Evidence that the G protein-coupled membrane receptor GPR30 contributes to the cardiovascular actions of estrogen

Gender Medicine

Volumn 8, Issue 6, 2011, Pages 343-354

  Lindsey, Sarah H ^a   Chappell, Mark C ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

blood pressure; cardiovascular; estrogen receptors; GPR30; renin angiotensin aldosterone system

Indexed keywords

ANGIOTENSIN CONVERTING ENZYME 2; ANGIOTENSIN II; ANGIOTENSINOGEN; CATECHOLAMINE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR 30; MEGALIN; MEMBRANE METALLOENDOPEPTIDASE; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PROSTAGLANDIN SYNTHASE;

AORTA; APOPTOSIS; ARTERIAL WALL THICKNESS; ATTENUATION; BRAIN ARTERY; CARDIOVASCULAR EFFECT; CARDIOVASCULAR FUNCTION; CARDIOVASCULAR SYSTEM; CAROTID ARTERY; CELL PROLIFERATION; CORONARY VASCULAR RESISTANCE; DIASTOLIC DYSFUNCTION; DRUG ACTIVITY; ENDOTHELIUM CELL; GANGLION BLOCK; GENE DELETION; HEART; HEART INFARCTION SIZE; HEART PROTECTION; HIGH SODIUM INTAKE; HORMONE SUBSTITUTION; HUMAN; HYPERTENSION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; IMMUNOREACTIVITY; KIDNEY MEDULLA; KIDNEY PELVIS; KIDNEY PROXIMAL TUBULE; MEDLINE; MUSCLE HYPERTROPHY; NONHUMAN; POSTMENOPAUSE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RENAL PROTECTION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SMOOTH MUSCLE FIBER; SODIUM TRANSPORT; SOLITARY TRACT NUCLEUS; SURVIVAL RATE; SYSTEMATIC REVIEW; SYSTOLIC BLOOD PRESSURE; UPREGULATION; VAGUS NERVE NUCLEUS; VASODILATATION;

ANIMALS; CARDIOVASCULAR PHYSIOLOGICAL PHENOMENA; CARDIOVASCULAR SYSTEM; ESTRADIOL; ESTROGEN REPLACEMENT THERAPY; ESTROGENS; FEMALE; HUMANS; RECEPTORS, ESTROGEN; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION; WOMEN'S HEALTH;

EID: 83155184553     PISSN: 15508579     EISSN: 18787398     Source Type: Journal    
DOI: 10.1016/j.genm.2011.10.004     Document Type: Review

References (86)

1. V.L. Roger, A.S. Go, D.M. Lloyd-Jones Heart disease and stroke statistics2011 update: a report from the American Heart Association Circulation 123 2011 e18 e209
2. J.E. Rossouw, G.L. Anderson, R.L. Prentice Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial JAMA 288 2002 321 333 (Pubitemid 34761611)
3. G.L. Anderson, M. Limacher, A.R. Assaf Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled Trial JAMA 291 2004 1701 1712 (Pubitemid 38489892)
4. R.J. Pietras, C.M. Szego Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells Nature 265 1977 69 72 (Pubitemid 8004314)
5. Z. Wang, X. Zhang, P. Shen Identification, cloning, and expression of human estrogen receptor-alpha36, a novel variant of human estrogen receptor-alpha66 Biochem Biophys Res Commun 336 2005 1023 1027 (Pubitemid 41383424)
6. C. Carmeci, D.A. Thompson, H.Z. Ring Identification of a gene (GPR30) with homology to the G-protein-coupled receptor superfamily associated with estrogen receptor expression in breast cancer Genomics 45 1997 607 617 (Pubitemid 27506136)
7. D. Wang, L. Hu, G. Zhang G protein-coupled receptor 30 in tumor development Endocrine 38 2010 29 37
8. M.C. Chappell, P.E. Gallagher, D.B. Averill Estrogen or the AT1 antagonist olmesartan reverses the development of profound hypertension in the congenic mRen(2).Lewis rat Hypertension 42 2003 781 786 (Pubitemid 37237325)
9. J.T. Crofton, L. Share Gonadal hormones modulate deoxycorticosterone-salt hypertension in male and female rats Hypertension 29 1997 494 499 (Pubitemid 27074089)
10. L.M. Harrison-Bernard, I.H. Schulman, L. Raij Postovariectomy hypertension is linked to increased renal AT1 receptor and salt sensitivity Hypertension 42 2003 1157 1163 (Pubitemid 37549071)
11. K.B. Brosnihan, A. Moriguchi, H. Nakamoto Estrogen augments the contribution of nitric oxide to blood pressure regulation in transgenic hypertensive rats expressing the mouse Ren-2 gene Am J Hypertens 7 1994 576 582 (Pubitemid 24265151)
12. K.D. Pendergrass, B.M. Westwood, M.C. Chappell Differential expression of neprilysin and angiotensin-converting enzyme 2 may contribute to the gender disparity in the hypertensive mRen2.Lewis strain Hypertension 50 2007 e75 e155
13. M.C. Chappell, L.M. Yamaleyeva, B.M. Westwood Estrogen and salt sensitivity in the female mRen(2).Lewis rat Am J Physiol Regul Integr Comp Physiol 291 2006 R1557 R1563
14. M.C. Chappell Emerging evidence for a functional angiotensin-converting enzyme 2-angiotensin-(1-7)-MAS receptor axis: more than regulation of blood pressure? Hypertension 50 2007 596 599 (Pubitemid 47442717)
15. S.H. Lindsey, J.A. Cohen, K.B. Brosnihan Chronic treatment with the G protein-coupled receptor 30 agonist G-1 decreases blood pressure in ovariectomized mRen2.Lewis rats Endocrinology 150 2009 3753 3758
16. A. Pines, E.Z. Fisman, Y. Drory The effects of sublingual estradiol on left ventricular function at rest and exercise in postmenopausal women: an echocardiographic assessment Menopause 5 1998 79 85 (Pubitemid 28283035)
17. F. Leonardo, C. Medeirus, G.M. Rosano Effect of acute administration of estradiol 17 beta on aortic blood flow in menopausal women Am J Cardiol 80 1997 791 793 (Pubitemid 27413597)
18. M. Perera, J.R. Petrie, C. Hillier Hormone replacement therapy can augment vascular relaxation in post-menopausal women with type 2 diabetes Hum Reprod 17 2002 497 502 (Pubitemid 34168466)
19. M.N. Cruz, G. Douglas, J.A. Gustafsson Dilatory responses to estrogenic compounds in small femoral arteries of male and female estrogen receptor-beta knockout mice Am J Physiol Heart Circ Physiol 290 2006 H823 H829
20. G.M. Rubanyi, A.D. Freay, K. Kauser Vascular estrogen receptors and endothelium-derived nitric oxide production in the mouse aorta Gender difference and effect of estrogen receptor gene disruption J Clin Invest 99 1997 2429 2437 (Pubitemid 27227721)
21. S.H. Lindsey, K.A. Carver, E.R. Prossnitz, M.C. Chappell Vasodilation in response to the GPR30 agonist G-1 is not different from estradiol in the mRen2.Lewis female rat J Cardiovasc Pharmacol 57 2011 598 603
22. B.O. Nilsson, E. Ekblad, T. Heine, J.A. Gustafsson Increased magnitude of relaxation to oestrogen in aorta from oestrogen receptor beta knock-out mice J Endocrinol 166 2000 R5 R9 (Pubitemid 30650586)
23. M.D. Iafrati, R.H. Karas, M. Aronovitz Estrogen inhibits the vascular injury response in estrogen receptor alpha-deficient mice Nat Med 3 1997 545 548 (Pubitemid 27198653)
24. R.H. Karas, J.B. Hodgin, M. Kwoun Estrogen inhibits the vascular injury response in estrogen receptor beta-deficient female mice Proc Natl Acad Sci U S A 96 1999 15133 15136 (Pubitemid 30019777)
25. R. Ogata, Y. Inoue, H. Nakano Oestradiol-induced relaxation of rabbit basilar artery by inhibition of voltage-dependent Ca channels through GTP-binding protein Br J Pharmacol 117 1996 351 359 (Pubitemid 26030291)
26. T. Kitazawa, E. Hamada, K. Kitazawa, A.K. Gaznabi Non-genomic mechanism of 17 beta-oestradiol-induced inhibition of contraction in mammalian vascular smooth muscle J Physiol 499 pt 2 1997 497 511 (Pubitemid 27129430)
27. E. Haas, M.R. Meyer, U. Schurr Differential effects of 17beta-estradiol on function and expression of estrogen receptor alpha, estrogen receptor beta, and GPR30 in arteries and veins of patients with atherosclerosis Hypertension 49 2007 1358 1363 (Pubitemid 46809380)
28. U.E. Martensson, S.A. Salehi, S. Windahl Deletion of the G protein-coupled receptor GPR30 impairs glucose tolerance, reduces bone growth, increases blood pressure, and eliminates estradiol-stimulated insulin release in female mice Endocrinology 150 2008 687 698
29. E. Haas, I. Bhattacharya, E. Brailoiu Regulatory role of G protein-coupled estrogen receptor for vascular function and obesity Circ Res 104 2009 288 291
30. B.R. Broughton, A.A. Miller, C.G. Sobey Endothelium-dependent relaxation by G protein-coupled receptor 30 agonists in rat carotid arteries Am J Physiol Heart Circ Physiol 298 2010 H1055 H1061
31. M.R. Meyer, O. Baretella, E.R. Prossnitz, M. Barton Dilation of epicardial coronary arteries by the G protein-coupled estrogen receptor agonists G-1 and ICI 182,780 Pharmacology 86 2010 58 64
32. Q. Ding, R. Gros, L.E. Limbird Estradiol-mediated ERK phosphorylation and apoptosis in vascular smooth muscle cells requires GPR 30 Am J Physiol Cell Physiol 297 2009 C1178 C1187
33. R. Gros, Q. Ding, L.A. Sklar GPR30 expression is required for the mineralocorticoid receptor-independent rapid vascular effects of aldosterone Hypertension 57 2011 442 451
34. Y. Ma, X. Qiao, A.E. Falone Gender-specific reduction in contraction is associated with increased estrogen receptor expression in single vascular smooth muscle cells of female rat Cell Physiol Biochem 26 2010 457 470
35. S.H. Lindsey, L.M. Yamaleyeva, K.B. Brosnihan Estrogen receptor GPR30 reduces oxidative stress and proteinuria in the salt-sensitive female mRen2.Lewis rat Hypertension 58 2011 665 671
36. K.K. Ho, K.M. Anderson, W.B. Kannel Survival after the onset of congestive heart failure in Framingham Heart Study subjects Circulation 88 1993 107 115 (Pubitemid 23195439)
37. F.A. Masoudi, E.P. Havranek, G. Smith Gender, age, and heart failure with preserved left ventricular systolic function J Am Coll Cardiol 41 2003 217 223 (Pubitemid 36092188)
38. C.K. Sites, M.D. Tischler, J.A. Blackman Effect of short-term hormone replacement therapy on left ventricular mass and contractile function Fertil Steril 71 1999 137 143 (Pubitemid 29042357)
39. L. Groban, L.M. Yamaleyeva, B.M. Westwood Progressive diastolic dysfunction in the female mRen(2) Lewis rat: influence of salt and ovarian hormones J Gerontol A Biol Sci Med Sci 63 2008 3 11 (Pubitemid 351738458)
40. G.L. Brower, J.D. Gardner, J.S. Janicki Gender mediated cardiac protection from adverse ventricular remodeling is abolished by ovariectomy Mol Cell Biochem 251 2003 89 95 (Pubitemid 37220714)
41. F.D. Kolodgie, A. Farb, S.H. Litovsky Myocardial protection of contractile function after global ischemia by physiologic estrogen replacement in the ovariectomized rat J Mol Cell Cardiol 29 1997 2403 2414 (Pubitemid 27404433)
42. M.A. Cavasin, S.S. Sankey, A.L. Yu Estrogen and testosterone have opposing effects on chronic cardiac remodeling and function in mice with myocardial infarction Am J Physiol Heart Circ Physiol 284 2003 H1560 H1569 (Pubitemid 36460767)
43. R.D. Patten, I. Pourati, M.J. Aronovitz 17Beta-estradiol reduces cardiomyocyte apoptosis in vivo and in vitro via activation of phospho-inositide-3 kinase/Akt signaling Circ Res 95 2004 692 699 (Pubitemid 39331929)
44. R.K. Dubey, D.G. Gillespie, E.K. Jackson, P.J. Keller 17Beta-estradiol, its metabolites, and progesterone inhibit cardiac fibroblast growth Hypertension 31 1998 522 528
45. A.M. Deschamps, E. Murphy Activation of a novel estrogen receptor, GPER, is cardioprotective in male and female rats Am J Physiol Heart Circ Physiol 297 2009 H1806 H1813
46. E. Filice, A.G. Recchia, D. Pellegrino A new membrane G protein-coupled receptor (GPR30) is involved in the cardiac effects of 17beta-estradiol in the male rat J Physiol Pharmacol 60 2009 3 10
47. V.H. Patel, J. Chen, M. Ramanjaneya G-protein coupled estrogen receptor 1 expression in rat and human heart: protective role during ischaemic stress Int J Mol Med 26 2010 193 199
48. B.R. Weil, M.C. Manukyan, J.L. Herrmann Signaling Via GPR30 protects the myocardium from ischemia/reperfusion injury Surgery 148 2010 436 443
49. J.C. Bopassa, M. Eghbali, L. Toro, E. Stefani A novel estrogen receptor GPER inhibits mitochondria permeability transition pore opening and protects the heart against ischemia-reperfusion injury Am J Physiol Heart Circ Physiol 298 2010 H16 H23
50. A.G. Recchia, E.M. De Francesco, A. Vivacqua The G protein-coupled receptor 30 is up-regulated by hypoxia-inducible factor-1alpha (HIF-1alpha) in breast cancer cells and cardiomyocytes J Biol Chem 286 2011 10773 10782
51. J.A. Jessup, S.H. Lindsey, H. Wang Attenuation of salt-induced cardiac remodeling and diastolic dysfunction by the GPER agonist G-1 in female mRen2.Lewis rats PLoS One 5 2010 e15433
52. M. Delbeck, S. Golz, R. Vonk Impaired left-ventricular cardiac function in male GPR30-deficient mice Mol Med Report 4 2011 37 40
53. E.A. Booth, N.R. Obeid, B.R. Lucchesi Activation of estrogen receptor-alpha protects the in vivo rabbit heart from ischemia-reperfusion injury Am J Physiol Heart Circ Physiol 289 2005 H2039 H2047 (Pubitemid 41507355)
54. D. Fliegner, C. Schubert, A. Penkalla Female sex and estrogen receptor-beta attenuate cardiac remodeling and apoptosis in pressure overload Am J Physiol Regul Integr Comp Physiol 298 2010 R1597 R1606
55. M. Skavdahl, C. Steenbergen, J. Clark Estrogen receptor-beta mediates male-female differences in the development of pressure overload hypertrophy Am J Physiol Heart Circ Physiol 288 2005 H469 H476 (Pubitemid 40139627)
56. Y. Yamori, L. Liu, K. Ikeda Different associations of blood pressure with 24-hour urinary sodium excretion among pre- and post-menopausal women WHO Cardiovascular Diseases and Alimentary Comparison (WHO-CARDIAC) Study J Hypertens 19 2001 535 538 (Pubitemid 32280944)
57. I.H. Schulman, P. Aranda, L. Raij Surgical menopause increases salt sensitivity of blood pressure Hypertension 47 2006 1168 1174 (Pubitemid 44289175)
58. A. Scuteri, E.G. Lakatta, D.E. Anderson, J.L. Fleg Transdermal 17 beta-oestradiol reduces salt sensitivity of blood pressure in postmenopausal women J Hypertens 21 2003 2419 2420 (Pubitemid 38293582)
59. J.A. Cohen, S.H. Lindsey, N.T. Pirro Influence of estrogen depletion and salt loading on renal angiotensinogen expression in the mRen(2) Lewis strain Am J Physiol Renal Physiol 299 2010 F35 F42
60. W. Zheng, H. Ji, C. Maric Effect of dietary sodium on estrogen regulation of blood pressure in Dahl salt-sensitive rats Am J Physiol Heart Circ Physiol 294 2008 H1508 H1513 (Pubitemid 351490578)
61. R.W. Mankhey, F. Bhatti, C. Maric 17Beta-estradiol replacement improves renal function and pathology associated with diabetic nephropathy Am J Physiol Renal Physiol 288 2005 F399 F405 (Pubitemid 40105399)
62. M.P. Hutchens, T. Nakano, Y. Kosaka Estrogen is renoprotective via a nonreceptor-dependent mechanism after cardiac arrest in vivo Anesthesiology 112 2010 395 405
63. H. Ji, S. Menini, K. Mok Gonadal steroid regulation of renal injury in renal wrap hypertension Am J Physiol Renal Physiol 288 2005 F513 F520 (Pubitemid 40279457)
64. G.G. Hazell, S.T. Yao, J.A. Roper Localisation of GPR30, a novel G protein-coupled oestrogen receptor, suggests multiple functions in rodent brain and peripheral tissues J Endocrinol 202 2009 223 236
65. S.B. Cheng, C.T. Graeber, J.A. Quinn, E.J. Filardo Retrograde transport of the transmembrane estrogen receptor, G-protein-coupled-receptor-30 (GPR30/GPER) from the plasma membrane towards the nucleus Steroids 76 2011 892 896
66. D.D. Christou, P.P. Jones, J. Jordan Women have lower tonic autonomic support of arterial blood pressure and less effective baroreflex buffering than men Circulation 111 2005 494 498 (Pubitemid 40204435)
67. N. Hirshoren, I. Tzoran, I. Makrienko Menstrual cycle effects on the neurohumoral and autonomic nervous systems regulating the cardiovascular system J Clin Endocrinol Metab 87 2002 1569 1575 (Pubitemid 34615241)
68. C.T. Minson, J.R. Halliwill, T.M. Young, M.J. Joyner Influence of the menstrual cycle on sympathetic activity, baroreflex sensitivity, and vascular transduction in young women Circulation 101 2000 862 868 (Pubitemid 30117881)
69. R.K. Goldman, A.S. Azar, J.M. Mulvaney Baroreflex sensitivity varies during the rat estrous cycle: role of gonadal steroids Am J Physiol Regul Integr Comp Physiol 296 2009 R1419 R1426
70. M.C. Saleh, B.J. Connell, T.M. Saleh Autonomic and cardiovascular reflex responses to central estrogen injection in ovariectomized female rats Brain Res 879 2000 105 114
71. B. Xue, Y. Zhao, A.K. Johnson, M. Hay Central estrogen inhibition of angiotensin II-induced hypertension in male mice and the role of reactive oxygen species Am J Physiol Heart Circ Physiol 295 2008 H1025 H1032
72. E. Brailoiu, S.L. Dun, G.C. Brailoiu Distribution and characterization of estrogen receptor G protein-coupled receptor 30 in the rat central nervous system J Endocrinol 193 2007 311 321
73. S.L. Dun, G.C. Brailoiu, X. Gao Expression of estrogen receptor GPR30 in the rat spinal cord and in autonomic and sensory ganglia J Neurosci Res 87 2009 1610 1619
74. E.J. Spary, A. Maqbool, T.F. Batten Oestrogen receptors in the central nervous system and evidence for their role in the control of cardiovascular function J Chem Neuroanat 38 2009 185 196
75. G.F. Qiao, B.Y. Li, Y.J. Lu 17Beta-estradiol restores excitability of a sexually dimorphic subset of myelinated vagal afferents in ovariectomized rats Am J Physiol Cell Physiol 297 2009 C654 C664
76. H. Schunkert, A.H. Danser, H.W. Hense Effects of estrogen replacement therapy on the renin-angiotensin system in postmenopausal women Circulation 95 1997 39 45 (Pubitemid 27029940)
77. K.B. Brosnihan, D. Weddle, M.S. Anthony Effects of chronic hormone replacement on the renin-angiotensin system in cynomolgus monkeys J Hypertens 15 1997 719 726 (Pubitemid 27249987)
78. C. Klett, D. Ganten, W. Hellmann Regulation of hepatic angiotensinogen synthesis and secretion by steroid hormones Endocrinology 130 1992 3660 3668
79. P.E. Gallagher, P. Li, J.R. Lenhart Estrogen regulation of angiotensin-converting enzyme MRNA Hypertension 33 1999 323 328 (Pubitemid 29065679)
80. G. Nickenig, A.T. Baumer, C. Grohe Estrogen modulates AT1 receptor gene expression in vitro and in vivo Circulation 97 1998 2197 2201 (Pubitemid 28265380)
81. K.B. Brosnihan, J.B. Hodgin, O. Smithies Tissue-specific regulation of ACE/ACE2 and AT1/AT2 receptor gene expression by oestrogen in apolipoprotein E/oestrogen receptor-alpha knock-out mice Exp Physiol 93 2008 658 664 (Pubitemid 351595045)
82. A.J. Allred, D.I. Diz, C.M. Ferrario, M.C. Chappell Pathways for angiotensin-(1-7) metabolism in pulmonary and renal tissues Am J Physiol Renal Physiol 279 2000 F841 F850
83. K. Yamada, S.N. Iyer, M.C. Chappell Converting enzyme determines plasma clearance of angiotensin-(1-7) Hypertension 32 1998 496 502 (Pubitemid 28429139)
84. H. Ji, S. Menini, W. Zheng Role of angiotensin-converting enzyme 2 and angiotensin(1-7) in 17beta-oestradiol regulation of renal pathology in renal wrap hypertension in rats Exp Physiol 93 2008 648 657 (Pubitemid 351595057)
85. C. Muller, S. Shewale, S.B. Gurley et al. Sex and species differences in ACE, ACE2 and neprilysin of the renal brush border Hypertension 58 2011 e153
86. K. Shimada, K.T. Kitazato, T. Kinouchi Activation of estrogen receptor-alpha and of angiotensin-converting enzyme 2 suppresses ischemic brain damage in oophorectomized rats Hypertension 57 2011 1161 1166