Growth factor activation of the estrogen receptor in vascular cells occurs via a mitogen-activated protein kinase-independent pathway

Journal of Clinical Investigation

Volumn 101, Issue 12, 1998, Pages 2851-2861

  Karas, Richard H ^a,b   Gauer, Elizabeth Ann ^a   Bieber, Hallie E ^a   Baur, Wendy E ^a   Mendelsohn, Michael E ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b TUFTS MEDICAL CENTER   (United States)

Author keywords

Crosstalk; Gene transcription; Steroid hormone receptors; Vascular endothelial cells; Vascular smooth muscle cells

Indexed keywords

ESTROGEN; ESTROGEN RECEPTOR; GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; STEROID RECEPTOR; VASCULOTROPIN;

AMINO ACID SUBSTITUTION; ARTICLE; ESTROGEN DEFICIENCY; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PULMONARY VEIN; SAPHENOUS VEIN; SMOOTH MUSCLE FIBER; VASCULAR TISSUE;

EID: 0032526052     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1416     Document Type: Article

References (94)

1. Colditz, G.A., W.C. Willett, M.J. Stampfer, B. Rosner, F.E. Speizer, and C.H. Hennekens. 1987. Menopause and the risk of coronary heart disease in women. N. Engl. J. Med. 316:1105-1110.
2. Stampfer, M.J., G.A. Colditz, W.C. Willett, J.E. Manson, B. Rosner, F.E. Speizer, and C.H. Hennekens. 1991. Postmenopausal estrogen therapy and cardiovascular disease. N. Engl. J. Med. 325:756-762.
3. Bush, T.L., E. Barrett-Connor, L.D. Cowan, M.H. Crigui, R.B. Wallace, C.M. Suchindran, H.A. Tyroler, and B.M. Rifkind. 1987. Cardiovascular mortality and noncontraceptive use of estrogen in women: results from the lipid research clinics program follow-up study. Circulation. 75:1102-1109.
4. Grady, D., S.M. Rubin, D.B. Petitti, C.S. Fox, D. Black, B. Ettinger, V.L. Ernster, and S.R. Cummings. 1992. Hormone therapy to prevent disease and prolong life in postmenopausal women. Ann. Intern. Med. 117:1016-1037.
5. Writing Group for the PEPI Trial. 1995. Effects of estrogen or estrogen/ progestin regimens on heart disease risk factors in postmenopausal women: the Postmenopausal Estrogen/Progestin Interventions (PEPI) Trial. JAMA (J. Am. Med. Assoc.) 273:199-208.
6. Nabulsi, A.A., A.R. Folsom, A. White, W. Patsch, G. Geiss, K.K. Wu, and M. Szklo. 1993. Association of hormone-replacement therapy with various cardiovascular risk factors in postmenopausal women. N. Engl. J. Med 328: 1069-1075.
7. Gebara, O.C.E., M.A. Mittleman, P. Sutherland, I. Lipinska, T. Matheney, P. Xu, F.K. Welty, P.W.F. Wilson, D. Levy, J.E. Muller, and G.H. Tofler. 1995. Association between increased estrogen status and increased fibrinolytic potential in the Framingham Offspring Study. Circulation. 91:1952-1958.
8. Mendelsohn, M.E., and R.H. Karas. 1994. Estrogen and the blood vessel wall. Curr. Op. Cardiol. 9:619-626.
9. Williams, J.K., M.R. Adams, and H.S. Klopfenstein. 1990. Estrogen modulates responses of atherosclerotic coronary arteries. Circulation. 81:1680-1687.
10. Williams, J.K., M.R. Adams, D.M. Herrington, and T.B. Clarkson. 1992. Short-term administration of estrogen and vascular responses of atherosclerotic coronary arteries. J. Am. Coll. Cardiol. 20:452-457.
11. Reis, S.E., S.T. Gloth, R.S. Blumenthal, J.R. Resar, H.A. Zacur, G. Gerstenblith, and J.A. Brinker. 1994. Ethinyl estradiol acutely attenuates abnormal coronary vasomotor responses to acetylcholine in postmenopausal women. Circulation. 89:52-60.
12. 2+ currents in A7r5 vascular smooth muscle cell line. Am. J. Physiol. (Cell Physiol.) 266:C975-C980.
13. Chang, W.C., J. Nakao, H. Orimo, and S.I. Murota. 1980. Stimulation of prostaglandin cyclooxygenase and prostacyclin synthetase activities by estradiol in rat aortic smooth muscle cells. Biochim. Biophys. Acta. 620:472-482.
14. Jiang, C. P.M. Sarrel, P.A. Poole-Wilson, and P. Collins. 1992. Acute effect of 17β-estradiol on rabbit coronary artery contractile responses to endothelin-1. Am. J. Physiol. 263:H271-H275.
15. Collins, P., J. Shay, C. Jiang, and J. Moss. 1994. Nitric oxide accounts for dose-dependent estrogen-mediated coronary relaxation after acute estrogen withdrawal. Circulation. 90:1964-1968.
16. Redmond, E.M., M.N. Cherian, and R.C. Wetzel. 1994. 17β-Estradiol inhibits flow- and acute hypoxia-induced prostacyclin release from perfused endocardial endothelial cells. Circulation. 90:2519-2524.
17. Koike, H., R.H. Karas, W. Baur, T.F. O'Donnell, Jr., and M.E. Mendelsohn. 1996. Differential display PCR identifies nucleophosmin as an estrogen-regulated gene in human vascular smooth muscle cells. J. Vasc. Surg. 23:477-482.
18. Orimo, A., S. Inoue, A. Ikegami, T. Hosoi, M. Akishita, Y. Ouchi, M. Muramatsu, and H. Orimo. 1993. Vascular smooth muscle cells as target for estrogen. Biochem. Biophys. Res. Commun. 195:730-736.
19. Jiang, C. P.M. Sarrel, D.C. Lindsey, P.A. Poole-Wilson, and P. Collins. 1991. Endothelium-independent relaxation of rabbit coronary artery by 17β-oestradiol in vitro. Br. J. Pharmacol. 104:1033-1037.
20. Ca channels through a cGMP-dependent mechanism. Circ. Res. 77:936-942.
21. Weiner, C.P., I. Lizasoain, S.A. Baylis, R.G. Knowles, I.G. Charles, and S. Moncada. 1994. Induction of calcium-dependent nitric oxide synthases by sex hormones. Proc. Natl. Acad. Sci. USA. 91:5212-5216.
22. Bhalla, R.C., K.F. Toth, R.A. Bhatty, L.P. Thompson, and R.V. Sharma. 1997. Estrogen reduces proliferation and agonist-induced calcium increase in coronary artery smooth muscle cells. Am. J. Physiol. 272:H1996-H2003.
23. Fischer-Dzoga, K., R. Wissler, and D. Vesselinovitch. 1983. The effect of estradiol on the proliferation of rabbit aortic medial tissue cells induced by hyperlipemic serum. Exp. Mol. Pathol. 39:355-363.
24. Vargas, R., B. Wroblewska, A. Rego, J. Hatch, and P.W. Ramwell. 1993. Oestradiol inhibits smooth muscle cell proliferation of pig coronary artery. Br. J. Pharmacol. 109:612-617.
25. Kolodgie, F.D., A. Jacob, P.S. Wilson, G.C. Carlson, A. Farb, A. Verma, and R. Virmani. 1996. Estradiol attenuates directed migration of vascular smooth muscle cells in vitro. Am. J. Pathol. 148:969-976.
26. Morales, D.E., K.A. McGowan, D.S. Grant, S. Maheshwari, D. Bhartiya, M.C. Cid, H.K. Kleinman, and W. Schnaper. 1995. Estrogen promotes angiogenic activity in human umbilical vein endothelial cells in vitro and in a murine model. Circulation. 91:755-763.
27. Losordo, D.W., M. Kearney, E.A. Kim, J. Jekanowski, and J.M. Isner. 1994. Variable expression of the estrogen receptor in normal and atherosclerotic coronary arteries of premenopausal women. Circulation. 89:1501-1510.
28. Karas, R.H., B.L. Patterson, and M.E. Mendelsohn. 1994. Human vascular smooth muscle cells contain functional estrogen receptor. Circulation 89: 1943-1950.
29. Kim-Schulze, S., K.A. McGowan, S.C. Hubchak, M.C. Cid, M.B. Martin, H.K. Kleinman, G.L. Greene, and H.W. Schnaper. 1996. Expression of an estrogen receptor by human coronary artery and umbilical vein endothelial cells. Circulation. 94:1402-1407.
30. Venkov, C.D., A.B. Rankin, and D.E. Vaughan. 1996. Identification of authentic estrogen receptor in cultured endothelial cells: a potential mechanism for steroid hormone regulation of endothelial function. Circulation. 44:727-733.
31. Caulin-Glaser, T., G.A. Watson, R. Pardi, and J.R. Bender. 1996. Effects of 17β-estradiol on cytokine-induced endothelial cell adhesion molecular expression. J. Clin. Invest. 98:36-12.
32. Lantin-Hermoso, R.L., C.R. Rosenfeld, I.S. Yuhanna, Z. German, Z. Chen, and P.W. Shaul. 1497. Estrogen acutely stimulates nitric oxide synthase activity in fetal pulmonary artery endothelium. Am. J. Physiol. (Lung Cell. Mol. Physiol.) 273:L119-L126.
33. 2+ mobilization. Circ. Res. 81:885-892.
34. Gishel, N., K.E. Timmins, S.J. Duffy, T.T. Binh, R.C. O'Brien, R.W. Harper, and I.T. Meredith. 1997. Long-term estrogen therapy improves vascular function in male to female transsexuals. Am. Coll. Cardiol. 29:1437-1444.
35. McCrohon, J.A., W.A.W. Walters, J.T.C. Robinson, R.J. McCredie, L. Turner, M.R. Adams, D.J. Handelsman, and D.S. Celermajer. 1997. Arterial reactivity is enhanced in genetic males taking high dose estrogens. Am. Coll. Cardiol. 24:1432-1436.
36. Blumenthal, R.S., A.W. Heldman, J.A. Brinker, J.R. Resar, V.J. Coombs, S.T. Gloth, and G. Gerstenblith. 1947. Acute effects of conjugated estrogens on coronary blood flow response to acetylcholine in men. Am. J. Cardiol. 80:1021-1024.
37. Chen, S.J., H.B. Li, J. Durand, S. Oparil, and Y.F. Chen. 1996. Estrogen reduces myointimal proliferation after balloon injury of rat carotid artery. Circulation. 93:577-584.
38. Bourassa, P.A.K., P.M. Milos, B.J. Gaynor, J.E. Breslow, and R.J. Aiello. 1996. Estrogen reduces atherosclerotic lesion development in apolipoprotein E-deficient mice. Proc. Natl. Acad. Sci. USA. 93:10022-10027.
39. Eddy, E.M., T.F. Washburn, D.O. Bunch, E.H. Goulding, B.C. Gladen, D.B. Lubahn, and K.S. Korach. 1996. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology 137:4796-4805.
40. Ogawa, S., D.B. Lubahn, S.K. Korach, and D.W. Pfaff. 1997. Behavioral effects of estrogen receptor gene disruption in male mice. Proc. Natl. Acad. Sci. USA. 94:1476-1481.
41. Lubahn, D.B., J.S. Moyer, T.S. Golding, J.F. Couse, K.S. Korach, and O. Smithies. 1993. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. USA. 90:11162-11166.
42. Hess, R.A., D. Bunick, K.-H. Lee, J. Bahr, J.A. Taylor, K.S. Korach, and D.B. Lubahn. 1997. A role for oestrogens in the male reproductive system. Nature. 390:509-512.
43. Sudhir, K., T.M. Chou, E.M. Messina, S.J. Hutchison, K.S. Korach, K. Chatterjee, and G. M. Rubanyi. 1997. Endothelial dysfunction in a man with disruptive mutation in oestrogen-receptor gene. Lancet. 349:1146-1147.
44. Smith, E.P., J. Boyd, G.R. Frank, H. Takahashi, R.M. Cohen, B. Specker, T.C. Williams, D.B. Lubahn, and K.S. Korach. 1994. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N. Engl. J. Med. 331:1056-1061.
45. Evans, R.M. 1988. The steroid and thyroid hormone receptor superfamily. Science. 240:889-895.
46. King, R.J.B. 1987. Structure and function of steroid receptors. J. Endocrinol. 114:341-349.
47. Power, R.F., S.K. Mani, J. Codina, O.M. Conneely, and B.W. O'Malley. 1991. Dopaminergic and ligand-dependent activation of steroid hormone receptors. Science. 254:1636-1639.
48. El-Tanani, M.K.K., and C.D. Green. 1947. Two separate mechanisms for ligand-independent activation of the estrogen receptor. Mol. Endocrinol. 11:428-937.
49. Zwijsen, R.M.E., E. Wientjens, R. Klompmaker, J. Van der Sman, R. Bernards, and R.J.A.M. Michalides. 1447. CDK-independent activation of estrogen receptor by cyclin D1. Cell. 88:405-415.
50. Trowbridge, J.M., I. Rogatsky, and M.J. Garabedian. 1997. Regulation of estrogen receptor transcriptional enhancement by the cyclin A Cdk2 complex. Proc. Natl. Acad. Sci. USA. 94:10132-10137.
51. Ignar-Trowbridge, D.M., C.T. Teng, K.A. Ross, M.G. Parker, K.S. Korach, and J.A. McLachlan. 1993. Peptide growth factors elicit estrogen receptor-dependent transcriptional activation of an estrogen-responsive element. Mol. Endocrinol. 7:992-998.
52. Ignar-Trowbridge, D.M., K.G. Nelson, M.C. Bidwell, S.W. Curtis, T.F. Washburn, J.A. McLachlan, and K.S. Korach. 1942. Coupling of dual signaling pathways: epidermal growth factor action involves the estrogen receptor. Proc. Natl. Acad. Sci. USA. 89:4658-4662.
53. Ignar-Trowbridge, D.M., C.T. Teng, K.A. Ross, M.G. Parker, K.S. Korach, and J.A. McLachlan. 1993. Peptide growth factors elicit estrogen receptor-dependent transcriptional activation of an estrogen-responsive element. Mol. Endocrinol. 7:992-998.
54. Bunone, G., P.A. Briand, R.J. Miksicek, and D. Picard. 1996. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO (Eur. Mol. Biol. Organ.) J. 15:2174-2183.
55. Kato, S., H. Endoh, Y. Masuhiro, T. Kitamoto, S. Uchiyama, H. Sasaki, S. Masushige, Y. Gotoh, E. Nishida, H. Kawashima, D. Metzger, and P. Chambon. 1995. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science. 270:1491-1494.
56. Libby, P., and K.V. O'Brien. 1983. Culture of quiescent arterial smooth muscle cells in a defined serum-free medium. J. Cell. Physiol. 115:217-223.
57. Glass, C.K., J.M. Holloway, O.V. Devary, and M.G. Rosenfeld. 1988. The thyroid hormone receptor hinds with opposite transcriptional effects to a common sequence motif in thyroid hormone and estrogen response elements. Cell. 54:313-323.
58. Kunkel, T.A., J.D. Roberts, and R.A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154:367-382.
59. Gotoh, Y., S. Matsuda, K. Takenaka, S. Hattori, A. Iwamatsu, M. Ishikawa, H. Kosako, and E. Nishida. 1994. Characterization of recombinant Xenopus MAP kinase kinases mutated at potential phosphorylation sites. Oncogene. 9:1891-1898.
60. Pumiglia, K.M., and S.J. Decker. 1997. Cell cycle arrest mediated by the MEK/mitogen-activated protein kinase pathway. Proc. Natl. Acad. Sci. USA. 94:1476-1481.
61. Brown, P.J., and A. Schonbrunn. 1993. Affinity purification of a somatostatin receptor-G-protein complex demonstrates specificity in receptor-G-protein coupling. J. Biol. Chem. 268:6668-6676.
62. Green, S., P. Walter, V. Kumar, A. Krust, J.-M. Bornert, P. Argos, and P. Chambon. 1986. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A., Nature, 320:134-139.
63. Tzukerman, M.T., A. Esty, D. Santiso-Mere, P. Danielian, M.G. Parker, R.B. Stein, J.W. Pike, and D.P. McDonnell. 1994. Human estrogen receptor transactivational capacity is determined by both cellular and promoter context and mediated by two functionally distinct intramolecular regions. Mol. Endocrinol. 8:21-30.
64. McDonnell, D.P., D.L. Clemm, T. Hermann, M.E. Goldman, and J.W. Pike. 1995. Analysis of estrogen receptor function in vitro reveals three distinct classes of antiestrogens. Mol. Endocrinol. 9:659-669.
65. Metzger, D., M. Berry, S. Ali, and P. Chambon. 1995. Effect of antagonists on DNA binding properties of the human estrogen receptor in vitro and in vivo. Mol. Endocrinol. 9:579-591.
66. Ferrara, N., J. Winer, and T. Burton. 1991. Aortic smooth muscle cells express and secrete vascular endothelial growth factor. Growth Factors. 5:141-148.
67. Fox, J.C., and J.L. Swain. 1996. Angiogenic gene therapy: a leg to stand on? Circulation. 94:3065-3066.
68. Majesky, M.W. 1996. A little VEGF goes a long way: Therapeutic angiogenesis by direction of injection of vascular endothelial growth factor-encoding plasmid DNA. Circulation. 94:3062-3064.
69. Tsurumi, Y., S. Takeshita, D. Chen, M. Kearney, S.T. Rossow, J. Passeri, J.R. Horowitz, J.F. Symes, and J.M. Isner. 1996. Direct intramuscular gene transfer of naked DNA encoding vascular endothetial growth factor augments collateral development and tissue perfusion. Circulation. 94:3281-3290.
70. Ferrara, N., K. Carver-Moore, H. Chen, M. Dowd, L. Lu, K.S. O'Shea, L. Powell-Braxton, K.J. Hillan, and M.W. Moore. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 380: 439-442.
71. Carmeliet, P., V. Ferreira, G. Breir, S. Pollefeyt, L. Kiechens, M. Gertsenstein, M. Fahrig, A. Vandenhoeck, K. Harpal, C. Eberhardt, C. Declercq, J. Pawling, L. Moons, D. Collen, W. Risau, and A. Nagy. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature. 380:435-439.
72. 165 gene transfer. Circulation. 94:3291-3302.
73. Krasinski, K., I. Spyridopoulos, T. Asahara, R. Van der Zee, J.M. Isner, and D.W. Losordo. 1997. Estradiol accelerates functional endothelial recovery after arterial injury. Circulation. 95:1768-1772.
74. Brogi, E., T. Wu, A. Namiki, and J.M. Isner. 1994. Indirect angiogenic cytokines upregulated VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only. Circulation. 90:649-652.
75. Levy, A.P., N.S. Levy, S. Wegner, and M.A. Goldberg. 1995. Transcriptional regulation of the rat vascular endothelial growth factor gene by hypoxia. J. Biol. Chem. 270:13333-13340.
76. Shweiki, D., A. Itin, D. Soffer, and E. Keshet. 1992. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature. 359:843-845.
77. Cullinan-Bove, K., and R.D. Koos. 1993. Vascular endothelial growth factor/vascular permeability factor expression in the rat uterus: rapid stimulation by estrogen correlates with estrogen-induced increases in uterine capillary permeability and growth. Endocrinology. 133:829-837.
78. Karas, R.H., H.E. Bieber, W.E. Baur, and M.E. Mendelsohn. 1996. Estrogen enhances vascular endothelial growth factor (VEGF) gene expression in human vascular smooth muscle cells. Circulation. 94:1595.
79. Smith, C.L., S.A. Oñate, M.J. Tsai, and B.W. O'Malley. 1996. CREB binding protein acts synergistically with steroid receptor coactivator-1 to enhance steroid receptor-dependent transcription. Proc. Natl. Acad. Sci. USA. 93: 8884-8888.
80. Hanstein, B., R. Eckner, J. DiRenzo, S. Halachmi, H. Liu, B. Searcy, R. Kurokawa, and M. Brown. 1996. p300 is a component of an estrogen receptor coactivator complex. Proc. Natl. Acad. Sci. USA. 93:11540-11545.
81. Cavaillès, V., S. Cauvois, F. L'Horset, G. Lopez, S. Hoare, P.J. Kushner, and M.G. Parker. 1995. Nuclear factor R1P140 modulates transcriptional activation by the estrogen receptor. EMBO (Eur. Mol. Biol. Organ) J. 14-1741-3751.
82. Onate, S.A., S.Y. Tsai, M.J. Tsai, and B.W. O'Malley. 1995. Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science. 270:1354-1357.
83. Cavaillès, V., S. Dauvois, P.S. Danielian, and M.G. Parker. 1994. Interaction of proteins with transcriptionally active estrogen receptors. Proc. Natl. Acad. Sci. USA. 91:10009-10013.
84. Hunter, T. 1996. A growing coactivator network. Nature. 383:22-23.
85. Baniahmad, C., Z. Nawaz, A. Baniahmad, M.A.G. Gleeson, M.-J. Tsai, and B.W. O'Malley. 1995. Enhancement of human estrogen receptor activity by SPT6: a potential coactivator. Mol. Endocrinol. 9:34-43.
86. Halachmi, S., E. Marden, G. Martin, H. MacKay, C. Abbondanza, and M. Brown. 1994. Estrogen receptor-associated proteins: possible mediators of hormone-induced transcription. Science. 264:1455-1458.
87. McInerney, E.M., M.J. Tsai, B.W. O'Malley, and B.S. Katzenellenbogen. 1996. Analysis of estrogen receptor transcriptional enhancement by a nuclear hormone receptor coactivator. Proc. Natl. Acad. Sci. USA. 93:10069-10073.
88. Horlein, A.J. 1995. Ligand-dependent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature. 377:397-404.
89. Kurokawa, R. 1995. Polarity-specific activities of retinoic acid receptors determined by a co-repressor. Nature. 377:451-454.
90. Chen, J.D., and R.M. Evans. 1995. A transcriptional co-repressor that interacts with nuclear hormone receptors. Nature. 377:454-457.
91. Chen, J.D., and R.M. Evans. 1996. SMRT isoforms mediate repression and anti-repression of nuclear receptor heterodimers. Proc. Natl. Acad. Sci. USA. 93:7567-7571.
92. Chakravarti, D. 1996. Role of CBP/P300 in nuclear receptor signalling. Nature. 383:99-103.
93. Gu, W., X.L. Shi, and R.G. Roeder. 1997. Synergistic activation of transcription by CBP and p53. Nature. 387:819-823.
94. Lill, N.L., S.R. Grossman, D. Ginsberg, J. DeCaprio, and D.M. Livingston. 1997. Binding and modulation of p53 by p300/CBP coactivators. Nature. 387:823-827.