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Angiotensin II, Oxidative Stress, and Nitric Oxide

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Endocrinology of Cardiovascular Function

Part of the book series: Endocrine Updates ((ENDO,volume 1))

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Abstract

Angiotensin II and nitric oxide are two potent vasoactive agents that are critical to the regulation of vascular tone. The renin-angiotensin system, with angiotensin II as its final effector, has been implicated in blood pressure and volume regulation, sodium homeostasis, and control of heart rate and contractility. Nitric oxide, originally identified as endothelium-derived relaxing factor, is among the most potent and universal vasorelaxants. Recently, it has become clear that these two apparently disparate systems are intimately intertwined in their effects on the vasculature. This interaction is based on the effects of oxidant stress on angiotensin II signaling and on the integrity of nitric oxide. This review will discuss the role of oxidant stress in the physiology of these two important pathways, and its abnormal regulation in hypertension.

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References

  1. Lu D, Maulik N, Moraru II, Kreutzer DL, and Das DK. Molecular adaptation of vascular endothelial cells to oxidative stress. Am J Physiol 1993; 264: C715–C722.

    PubMed  CAS  Google Scholar 

  2. Pagano PJ, Tornheim K, and Cohen RA. Superoxide anion production by rabbit thoracic aorta: effect of endothelium-derived nitric oxide. Am J Physiol 1993; 265: H707–H712.

    PubMed  CAS  Google Scholar 

  3. Panus PC, Radi R, Chumley PH, Lillard RH, and Freeman BA. Detection of H2O2 release from vascular endothelial cells. Free Rad Biol & Med 1993; 14: 217–233.

    Article  CAS  Google Scholar 

  4. Rajagopalan S, Kurz S, Munzel T, Tarpey M, Freeman BA, Griendling KK, and Harrison DG. Angiotensin II mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation: contribution to alterations of vasomotor tone. J Clin Invest 1996; 97: 1916–1923.

    Article  PubMed  CAS  Google Scholar 

  5. Friedl HP, Till GO, Ryan US, and Ward PA. Mediator-induced activation of xanthine oxidase in endothelial cells. FASEB J 1989; 3: 2512–2518.

    PubMed  CAS  Google Scholar 

  6. Mohazzab-H. KM, and Wolin MS. Sites of superoxide anion production detected by lucigenin in calf pulmonary artery smooth muscle. Am J Physiol 1994; 267: L815–L822.

    PubMed  CAS  Google Scholar 

  7. Mohazzab-H. KM, Kaminski PM, and Wolin MS. NADH oxidoreductase is a major source of superoxide anion in bovine coronary artery endothelium. Am J Physiol 1994; 266: H2568–H2572.

    PubMed  CAS  Google Scholar 

  8. Griendling KK, Minieri CA, Ollerenshaw JD, and Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 1994; 74: 1141–1148.

    Article  PubMed  CAS  Google Scholar 

  9. Jones SA, O’Donnell VB, Wood JD, Broughton JP, Hughes EJ, and Jones OTG. Expression of phagocyte NADPH oxidase components in human endothelial cells. Am J Physiol 1996; 271: H1626–H1634.

    PubMed  CAS  Google Scholar 

  10. .Fukui T, Lassegue B, Kai H, Alexander RW, and Griendling KK. cDNA cloning and mRNA expression of cytochrome b558 α-subunit in rat vascular smooth muscle cells. Biochim Biophys Acta 1995; 1231: 215–219.

    Article  PubMed  Google Scholar 

  11. Ushio-Fukai M, Zafari AM, Fukui T, Ishizaka N, and Griendling KK. p22phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J Biol Chem 1996; 271: 23317–23321.

    Article  PubMed  CAS  Google Scholar 

  12. Sulciner DJ, Irani K, Yu Z, Ferrans VJ, Goldschmidt-Clermont P, and Finkel T. Rad regulates a cytokine-stimulated, redox-dependent pathway necessary for NF-κB activation and VCAM-1 expression. Circulation 1996; 94: 1–708.

    Article  Google Scholar 

  13. Watson F, Robinson J, and Edwards SW. Protein kinase C-dependent and-independent activation of the NADPH oxidase of human neutrophils. J Biol Chem 1991; 266: 7432–7439.

    PubMed  CAS  Google Scholar 

  14. Mohazzab-H. KM, Kaminski PM, Fayngersh RP, and Wolin MS. Oxygen-elicted responses in calf coronary arteries: role of H2O2 production via NADH-derived superoxide. Am J Physiol 1996; 270: H1044–H1053.

    Google Scholar 

  15. Beckman JS, Beckman TW, Chen J, Marshall PA, and Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 1990; 87: 1620–1624.

    Article  PubMed  CAS  Google Scholar 

  16. Suzuki YJ, Forman HJ, and Sevanian A. Oxidants as stimulators of signal transduction. Free Radic Biol Med 1997; 22: 269–285.

    Article  PubMed  CAS  Google Scholar 

  17. Burdon RH. Superoxide and hydrogen peroxide in relation to mammalian cell proliferation. Free Radic Biol & Med 1995; 18: 775–794.

    Article  CAS  Google Scholar 

  18. Rao GN, Runge MS, and Alexander RW. Hydrogen peroxide activation of cytosolic phospholipase A2 in vascular smooth muscle cells. Biochim Biophys Acta 1995; 1265: 67–72.

    Article  PubMed  Google Scholar 

  19. Natarajan V, Taher MM, Roehm B, Parinandi NL, Schmid HHO, Kiss Z, and Garcia JGN. Activation of endothelial cell phospholipase D by hydrogen peroxide and fatty acid hydroperoxide. J Biol Chem 1993; 268: 930–937.

    PubMed  CAS  Google Scholar 

  20. Chen CC, Liau CS, and Lee YT. Tumor necrosis factor-alpha, platelet-activating factor, and hydrogen peroxide activate protein kinase C subtypes alpha and epsilon in human saphenous vein endothelial cells. J Cardiovasc Pharmacol 1996; 28: 240–244.

    Article  PubMed  CAS  Google Scholar 

  21. Baas AS, and Berk BC. Differential activation of mitogen-activated protein kinases by H2O2 and O2–in vascular smooth muscle cells. Circ Res 1995; 77: 29–36.

    Article  PubMed  CAS  Google Scholar 

  22. Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T, and Goldschmidt-Clermont PJ. Mitogenic signaling mediated by oxidants in ras-transformed fibroblasts. Science 1997; 275: 1649–52.

    Article  PubMed  CAS  Google Scholar 

  23. Rao GN, Lassegue B, Griendling KK, and Alexander RW. Hydrogen peroxide stimulates transcription of c-jun in vascular smooth muscle cells: role of arachidonic acid. Oncogene 1993; 8: 2759–2764.

    PubMed  CAS  Google Scholar 

  24. Rao GN, Lassegue B, Griendling KK, Alexander RW, and Berk BC. Hydrogen peroxide-induced c-fos expression is mediated by arachidonic acid release: Role of protein kinase C. Nucleic Acids Res 1993; 21: 1259–1263.

    Article  PubMed  CAS  Google Scholar 

  25. Rao GN, and Berk BC. Active oxygen species stimulate vascular smooth muscle cell growth and proto-oncogene expression. Circ Res 1992; 70: 593–599.

    Article  PubMed  CAS  Google Scholar 

  26. Puri PL, Avantaggiati ML, Burgio VL, Chirillo P, Collepardo D, Natoli G, Balsano C, and Levrero M. Reactive oxygen intermediates mediate angiotensin II-induced c-jun, c-fos heterodimer DNA binding activity and proliferative hypertrophic responses in myogenic cells. J Biol Chem 1995; 270: 22129–22134.

    Article  PubMed  CAS  Google Scholar 

  27. Rao GN, Alexander RW, and Runge MS. Linoleic acid and its metabolites, hydroperoxyoctadecadienoic acids, stimulate c-fos, c-jun, and c-myc mRNA expression, mitogen-activated protein kinase activation, and growth in rat aortic smooth muscle cells. J Clin Invest 1995; 96: 842–847.

    Article  PubMed  CAS  Google Scholar 

  28. Marui N, Offerman M, Swerlick R, Kunsch C, Roxen CA, Ahmad M, Alexander RW, and Medford RM. Vascular cell-adhesion molecule-1 (VCAM-1) gene-transcription and expression are regulated through an antioxidant sensitive mechanism in human vascular endothelial cells. J Clin Invest 1993; 92: 1866–1874.

    Article  PubMed  CAS  Google Scholar 

  29. Cushing SD, Berliner JA, Valente AJ, Territo MC, Navab M, Parhami F, Gerrity R, Schwartz CJ, and Fogelman AM. Minimally modified low density lipoprotein induces monocyte chemotactic protein 1 in human endothelial cells and smooth muscle cells. Proc Natl Acad Sci USA 1990; 87: 5134–5138.

    Article  PubMed  CAS  Google Scholar 

  30. Nath KA, Balla G, Vercellotti GM, Balla J, Hacob HS, Levitt MD, and Rosenberg MEJ. Induction of heme oxygenase is a rapid, protective response in rhabdomyolysis in the rat. J Clin Invest 1992; 90: 267–270.

    Article  PubMed  CAS  Google Scholar 

  31. Zeiher AM, Fisslthaler B, Schray-Utz B, and Busse R. Nitric oxide modulates the expression of monocyte chemoattractant protein 1 in cultured human endothelial cells. Circ Res 1995; 76: 980–986.

    Article  PubMed  CAS  Google Scholar 

  32. Khan BV, Harrison DG, Olbrych MT, Alexander RW, and Medford RM. Nitric oxide regulates VCAM-1 gene expression and redoxsensitive transcriptional events in human vascular endothelial cells. Proc Natl Acad Sci, USA 1996; 93: 9114–9119.

    Article  PubMed  CAS  Google Scholar 

  33. Peng HB, Libby P, and Liao JK. Induction and stabilization of I kappa B alpha by nitric oxide mediates inhibition of NF-kappa B. J Biol Chem 1995; 270: 14214–14219.

    Article  PubMed  CAS  Google Scholar 

  34. Rubanyi GM, and Vanhoutte PM. Oxygen-derived free radicals, endothelium, and the responsiveness of vascular smooth muscle. Am J Physiol 1986; 250: H815–H821.

    PubMed  CAS  Google Scholar 

  35. Gryglewski RJ, Palmer RMJ, and Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived relaxing factor. Nature 1986; 320: 454–456.

    Article  PubMed  CAS  Google Scholar 

  36. Mugge A, Elwell JH, Peterson TE, and Harrison DG. Release of Intact endothelium-derived relaxing factor depends on endothelial superoxide dismutase activity. Am J Physiol 1991; 260: C219–C225.

    PubMed  CAS  Google Scholar 

  37. Afanas’ev IB. Superoxide ion: chemistry and biological implications. Boca Raton, FL: CRC Press, 1989.

    Google Scholar 

  38. Ohara Y, Peterson TE, and Harrison DG. Hypercholesterolemia increases endothelial superoxide anion production. J Clin Invest 1993; 91: 2546–2551.

    Article  PubMed  CAS  Google Scholar 

  39. Ting HH, Timimi FK, Boles K, Creager S, and Ganz P, Creager, MA. Vitamin C acutely improves endothelium-dependent vasodilation in patients with non-insulin-dependent diabetes mellitus. Circ 1995; 92 (suppl 1): 1747 (abstract).

    Google Scholar 

  40. Mugge A, Elwell JH, Peterson TE, Hofmeyer TG, Heistad DD, and Harrison DG. Chronic treatment with polyethylene-glycolated superoxide dismutase partially restores endothelium-dependent vascular relaxations in cholesterol-fed rabbits. Circ Res 1991; 69: 1293–1300.

    Article  PubMed  CAS  Google Scholar 

  41. Buga GM, Gold ME, Fukuto JM, and Ignarro LJ. Shear stress-induced release of nitric oxide from endothelial cells grown on beads. Hypertension 1991; 17: 187–193.

    Article  PubMed  CAS  Google Scholar 

  42. Inoue N, Ramaswamy S, Fukai R, Nerem RM, and Harrison DG. Shear stress modulates expression of Cu/Zn superoxide dismutase in human aortic endothelial cells. Circ Res 1996; 79: 32–37.

    Article  PubMed  CAS  Google Scholar 

  43. Howard AB, Alexander RW, Nerem RM, Griendling KK, and Taylor WR. Cyclic strain induces an oxidative stress in endothelial cells. Am J Physiol 1997; 272: C421–C427.

    PubMed  CAS  Google Scholar 

  44. Chappell DC, Varner SE, Nerem RM, Medford RM, and Alexander RW. Oscillatory shear stimulates adhesion molecule expression in cultured human endothelium. Circ Res In press.

    Google Scholar 

  45. DeKeulenaer GW, Chappell DC, Ishizaka N, Nerem RM, Alexander RW, and Griendling KK. Oscillatory and steady laminar shear stress differentially affect endothelial redox-state. Circ 1997; 96: 1–44.

    Google Scholar 

  46. Ku D, Giddens D, Zarins C, and Glagov S. Pulsatile flow and atherosclerosis in the human carotid bifurcation: positive correlation between plaque location and low and oscillating shear stress. Arteriosclerosis 1985; 5: 293–302.

    Article  PubMed  CAS  Google Scholar 

  47. Wolin MS, Omar HA, Mortelliti MP, and Cherry PD. Association of pulmonary artery photorelaxation with H2O2 metabolism by catalase. Am J Physiol 1991; 261: H1141–H1147.

    PubMed  CAS  Google Scholar 

  48. Boscoboinik D, Szewczyk A, Hensey C, and Azzi A. Inhibition of cell proliferation by α-tocopherol. Role of protein kinase C. J Biol Chem 1991; 266: 6188–6194.

    PubMed  CAS  Google Scholar 

  49. Tsai J-C, Jain M, Hsieh C-M, Lee W-S, Yoshizumi M, Patterson C, Perrella MA, Cooke C, Wang H, Haber E, Schlegel R, and Lee M-E. Induction of apoptosis by pyrrolidinedithiocarbamate and N-acetylcysteine in vascular smooth muscle cells. J Biol Chem 1996; 271: 3667–3670.

    Article  PubMed  CAS  Google Scholar 

  50. Sundaresan M, Zu-Xi Y, Ferrans VJ, Irani K, and Finkel T. Requirement for generation of H2O2 for platelet-derived growth factor signal transduction. Science 1995; 270: 296–299.

    Article  PubMed  CAS  Google Scholar 

  51. Garg UC, and Hassid A. Nitric oxide generating vasodilators and 8-bromo cyclic GMP inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 1989; 83: 1774–1777.

    Article  PubMed  CAS  Google Scholar 

  52. Dubey RK, Jackson EK, and Luscher TF. Nitric oxide inhibits angiotensin II-induced migration of rat aortic smooth muscle cells. Role of cyclic nucleotides and angiotensin-1 receptors. J Clin Invest 1995; 96: 141–149.

    Article  PubMed  CAS  Google Scholar 

  53. Pollman MJ, Yamada T, Horiuchi M, and Gibbons GH. Vasoactive substances regulate vascular smooth muscle cell apoptosis. Countervailing influences of nitric oxide and angiotensin II. Circ Res 1996; 79: 748–756.

    Article  PubMed  CAS  Google Scholar 

  54. Fiorani M, Cantoni O, Tasinato A, Boscoboinik D, and Azzi A. Hydrogen peroxide-and fetal bovine serum-induced DNA synthesis in vascular smooth muscle cells: positive and negative regulation by protein kinase C isoforms. Biochim Biophys Acta 1995; 1269: 98–104.

    Article  PubMed  Google Scholar 

  55. Li PF, Dietz R, and von Harsdorf R. Reactive oxygen species induce apopotosis of vascular smooth muscle. FEBS Lett 1997; 404: 249–252.

    Article  PubMed  CAS  Google Scholar 

  56. Nakazono K, Watanabe N, Matsuno K, Sasaki J, Sato T, and Inoue M. Does superoxide underlie the pathogenesis of hypertension? Proc Natl Acad Sci USA 1991; 88: 10045–10108.

    Article  PubMed  CAS  Google Scholar 

  57. Fukui T, Ishizaka N, Rajagopalan S, Laursen JB, Capers Q, IV, Taylor WR, Harrison DG, de Leon H, Wilcox JN, and Griendling KK. p22phox mRNA expression and NADPH oxidase activity are increased in aortas from hypertensive rats. Circ Res 1997; 80: 45–51.

    Article  PubMed  CAS  Google Scholar 

  58. Bech-Laursen J, Rajagopalan S, Galis Z, Tarpey M, Freeman BA, and Harrison DG. Role of superoxide in angiotensin II-induced but not catecholamine-induced hypertension. Circulation 1997; 95: 588–593.

    Article  Google Scholar 

  59. Kwan CY, and Beazley JS. Mechanism of inhibition by alloxan of ATP-driven calcium transport by vascular smooth muscle microsomes. J Bioenerg Biomembr 1988; 20: 517–531.

    Article  PubMed  CAS  Google Scholar 

  60. Reilly M, Delanty N, Lawson JA, and Fitzgerald GA. Modulation of oxidant stress in vivo in chronic cigarette smokers. Circ 1996; 94: 19–25.

    Article  CAS  Google Scholar 

  61. Bachi A, Zuccato E, Baraldi M, Fanelli R, and Chiabrando C. Measurement of urinary 8-epi-prostaglandin F2alpha, a novel index of lipid peroxidation in vivo, by immunoaffinity/gas chromatography-mass spectrometry. Basal levels in smokers and nonsmokers. Free Radic Biol Med 1996; 20: 619–624.

    Article  PubMed  CAS  Google Scholar 

  62. Chua BH, Chua CC, Diglio CA, and Siu BB. Regulation of endothelin-1 mRNA by angiotensin II in rat heart endothelial cells. Biochim Biophys Acta 1993; 1178: 201–206.

    Article  PubMed  CAS  Google Scholar 

  63. Imai T, Hirata Y, Emori T, Yanagisawa M, Masaki T, and Marumo F. Induction of endothelin-1 gene by angiotensin and vasopressin in endothelial cells. Hypertension 1992; 19: 753–757.

    Article  PubMed  CAS  Google Scholar 

  64. Rajagopalan S, Bech-Laursen J, Borthayre A, Kurz S, Keiser J, Haleen S, Giaid A, and Harrison D. A role for endothelin-1 in angiotensin II mediated hypertension. Hypertension 1997; 29–34.

    Google Scholar 

  65. d’Uscio LV, Moreau P, Shaw S, Takase H, Barton M, and Luscher TF. Effects of chronic ETA-receptor blockade in angiotensin II-induced hypertension. Hypertensioni 1997; 29: 435–441.

    Article  CAS  Google Scholar 

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Authors
  1. Kathy K. Griendling
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  2. David G. Harrison
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Editors and Affiliations

  1. DVA Medical Center and University of California, Irvine, USA

    Ellis R. Levin M.D.

  2. City of Hope Medical Center, Duarte, California, USA

    Jerry L. Nadler M.D.

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Griendling, K.K., Harrison, D.G. (1998). Angiotensin II, Oxidative Stress, and Nitric Oxide. In: Levin, E.R., Nadler, J.L. (eds) Endocrinology of Cardiovascular Function. Endocrine Updates, vol 1. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-5569-8_5

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  • DOI: https://doi.org/10.1007/978-1-4615-5569-8_5

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