Reactive oxygen species cause endothelial dysfunction in chronic flow overload

Journal of Applied Physiology

Volumn 110, Issue 2, 2011, Pages 520-527

  Lu, X ^a   Guo, X ^a   Wassall, C D ^b   Kemple, M D ^b   Unthank, J L ^b   Kassab, G S ^a,b  

^a Indiana University Purdue University Indianapolis   (United States)

^b INDIANA UNIVERSITY   (United States)

Author keywords

Chronic flow overload; Endothelial dysfunction; NADPH oxidase; Reactive oxygen species

Indexed keywords

REACTIVE OXYGEN METABOLITE;

ANIMAL; ARTICLE; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY DISEASE; CORONARY BLOOD VESSEL; HEART LEFT VENTRICLE FUNCTION; MALE; METABOLISM; PATHOPHYSIOLOGY; SWINE; VASCULAR ENDOTHELIUM;

ANIMALS; CORONARY ARTERY DISEASE; CORONARY CIRCULATION; CORONARY VESSELS; ENDOTHELIUM, VASCULAR; MALE; REACTIVE OXYGEN SPECIES; SWINE; VENTRICULAR DYSFUNCTION, LEFT;

EID: 79851476020     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00786.2009     Document Type: Article

References (53)

1. Bailey DM, Davies B, Young IS, Jackson MJ, Davison GW, Isaacson R, Richardson RS. EPR spectroscopic detection of free radical outflow from an isolated muscle bed in exercising humans. J Appl Physiol 94:1714-1718, 2003. (Pubitemid 36457416)
2. Bedard K, Krause KH. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 87:245-313, 2007. (Pubitemid 46209993)
3. Brandes RP, Schmitz-Winnenthal FH, Feletou M, Godecke A, Huang Vanhoutte PM PL, Fleming I, Busse R. An endothelium-derived hyperpolarizing factor distinct from NO and prostacyclin is a major endothelium-dependent vasodilator in resistance vessels of wild-type and endothelial NO synthase knockout mice. Proc Natl Acad Sci USA 97:9747-9752, 2000. (Pubitemid 30650847)
4. Bouvet C, Belin de Chanteméle E, Guihot AL, Vessiéres E, Bocquet A, Dumont O, Jardel A, Loufrani L, Moreau P, Henrion D. Flow-induced remodeling in resistance arteries from obese Zucker rats is associated with endothelial dysfunction. Hypertension 50:248-254, 2007. (Pubitemid 46986048)
5. Cai H, Harrison DG. Endothelial dysfunction in cardiovascular diseases: the role of oxidant stress. Circ Res 87:840-844, 2000.
6. Castier Y, Brandes RP, Leseche G, Tedgui A, Lehoux S. p47phox-Dependent NADPH oxidase regulates flow-induced vascular remodeling. Circ Res 97:533-540, 2005. (Pubitemid 41361743)
7. De Keulenaer GW, Chappell DC, Ishizaka N, Nerem RM, Alexander RW, Griendling KK. Oscillatory and steady laminar shear stress differentially affect human endothelial redox state. Circ Res 82:1094-1101, 1998. (Pubitemid 28249070)
8. Di Stefano I, Koopmans DR, Langille BL. Modulation of arterial growth of the rabbit carotid artery associated with experimental elevation of blood flow. J Vasc Res 35:1-7, 1998. (Pubitemid 28096343)
9. Garland CJ, Plane F, Kemp Cocks TM BK. Endothelium-dependent hyperpolarization: a role in the control of vascular tone. Trends Pharmacol Sci 16:23-30, 1995.
10. Geiszt M, Kopp JB, Varnai P, Leto TL. Identification of renox, an NAD (P) H oxidase in kidney. Proc Natl Acad Sci USA 97:8010-8014, 2000. (Pubitemid 30460764)
11. Guzik TJ, Mussa S, Gastaldi D, Sadowski J, Ratnatunga C, Pillai R, Channon KM. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD (P) H oxidase and endothelial nitric oxide synthase. Circulation 105:1656-1662, 2002. (Pubitemid 34298608)
12. Harrison D, Griendling KK, Landmesser U, Hornig B, Drexler H. Role of oxidative stress in atherosclerosis. Am J Cardiol 91:7A-11A, 2003. (Pubitemid 36351457)
13. Heumüller S, Wind S, Barbosa-Sicard E, Schmidt HH, Busse R, Schröder K, Brandes RP. Apocynin is not an inhibitor of vascular NADPH oxidases but an antioxidant. Hypertension 51:211-217, 2008. (Pubitemid 351159930)
14. Howard AB, Alexander RW, Nerem RM, Griendling KK, Taylor WR. Cyclic strain induces an oxidative stress in endothelial cells. Am J Physiol Cell Physiol 272: C421-C427, 1997.
15. Huang SY, Tawney KW, Bender PR, Groves BM, McCullough RG, McCullough RE, Micco AJ, Macno-Johnson A, Cymerman A, Greene Reeves JT ER. Internal carotid arterial flow velocity with exercise before and after acclimatization to 4, 300 m. JApplPhysiol 71:1469-1476, 1991.
16. Hull SS, Kaiser L, Jaffe MD, Sparks HV. Endothelium-dependent flow-induced dilation of canine femoral and saphenous arteries. Blood Vessels 23:183-198, 1986. (Pubitemid 17183597)
17. 2 from p47phox-dependent NAD (P) H oxidases, leading to monocyte adhesion. J Biol Chem 278:47291-47298, 2003. (Pubitemid 37452318)
18. Kamiya A, Togawa T. Adaptive regulation of wall shear stress to flow change in the canine carotid artery. Am J Physiol Heart Circ Physiol 239: H14-H21, 1980.
19. Kassab GS, Imoto K, White FC, Rider CA, Fung YC, Bloor CM. Coronary arterial tree remodeling in right ventricular hypertrophy. Am J Physiol Heart Circ Physiol 265: H366-H375, 1993. (Pubitemid 23224731)
20. Griendling KK, Sorescu D, Ushio-Fukai M. NAD (P) H oxidase: role in cardiovascular biology and disease. Circ Res 86:494-501, 2000. (Pubitemid 30165039)
21. Kozlov AV, Szalay L, Umar F, Fink B, Kropik K, Nhl H, Redl H, Bahrami S. EPR analysis reveals three tissues responding to endotoxin by increased formation of reactive oxygen and nitrogen species. Free Radic Biol Med 34:1555-1562, 2003. (Pubitemid 36638715)
22. Laurindo FR, Pedro Mde A, Barbeiro HV, Pileggi F, Carvalho MH, Augusto O, da Luz PL. Vascular free radical release. Ex vivo and in vivo evidence for a flow-dependent endothelial mechanism. Circ Res 74:700-709, 1994.
23. 2 generation play a key role in flow-mediated dilation in human coronary resistance arteries. Circ Res 93:573-580, 2003. (Pubitemid 37163238)
24. Lu X, Kassab GS. Vasoactivity of blood vessels using a novel isovolumic myograph. Ann Biomed Eng 35:356-366, 2007. (Pubitemid 46325723)
25. Manevich Y, Al-Mehdi A, Muzykantov V, Fisher AB. Oxidative burst and NO generation as initial response to ischemia in flow-adapted endothelial cells. Am J Physiol Heart Circ Physiol 280: H2126-H2135, 2001.
26. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 28:28, 2005.
27. Matsumoto T, Miyamori K, Kobayashi T, Kamata K. Apocynin normalizes hyperreactivity to phenylephrine in mesenteric arteries from cholesterol-fed mice by improving endothelium-derived hyperpolarizing factor response. Free Radic Biol Med 41:1289-1303, 2006. (Pubitemid 44466326)
28. McNally JS, Davis ME, Giddens DP, Saha A, Hwang J, Dikalov S, Jo H, Harrison DG. Role of xanthine oxidoreductase and NAD (P) H oxidase in endothelial superoxide production in response to oscillatory shear stress. Am J Physiol Heart Circ Physiol 285: H2290-H2297, 2003. (Pubitemid 37443044)
29. Miller VM, Burnett JCJ. Modulation of NO and endothelin by chronic increases in blood flow in canine femoral arteries. Am J Physiol Heart Circ Physiol 263: H103-H108, 1992.
30. Mueller CF, Laude K, McNally JS, Harrison DG. ATVB in focus: redox mechanisms in blood vessels. Arterioscler Thromb Vasc Biol 25:274-278, 2005. (Pubitemid 40189145)
31. Oeckler RA, Kaminski PM, Wolin MS. Stretch enhances contraction of bovine coronary arteries via an NAD (P) H oxidase-mediated activation of the extracellular signal-regulated kinase mitogen-activated protein kinase cascade. Circ Res 92:23-31, 2003. (Pubitemid 36105603)
32. Oelze M, Warnholtz A, Faulhaber J, Wenzel P, Kleschyov AL, Coldewey M, Hink U, Pongs O, Fleming I, Wassmann S, Meinertz T, Ehmke H, Daiber A, Munzel T. NADPH oxidase accounts for enhanced superoxide production and impaired endothelium-dependent smooth muscle relaxation in BKbeta1-/-mice. Arterioscler Thromb Vasc Biol 26:1753-1759, 2006. (Pubitemid 44305328)
33. Ohara Y, Peterson TE, Harrison DG. Hypercholesterolemia increases endothelial superoxide anion production. J Clin Invest 91:2546-2551, 1993. (Pubitemid 23182507)
34. Pagano PJ, Ito Y, Tornheim K, Gallop PM, Tauber AI, Cohen RA. An NADPH oxidase superoxide-generating system in the rabbit aorta. Am J Physiol Heart Circ Physiol 268: H2274-H2280, 1995.
35. Pourageaud F, De Mey JG. Vasomotor responses in chronically hyper-perfused and hypoperfused rat mesenteric arteries. Am J Physiol Heart Circ Physiol 274: H1301-H1307, 1998.
36. Schlüter T, Steinbach AC, Steffen A, Rettig R, Grisk O. Apocynin-induced vasodilation involves Rho kinase inhibition but not NADPH oxidase inhibition. Cardiovasc Res 80:271-279, 2008.
37. Scotland RS, Madhani M, Chauhan S, Moncada S, Andresen J, Nilsson H, Hobbs AJ, Ahluwalia A. Investigation of vascular responses in endothelial nitric oxide synthase/cyclooxygenase-1 double-knockout mice: key role for endothelium-derived hyperpolarizing factor in the regulation of blood pressure in vivo. Circulation 111:796-803, 2005. (Pubitemid 40259720)
38. Shiose A, Kuroda J, Tsuruya K, Hirai M, Hirakata H, Naito S, Hattori M, Sakaki Y, Sumimoto H. A novel superoxide-producing NAD (P) H oxidase in kidney. J Biol Chem 276:1417-1423, 2001. (Pubitemid 32096573)
39. Silacci P, Desgeorges A, Mazzolai L, Chambaz C, Hayoz D. Flow pulsatility is a critical determinant of oxidative stress in endothelial cells. Hypertension 38:1162-1166, 2001. (Pubitemid 34252823)
40. Smiesko V, Kozik J, Dolezel S. Role of endothelium in the control of arterial diameter by blood flow. Blood Vessels 22:247-251, 1985. (Pubitemid 16197674)
41. Sonta T, Inoguchi T, Tsubouchi H, Sekiguchi N, Kobayashi K, Matsumoto S, Utsumi H, Nawata H. Evidence for contribution of vascular NAD (P) H oxidase to increased oxidative stress in animal models of diabetes and obesity. Free Radic Biol Med 37:115-123, 2004. (Pubitemid 38746655)
42. Sun D, Huang A, Smith CJ, Stackpole CJ, Connetta JA, Shesely EG, Koller A, Kaley G. Enhanced release of prostaglandins contributes to flow-induced arteriolar dilation in eNOS knockout mice. Circ Res 85:288-293, 1999. (Pubitemid 29377301)
43. Taniyama Y, Griendling KK. Reactive oxygen species in the vasculature: molecular and cellular mechanisms. Hypertension 426:1075-1081, 2003. (Pubitemid 37549058)
44. Fukui T, Ishizaka N, Rajagopalan S, Laursen JB, Capers Q, Taylor WR, Harrison DG, de Leon H, Wilcox JN, Griendling KK. p22phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. Circ Res 80:45-51, 1997. (Pubitemid 27030367)
45. Touyz RM, Schiffrin EL. Reactive oxygen species in vascular biology: implications in hypertension. Histochem Cell Biol 122:339-352, 2004. (Pubitemid 39506592)
46. Touyz RM. Apocynin, NADPH oxidase, and vascular cells: a complex matter. Hypertension 51:172-174, 2008. (Pubitemid 351159922)
47. Tronc F, Mallat Z, Lehoux S, Wassef M, Esposito B, Tedgui A. Role of matrix metalloproteinases in blood flow-induced arterial enlargement. Arterioscler Thromb Vasc Biol 20: e120-e126, 2000.
48. Tuttle JL, Nachreiner RD, Bhuller AS, Condict KW, Connors BA, Herring BP, Dalsing MC, Unthank JL. Shear level influences resistance artery remodeling: wall dimensions, cell density, and eNOS expression. Am J Physiol Heart Circ Physiol 281: H1380-H1389, 2001.
49. Ungvari Z, Csiszar A, Huang A, Kaminski PM, Wolin MS, Koller A. High pressure induces superoxide production in isolated arteries via protein kinase C-dependent activation of NAD (P) H oxidase. Circulation 108:1253-1258, 2003. (Pubitemid 37099996)
50. Wang J, Wolin MS, Hintze TH. Chronic exercise enhances endothelium-mediated dilation of epicardial coronary artery in conscious dogs. Circ Res 73:829-838, 1993. (Pubitemid 23306128)
51. Zafari AM, Ushio-Fukai M, Akers M, Yin Q, Shah A, Harrison DG, Taylor WR, Griendling KK. Novel role of NADH/NADPH oxidase derived hydrogen peroxide in angiotensin II-induced hypertrophy of rat vascular smooth muscle cells. Hypertension 32:488-495, 1998.
52. Zarins CK, Zatina MA, Giddens DP, Ku DN, Glagov S. Shear stress regulation of artery lumen diameter in experimental atherogenosis. J Vasc Surg 5:413-420, 1987. (Pubitemid 17040159)
53. Zhu J, Mori T, Huang T, Lombard JH. Effect of high-salt diet on NO release and superoxide production in rat aorta. Am J Physiol Heart Circ Physiol 286: H575-H583, 2004. (Pubitemid 38140338)