L-Arginine restores endothelial nitric oxide synthase-coupled activity and attenuates monocrotaline-induced pulmonary artery hypertension in rats

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 6, 2010, Pages

  Ou, Zhi Jun ^a   Wei, Wei ^b   Huang, Da De ^b   Luo, Wei ^c   Luo, Dan ^a   Wang, Zhi Ping ^a   Zhang, Xi ^a   Ou, Jing Song ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b GUANGZHOU FIRST PEOPLE'S HOSPITAL   (China)

^c GUANGZHOU MEDICAL UNIVERSITY   (China)

Author keywords

Heat shock protein 90; Nitric oxide; Superoxide anion

Indexed keywords

ARGININE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEAT SHOCK PROTEIN 90; MONOCROTALINE; NITRIC OXIDE; SUPEROXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL WALL THICKNESS; ARTICLE; CONTROLLED STUDY; HEART HYPERTROPHY; HEART RIGHT VENTRICLE; IMMUNOPRECIPITATION; LUNG ARTERY PRESSURE; MOLECULAR MECHANICS; MORTALITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PULMONARY ARTERY; PULMONARY HYPERTENSION; RAT; SURVIVAL RATE; SYSTOLIC BLOOD PRESSURE; WESTERN BLOTTING;

ANIMALS; ARGININE; BLOOD PRESSURE; BLOTTING, WESTERN; BODY WEIGHT; HSP90 HEAT-SHOCK PROTEINS; HYPERTENSION, PULMONARY; IMMUNOPRECIPITATION; KAPLAN-MEIERS ESTIMATE; MALE; MONOCROTALINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PHOSPHORYLATION; PULMONARY ARTERY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 77952667734     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00107.2010     Document Type: Article

References (49)

1. Chandrasekar I, Eis A, Konduri GG. Betamethasone attenuates oxidant stress in endothelial cells from fetal lambs with persistent pulmonary hypertension. Pediatr Res 63: 67-72, 2008.
2. Chen JX, Lawrence ML, Cunningham G, Christman BW, Meyrick B. HSP90 and Akt modulate Ang-1-induced angiogenesis via NO in coronary artery endothelium. J Appl Physiol 96: 612-620, 2004. (Pubitemid 38140163)
3. Cox RH, Bagshaw RJ. Influence of anesthesia on the response to carotid hypotension in dogs. Am J Physiol Heart Circ Physiol 237: H424-H432, 1979. (Pubitemid 10249644)
4. Dasgupta T, Hebbel RP, Kaul DK. Protective effect of arginine on oxidative stress in transgenic sickle mouse models. Free Radic Biol Med 41: 1771-1780, 2006. (Pubitemid 44839141)
5. Fagan JM, Rex SE, Hayes-Licitra SA, Waxman L. L-arginine reduces right heart hypertrophy in hypoxia-induced pulmonary hypertension. Biochem Biophys Res Commun 254: 100-103, 1999. (Pubitemid 29292022)
6. Fagan KA, Fouty BW, Tyler RC, Morris KG Jr, Hepler LK, Sato K, LeCras TD, Abman SH, Weinberger HD, Huang PL, McMurtry IF, Rodman DM. The pulmonary circulation of homozygous or heterozygous eNOS-null mice is hyperresponsive to mild hypoxia. J Clin Invest 103: 291-299, 1999.
7. Fike CD, Aschner JL, Zhang Y, Kaplowitz MR. Impaired NO signaling in small pulmonary arteries of chronically hypoxic newborn piglets. Am J Physiol Lung Cell Mol Physiol 286: L1244-L1254, 2004.
8. Fike CD, Kaplowitz MR, Rehorst-Paea LA, Nelin LD. L-Arginine increases nitric oxide production in isolated lungs of chronically hypoxic newborn pigs. J Appl Physiol 88: 1797 - 1803, 2000.
9. Garcia-Cardena G, Fan R, Shah V, Sorrentino R, Cirino G, Papapetropoulos A, Sessa WC. Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature 392: 821-824, 1998. (Pubitemid 28225323)
10. Giaid A, Saleh D. Reduced expression of endothelial nitric oxide synthase in the lungs of patients with pulmonary hypertension. N Engl J Med 333: 214-221, 1995.
11. Giraldelo CM, Zappellini A, Muscara MN, De Luca IM, Hyslop S, Cirino G, Zatz R, De Nucci G, Antunes E. Effect of arginine analogues on rat hind paw oedema and mast cell activation in vitro. Eur J Pharmacol 257: 87-93, 1994. (Pubitemid 24178555)
12. Girgis RE, Champion HC, Diette GB, Johns RA, Permutt S, Sylvester JT. Decreased exhaled nitric oxide in pulmonary arterial hypertension: response to bosentan therapy. Am J Respir Crit Care Med 172: 352-357, 2005. (Pubitemid 41026146)
13. Giugliano D, Marfella R, Verrazzo G, Acampora R, Coppola L, Cozzolino D, D'Onofrio F. The vascular effects of L-Arginine in humans. The role of endogenous insulin. J Clin Invest 99: 433-438, 1997. (Pubitemid 27414800)
14. Hironaka E, Hongo M, Sakai A, Mawatari E, Terasawa F, Okumura N, Yamazaki A, Ushiyama Y, Yazaki Y, Kinoshita O. Serotonin receptor antagonist inhibits monocrotaline-induced pulmonary hypertension and prolongs survival in rats. Cardiovasc Res 60: 692-699, 2003.
15. Howell K, Costello CM, Sands M, Dooley I, McLoughlin P. L-Arginine promotes angiogenesis in the chronically hypoxic lung: a novel mechanism ameliorating pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 296: L1042-L1050, 2009.
16. Huang J, Kaminski PM, Edwards JG, Yeh A, Wolin MS, Frishman WH, Gewitz MH, Mathew R. Pyrrolidine dithiocarbamate restores endothelial cell membrane integrity and attenuates monocrotaline-induced pulmonary artery hypertension. Am J Physiol Lung Cell Mol Physiol 294: L1250-L1259, 2008.
17. Konduri GG, Bakhutashvili I, Eis A, Pritchard K Jr. Oxidant stress from uncoupled nitric oxide synthase impairs vasodilation in fetal lambs with persistent pulmonary hypertension. Am J Physiol Heart Circ Physiol 292: H1812-H1820, 2007.
18. Konduri GG, Ou J, Shi Y, Pritchard KA Jr. Decreased association of HSP90 impairs endothelial nitric oxide synthase in fetal lambs with persistent pulmonary hypertension. Am J Physiol Heart Circ Physiol 285: H204-H211, 2003.
19. Koshida R, Ou J, Matsunaga T, Chilian WM, Oldham KT, Ackerman AW, Pritchard KA Jr. Angiostatin, a negative regulator of endothelial-dependent vasodilation. Circulation 107: 803-806, 2003. (Pubitemid 36241035)
20. Leblais V, Delannoy E, Fresquet F, Begueret H, Bellance N, Banquet S, Allieres C, Leroux L, Desgranges C, Gadeau A, Muller B. Beta-adrenergic relaxation in pulmonary arteries: preservation of the endothelial nitric oxide-dependent beta2 component in pulmonary hypertension. Cardiovasc Res 77: 202-210, 2008.
21. Liao X, Liu JM, Du L, Tang A, Shang Y, Wang SQ, Chen LY, Chen Q. Nitric oxide signaling in stretch-induced apoptosis of neonatal rat cardiomyocytes. FASEB J 20: 1883-1885, 2006.
22. Loscalzo J. What we know and don't know about L-arginine and NO. Circulation 101: 2126-2129, 2000.
23. Mathew R, Gloster ES, Sundararajan T, Thompson CI, Zeballos GA, Gewitz MH. Role of inhibition of nitric oxide production in monocrotaline-induced pulmonary hypertension. J Appl Physiol 82: 1493-1498, 1997. (Pubitemid 27203858)
24. Mathew R, Huang J, Shah M, Patel K, Gewitz M, Sehgal PB. Disruption of endothelial-cell caveolin-1alpha/raft scaffolding during development of monocrotaline-induced pulmonary hypertension. Circulation 110: 1499-1506, 2004. (Pubitemid 39238030)
25. McCabe TJ, Fulton D, Roman LJ, Sessa WC. Enhanced electron flux and reduced calmodulin dissociation may explain "calcium-independent" eNOS activation by phosphorylation. J Biol Chem 275: 6123-6128, 2000.
26. McCaffrey MJ, Bose CL, Reiter PD, Stiles AD. Effect of L-arginine infusion on infants with persistent pulmonary hypertension of the newborn. Biol Neonate 67: 240-243, 1995.
27. Mehta S, Stewart DJ, Langleben D, Levy RD. Short-term pulmonary vasodilation with L-arginine in pulmonary hypertension. Circulation 92: 1539-1545, 1995.
28. Mitani Y, Maruyama K, Sakurai M. Prolonged administration of L-arginine ameliorates chronic pulmonary hypertension and pulmonary vascular remodeling in rats. Circulation 96: 689-697, 1997. (Pubitemid 27329452)
29. Nagaya N, Uematsu M, Oya H, Sato N, Sakamaki F, Kyotani S, Ueno K, Nakanishi N, Yamagishi M, Miyatake K. Short-term oral administration of L-arginine improves hemodynamics and exercise capacity in patients with precapillary pulmonary hypertension. Am J Respir Crit Care Med 163: 887-891, 2001.
30. Oishi P, Grobe A, Benavidez E, Ovadia B, Harmon C, Ross GA, Hendricks-Munoz K, Xu J, Black SM, Fineman JR. Inhaled nitric oxide induced NOS inhibition and rebound pulmonary hypertension: a role for superoxide and peroxynitrite in the intact lamb. Am J Physiol Lung Cell Mol Physiol 290: L359-L366, 2006.
31. Ou J, Fontana JT, Ou Z, Jones DW, Ackerman AW, Oldham KT, Yu J, Sessa WC, Pritchard KA Jr. Heat shock protein 90 and tyrosine kinase regulate eNOS·NO generation but not·NO bioactivity. Am J Physiol Heart Circ Physiol 286: H561-H569, 2004.
32. Ou J, Ou Z, McCarver DG, Hines RN, Oldham KT, Ackerman AW, Pritchard KA Jr. Trichloroethylene decreases heat shock protein 90 interactions with endothelial nitric oxide synthase: implications for endothelial cell proliferation. Toxicol Sci 73: 90-97, 2003. (Pubitemid 36609090)
33. Ou Z, Ou J, Ackerman AW, Oldham KT, Pritchard KA Jr. L-4F, an apolipoprotein A-1 mimetic, restores nitric oxide and superoxide anion balance in low-density lipoprotein-treated endothelial cells. Circulation 107: 1520-1524, 2003. (Pubitemid 36378491)
34. Pi X, Patterson C. Twin layers of lightning: a new role for the chaperone Hsp90 in angiogenesis. Arterioscler Thromb Vasc Biol 28: 6-7, 2008.
35. Pritchard KA Jr, Ackerman AW, Gross ER, Stepp DW, Shi Y, Fontana JT, Baker JE, Sessa WC. Heat shock protein 90 mediates the balance of nitric oxide and superoxide anion from endothelial nitric-oxide synthase. J Biol Chem 276: 17621-17624, 2001.
36. Quyyumi AA. Does acute improvement of endothelial dysfunction in coronary artery disease improve myocardial ischemia? A double-blind comparison of parenteral D- and L-arginine. J Am Coll Cardiol 32: 904-911, 1998.
37. Rabinovitch M, Gamble WJ, Miettinen OS, Reid L. Age and sex influence on pulmonary hypertension of chronic hypoxia and on recovery. Am J Physiol Heart Circ Physiol 240: H62-H72, 1981.
38. Sasaki S, Asano M, Ukai T, Nomura N, Maruyama K, Manabe T, Mishima A. Nitric oxide formation and plasma L-arginine levels in pulmonary hypertensive rats. Respir Med 98: 205-212, 2004.
39. Schermuly RT, Kreisselmeier KP, Ghofrani HA, Yilmaz H, Butrous G, Ermert L, Ermert M, Weissmann N, Rose F, Guenther A, Walmrath D, Seeger W, Grimminger F. Chronic sildenafil treatment inhibits monocrotaline-induced pulmonary hypertension in rats. Am J Respir Crit Care Med 169: 39-45, 2004.
40. Schneider R, Raff U, Vornberger N, Schmidt M, Freund R, Reber M, Schramm L, Gambaryan S, Wanner C, Schmidt HH, Galle J. L-Arginine counteracts nitric oxide deficiency and improves the recovery phase of ischemic acute renal failure in rats. Kidney Int 64: 216-225, 2003. (Pubitemid 36714174)
41. Sharma S, Kumar S, Sud N, Wiseman DA, Tian J, Rehmani I, Datar S, Oishi P, Fratz S, Venema RC, Fineman JR, Black SM. Alterations in lung arginine metabolism in lambs with pulmonary hypertension associated with increased pulmonary blood flow. Vascul Pharmacol 51: 359-364, 2009.
42. Stepp DW, Ou J, Ackerman AW, Welak S, Klick D, Pritchard KA Jr. Native LDL and minimally oxidized LDL differentially regulate superoxide anion in vascular endothelium in situ. Am J Physiol Heart Circ Physiol 283: H750-H759, 2002. (Pubitemid 34790871)
43. Sud N, Sharma S, Wiseman DA, Harmon C, Kumar S, Venema RC, Fineman JR, Black SM. Nitric oxide and superoxide generation from endothelial NOS: modulation by HSP90. Am J Physiol Lung Cell Mol Physiol 293: L1444-L1453, 2007.
44. Sun J, Liao JK. Induction of angiogenesis by heat shock protein 90 mediated by protein kinase Akt and endothelial nitric oxide synthase. Arterioscler Thromb Vasc Biol 24: 2238-2244, 2004.
45. Takahashi S, Mendelsohn ME. Synergistic activation of endothelial nitric-oxide synthase (eNOS) by HSP90 and Akt: calcium-independent eNOS activation involves formation of an HSP90-Akt-CaM-bound eNOS complex. J Biol Chem 278: 30821-30827, 2003. (Pubitemid 36994590)
46. Tan X, Sun WD, Li JC, Pan JQ, Liu YJ, Wang JY, Wang XL. L-Arginine prevents reduced expression of endothelial nitric oxide synthase (NOS) in pulmonary arterioles of broilers exposed to cool temperatures. Vet J 173: 151-157, 2007.
47. Tarpey MM, Wink DA, Grisham MB. Methods for detection of reactive metabolites of oxygen and nitrogen: in vitro and in vivo considerations. Am J Physiol Regul Integr Comp Physiol 286: R431-R444, 2004.
48. Wedgwood S, McMullan DM, Bekker JM, Fineman JR, Black SM. Role for endothelin-1-induced superoxide and peroxynitrite production in rebound pulmonary hypertension associated with inhaled nitric oxide therapy. Circ Res 89: 357-364, 2001. (Pubitemid 34132675)
49. Yu J, deMuinck ED, Zhuang Z, Drinane M, Kauser K, Rubanyi GM, Qian HS, Murata T, Escalante B, Sessa WC. Endothelial nitric oxide synthase is critical for ischemic remodeling, mural cell recruitment, and blood flow reserve. Proc Natl Acad Sci USA 102: 10999-11004, 2005.