-7 cell migration by Smad3-repression. Eur. J. Pharmacol. 534 1-3 (2006) 39-47
106. Malgrange B., Rigo J.M., Coucke P., Thiry M., Hans G., Nguyen L., van de Water T.R., Moonen G., and Lefebvre P.P. Identification of factors that maintain mammalian outer hair cells in adult organ of Corti explants. Hear Res. 170 1-2 (2002) 48-58
107. Marino M., Galluzzo P., and Ascenzi P. Estrogen signaling multiple pathways to impact gene transcription. Curr. Genomics 7 8 (2006) 497-508
108. Marquez D.C., Lee J., Lin T., and Pietras R.J. Epidermal growth factor receptor and tyrosine phosphorylation of estrogen receptor. Endocrine 16 2 (2001) 73-81
109. Martinez-Monedero R., Oshima K., Heller S., and Edge A.S. The potential role of endogenous stem cells in regeneration of the inner ear. Hear Res. 227 1-2 (2007) 48-52
110. Matsuda K., Sakamoto H., Mori H., Hosokawa K., Kawamura A., Itose M., Nishi M., Prossnitz E.R., and Kawata M. Expression and intracellular distribution of the G protein-coupled receptor 30 in rat hippocampal formation. Neurosci. Lett. 441 1 (2008) 94-99
111. Matthews J., and Gustafsson J.A. Estrogen signaling: a subtle balance between ER alpha and ER beta. Mol. Interv. 3 5 (2003) 281-292
112. McCroskery S., Thomas M., Maxwell L., Sharma M., and Kambadur R. Myostatin negatively regulates satellite cell activation and self-renewal. J. Cell Biol. 162 6 (2003) 1135-1147
113. McFadden D. Masculinization effects in the auditory system. Arch. Sex Behav. 31 1 (2002) 99-111
114. Meltser I., Tahera Y., Simpson E., Hultcrantz M., Charitidi K., Gustafsson J.K., and Canlon B. Estrogen receptor beta protects against acoustic trauma in mice. J. Clin. Invest. 118 4 (2008) 1563-1570
115. Moeller M.P. Current state of knowledge: psychosocial development in children with hearing impairment. Ear Hear. 28 6 (2007) 729-739
116. Moeller M.P., Tomblin J.B., Yoshinaga-Itano C., Connor C.M., and Jerger S. Current state of knowledge: language and literacy of children with hearing impairment. Ear Hear. 28 6 (2007) 740-753
117. Montcouquiol M., and Corwin J. Intracellular signals that control cell proliferation in mammalian balance epithelia: key roles for phosphatidylinositol-3 kinase, mammalian target of rapamycin, and S6 kinases in preference to calcium, protein kinase C, and mitogen-activated protein kinase. J. Neurosci. 21 2 (2001) 570-580
118. Moraghan T., Antoniucci D.M., Grenert J.P., Sieck G.C., Johnson C., Miller V.M., and Fitzpatrick L.A. Differential response in cell proliferation to beta estradiol in coronary arterial vascular smooth muscle cells obtained from mature female versus male animals. Endocrinology 137 11 (1996) 5174-5177
119. Morales A., Gonzalez M., Marin R., Diaz M., and Alonso R. Estrogen inhibition of norepinephrine responsiveness is initiated at the plasma membrane of GnRH-producing GT1-7 cells. J. Endocrinol. 194 1 (2007) 193-200
120. Nagashima T., Suzuki T., Kondo S., Kuroki Y., Takahashi K., Ide K., Yumoto N., Hasegawa A., Toyoda T., Kojima T., Konagaya A., Suzuki H., Hayashizaki Y., Sakaki Y., and Hatakeyama M. Integrative genome-wide expression analysis bears evidence of estrogen receptor-independent transcription in heregulin-stimulated MCF-7 cells. PLoS ONE 3 3 (2008) e1803
121. Nephew K.P., Long X., Osborne E., Burke K.A., Ahluwalia A., and Bigsby R.M. Effect of estradiol on estrogen receptor expression in rat uterine cell types. Biol. Reprod. 62 1 (2000) 168-177
122. Nilsson S., Makela S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Warner M., and Gustafsson J.A. Mechanisms of estrogen action. Physiol. Rev. 81 4 (2001) 1535-1565
123. Oesterle E., Cunningham D., Westrum L., and Rubel E. Ultrastructural analysis of [3H]thymidine-labeled cells in the rat utricular macula. J. Comp. Neurol. 463 2 (2003) 177-195
124. Ogata Y., Slepecky N.B., and Takahashi M. Study of the gerbil utricular macula following treatment with gentamicin, by use of bromodeoxyuridine and calmodulin immunohistochemical labelling. Hear Res. 133 1-2 (1999) 53-60
125. Ogawa S., Inoue S., Watanabe T., Orimo A., Hosoi T., Ouchi Y., and Muramatsu M. Molecular cloning and characterization of human estrogen receptor betacx: a potential inhibitor ofestrogen action in human. Nucleic Acids Res. 26 15 (1998) 3505-3512
126. Ohnemus U., Uenalan M., Inzunza J., Gustafsson J.A., and Paus R. The hair follicle as an estrogen target and source. Endocr. Rev. 27 6 (2006) 677-706
127. Okulicz G. Inner ear disturbance following long-term usage of hormonal contraceptives (author's transl). HNO 26 10 (1978) 330-334
128. Osborne C.K., Schiff R., Fuqua S.A., and Shou J. Estrogen receptor: current understanding of its activation and modulation. Clin. Cancer Res. 7 12 Suppl. (2001) 4338s-4342s (discussion 4411s-4412s)
129. Oshima K., Grimm C.M., Corrales C.E., Senn P., Martinez Monedero R., Geleoc G.S., Edge A., Holt J.R., and Heller S. Differential distribution of stem cells in the auditory and vestibular organs of the inner ear. J. Assoc. Res. Otolaryngol. 8 1 (2007) 18-31
130. Paez-Pereda M., Giacomini D., Refojo D., Nagashima A.C., Hopfner U., Grubler Y., Chervin A., Goldberg V., Goya R., Hentges S.T., Low M.J., Holsboer F., Stalla G.K., and Arzt E. Involvement of bone morphogenetic protein 4 (BMP-4) in pituitary prolactinoma pathogenesis through a Smad/estrogen receptor crosstalk. Proc. Natl. Acad. Sci. USA 100 3 (2003) 1034-1039
131. Pak T.R., Chung W.C., Roberts J.L., and Handa R.J. Ligand-independent effects of estrogen receptor beta on mouse gonadotropin-releasing hormone promoter activity. Endocrinology 147 4 (2006) 1924-1931
132. Pappas T.C., Gametchu B., and Watson C.S. Membrane estrogen receptors identified by multiple antibody labeling and impeded-ligand binding. Faseb J. 9 5 (1995) 404-410
133. Picciotti P.M., Fetoni A.R., Paludetti G., Wolf F.I., Torsello A., Troiani D., Ferraresi A., Pola R., and Sergi B. Vascular endothelial growth factor (VEGF) expression in noise-induced hearing loss. Hear Res. 214 1-2 (2006) 76-83
134. Pietras R.J., Arboleda J., Reese D.M., Wongvipat N., Pegram M.D., Ramos L., Gorman C.M., Parker M.G., Sliwkowski M.X., and Slamon D.J. HER-2 tyrosine kinase pathway targets estrogen receptor and promotes hormone-independent growth in human breast cancer cells. Oncogene 10 12 (1995) 2435-2446
135. Pirskanen A., Kiefer J.C., and Hauschka S.D. IGFs, insulin, Shh, bFGF, and TGF-beta1 interact synergistically to promote somite myogenesis in vitro. Dev. Biol. 224 2 (2000) 189-203
136. Pleis J.R., and Lethbridge-Cejku M. Summary health statistics for US adults: National Health Interview Survey, 2005. Vital Health Stat. 10 232 (2006) 1-153
137. Power R.F., Mani S.K., Codina J., Conneely O.M., and O'Malley B.W. Dopaminergic and ligand-independent activation of steroid hormone receptors. Science 254 5038 (1991) 1636-1639
138. Presson J.C., and Popper A.N. Possible precursors to new hair cells, support cells, and Schwann cells in the ear of a post-embryonic fish. Hear Res. 46 1-2 (1990) 9-21
139. Ramsey T.L., Risinger K.E., Jernigan S.C., Mattingly K.A., and Klinge C.M. Estrogen receptor beta isoforms exhibit differences in ligand-activated transcriptional activity in an estrogen response element sequence-dependent manner. Endocrinology 145 1 (2004) 149-160
140. Raphael Y., Adler H.J., Wang Y., and Finger P.A. Cell cycle of transdifferentiating supporting cells in the basilar papilla. Hear Res. 80 1 (1994) 53-63
141. Revankar C.M., Cimino D.F., Sklar L.A., Arterburn J.B., and Prossnitz E.R. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 307 5715 (2005) 1625-1630
142. Riese II D.J., and Stern D.F. Specificity within the EGF family/ErbB receptor family signaling network. Bioessays 20 1 (1998) 41-48
143. Roberson D., and Rubel E. Cell division in the gerbil cochlea after acoustic trauma. Am. J. Otol. 15 1 (1994) 28-34
144. Roberson D.W., Alosi J.A., and Cotanche D.A. Direct transdifferentiation gives rise to the earliest new hair cells in regenerating avian auditory epithelium. J. Neurosci. Res. 78 4 (2004) 461-471
145. Roepke T.A., Xue C., Bosch M.A., Scanlan T.S., Kelly M.J., and Ronnekleiv O.K. Genes Associated with Membrane-initiated Signaling of Estrogen and Energy Homeostasis. Endocrinology. 149 12 (2008) 6113-6124
146. Rubel E., Dew L., and Roberson D. Mammalian vestibular hair cell regeneration. Science 267 5198 (1995) 701-707
147. Ruben R.J. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol.: Suppl. 220 (1967) 1-44
148. Ryals B., and Rubel E. Hair cell regeneration after acoustic trauma in adult Coturnix quail. Science 240 4860 (1988) 1774-1776
149. Sajan S.A., Warchol M.E., and Lovett M. Toward a systems biology of mouse inner ear organogenesis: gene expression pathways, patterns and network analysis. Genetics 177 1 (2007) 631-653
150. Shifren J.L., Tseng J.F., Zaloudek C.J., Ryan I.P., Meng Y.G., Ferrara N., Jaffe R.B., and Taylor R.N. Ovarian steroid regulation of vascular endothelial growth factor in the human endometrium: implications for angiogenesis during the menstrual cycle and in the pathogenesis of endometriosis. J. Clin. Endocrinol. Metab. 81 8 (1996) 3112-3118
151. Sinkevicius K.W., Burdette J.E., Woloszyn K., Hewitt S.C., Hamilton K., Sugg S.L., Temple K.A., Wondisford F.E., Korach K.S., Woodruff T.K., and Greene G.L. An estrogen receptor-alpha knock-in mutation provides evidence of ligand-independent signaling and allows modulation of ligand-induced pathways in vivo. Endocrinology 149 6 (2008) 2970-2979
152. Sobkowicz H.M., August B.K., and Slapnick S.M. Epithelial repair following mechanical injury of the developing organ of Corti in culture: an electron microscopic and autoradiographic study. Exp. Neurol. 115 1 (1992) 44-49
153. Sobkowicz H.M., August B.K., and Slapnick S.M. Post-traumatic survival and recovery of the auditory sensory cells in culture. Acta Otolaryngol. 116 2 (1996) 257-262
154. Sobkowicz H.M., August B.K., and Slapnick S.M. Cellular interactions as a response to injury in the organ of Corti in culture. Int. J. Dev. Neurosci. 15 4-5 (1997) 463-485
155. Son E., Lee J., Lee S., Kim M., Lee B., Chang I., and Chung J. Topical application of 17beta-estradiol increases extracellular matrix protein synthesis by stimulating tgf-Beta signaling in aged human skin in vivo. J. Invest. Dermatol. 124 6 (2005) 1149-1161
156. Stenberg A., Wang H., Sahlin L., and Hultcrantz M. Mapping of estrogen receptors alpha and beta in the inner ear of mouse and rat. Hear Res. 136 1-2 (1999) 29-34
157. Strachan D. Sudden sensorineural deafness and hormone replacement therapy. J. Laryngol. Otol. 110 12 (1996) 1148-1150
158. Talwar R.M., Wong B.S., Svoboda K., and Harper R.P. Effects of estrogen on chondrocyte proliferation and collagen synthesis in skeletally mature articular cartilage. J. Oral Maxillofac. Surg. 64 4 (2006) 600-609
159. Tanapat P., Hastings N.B., Reeves A.J., and Gould E. Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J. Neurosci. 19 14 (1999) 5792-5801
160. Tang S., Tan S.L., Ramadoss S.K., Kumar A.P., Tang M.H., and Bajic V.B. Computational method for discovery of estrogen responsive genes. Nucleic Acids Res. 32 21 (2004) 6212-6217
161. Teng J., Wang Z.Y., Prossnitz E.R., and Bjorling D.E. The G protein-coupled receptor GPR30 inhibits human urothelial cell proliferation. Endocrinology 149 8 (2008) 4024-4034
162. Thomas P., and Dong J. Binding and activation of the seven-transmembrane estrogen receptor GPR30 by environmental estrogens: a potential novel mechanism of endocrine disruption. J. Steroid Biochem. Mol. Biol. 102 1-5 (2006) 175-179
163. Thomas P., Pang Y., Filardo E.J., and Dong J. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 146 2 (2005) 624-632
164. Vyhlidal C., Samudio I., Kladde M.P., and Safe S. Transcriptional activation of transforming growth factor alpha by estradiol: requirement for both a GC-rich site and an estrogen response element half-site. J. Mol. Endocrinol. 24 3 (2000) 329-338
165. Wang C., Prossnitz E.R., and Roy S.K. G protein-coupled receptor 30 expression is required for estrogen stimulation of primordial follicle formation in the hamster ovary. Endocrinology 149 9 (2008) 4452-4461
166. Warchol M., Lambert P., Goldstein B., Forge A., and Corwin J. Regenerative proliferation in inner ear sensory epithelia from adult guinea pigs and humans. Science 259 5101 (1993) 1619-1622
167. Watson C.S., Alyea R.A., Hawkins B.E., Thomas M.L., Cunningham K.A., and Jakubas A.A. Estradiol effects on the dopamine transporter - protein levels, subcellular location, and function. J. Mol. Signal. 1 (2006) 5
168. Watson C.S., Jeng Y.J., and Kochukov M.Y. Nongenomic actions of estradiol compared with estrone and estriol in pituitary tumor cell
169. Weigel N.L., and Zhang Y. Ligand-independent activation of steroid hormone receptors. J. Mol. Med. 76 7 (1998) 469-479
170. Xu L. Regulation of Smad activities. Biochim. Biophys. Acta 1759 11-12 (2006) 503-513
171. Yamamoto T., Saatcioglu F., and Matsuda T. Cross-talk between bone morphogenic proteins and estrogen receptor signaling. Endocrinology 143 7 (2002) 2635-2642
172. Yamashita H., and Oesterle E. Induction of cell proliferation in mammalian inner-ear sensory epithelia by transforming growth factor alpha and epidermal growth factor. Proc. Natl. Acad. Sci. USA 92 8 (1995) 3152-3155
173. Yarden Y., and Sliwkowski M.X. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2 2 (2001) 127-137
174. Zhang M., Yan J.D., Zhang L., Wang Q., Lu S.J., Zhang J., and Zhu T.H. Activation of bone morphogenetic protein-6 gene transcription in MCF-7 cells by estrogen. Chin. Med. J. (Engl.) 118 19 (2005) 1629-1636
175. Zheng J.L., Frantz G., Lewis A.K., Sliwkowski M., and Gao W.Q. Heregulin enhances regenerative proliferation in postnatal rat utricular sensory epithelium after ototoxic damage. J. Neurocytol. 28 10-11 (1999) 901-912
176. Zheng J.L., and Gao W.Q. Analysis of rat vestibular hair cell development and regeneration using calretinin as an early marker. J. Neurosci. 17 21 (1997) 8270-8282
177. Zheng J.L., Helbig C., and Gao W.Q. Induction of cell proliferation by fibroblast and insulin-like growth factors in pure rat inner ear epithelial cell cultures. J. Neurosci. 17 1 (1997) 216-226
178. Zhou S., Turgeman G., Harris S.E., Leitman D.C., Komm B.S., Bodine P.V., and Gazit D. Estrogens activate bone morphogenetic protein-2 gene transcription in mouse mesenchymal stem cells. Mol. Endocrinol. 17 1 (2003) 56-66
179. Zine A., and de Ribaupierre F. Replacement of mammalian auditory hair cells. Neuroreport 9 2 (1998) 263-268