Dual role of endothelial nitric oxide synthase in oxidized LDL-induced, p66Shc-mediated oxidative stress in cultured human endothelial cells

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Shi, Yi ^a,b,c   Lüscher, Thomas F ^a,b   Camici, Giovanni G ^a,b  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; IONOPHORE; LOW DENSITY LIPOPROTEIN; N(G) NITROARGININE METHYL ESTER; PROTEIN P66; PROTEIN P66 SHC; REACTIVE OXYGEN METABOLITE; SERINE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; BIOPTERIN; NITRIC OXIDE; NOS3 PROTEIN, HUMAN; OXIDIZED LOW DENSITY LIPOPROTEIN; PROTEIN KINASE B; PROTEIN SHC; SAPROPTERIN; SHC1 PROTEIN, HUMAN; SUPEROXIDE;

ANALYSIS OF VARIANCE; ARTICLE; CONTROLLED STUDY; COUPLING FACTOR; DENSITOMETRY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; CELL CULTURE; DRUG EFFECTS; GENETICS; METABOLISM; PHOSPHORYLATION;

BIOPTERIN; CELLS, CULTURED; ENDOTHELIAL CELLS; HUMANS; LIPOPROTEINS, LDL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; SUPEROXIDES;

EID: 84907477378     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107787     Document Type: Article

References (59)

1. Furchgott RF, Zawadzki J.V. (1980) The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288: 373-376.
2. Rubanyi GM, Vanhoutte P.M. (1986) Superoxide anions and hyperoxia inactivate endothelium-derived relaxing factor. Am J Physiol 250: H822-827.
3. Bath PM (1993) The effect of nitric oxide-donating vasodilators on monocyte chemotaxis and intracellular cGMP concentrations in vitro. Eur J Clin Pharmacol 45: 53-58.
4. Moncada S, Palmer RM, Higgs E.A. (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev 43: 109-142.
5. Landmesser U, Dikalov S, Price S.R., McCann L., Fukai T, et al. (2003) Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 111: 1201-1209.
6. Zou MH, Shi C, Cohen R.A. (2002) Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite. J Clin Invest 109: 817-826.
7. Cosentino F, Lüscher TF (1999) Tetrahydrobiopterin and endothelial nitric oxide synthase activity. Cardiovasc Res 43: 274-278.
8. Alp NJ, McAteer MA, Khoo J, Choudhury R.P., Channon K.M. (2004) Increased endothelial tetrahydrobiopterin synthesis by targeted transgenic GTP-cyclohy-drolase I overexpression reduces endothelial dysfunction and atherosclerosis in ApoE-knockout mice. Arterioscler Thromb Vasc Biol 24: 445-450.
9. Fleming I, Mohamed A, Galle J., Turchanowa L, Brandes RP, et al (2005) Oxidized low-density lipoprotein increases superoxide production by endothelial nitric oxide synthase by inhibiting PKCalpha. Cardiovasc Res 65: 897-906.
10. Franzeck FC, Hof D, Spescha R.D., Hasun M., Akhmedov A, et al. Expression of the aging gene p66Shc is increased in peripheral blood monocytes of patients with acute coronary syndrome but not with stable coronary artery disease. Atherosclerosis 220: 282-286.
11. Spescha RD, Shi Y, Wegener S., Keller S, Weber B, et al Deletion of the ageing gene p66(Shc) reduces early stroke size following ischaemia/reperfusion brain injury. Eur Heart J 34: 96-103.
12. Camici GG, Cosentino F, Tanner F.C., Lüscher TF (2008) The role of p66Shc deletion in age-associated arterial dysfunction and disease states. J Appl Physiol 105: 1628-1631.
13. Bonfini L, Migliaccio E, Pelicci G., Lanfrancone L, Pelicci P.G. (1996) Not all Shc's roads lead to Ras. Trends Biochem Sci 21: 257-261.
14. Shi Y, Camici GG, Luscher T.F. (2010) Cardiovascular determinants of life span. Pflugers Arch 459: 315-324.
15. Camici GG, Shi Y, Cosentino F., Francia P, Luscher T.F. (2010) Anti-Aging Medicine: Molecular Basis for Endothelial Cell-Targeted Strategies - A MiniReview. Gerontology.
16. Migliaccio E, Giorgio M, Mele S., Pelicci G, Reboldi P, et al (1999) The p66shc adaptor protein controls oxidative stress response and life span in mammals. Nature 402: 309-313.
17. Napoli C, Martin-Padura I, de Nigris F, Giorgio M, Mansueto G., et al. (2003) Deletion of the p66Shc longevity gene reduces systemic and tissue oxidative stress, vascular cell apoptosis, and early atherogenesis in mice fed a high-fat diet. Proc Natl Acad Sci U S A 100: 2112-2116.
18. Shi Y, Cosentino F, Camici G.G., Akhmedov A., Vanhoutte PM, et al. (2011) Oxidized Low-Density Lipoprotein Activates p66Shc via Lectin-Like Oxidized Low-Density Lipoprotein Receptor-1, Protein Kinase C-{beta}, and c-Jun N-Terminal Kinase Kinase in Human Endothelial Cells. Arterioscler Thromb Vasc Biol 31: 2090-2097.
19. Giorgio M, Migliaccio E, Orsini F., Paolucci D, Moroni M, et al (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122: 221-233.
20. Tomilov AA, Bicocca V, Schoenfeld R.A., Giorgio M., Migliaccio E, et al. Decreased superoxide production in macrophages of long-lived p66Shc knockout mice. J Biol Chem 285: 1153-1165.
21. Kim CS, Jung SB, Naqvi A, Hoffman T.A., DeRicco J., et al. (2008) p53 impairs endothelium-dependent vasomotor function through transcriptional upregulation of p66shc. Circ Res 103: 1441-1450.
22. Yamamori T, White AR, Mattagajasingh I, Khanday F.A., Haile A., et al. (2005) P66shc regulates endothelial NO production and endothelium-dependent vasorelaxation: implications for age-associated vascular dysfunction. J Mol Cell Cardiol 39: 992-995.
23. Mooradian DL, Hutsell TC, Keefer L.K. (1995) Nitric oxide (NO) donor molecules: effect of NO release rate on vascular smooth muscle cell proliferation in vitro. J Cardiovasc Pharmacol 25: 674-678.
24. Morley D, Maragos CM, Zhang X.Y., Boignon M., Wink DA, et al. (1993) Mechanism of vascular relaxation induced by the nitric oxide (NO)/nucleophile complexes, a new class of NO-based vasodilators. J Cardiovasc Pharmacol 21: 670-676.
25. Mullane KM, Moncada S, Vane J.R. (1980) Prostacyclin release induced by bradykinin may contribute to the antihypertensive action of angiotensin-converting enzyme inhibitors. Adv Prostaglandin Thromboxane Res 7: 1159-1161.
26. Vanhoutte PM, Collis MG, Janssens W.J., Verbeuren T.J. (1981) Calcium dependence of prejunctional inhibitory effects of adenosine and acetylcholine on adrenergic neurotransmission in canine saphenous veins. Eur J Pharmacol 72: 189-198.
27. Southgate K, Newby A.C. (1990) Serum-induced proliferation of rabbit aortic smooth muscle cells from the contractile state is inhibited by 8-Br-cAMP but not 8-Br-cGMP. Atherosclerosis 82: 113-123.
28. Garthwaite J, Southam E, Boulton C.L., Nielsen EB, Schmidt K, et al. (1995) Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol 48: 184-188.
29. Wyatt TA, Pryzwansky KB, Lincoln T.M. (1991) KT5823 activates human neutrophils and fails to inhibit cGMP-dependent protein kinase phosphorylation of vimentin. Res Commun Chem Pathol Pharmacol 74: 3-14.
30. Tayeh MA, Marletta M.A. (1989) Macrophage oxidation of L-arginine to nitric oxide, nitrite, and nitrate. Tetrahydrobiopterin is required as a cofactor. J Biol Chem 264: 19654-19658.
31. Camici GG, Schiavoni M, Francia P., Bachschmid M, Martin-Padura I, et al. (2007) Genetic deletion of p66(Shc) adaptor protein prevents hyperglycemia-induced endothelial dysfunction and oxidative stress. Proc Natl Acad Sci U S A 104: 5217-5222.
32. Le S, Connors TJ, Maroney A.C. (2001) c-Jun N-terminal kinase specifically phosphorylates p66ShcA at serine 36 in response to ultraviolet irradiation. J Biol Chem 276: 48332-48336.
33. Pinton P, Rimessi A, Marchi S., Orsini F, Migliaccio E, et al (2007) Protein kinase C beta and prolyl isomerase 1 regulate mitochondrial effects of the lifespan determinant p66Shc. Science 315: 659-663.
34. Feletou M, Tang EH, Vanhoutte P.M. (2008) Nitric oxide the gatekeeper of endothelial vasomotor control. Front Biosci 13: 4198-4217.
35. Cosentino F, Patton S, d'Uscio LV, Werner ER, Werner-Felmayer G, et al. (1998) Tetrahydrobiopterin alters superoxide and nitric oxide release in prehypertensive rats. J Clin Invest 101: 1530-1537.
36. Li H, Forstermann U. (2009) Prevention of atherosclerosis by interference with the vascular nitric oxide system. Curr Pharm Des 15: 3133-3145.
37. Hink U, Li H, Mollnau H., Oelze M, Matheis E, et al (2001) Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res 88: E14-22.
38. Channon KM (2004) Tetrahydrobiopterin: regulator of endothelial nitric oxide synthase in vascular disease. Trends Cardiovasc Med 14: 323-327.
39. Pritchard KA J.r., Ackerman AW, Gross E.R., Stepp DW, Shi Y, et al. (2001) Heat shock protein 90 mediates the balance of nitric oxide and superoxide anion from endothelial nitric-oxide synthase. J Biol Chem 276: 17621-17624.
40. Sud N, Wells SM, Sharma S, Wiseman D.A., Wilham J., et al. (2008) Asymmetric dimethylarginine inhibits HSP90 activity in pulmonary arterial endothelial cells: role of mitochondrial dysfunction. Am J Physiol Cell Physiol 294: C1407-1418.
41. Chen CA, Wang TY, Varadharaj S, Reyes L.A., Hemann C., et al. (2010) S-glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature 468: 1115-1118.
42. Gao YT, Roman LJ, Martasek P, Panda S.P., Ishimura Y., et al. (2007) Oxygen metabolism by endothelial nitric-oxide synthase. J Biol Chem 282: 28557-28565.
43. Fukai T (2007) Endothelial GTPCH in eNOS uncoupling and atherosclerosis. Arterioscler Thromb Vasc Biol 27: 1493-1495.
44. Rosenkranz-Weiss P., Sessa WC, Milstien S, Kaufman S., Watson CA, et al. (1994) Regulation of nitric oxide synthesis by proinflammatory cytokines in human umbilical vein endothelial cells. Elevations in tetrahydrobiopterin levels enhance endothelial nitric oxide synthase specific activity. J Clin Invest 93: 2236-2243.
45. Huang A, Vita JA, Venema R.C., Keaney JF Jr (2000) Ascorbic acid enhances endothelial nitric-oxide synthase activity by increasing intracellular tetrahydro-biopterin. J Biol Chem 275: 17399-17406.
46. Rosenblum WI (1997) Tetrahydrobiopterin, a cofactor for nitric oxide synthase, produces endothelium-dependent dilation of mouse pial arterioles. Stroke 28: 186-189.
47. Faria AM, Papadimitriou A, Silva K.C., Lopes de Faria JM, Lopes de Faria JB (2012) Uncoupling endothelial nitric oxide synthase is ameliorated by green tea in experimental diabetes by re-establishing tetrahydrobiopterin levels. Diabetes 61: 1838-1847.
48. Shinozaki K, Nishio Y, Okamura T., Yoshida Y, Maegawa H, et al (2000) Oral administration of tetrahydrobiopterin prevents endothelial dysfunction and vascular oxidative stress in the aortas of insulin-resistant rats. Circ Res 87: 566-573.
49. Youn JY, Wang T, Blair J., Laude KM, Oak JH, et al. (2012) Endothelium-specific sepiapterin reductase deficiency in DOCA-salt hypertension. Am J Physiol Heart Circ Physiol 302: H2243-2249.
50. Perkins KA, Pershad S, Chen Q., McGraw S, Adams JS, et al (2012) The effects of modulating eNOS activity and coupling in ischemia/reperfusion (I/R). Naunyn Schmiedebergs Arch Pharmacol 385: 27-38.
51. Moreau KL, Meditz A, Deane K.D., Kohrt W.M. (2012) Tetrahydrobiopterin improves endothelial function and decreases arterial stiffness in estrogen-deficient postmenopausal women. Am J Physiol Heart Circ Physiol 302: H1211-1218.
52. Holowatz LA, Kenney W.L. (2011) Acute localized administration of tetra-hydrobiopterin and chronic systemic atorvastatin treatment restore cutaneous microvascular function in hypercholesterolaemic humans. J Physiol 589: 4787-4797.
53. Maier W, Cosentino F, Lutolf R.B., Fleisch M., Seiler C, et al. (2000) Tetrahydrobiopterin improves endothelial function in patients with coronary artery disease. J Cardiovasc Pharmacol 35: 173-178.
54. Ueda S, Matsuoka H, Miyazaki H., Usui M, Okuda S, et al (2000) Tetrahydrobiopterin restores endothelial function in long-term smokers. J Am Coll Cardiol 35: 71-75.
55. Heitzer T, Krohn K, Albers S., Meinertz T. (2000) Tetrahydrobiopterin improves endothelium-dependent vasodilation by increasing nitric oxide activity in patients with Type II diabetes mellitus. Diabetologia 43: 1435-1438.
56. Cunnington C, Van Assche T, Shirodaria C, Kylintireas I., Lindsay AC, et al. (2012) Systemic and vascular oxidation limits the efficacy of oral tetrahydro-biopterin treatment in patients with coronary artery disease. Circulation 125: 1356-1366.
57. Liu S, Lee IM, Song Y, Van Denburgh M, Cook NR, et al (2006) Vitamin E and risk of type 2 diabetes in the women's health study randomized controlled trial. Diabetes 55: 2856-2862.
58. Ward NC, Wu JH, Clarke M.W., Puddey IB, Burke V, et al. (2007) The effect of vitamin E on blood pressure in individuals with type 2 diabetes: a randomized, double-blind, placebo-controlled trial. J Hypertens 25: 227-234.
59. Sesso HD, Buring JE, Christen W.G., Kurth T., Belanger C, et al. (2008) Vitamins E and C in the prevention of cardiovascular disease in men: the Physicians' Health Study II randomized controlled trial. JAMA 300: 2123-2133.