Nongenomic, endothelium-independent effects of estrogen on human coronary smooth muscle are mediated by type I (neuronal) NOS and PI3-kinase-Akt signaling

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 293, Issue 1, 2007, Pages

  Han, Guichun ^a   Ma, Handong ^a   Chintala, Rajesh ^a   Miyake, Katsuya ^a   Fulton, David J R ^a   Barman, Scott A ^a   White, Richard E ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Heat shock protein 90; Human coronary circulation; Nitric oxide

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; ESTRADIOL; ESTROGEN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; WORTMANNIN;

ARTICLE; CELL ADHESION; CONTROLLED STUDY; CORONARY ARTERY; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY DILATATION; ENDOTHELIUM; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FLUORESCENCE; HORMONE ACTION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELLS, CULTURED; CORONARY VESSELS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOTHELIUM, VASCULAR; ESTROGENS; HUMANS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NITRIC OXIDE SYNTHASE TYPE I; ONCOGENE PROTEIN V-AKT; SIGNAL TRANSDUCTION; SWINE;

EID: 34547095758     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.01342.2006     Document Type: Article

References (42)

1. Alpaslan M, Shimokawa H, Kuroiwa-Matsumoto M, Harasawa Y, Takeshita A. Short-term estrogen administration ameliorates dobutamine-induced myocardial ischemia in postmenopausal women with coronary artery disease. J Am Coll Cardiol 30: 1466-1471, 1997.
2. Bartlett SR, Bennett PR, Campa JS, Dennes WJ, Slater DM, Mann GE, Poston L, Poston R. Expression of nitric oxide synthase isoforms in pregnant human myometrium. J Physiol 521: 705-716, 1999.
3. Blumenthal RS, Heldman AW, Brinker JA, Resar JR, Coombs VJ, Gloth ST, Gerstenblith G, Reis SE. Acute effects of conjugated estrogens on coronary blood flow response to acetylcholine in men. Am J Cardiol 80: 1021-1024, 1997.
4. Boulanger CM, Heymes C, Benessiano J, Geske RS, Levy BI, Vanhoutte PM. Neuronal nitric oxide synthase is expressed in rat vascular smooth muscle cells: activation by angiotensin II in hypertension. Circ Res 83: 1271-1278, 1998.
5. Brophy CM, Knoepp L, Xin J, Pollock JS. Functional expression of NOS 1 in vascular smooth muscle. Am J Physiol Heart Circ Physiol 278: H991-H997, 2000.
6. Camper-Kirby D, Welch S, Walker A, Shiraishi I, Setchell KD, Schaefer E, Kajstura J, Anversa P, Sussman MA. Myocardial Akt activation and gender: increased nuclear activity in females versus males. Circ Res 88: 1020-1027, 2001.
7. Chen Z, Yuhanna IS, Galcheva-Gargova Z, Karas RH, Mendelsohn ME, Shaul PW. Estrogen receptor alpha mediates the nongenomic activation of endothelial nitric oxide synthase by estrogen. J Clin Invest 103: 401-406, 1999.
8. Chester AH, Jiang C, Borland JA, Yacoub MH, Collins P. Oestrogen relaxes human epicardial coronary arteries through non-endothelium-dependent mechanisms. Coron Artery Dis 6: 417-422, 1995.
9. Conrad KP, Joffe GM, Kruszyna H, Kruszyna R, Rochelle LG, Smith RP, Chavez JE, Mosher MD. Identification of increased nitric oxide biosynthesis during pregnancy in rats. FASEB J 7: 566-571, 1993.
10. Diano S, Horvath TL, Mor G, Register T, Adams M, Harada N, Naftolin F. Aromatase and estrogen receptor immunoreactivity in the coronary arteries of monkeys and human subjects. Menopause 6: 21-28, 1999.
11. Douglas P. Coronary artery disease in women. In: Heart Disease, edited by Braunwald E, Zipes DP, Libby P. Philadelphia, PA: Saunders, 2001, p. 2038-2051.
12. Douglas P. Coronary artery disease in women. In: Heart Disease, edited by Braunwald E, Zipes DP, Libby P. Philadelphia, PA: Saunders, 1997, p. 1704-1714.
13. Durkee TJ, Mueller M, Zinaman M. Identification of estrogen receptor protein and messenger ribonucleic acid in human spermatozoa. Am J Obstet Gynecol 178: 1288-1297, 1998.
14. Fletcher SW, Colditz GA. Failure of estrogen plus progestin therapy for prevention. JAMA 288: 366-368, 2002.
15. Ginsburg ES, Walsh BW, Gao X, Gleason RE, Feltmate C, Barbieri RL. The effect of acute ethanol ingestion on estrogen levels in postmenopausal women using transdermal estradiol. J Soc Gynecol Investig 2: 26-29, 1995.
16. Gomperts BD, Kramer IM, Tatham PER. Phosphoinositide 3-kinases, protein kinase B, and signalling through the insulin receptor. In: Signal Transduction. San Diego, CA: Academic, 2002, p. 299-313.
17. Grohe C, Kann S, Fink L, Djoufack PC, Paehr M, van Eickels M, Vetter H, Meyer R, Fink KB. 17Beta-estradiol regulates nNOS and eNOS activity in the hippocampus. Neuroreport 15: 89-93, 2004.
18. Ca channels by cyclic AMP-induced stimulation of the cyclic GMP-dependent protein kinase. J Cardiovasc Pharmacol 34: 619-627, 1999.
19. Han G, Yu X, Lu L, Li S, Ma H, Zhu S, Cui X, White RE. Estrogen receptor alpha mediates acute potassium channel stimulation in human coronary artery smooth muscle cells. J Pharmacol Exp Ther 316: 1025-1030, 2006.
20. Harada N, Sasano H, Murakami H, Ohkuma T, Nagura H, Takagi Y. Localized expression of aromatase in human vascular tissues. Circ Res 84: 1285-1291, 1999.
21. Hayashi T, Fukuto JM, Ignarro LJ, Chaudhuri G. Basal release of nitric oxide from aortic rings is greater in female rabbits than in male rabbits: implications for atherosclerosis. Proc Natl Acad Sci USA 89: 11259-11263, 1992.
22. Haynes MP, Sinha D, Russell KS, Collinge M, Fulton D, Morales-Ruiz M, Sessa WC, Bender JR. Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ Res 87: 677-682, 2000.
23. Hellstrom WJ, Bell M, Wang R, Sikka SC. Effect of sodium nitroprusside on sperm motility, viability, and lipid peroxidation. Fertil Steril 61: 1117-1122, 1994.
24. Huang A, Sun D, Shesely EG, Levee EM, Koller A, Kaley G. Neuronal NOS-dependent dilation to flow in coronary arteries of male eNOS-KO mice. Am J Physiol Heart Circ Physiol 282: H429-H436, 2002.
25. Kawano H, Motoyama T, Ohgushi M, Kugiyama K, Ogawa H, Yasue H. Menstrual cyclic variation of myocardial ischemia in premenopausal women with variant angina. Ann Intern Med 135: 977-981, 2001.
26. LeBlanc ES, Janowsky J, Chan BK, Nelson HD. Hormone replacement therapy and cognition: systematic review and meta-analysis. JAMA 285: 1489-1499, 2001.
27. Lewis SE, Donnelly ET, Sterling ES, Kennedy MS, Thompson W, Chakravarthy U. Nitric oxide synthase and nitrite production in human spermatozoa: evidence that endogenous nitric oxide is beneficial to sperm motility. Mol Hum Reprod 2: 873-878, 1996.
28. + channels of coronary smooth muscle. In: Heart Physiology and Pathophysiology, edited by Sperelakis N. San Diego, CA: Academic, 2001, p. 309-325.
29. Mugge A, Riedel M, Barton M, Kuhn M, Lichtlen PR. Endothelium independent relaxation of human coronary arteries by 17beta-oestradiol in vitro. Cardiovasc Res 27: 1939-1942, 1993.
30. Papadaki M, Tilton RG, Eskin SG, McIntire LV. Nitric oxide production by cultured human aortic smooth muscle cells: stimulation by fluid flow. Am J Physiol Heart Circ Physiol 274: H616-H626, 1998.
31. Patten RD, Karas RH. Estrogen replacement and cardiomyocyte protection. Trends Cardiovasc Med 16: 69-75, 2006.
32. Purohit V. Can alcohol promote aromatization of androgens to estrogens? A review. Alcohol 22: 123-127, 2000.
33. Reis SE, Gloth ST, Blumenthal RS, Resar JR, Zacur HA, Gerstenblith G, Brinker JA. Ethinyl estradiol acutely attenuates abnormal coronary vasomotor responses to acetylcholine in postmenopausal women. Circulation 89: 52-60, 1994.
34. Rosano GM, Caixeta AM, Chierchia S, Arie S, Lopez-Hidalgo M, Pereira WI, Leonardo F, Webb CM, Pileggi F, Collins P. Short-term anti-ischemic effect of 17beta-estradiol in postmenopausal women with coronary artery disease. Circulation 96: 2837-2841, 1997.
35. Rosano GM, Sarrel PM, Poole-Wilson PA, Collins P. Beneficial effect of oestrogen on exercise-induced myocardial ischaemia in women with coronary artery disease. Lancet 342: 133-136, 1993.
36. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC, Kotchen JM, Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288: 321-333, 2002.
37. Salhab WA, Shaul PW, Cox BE, Rosenfeld CR. Regulation of types I and III NOS in ovine uterine arteries by daily and acute estrogen exposure. Am J Physiol Heart Circ Physiol 278: H2134-H2142, 2000.
38. White RE, Darkow DJ, Lang JL. Estrogen relaxes coronary arteries by opening BKCa channels through a cGMP-dependent mechanism. Circ Res 77: 936-942, 1995.
39. White RE, Han G, Dimitropoulou C, Zhu S, Miyake K, Fulton D, Dave S, Barman SA. Estrogen-induced contraction of coronary arteries is mediated by superoxide generated in vascular smooth muscle. Am J Physiol Heart Circ Physiol 289: H1468-H1475, 2005.
40. + channels in human coronary artery smooth muscle cells. Cardiovasc Res 53: 650-661, 2002.
41. Xu KY, Huso DL, Dawson TM, Bredt DS, Becker LC. Nitric oxide synthase in cardiac sarcoplasmic reticulum. Proc Natl Acad Sci USA 96: 657-662, 1999.
42. ω-propyl-L-arginine. J Med Chem 40: 3869-3870, 1997.