Neuronal nitric oxide synthase inhibition improves diastolic function and reduces oxidative stress in ovariectomized mRen2.Lewis rats

Menopause

Volumn 18, Issue 6, 2011, Pages 698-708

  Jessup, Jewell A ^a   Zhang, Lili ^b   Chen, Alex F ^b,c   Presley, Tennille D ^d   Kim Shapiro, Daniel B ^d,e   Chappell, Mark C ^a   Wang, Hao ^a   Groban, Leanne ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d WINSTON SALEM STATE UNIVERSITY   (United States)

^e WAKE FOREST UNIVERSITY   (United States)

Author keywords

Diastolic function; Fibrosis; Left ventricular modeling; Myocardial relaxation; Nitric oxide; Postmenopausal

Indexed keywords

BIOPTERIN; DIHYDROBIOPTERIN; ESTRADIOL; ESTROGEN; N5 (1 IMINO 3 BUTENYL)LEVO ORNITHINE; NEURONAL NITRIC OXIDE SYNTHASE; ORNITHINE DERIVATIVE; TETRAHYDROBIOPTERIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DIASTOLIC DYSFUNCTION; ECHOCARDIOGRAPHY; ESTRADIOL BLOOD LEVEL; FEMALE; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART VENTRICLE REMODELING; HYPERTENSION; MYOCARDIAL DISEASE; NONHUMAN; OVARIECTOMY; OXIDATIVE STRESS; RANDOMIZED CONTROLLED TRIAL; RAT; SHAM PROCEDURE; SYSTOLIC BLOOD PRESSURE; VASCULAR FIBROSIS; WESTERN BLOTTING;

ANIMALS; DIASTOLE; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FEMALE; HEART FAILURE, DIASTOLIC; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; ORNITHINE; OVARIECTOMY; OXIDATIVE STRESS; RATS; RATS, INBRED LEW;

EID: 79958814583     PISSN: 10723714     EISSN: 15300374     Source Type: Journal    
DOI: 10.1097/gme.0b013e31820390a2     Document Type: Article

References (54)

1. Lloyd-Jones D, Adams R, Carnethon M, et al. Heart disease and stroke statisticsV2009 update. A report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2009;119:E21-E181.
2. Owan TE, Hodge DO, Herges RM, Jacobsen SJ, Roger VL, Redfield MM. Trends in prevalence and outcome of heart failure with preserved ejection fraction. N Engl J Med 2006;355:251-259. (Pubitemid 44079340)
3. Roger VL, Weston SA, Redfield MM, et al. Trends in heart failure incidence and survival in a community-based population. JAMA 2004; 292:344-350. (Pubitemid 38944258)
4. Masoudi FA, Havranek EP, Smith G, et al. Gender, age, and heart failure with preserved left ventricular systolic function. J Am Coll Cardiol 2003;41:217-223. (Pubitemid 36092188)
5. Tsutsui H, Tsuchihashi-Makaya M, Kinugawa S, Goto D, Takeshita A. Clinical characteristics and outcome of hospitalized patients with heart failure in Japan. Circ J 2006;70:1617-1623.
6. Wong DT, Clark RA, Dundon BK, Philpott A, Molaee P, Shakib S. Caveat anicula! Beware of quiet little old ladies: demographic features, pharmacotherapy, readmissions and survival in a 10-year cohort of patients with heart failure and preserved systolic function. Med J Aust 2010;192:9-13.
7. Levy D, Kenchaiah S, Larson MG, et al. Long-term trends in the incidence of and survival with heart failure. N Engl J Med 2002;347: 1397-1402. (Pubitemid 35239711)
8. Rusinaru D, Mahjoub H, Goissen T, Massy Z, Peltier M, Tribouilloy C. Clinical features and prognosis of heart failure in women. A 5-year prospective study. Int J Cardiol 2009;133:327-335.
9. Agabiti-Rosei E, Muiesan ML. Left ventricular hypertrophy and heart failure in women. J Hypertens Suppl 2002;20:S34-S38. (Pubitemid 34913765)
10. Oberman A, Prineas RJ, Larson JC, Lacroix A, Lasser NL. Prevalence and determinants of electrocardiographic left ventricular hypertrophy among a multiethnic population of postmenopausal women (the Women's Health Initiative). Am J Cardiol 2006;97:512-519. (Pubitemid 43190042)
11. Fak AS, Erenus M, Tezcan H, Caymaz O, Oktay S, Oktay A. Effects of a single dose of oral estrogen on left ventricular diastolic function in hypertensive postmenopausal women with diastolic dysfunction. Fertil Steril 2000;73:66-71. (Pubitemid 30018024)
12. Rossouw JE, Anderson GL, Prentice RL, et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 2002;288:321-333. (Pubitemid 34761611)
13. Javeshghani D, Schiffrin EL, Sairam MR, Touyz RM. Potentiation of vascular oxidative stress and nitric oxideYmediated endothelial dysfunction by high-fat diet in a mouse model of estrogen deficiency and hyperandrogenemia. J Am Soc Hypertens 2009;3:295-305.
14. Maric C, Xu Q, Sandberg K, Hinojosa-Laborde C. Age-related renal disease in female Dahl salt-sensitive rats is attenuated with 17A-estradiol supplementation by modulating nitric oxide synthase expression. Gend Med 2008;5:147-159. (Pubitemid 351899437)
15. Santos RL, Abreu GR, Bissoli NS, Moyses MR. Endothelial mediators of 17A-estradiol-induced coronary vasodilation in the isolated rat heart. Braz J Med Biol Res 2004;37:569-575. (Pubitemid 38618553)
16. Staessen J, Bulpitt CJ, Fagard R, Lijnen P, Amery A. The influence of menopause on blood pressure. J Hum Hypertens 1989;3:427-433. (Pubitemid 20033325)
17. Raij L. Nitric oxide in the pathogenesis of cardiac disease. J Clin Hypertens (Greenwich) 2006;8:30-39.
18. Garcia-Duran M, de Frutos T, Diaz-Recasens J, et al. Estrogen stimulates neuronal nitric oxide synthase protein expression in human neutrophils. Circ Res 1999;85:1020-1026.
19. Molero L, Garcia-Duran M, Diaz-Recasens J, Rico L, Casado S, Lopez-Farre A. Expression of estrogen receptor subtypes and neuronal nitric oxide synthase in neutrophils from women and men: regulation by estrogen. Cardiovasc Res 2002;56:43-51. (Pubitemid 35247801)
20. Qian X, Jin L, Lloyd RV. Estrogen downregulates neuronal nitric oxide synthase in rat anterior pituitary cells and GH3 tumors. Endocrine 1999;11:123-130. (Pubitemid 30013602)
21. 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 2000;278:H2134-H2142. (Pubitemid 30439228)
22. Nuedling S, Karas RH, Mendelsohn ME, et al. Activation of estrogen receptor A is a prerequisite for estrogen-dependent upregulation of nitric oxide synthases in neonatal rat cardiac myocytes. FEBS Lett 2001;502: 103-108. (Pubitemid 32728269)
23. Groban L, Yamaleyeva LM, Westwood BM, et al. Progressive diastolic dysfunction in the female mRen(2).Lewis rat: influence of salt and ovarian hormones. J Gerontol A Biol Sci Med Sci 2008;63:3-11. (Pubitemid 351738458)
24. Ferrario CM, Jessup J, Chappell MC, et al. Effect of angiotensin- converting enzyme inhibition and angiotensin II receptor blockers on cardiac angiotensin-converting enzyme 2. Circulation 2005;111:2605-2610. (Pubitemid 40740859)
25. Chappell MC, Westwood BM, Yamaleyeva LM. Differential effects of sex steroids in young and aged female mRen2.Lewis rats: a model of estrogen and salt-sensitive hypertension. Gend Med 2008;5:S65-S75. (Pubitemid 351455232)
26. Yamaleyeva LM, Gallagher PE, Vinsant S, Chappell MC. Discoordinate regulation of renal nitric oxide synthase isoforms in ovariectomized mRen2.Lewis rats. Am J Physiol Regul Integr Comp Physiol 2007;292: R819-R826. (Pubitemid 46207735)
27. Jessup JA, Westwood BM, Chappell MC, Groban L. Dual ACE-inhibition and AT1 receptor antagonism improves ventricular lusitropy without affecting cardiac fibrosis in the congenic mRen2.Lewis rat. Ther Adv Cardiovasc Dis 2009;3:245-257.
28. Zheng JS, Yang XQ, Lookingland KJ, et al. Gene transfer of human guanosine 5¶-triphosphate cyclohydrolase I restores vascular tetrahy-drobiopterin level and endothelial function in low renin hypertension. Circulation 2003;108:1238-1245. (Pubitemid 37099994)
29. Bryan NS, Fernandez BO, Bauer SM, et al. Nitrite is a signaling molecule and regulator of gene expression in mammalian tissues. Nat Chem Biol 2005;1:290-297.
30. Lam KK, Lee YM, Hsiao G, Chen SY, Yen MH. Estrogen therapy replenishes vascular tetrahydrobiopterin and reduces oxidative stress in ovariectomized rats. Menopause 2006;13:294-302.
31. Shi W, Meininger CJ, Haynes TE, Hatakeyama K, Wu G. Regulation of tetrahydrobiopterin synthesis and bioavailability in endothelial cells. Cell Biochem Biophys 2004;41:415-434.
32. Sam F, Duhaney TA, Sato K, et al. Adiponectin deficiency, diastolic dysfunction, and diastolic heart failure. Endocrinology 2010;151:322-331.
33. Shieh FK, Kotlyar E, Sam F. Aldosterone and cardiovascular remodelling: focus on myocardial failure. J Renin Angiotensin Aldosterone Syst 2004;5:3-13. (Pubitemid 38477509)
34. Tsybouleva N, Zhang L, Chen S, et al. Aldosterone, through novel signaling proteins, is a fundamental molecular bridge between the genetic defect and the cardiac phenotype of hypertrophic cardiomyopathy. Circulation 2004;109:1284-1291. (Pubitemid 38372788)
35. Dubey RK, Gillespie DG, Jackson EK, Keller PJ. 17A-Estradiol, its metabolites, and progesterone inhibit cardiac fibroblast growth. Hypertension 1998;31:522-528.
36. Xu Y, Arenas IA, Armstrong SJ, Davidge ST. Estrogen modulation of left ventricular remodeling in the aged heart. Cardiovasc Res 2003; 57:388-394. (Pubitemid 36144217)
37. Silberman GA, Fan TH, Liu H, et al. Uncoupled cardiac nitric oxide synthase mediates diastolic dysfunction. Circulation 2010;121: 519-528.
38. Futai R, Ito T, Kawanishi Y, Terasaki F, Kitaura Y. Olmesartan ameliorates myocardial function independent of blood pressure control in patients with mild-to-moderate hypertension. Heart Vessels 2009;24: 294-300.
39. Nishio M, Sakata Y, Mano T, et al. Therapeutic effects of angiotensin II type 1 receptor blocker at an advanced stage of hypertensive diastolic heart failure. J Hypertens 2007;25:455-461. (Pubitemid 46071945)
40. Yoshida J, Yamamoto K, Mano T, et al. AT1 receptor blocker added to ACE inhibitor provides benefits at advanced stage of hypertensive dias-tolic heart failure. Hypertension 2004;43:686-691. (Pubitemid 38282448)
41. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J 2001;357:593-615. (Pubitemid 32735142)
42. Gorren AC, Schrammel A, Riethmuller C, et al. Nitric oxideYinduced autoinhibition of neuronal nitric oxide synthase in the presence of the autoxidation-resistant pteridine 5-methyltetrahydrobiopterin. Biochem J 2000;347:475-484.
43. Serova LI, Maharjan S, Sabban EL. Estrogen modifies stress response of catecholamine biosynthetic enzyme genes and cardiovascular system in ovariectomized female rats. Neuroscience 2005;132:249-259. (Pubitemid 40417901)
44. White RE, Han G, Dimitropoulou C, et al. Estrogen-induced contraction of coronary arteries is mediated by superoxide generated in vascular smooth muscle. Am J Physiol Heart Circ Physiol 2005;289: H1468-H1475. (Pubitemid 41368988)
45. Moens AL, Takimoto E, Tocchetti CG, et al. Reversal of cardiac hypertrophy and fibrosis from pressure overload by tetrahydrobiopterin: efficacy of recoupling nitric oxide synthase as a therapeutic strategy. Circulation 2008;117:2626-2636.
46. Takimoto E, Champion HC, Li M, et al. Oxidant stress from nitric oxide synthase-3 uncoupling stimulates cardiac pathologic remodeling from chronic pressure load. J Clin Invest 2005;115:1221-1231. (Pubitemid 40629040)
47. Moens AL, Leyton-Mange JS, Niu X, et al. Adverse ventricular remodeling and exacerbated NOS uncoupling from pressure-overload in mice lacking the A3-adrenoreceptor. J Mol Cell Cardiol 2009;47: 576-585.
48. Umar S, van der Laarse A. Nitric oxide and nitric oxide synthase isoforms in the normal, hypertrophic, and failing heart. Mol Cell Biochem 2010; 333:191-201.
49. Zhang GX, Kimura S, Murao K, Shimizu J, Matsuyoshi H, Takaki M. Role of neuronal NO synthase in regulating vascular superoxide levels and mitogen-activated protein kinase phosphorylation. Cardiovasc Res 2009;81:389-399.
50. 5-(1-imino-3-butenyl)-L-ornithine. A neuronal isoform selective mechanism-based inactivator of nitric oxide synthase. J Biol Chem 1998;273:8882-8889. (Pubitemid 28176170)
51. Ashley EA, Sears CE, Bryant SM, Watkins HC, Casadei B. Cardiac nitric oxide synthase 1 regulates basal and A-adrenergic contractility in murine ventricular myocytes. Circulation 2002;105:3011-3016. (Pubitemid 34693835)
52. Sears CE, Bryant SM, Ashley EA, et al. Cardiac neuronal nitric oxide synthase isoform regulates myocardial contraction and calcium handling. Circ Res 2003;92:E52-E59.
53. Lobo RA. Surgical menopause and cardiovascular risks. Menopause 2007;14:562-566. (Pubitemid 46716173)
54. Shuster LT, Gostout BS, Grossardt BR, Rocca WA. Prophylactic oophorectomy in premenopausal women and long-term health. Menopause Int 2008;14:111-116.