Subtype-specific estrogen receptor-mediated vasodilator activity in the cephalic, thoracic, and abdominal vasculature of female rat

Journal of Cardiovascular Pharmacology

Volumn 62, Issue 1, 2013, Pages 26-40

  Reslan, Ossama M ^a   Yin, Zongzhi ^a,b   Do Nascimento, Graciliano R A ^a   Khalil, Raouf A ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

endothelium; estrogen; sex hormones; vascular smooth muscle

Indexed keywords

ACETYLCHOLINE; CALCIUM ION; DIARYLPROPIONITRILE; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; G PROTEIN COUPLED RECEPTOR 30; INDOMETACIN; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; PHENOL DERIVATIVE; PHENYLEPHRINE; POTASSIUM CHLORIDE; QUINOLINE DERIVATIVE; TETRYLAMMONIUM; VASODILATOR AGENT;

ABDOMINAL AORTA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CAROTID ARTERY; CONTROLLED STUDY; ENDOTHELIUM; FEMALE; GENE EXPRESSION; HYPERPOLARIZATION; MAMMARY ARTERY; MESENTERIC ARTERY; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY ARTERY; RAT; RENAL ARTERY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THORACIC AORTA; VASCULAR SMOOTH MUSCLE; VASCULARIZATION; VASODILATATION; WESTERN BLOTTING;

ABDOMEN; ANIMALS; ARTERIES; BLOTTING, WESTERN; CEREBROVASCULAR CIRCULATION; ENDOTHELIUM, VASCULAR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; ISOMETRIC CONTRACTION; MUSCLE CONTRACTION; NITRATES; NITRITES; POTASSIUM CHLORIDE; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION; THORAX; VASOCONSTRICTION; VASODILATION;

EID: 84880571039     PISSN: 01602446     EISSN: 15334023     Source Type: Journal    
DOI: 10.1097/FJC.0b013e31828bc88a     Document Type: Article

References (70)

1. Barrett-Connor E, Bush TL. Estrogen and coronary heart disease in women. JAMA. 1991;265:1861-1867.
2. Gerhard M, Ganz P. How do we explain the clinical benefits of estrogen? From bedside to bench. Circulation. 1995;92:5-8.
3. Dubey RK, Imthurn B, Zacharia LC, et al. Hormone replacement therapy and cardiovascular disease: what went wrong and where do we go from here? Hypertension. 2004;44:789-795.
4. Orshal JM, Khalil RA. Gender, sex hormones, and vascular tone. Am J Physiol Regul Integr Comp Physiol. 2004;286:R233-R249.
5. Mendelsohn ME, Karas RH. Molecular and cellular basis of cardiovascular gender differences. Science. 2005;308:1583-1587.
6. Crews JK, Murphy JG, Khalil RA. Gender differences in Ca(2+) entry mechanisms of vasoconstriction in Wistar-Kyoto and spontaneously hypertensive rats. Hypertension. 1999;34(pt 2):931-936.
7. Murphy JG, Khalil RA. Gender-specific reduction in contractility and [Ca(2+)](i) in vascular smooth muscle cells of female rat. Am J Physiol Cell Physiol. 2000;278:C834-C844.
8. Li Z, Krause DN, Doolen S, et al. Ovariectomy eliminates sex differences in rat tail artery response to adrenergic nerve stimulation. Am J Physiol. 1997;272(pt 2):H1819-H1825.
9. Geary GG, Krause DN, Duckles SP. Estrogen reduces myogenic tone through a nitric oxide-dependent mechanism in rat cerebral arteries. Am J Physiol. 1998;275(pt 2):H292-H300.
10. Crews JK, Khalil RA. Antagonistic effects of 17 beta-estradiol, progesterone, and testosterone on Ca2+ entry mechanisms of coronary vasoconstriction. Arterioscler Thromb Vasc Biol. 1999;19:1034-1040.
11. Mendoza SG, Zerpa A, Carrasco H, et al. Estradiol, testosterone, apolipoproteins, lipoprotein cholesterol, and lipolytic enzymes in men with premature myocardial infarction and angiographically assessed coronary occlusion. Artery. 1983;12:1-23.
12. Bing RJ, Conforto A. Reversal of acetylcholine effect on atherosclerotic coronary arteries by estrogen: pharmacologic phenomenon of clinical importance? J Am Coll Cardiol. 1992;20:458-459.
13. Wolinsky H. Effects of estrogen and progestogen treatment on the response of the aorta of male rats to hypertension. Morphological and chemical studies. Circ Res. 1972;30:341-349.
14. Serock MR, Wells AK, Khalil RA. Modulators of vascular sex hormone receptors and their effects in estrogen-deficiency states associated with menopause. Recent Patents Cardiovasc Drug Discov. 2008;3:165-186.
15. Mendelsohn ME. Genomic and nongenomic effects of estrogen in the vasculature. Am J Cardiol. 2002;90:3F-6F.
16. Kanashiro CA, Khalil RA. Gender-related distinctions in protein kinase C activity in rat vascular smooth muscle. Am J Physiol Cell Physiol. 2001;280:C34-C45.
17. Gisclard V, Miller VM, Vanhoutte PM. Effect of 17 beta-estradiol on endothelium-dependent responses in the rabbit. J Pharmacol Exp Ther. 1988;244:19-22.
18. Herrington DM, Braden GA, Williams JK, et al. Endothelial-dependent coronary vasomotor responsiveness in postmenopausal women with and without estrogen replacement therapy. Am J Cardiol. 1994;73:951-952.
19. Jiang CW, Sarrel PM, Lindsay DC, et al. Endothelium-independent relaxation of rabbit coronary artery by 17 beta-oestradiol in vitro. Br J Pharmacol. 1991;104:1033-1037.
20. Smiley DA, Khalil RA. Estrogenic compounds, estrogen receptors and vascular cell signaling in the aging blood vessels. Curr Med Chem. 2009; 16:1863-1887.
21. Chambliss KL, Yuhanna IS, Mineo C, et al. Estrogen receptor alpha and endothelial nitric oxide synthase are organized into a functional signaling module in caveolae. Circ Res. 2000;87:E44-E52.
22. Zhu Y, Bian Z, Lu P, et al. Abnormal vascular function and hypertension in mice deficient in estrogen receptor beta. Science. 2002;295:505-508.
23. Pare G, Krust A, Karas RH, et al. Estrogen receptor-alpha mediates the protective effects of estrogen against vascular injury. Circ Res. 2002;90: 1087-1092.
24. Lindsey SH, Carver KA, Prossnitz ER, et al. Vasodilation in response to the GPR30 agonist G-1 is not different from estradiol in the mRen2. Lewis female rat. J Cardiovasc Pharmacol. 2011;57:598-603.
25. Revankar CM, Cimino DF, Sklar LA, et al. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science. 2005;307: 1625-1630.
26. Filardo E, Quinn J, Pang Y, et al. Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane. Endocrinology. 2007;148:3236-3245.
27. Haas E, Meyer MR, Schurr U, et al. 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. 2007;49:1358-1363.
28. Prossnitz ER, Oprea TI, Sklar LA, et al. The ins and outs of GPR30: a transmembrane estrogen receptor. J Steroid Biochem Mol Biol. 2008; 109:350-353.
29. Raffetto JD, Qiao X, Beauregard KG, et al. Estrogen receptor-mediated enhancement of venous relaxation in female rat: implications in sexrelated differences in varicose veins. J Vasc Surg. 2010;51:972-981.
30. Rubanyi GM, Freay AD, Kauser K, et al. 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. 1997;99:2429-2437.
31. Ma Y, Qiao X, Falone AE, et al. Gender-specific reduction in contraction is associated with increased estrogen receptor expression in single vascular smooth muscle cells of female rat. Cell Physiol Biochem. 2010;26: 457-470.
32. Mazzuca MQ, Wlodek ME, Dragomir NM, et al. Uteroplacental insufficiency programs regional vascular dysfunction and alters arterial stiffness in female offspring. J Physiol. 2010;588(pt 11):1997-2010.
33. Yener T, Turkkani Tunc A, Aslan H, et al. Determination of oestrous cycle of the rats by direct examination: how reliable? Anat Histol Embryol. 2007;36:75-77.
34. Sun J, Meyers MJ, Fink BE, et al. Novel ligands that function as selective estrogens or antiestrogens for estrogen receptor-alpha or estrogen receptorbeta. Endocrinology. 1999;140:800-804.
35. Stauffer SR, Coletta CJ, Tedesco R, et al. Pyrazole ligands: structure-affinity/activity relationships and estrogen receptor-alpha-selective agonists. J Med Chem. 2000;43:4934-4947.
36. Harrington WR, Sheng S, Barnett DH, et al. Activities of estrogen receptor alpha-and beta-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Mol Cell Endocrinol. 2003;206:13-22.
37. Filardo EJ, Quinn JA, Bland KI, et al. 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. 2000;14:1649-1660.
38. Kleuser B, Malek D, Gust R, et al. 17-Beta-estradiol inhibits transforming growth factor-beta signaling and function in breast cancer cells via activation of extracellular signal-regulated kinase through the G protein-coupled receptor 30. Mol Pharmacol. 2008;74:1533-1543.
39. Khalil RA, van Breemen C. Sustained contraction of vascular smooth muscle: calcium influx or C-kinase activation? J Pharmacol Exp Ther. 1988;244:537-542.
40. Giardina JB, Green GM, Rinewalt AN, et al. Role of endothelin B receptors in enhancing endothelium-dependent nitric oxide-mediated vascular relaxation during high salt diet. Hypertension. 2001;37(pt 2): 516-523.
41. Fleming I, Busse R. NO: the primary EDRF. J Mol Cell Cardiol. 1999; 31:5-14.
42. Busse R, Edwards G, Feletou M, et al. EDHF: bringing the concepts together. Trends Pharmacol Sci. 2002;23:374-380.
43. Feletou M, Vanhoutte PM. Endothelium-derived hyperpolarizing factor. Clin Exp Pharmacol Physiol. 1996;23:1082-1090.
44. Parkington HC, Coleman HA, Tare M. Prostacyclin and endotheliumdependent hyperpolarization. Pharmacol Res. 2004;49:509-514.
45. Davis JR, Giardina JB, Green GM, et al. Reduced endothelial NO-cGMP vascular relaxation pathway during TNF-alpha-induced hypertension in pregnant rats. Am J Physiol Regul Integr Comp Physiol. 2002;282:R390-R399.
46. Payne JA, Alexander BT, Khalil RA. Decreased endothelium-dependent NO-cGMP vascular relaxation and hypertension in growth-restricted rats on a high-salt diet. Hypertension. 2004;43:420-427.
47. Bolego C, Cignarella A, Sanvito P, et al. The acute estrogenic dilation of rat aorta is mediated solely by selective estrogen receptor-alpha agonists and is abolished by estrogen deprivation. J Pharmacol Exp Ther. 2005; 313:1203-1208.
48. Montgomery S, Shaw L, Pantelides N, et al. Acute effects of oestrogen receptor subtype-specific agonists on vascular contractility. Br J Pharmacol. 2003;139:1249-1253.
49. Broughton BR, Miller AA, Sobey CG. Endothelium-dependent relaxation by G protein-coupled receptor 30 agonists in rat carotid arteries. Am J Physiol Heart Circ Physiol. 2010;298:H1055-H1061.
50. Haas E, Bhattacharya I, Brailoiu E, et al. Regulatory role of G proteincoupled estrogen receptor for vascular function and obesity. Circ Res. 2009;104:288-291.
51. Lin AL, Shain SA. Estrogen-mediated cytoplasmic and nuclear distribution of rat cardiovascular estrogen receptors. Arteriosclerosis. 1985;5: 668-677.
52. Dan P, Cheung JC, Scriven DR, et al. Epitope-dependent localization of estrogen receptor-alpha, but not -beta, in en face arterial endothelium. Am J Physiol Heart Circ Physiol. 2003;284:H1295-H1306.
53. Aavik E, du Toit D, Myburgh E, et al. Estrogen receptor beta dominates in baboon carotid after endothelial denudation injury. Mol Cell Endocrinol. 2001;182:91-98.
54. Paredes-Carbajal MC, Juarez-Oropeza MA, Ortiz-Mendoza CM, et al. Effects of acute and chronic estrogenic treatment on vasomotor responses of aortic rings from ovariectomized rats. Life Sci. 1995;57:473-486.
55. MacRitchie AN, Jun SS, Chen Z, et al. Estrogen upregulates endothelial nitric oxide synthase gene expression in fetal pulmonary artery endothelium. Circ Res. 1997;81:355-362.
56. Lantin-Hermoso RL, Rosenfeld CR, Yuhanna IS, et al. Estrogen acutely stimulates nitric oxide synthase activity in fetal pulmonary artery endothelium. Am J Physiol. 1997;273(pt 1):L119-L126.
57. Sumi D, Ignarro LJ. Estrogen-related receptor alpha 1 up-regulates endothelial nitric oxide synthase expression. Proc Natl Acad Sci U S A. 2003; 100:14451-14456.
58. Jun SS, Chen Z, Pace MC, et al. Estrogen upregulates cyclooxygenase-1 gene expression in ovine fetal pulmonary artery endothelium. J Clin Invest. 1998;102:176-183.
59. Feletou M, Vanhoutte PM. Endothelium-derived hyperpolarizing factor: where are we now? Arterioscler Thromb Vasc Biol. 2006;26:1215-1225.
60. Luksha L, Poston L, Gustafsson JA, et al. The oestrogen receptor beta contributes to sex related differences in endothelial function of murine small arteries via EDHF. J Physiol. 2006;577(pt 3):945-955.
61. Traupe T, Stettler CD, Li H, et al. Distinct roles of estrogen receptors alpha and beta mediating acute vasodilation of epicardial coronary arteries. Hypertension. 2007;49:1364-1370.
62. Crews JK, Khalil RA. Gender-specific inhibition of Ca2+ entry mechanisms of arterial vasoconstriction by sex hormones. Clin Exp Pharmacol Physiol. 1999;26:707-715.
63. Murphy JG, Khalil RA. Decreased [Ca(2+)](i) during inhibition of coronary smooth muscle contraction by 17beta-estradiol, progesterone, and testosterone. J Pharmacol Exp Ther. 1999;291:44-52.
64. Freay AD, Curtis SW, Korach KS, et al. Mechanism of vascular smooth muscle relaxation by estrogen in depolarized rat and mouse aorta. Role of nuclear estrogen receptor and Ca2+ uptake. Circ Res. 1997;81:242-248.
65. Zhang F, Ram JL, Standley PR, et al. 17 Beta-estradiol attenuates voltagedependent Ca2+ currents in A7r5 vascular smooth muscle cell line. Am J Physiol. 1994;266(pt 1):C975-C980.
66. Nakajima T, Kitazawa T, Hamada E, et al. 17 Beta-estradiol inhibits the voltage-dependent L-type Ca2+ currents in aortic smooth muscle cells. Eur J Pharmacol. 1995;294:625-635.
67. Baxter JD, Funder JW. Hormone receptors. N Engl J Med. 1979;301: 1149-1161.
68. Webb P, Lopez GN, Greene GL, et al. The limits of the cellular capacity to mediate an estrogen response. Mol Endocrinol. 1992;6:157-167.
69. Trams G, Maass H. Specific binding of estradiol and dihydrotestosterone in human mammary cancers. Cancer Res. 1977;37:258-261.
70. Wynne FL, Payne JA, Cain AE, et al. Age-related reduction in estrogen receptor-mediated mechanisms of vascular relaxation in female spontaneously hypertensive rats. Hypertension. 2004;43:405-412.