Decreased production of neuronal NOS-derived hydrogen peroxide contributes to endothelial dysfunction in atherosclerosis

British Journal of Pharmacology

Volumn 164, Issue 6, 2011, Pages 1738-1748

  Capettini, L S A ^a   Cortes, S F ^a   Silva, J F ^a   Alvarez Leite, J I ^a   Lemos, V S ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

atherosclerosis; endothelial dysfunction; H 2O 2; nNOS

Indexed keywords

ANTISENSE OLIGODEOXYNUCLEOTIDE; APOLIPOPROTEIN E; ARGININE; CATALASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HYDROGEN PEROXIDE; ISOPROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; SERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; ENZYME INHIBITION; ENZYME SYNTHESIS; GENE SEQUENCE; IN VIVO STUDY; MALE; MOUSE; MUSCLE ISOMETRIC CONTRACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; VASODILATATION; WILD TYPE;

ACETYLCHOLINE; ANIMALS; AORTA, THORACIC; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CATALASE; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HYDROGEN PEROXIDE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE III; VASODILATION;

EID: 80054997757     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2011.01500.x     Document Type: Article

References (58)

1. Alderton WK, Cooper CE, Knowles RG, (2001). Nitric oxide synthases: structure, function and inhibition. Biochem J 357: 593-615. (Pubitemid 32735142)
2. Atochin DN, Demchenko IT, Astern J, Boso AE, Piantadosi CA, Huang PL, (2003). Contributions of endothelial and neuronal nitric oxide synthases to cerebrovascular responses to hyperoxia. J Cereb Blood Flow Metab 23: 1219-1226. (Pubitemid 37229525)
3. Bachetti T, Comini L, Curello S, Bastianon D, Palmieri M, Bresciani G, et al,. (2004). Co-expression and modulation of neuronal and endothelial nitric oxide synthase in human endothelial cells. J Mol Cell Cardiol 37: 939-945. (Pubitemid 39446819)
4. Boulanger CM, Heymes C, Benessiano J, Geske RS, Levy BI, Vanhoutte PM, (1998). Neuronal nitric oxide synthase is expressed in rat vascular smooth muscle cells: activation by angiotensin II in hypertension. Circ Res 83: 1271-1278. (Pubitemid 29006042)
5. Bouloumie A, Bauersachs J, Linz W, Scholkens BA, Wiemer G, Fleming I, et al,. (1997). Endothelial dysfunction coincides with an enhanced nitric oxide synthase expression and superoxide anion production. Hypertension 30: 934-941. (Pubitemid 27441125)
6. Busse R, Fleming I, (1996). Endothelial dysfunction in atherosclerosis. J Vasc Res 33: 181-194. (Pubitemid 26164469)
7. Cai H, Harrison DG, (2000). Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87: 840-844.
8. Capettini LS, Cortes SF, Gomes MA, Silva GA, Pesquero JL, Lopes MJ, et al,. (2008). Neuronal nitric oxide synthase-derived hydrogen peroxide is a major endothelium-dependent relaxing factor. Am J Physiol Heart Circ Physiol 295: H2503-H2511.
9. Capettini LS, Cortes SF, Lemos VS, (2010). Relative contribution of eNOS and nNOS to endothelium-dependent vasodilation in the mouse aorta. Eur J Pharmacol 643: 260-266.
10. Chlopicki S, Kozlovski VI, Lorkowska B, Drelicharz L, Gebska A, (2005). Compensation of endothelium-dependent responses in coronary circulation of eNOS-deficient mice. J Cardiovasc Pharmacol 46: 115-123. (Pubitemid 40917787)
11. Deckert V, Lizard G, Duverger N, Athias A, Palleau V, Emmanuel F, et al,. (1999). Impairment of endothelium-dependent arterial relaxation by high-fat feeding in ApoE-deficient mice: toward normalization by human ApoA-I expression. Circulation 100: 1230-1235. (Pubitemid 29426600)
12. Erdely A, Kepka-Lenhart D, Salmen-Muniz R, Chapman R, Hulderman T, Kashon M, et al,. (2010). Arginase activities and global arginine bioavailability in wild-type and ApoE-deficient mice: responses to high fat and high cholesterol diets. PLoS ONE 5: e15253.
13. Fernández-Hernando C, Ackah E, Yu J, Suárez Y, Murata T, Iwakiri Y, et al,. (2007). Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab 6: 446-457. (Pubitemid 350163050)
14. Fleming I, (2003). Brain in the brawn: the neuronal nitric oxide synthase as a regulator of myogenic tone. Circ Res 93: 586-588. (Pubitemid 37222152)
15. Fransen P, Van Assche T, Guns PJ, Van Hove CE, De Keuleaner GW, Herman AG, et al,. (2008). Endothelial function in aorta segments of apolipoprotein E-deficient mice before development of atherosclerotic lesions. Pflugers Arch 455: 811-815.
16. Freedman JE, Sauter R, Battinelli EM, Ault K, Knowles C, Huang PL, et al,. (1999). Deficient platelet-derived nitric oxide and enhanced hemostasis in mice lacking the NOSIII gene. Circ Res 84: 1416-1421. (Pubitemid 29293220)
17. Fu C, He J, Li C, Shyy JYJ, Zhu Y, (2010). Cholesterol increases adhesion of monocytes to endothelium by moving adhesion molecules out of caveolae. Biochim Biophys Acta 1801: 702-710.
18. Garland CJ, Plane F, Kemp BK, Cocks TM, (1995). Endothelium-dependent hyperpolarization: a role in the control of vascular tone. Trends Pharmacol Sci 16: 23-30.
19. Hagioka S, Takeda Y, Zhang S, Sato T, Morita K, (2005). Effects of 7-nitroindazole and N-nitro-L-arginine methyl ester on changes in cerebral blood flow and nitric oxide production preceding development of hyperbaric oxygen-induced seizures in rats. Neurosci Lett 382: 206-210. (Pubitemid 40733623)
20. Higashi Y, Maysuoka H, Umei H, Sugano R, Fujii Y, Soga J, et al,. (2009a). Endothelial function in subjects with isolated low HDL cholesterol: role of nitric oxide and circulating progenitor cells. Am J Physiol Endocrinol Metab 298: e202-e209.
21. Higashi Y, Noma K, Yoshizumi M, Kihara Y, (2009b). Endothelial function and oxidative stress in cardiovascular diseases. Circ J 73: 411-418.
22. Huang A, Sun D, Shesely EG, Levee EM, Koller A, Kaley G, (2002). Neuronal NOS-dependent dilation to flow in coronary arteries of male eNOS-KO mice. Am J Physiol Heart Circ Physiol 282: H429-H436. (Pubitemid 34654965)
23. Huang H, Martasek P, Roman LJ, Masters BSS, Silverman RB, (1999). Nω-Nitroarginine-containing dipeptide amides. Potent and highly selective inhibitors of neuronal nitric oxide synthase. J Med Chem 42: 3147-3153. (Pubitemid 29384050)
24. Iida Y, Katusic ZS, (2000). Mechanisms of cerebral arterial relaxations to hydrogen peroxide. Stroke 31: 2224-2230.
25. Katusic ZS, d'Uscio LV, (2004). Tetrahydrobiopterin: mediator of endothelial protection. Arterioscler Thromb Vasc Biol 24: F552-F558.
26. Kitaura H, Uozumi N, Tohmi M, Yamazaki M, Sakimura K, Kudoh M, et al,. (2007). Roles of nitric oxide as a vasodilator in neurovascular coupling of mouse somatosensory cortex. Neurosci Res 59: 160-171. (Pubitemid 47429772)
27. Kubes P, Suzuki M, Granger DN, (1991). Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc Natl Acad Sci U S A 88: 4651-4655. (Pubitemid 21914599)
28. Kuhlencordt PJ, Rosel E, Gerszten RE, Morales-Ruiz M, Dombkowski D, Atkinson WJ, et al,. (2004). Role of endothelial nitric oxide synthase in endothelial activation: insights from eNOS knockout endothelial cells. Am J Physiol Cell Physiol 286: C1195-C1202. (Pubitemid 38506935)
29. Kuhlencordt PJ, Hotten S, Schodel J, Rutzel S, Hu K, Widder J, et al,. (2006). Atheroprotective effects of neuronal nitric oxide synthase in apolipoprotein-e knockout mice. Arterioscler Thromb Vasc Biol 26: 1539-1544. (Pubitemid 44288980)
30. Kurihara N, Alfie ME, Sigmon DH, Rhaleb NE, Shesely EG, Carretero OA, (1998). Role of nNOS in blood pressure regulation in eNOS null mutant mice. Hypertension 32: 856-861. (Pubitemid 28530219)
31. Laursen JB, Somers M, Kurz S, McCann L, Warnholtz A, Freeman BA, et al,. (2001). Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation 103: 1282-1288. (Pubitemid 32221353)
32. Leopold JA, Loscalzo J, (2009). Oxidative risk for atherothrombotic cardiovascular disease. Free Radic Biol Med 47: 1673-1706.
33. Loesch A, Burnstock G, (1998). Perivascular nerve fibres and endothelial cells of the rat basilar artery: immuno-gold labelling of antigenic sites for type I and type III nitric oxide synthase. J Neurocytol 27: 197-204. (Pubitemid 28253070)
34. Luscher TF, Barton M, (1997). Biology of the endothelium. Clin Cardiol 20: II3-II10. (Pubitemid 28009557)
35. Matoba T, Shimokawa H, Nakashima M, Hirakawa Y, Mukai Y, Hirano K, et al,. (2000). Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in mice. J Clin Invest 106: 1521-1530. (Pubitemid 32040953)
36. Matoba T, Shimokawa H, Kubota H, Morikawa K, Fujiki T, Kunihiro I, et al,. (2002). Hydrogen peroxide is an endothelium-derived hyperpolarizing factor in human mesenteric arteries. Biochem Biophys Res Commun 290: 909-913. (Pubitemid 34687447)
37. Miura H, Bosnjak JJ, Ning G, Saito T, Miura M, Gutterman DD, (2003). Role for hydrogen peroxide in flow-induced dilation of human coronary arterioles. Circ Res 92: e31-e40.
38. Morishita T, Tsutsui M, Shimokawa H, Horiuchi M, Tanimoto A, Suda O, et al,. (2002). Vasculoprotective roles of neuronal nitric oxide synthase. FASEB J 16: 1994-1996.
39. Nangle MR, Cotter MA, Cameron NE, (2003). Effects of rosuvastatin on nitric oxide-dependent function in aorta and corpus cavernosum of diabetic mice: relationship to cholesterol biosynthesis pathway inhibition and lipid lowering. Diabetes 52: 2396-2402. (Pubitemid 37059512)
40. Nangle MR, Cotter MA, Cameron NE, (2004). An in vitro investigation of aorta and corpus cavernosum from eNOS and nNOS gene-deficient mice. Eur J Physiol 448: 139-145. (Pubitemid 38648173)
41. 2. Br J Pharmacol 138: 1215-1220. (Pubitemid 36543118)
42. Rosenblum WI, Murata S, (1996). Antisense evidence for two functionally active forms of nitric oxide synthase in brain microvascular endothelium. Biochem Biophys Res Commun 224: 535-543. (Pubitemid 26268221)
43. Ross R, (1999). Atherosclerosis is an inflammatory disease. Am Heart J 138: S419-S420. (Pubitemid 29523224)
44. Schodel J, Padmapriya P, Marx A, Huang PL, Ertl G, Kuhlencordt PJ, (2009). Expression of neuronal nitric oxide synthase splice variants in atherosclerotic plaques of apoE knockout mice. Atherosclerosis 206: 383-389.
45. Shimokawa H, (1999). Primary endothelial dysfunction: atherosclerosis. J Mol Cell Cardiol 31: 23-37. (Pubitemid 29078216)
46. Sima AV, Stancu CS, Simionescu M, (2009). Vascular endothelium in atherosclerosis. Cell Tissue Res 335: 191-203.
47. Sobey CG, Heistad DD, Faraci FM, (1997). Mechanisms of bradykinin-induced cerebral vasodilatation in rats. Evidence that reactive oxygen species activate K+ channels. Stroke 28: 2290-2295. (Pubitemid 27497936)
48. Talukder MA, Fujiki T, Morikawa K, Motoishi M, Kubota H, Morishita T, et al,. (2004). Up-regulated neuronal nitric oxide synthase compensates coronary flow response to bradykinin in endothelial nitric oxide synthase-deficient mice. J Cardiovasc Pharmacol 44: 437-445. (Pubitemid 39305084)
49. Toda N, Okamura T, (2003). The pharmacology of nitric oxide in the peripheral nervous system of blood vessels. Pharmacol Rev 55: 271-324. (Pubitemid 36666049)
50. Toma L, Stancu CS, Botez GM, Sima AV, Simionescu M, (2009). Irreversibly glycated LDL induce oxidative and inflammatory state in human endothelial cells; added effect of high glucose. Biochem Biophys Res Commun 390: 877-882.
51. Tsutsui M, (2004). Neuronal nitric oxide synthase as a novel anti-atherogenic factor. J Atheroscler Thromb 11: 41-48.
52. Urakami-Harasawa L, Shimokawa H, Nakashima M, Egashira K, Takeshita A, (1997). Importance of endothelium-derived hyperpolarizing factor in human arteries. J Clin Invest 100: 2793-2799. (Pubitemid 28007548)
53. Vanhoutte PM, (1986). The endothelium and arterial reactivity. J Mal Vasc 11: 213-221.
54. Wang F, Okamoto Y, Inoki I, Yoshioka K, Du W, Qi X, et al,. (2010). Sphingosine-1-phosphate receptor-2 deficiency leads to inhibition of macrophage proinflammatory activities and atherosclerosis in apoE-deficient mice. J Clin Invest 120: 3979-3995.
55. Wei G, Dawson VL, Zweier JL, (1999). Role of neuronal and endothelial nitric oxide synthase in nitric oxide generation in the brain following cerebral ischemia. Biochim Biophys Acta 1455: 23-34. (Pubitemid 29397486)
56. Wilcox JN, Subramanian RR, Sundell CL, Tracey WR, Pollock JS, Harrison DG, et al,. (1997). Expression of multiple isoforms of nitric oxide synthase in normal and atherosclerotic vessels. Arterioscler Thromb Vasc Biol 17: 2479-2488. (Pubitemid 28015984)
57. Yada T, Shimokawa H, Hiramatsu O, Kajita T, Shigeto F, Goto M, et al,. (2003). Hydrogen peroxide, an endogenous endothelium-derived hyperpolarizing factor, plays an important role in coronary autoregulation in vivo. Circulation 107: 1040-1045. (Pubitemid 36258729)
58. Yamashiro K, Milsom AB, Duchene J, Panayiotou C, Urabe T, Hattori N, et al,. (2010). Alterations in nitric oxide and endothelin-1 bioactivity underlie cerebrovascular dysfunction in ApoE-deficient mice. J Cereb Blood Flow Metab 30: 1494-1503.