Peroxynitrite mediates testosterone-induced vasodilation of microvascular resistance vessels

Journal of Pharmacology and Experimental Therapeutics

Volumn 345, Issue 1, 2013, Pages 7-14

  Puttabyatappa, Yashoda ^a   Stallone, John N ^c   Ergul, Adviye ^a   El Remessy, Azza B ^b   Kumar, Sanjiv ^a   Black, Stephen ^a   Johnson, Maribeth ^a   Owen, Mary P ^d   White, Richard E ^d  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

^d PHILADELPHIA COLLEGE OF OSTEOPATHIC MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; ANDROGEN RECEPTOR; CYCLIC GMP; DICHLOROFLUORESCEIN; ESTRADIOL; NITRIC OXIDE; PEROXYNITRITE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; SUPEROXIDE; TESTOSTERONE; XANTHINE OXIDASE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; AROMATIZATION; ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORONARY ARTERY; ENZYME ACTIVATION; ENZYME ACTIVITY; FLUORESCENCE; HORMONE ACTION; IMMUNOBLOTTING; MALE; MICROVASCULAR ARTERY; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; SIGNAL TRANSDUCTION; VASCULAR RESISTANCE; VASODILATATION;

ANDROGENS; ANIMALS; BLOTTING, WESTERN; CYCLIC GMP; ELECTRON SPIN RESONANCE SPECTROSCOPY; MALE; MICROVESSELS; NITRIC OXIDE; PEROXYNITROUS ACID; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDES; TESTOSTERONE; VASCULAR RESISTANCE; VASODILATION; XANTHINE OXIDASE;

EID: 84875466416     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.112.201947     Document Type: Article

References (45)

1. Berry CE and Hare JM (2004) Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J Physiol 555: 589-606.
2. Bhasin S and Buckwalter JG (2001) Testosterone supplementation in older men: a rational idea whose time has not yet come. J Androl 22:718-731.
3. Casey DB, Pankey EA, Badejo AM, Bueno FR, Bhartiya M, Murthy SN, Uppu RM, Nossaman BD, and Kadowitz PJ (2012) Peroxynitrite has potent pulmonary vasodilator activity in the rat. Can J Physiol Pharmacol 90:485-500.
4. Chou TM, Sudhir K, Hutchison SJ, Ko E, Amidon TM, Collins P, and Chatterjee K (1996) Testosterone induces dilation of canine coronary conductance and resistance arteries in vivo. Circulation 94:2614-2619.
5. Costarella CE, Stallone JN, Rutecki GW, and Whittier FC (1996) Testosterone causes direct relaxation of rat thoracic aorta. J Pharmacol Exp Ther 277:34-39.
6. Deenadayalu V, Puttabyatappa Y, Liu AT, Stallone JN, and White RE (2012) Testosterone-induced relaxation of coronary arteries: activation of BKCa channels via the cGMP-dependent protein kinase. Am J Physiol Heart Circ Physiol 302: H115-H123.
7. Deenadayalu VP, White RE, Stallone JN, Gao X, and Garcia AJ (2001) Testosterone relaxes coronary arteries by opening the large-conductance, calcium-activated potassium channel. Am J Physiol Heart Circ Physiol 281:H1720-H1727.
8. Diano S, Horvath TL, Mor G, Register T, Adams M, Harada N, and Naftolin F (1999) Aromatase and estrogen receptor immunoreactivity in the coronary arteries of monkeys and human subjects. Menopause 6:21-28.
9. Ding AQ and Stallone JN (2001) Testosterone-induced relaxation of rat aorta is androgen structure specific and involves K1 channel activation. J Appl Physiol 91: 2742-2750.
10. El-Remessy AB, Abou-Mohamed G, Caldwell RW, and Caldwell RB (2003) High glucose-induced tyrosine nitration in endothelial cells: role of eNOS uncoupling and aldose reductase activation. Invest Ophthalmol Vis Sci 44:3135-3143.
11. El-Remessy AB, Al-Shabrawey M, Platt DH, Bartoli M, Behzadian MA, Ghaly N, Tsai N, Motamed K, and Caldwell RB (2007) Peroxynitrite mediates VEGF's angiogenic signal and function via a nitration-independent mechanism in endothelial cells. FASEB J 21:2528-2539.
12. English KM, Jones RD, Jones TH, Morice AH, and Channer KS (2002) Testosterone acts as a coronary vasodilator by a calcium antagonistic action. J Endocrinol Invest 25:455-458.
13. Er F, Michels G, Brandt MC, Khan I, Haase H, Eicks M, Lindner M, and Hoppe UC (2007) Impact of testosterone on cardiac L-type calcium channels and Ca21 sparks: acute actions antagonize chronic effects. Cell Calcium 41:467-477.
14. Gorczynska E and Handelsman DJ (1995) Androgens rapidly increase the cytosolic calcium concentration in Sertoli cells. Endocrinology 136:2052-2059.
15. Graves JE, Lewis SJ, and Kooy NW (2005) Role of ATP-sensitive K1 -channels in hemodynamic effects of peroxynitrite in anesthetized rats. J Cardiovasc Pharmacol 46:653-659.
16. Han G, Ma H, Chintala R, Miyake K, Fulton DJ, Barman SA, and White RE (2007) Nongenomic, endothelium-independent effects of estrogen on human coronary smooth muscle are mediated by type I (neuronal) NOS and PI3-kinase-Akt signaling. Am J Physiol Heart Circ Physiol 293:H314-H321.
17. Haynes MP, Sinha D, Russell KS, Collinge M, Fulton D, Morales-Ruiz M, Sessa WC, and Bender JR (2000) Membrane estrogen receptor engagement activates endothelial nitric oxide synthase via the PI3-kinase-Akt pathway in human endothelial cells. Circ Res 87:677-682.
18. Iliescu R, Cucchiarelli VE, Yanes LL, Iles JW, and Reckelhoff JF (2007) Impact of androgen-induced oxidative stress on hypertension in male SHR. Am J Physiol Regul Integr Comp Physiol 292:R731-R735.
19. Katori T, Donzelli S, Tocchetti CG, Miranda KM, Cormaci G, Thomas DD, Ketner EA, Lee MJ, Mancardi D, and Wink DA, et al. (2006) Peroxynitrite and myocardial contractility: in vivo versus in vitro effects. Free Radic Biol Med 41:1606-1618.
20. Keating NL, O'Malley AJ, and Smith MR (2006) Diabetes and cardiovascular disease during androgen deprivation therapy for prostate cancer. J Clin Oncol 24: 4448-4456.
21. Khaw KT and Barrett-Connor E (1988) Blood pressure and endogenous testosterone in men: an inverse relationship. J Hypertens 6:329-332.
22. Khaw KT, Dowsett M, Folkerd E, Bingham S, Wareham N, Luben R, Welch A, and Day N (2007) Endogenous testosterone and mortality due to all causes, cardiovascular disease, and cancer in men: European prospective investigation into cancer in Norfolk (EPIC-Norfolk) Prospective Population Study. Circulation 116: 2694-2701.
23. Kohr MJ, Traynham CJ, Roof SR, Davis JP, and Ziolo MT (2010) cAMP-independent activation of protein kinase A by the peroxynitrite generator SIN-1 elicits positive inotropic effects in cardiomyocytes. J Mol Cell Cardiol 48:645-648.
24. Kouloumenta V, Hatziefthimiou A, Paraskeva E, Gourgoulianis K, and Molyvdas PA (2006) Non-genomic effect of testosterone on airway smooth muscle. Br J Pharmacol 149:1083-1091.
25. Lakshminrusimha S, Wiseman D, Black SM, Russell JA, Gugino SF, Oishi P, Steinhorn RH, and Fineman JR (2007) The role of nitric oxide synthase-derived reactive oxygen species in the altered relaxation of pulmonary arteries from lambs with increased pulmonary blood flow. Am J Physiol Heart Circ Physiol 293: H1491-H1497.
26. Levinson DJ and Chalker D (1980) Rat hepatic xanthine oxidase activity: age and sex specific differences. Arthritis Rheum 23:77-82.
27. Li J, Li W, Altura BT, and Altura BM (2005) Peroxynitrite-induced relaxation in isolated rat aortic rings and mechanisms of action. Toxicol Appl Pharmacol 209: 269-276.
28. Lyng FM, Jones GR, and Rommerts FF (2000) Rapid androgen actions on calcium signaling in rat sertoli cells and two human prostatic cell lines: similar biphasic responses between 1 picomolar and 100 nanomolar concentrations. Biol Reprod 63: 736-747.
29. Maggio M, Lauretani F, Ceda GP, Bandinelli S, Ling SM, Metter EJ, Artoni A, Carassale L, Cazzato A, and Ceresini G, et al. (2007) Relationship between low levels of anabolic hormones and 6-year mortality in older men: the aging in the Chianti Area (InCHIANTI) study. Arch Intern Med 167:2249-2254.
30. Marrachelli VG, Miranda FJ, Centeno JM, Salom JB, Torregrosa G, Jover-Mengual T, Pérez AM, Moro MA, and Alborch E (2010) Role of NO-synthases and cyclooxygenases in the hyperreactivity of male rabbit carotid artery to testosterone under experimental diabetes. Pharmacol Res 61:62-70.
31. Mathur A, Malkin C, Saeed B, Muthusamy R, Jones TH, and Channer K (2009) Longterm benefits of testosterone replacement therapy on angina threshold and atheroma in men. Eur J Endocrinol 161:443-449.
32. Mayer B, Schrammel A, Klatt P, Koesling D, and Schmidt K (1995) Peroxynitriteinduced accumulation of cyclic GMP in endothelial cells and stimulation of purified soluble guanylyl cyclase. Dependence on glutathione and possible role of S-nitrosation. J Biol Chem 270:17355-17360.
33. Mulvany MJ and Halpern W (1977) Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats. Circ Res 41:19-26.
34. Paolocci N, Ekelund UE, Isoda T, Ozaki M, Vandegaer K, Georgakopoulos D, Harrison RW, Kass DA, and Hare JM (2000) cGMP-independent inotropic effects of nitric oxide and peroxynitrite donors: potential role for nitrosylation. Am J Physiol Heart Circ Physiol 279:H1982-H1988.
35. Rosano GM, Sheiban I, Massaro R, Pagnotta P, Marazzi G, Vitale C, Mercuro G, Volterrani M, Aversa A, and Fini M (2007) Low testosterone levels are associated with coronary artery disease in male patients with angina. Int J Impot Res 19: 176-182.
36. Seyrek M, Yildiz O, Ulusoy HB, and Yildirim V (2007) Testosterone relaxes isolated human radial artery by potassium channel opening action. J Pharmacol Sci 103: 309-316.
37. Sullivan JC, Sasser JM, and Pollock JS (2007) Sexual dimorphism in oxidant status in spontaneously hypertensive rats. Am J Physiol Regul Integr Comp Physiol 292: R764-R768.
38. Sullivan ML, Martinez CM, Gennis P, and Gallagher EJ (1998) The cardiac toxicity of anabolic steroids. Prog Cardiovasc Dis 41:1-15.
39. Szasz T, Thompson JM, and Watts SW (2008) A comparison of reactive oxygen species metabolism in the rat aorta and vena cava: focus on xanthine oxidase. Am J Physiol Heart Circ Physiol 295:H1341-H1350.
40. Tep-areenan P, Kendall DA, and Randall MD (2002) Testosterone-induced vasorelaxation in the rat mesenteric arterial bed is mediated predominantly via potassium channels. Br J Pharmacol 135:735-740.
41. White RE, Han G, Dimitropoulou C, Zhu S, Miyake K, Fulton D, Dave S, and Barman SA (2005) Estrogen-induced contraction of coronary arteries is mediated by superoxide generated in vascular smooth muscle. Am J Physiol Heart Circ Physiol 289:H1468-H1475.
42. White RE, Han G, Maunz M, Dimitropoulou C, El-Mowafy AM, Barlow RS, Catravas JD, Snead C, Carrier GO, and Zhu S, et al. (2002) Endothelium- independent effect of estrogen on Ca(21)-activated K(1) channels in human coronary artery smooth muscle cells. Cardiovasc Res 53:650-661.
43. White RE, Kryman JP, El-Mowafy AM, Han G, and Carrier GO (2000) cAMPdependent vasodilators cross-activate the cGMP-dependent protein kinase to stimulate BK(Ca) channel activity in coronary artery smooth muscle cells. Circ Res 86:897-905.
44. Yu J, Akishita M, Eto M, Ogawa S, Son BK, Kato S, Ouchi Y, and Okabe T (2010) Androgen receptor-dependent activation of endothelial nitric oxide synthase in vascular endothelial cells: role of phosphatidylinositol 3-kinase/akt pathway. Endocrinology 151:1822-1828.
45. Yue P, Chatterjee K, Beale C, Poole-Wilson PA, and Collins P (1995) Testosterone relaxes rabbit coronary arteries and aorta. Circulation 91:1154-1160.