Oxidative stress improves coronary endothelial function through activation of the pro-survival kinase AMPK

Aging

Volumn 5, Issue 7, 2013, Pages 515-530

  Shafique, Ehtesham ^a   Choy, Wing C ^a   Liu, Yuhong ^a,b   Feng, Jun ^a,b   Arthur Lyra, Brenda Cordeiro ^a,d   Arafah, Mohammed ^a,c   Yassin Kassab, Abdulmounem ^a,c   Zanetti, Arthus V D ^a,d   Clements, Richard T ^a,b   Bianchi, Cesario ^a,b   Benjamin, Laura E ^e   Sellke, Frank W ^a,b   Abid, M Ruhul ^a,b  

^a RHODE ISLAND HOSPITAL   (United States)

^b BROWN UNIVERSITY   (United States)

^c ALFAISAL UNIVERSITY   (Saudi Arabia)

^d FACULDADE DE CIÊNCIAS MÉDICAS DA SANTA CASA DE SÃO PAULO   (Brazil)

^e ELI LILLY AND COMPANY   (United States)

Author keywords

Aging; Autophagy; Endothelial function; Nadph oxidase; Reactive oxygen species; Signal transduction

Indexed keywords

EID: 84881110201     PISSN: 19454589     EISSN: None     Source Type: Journal    
DOI: 10.18632/aging.100569     Document Type: Article

References (58)

1. Datla SR and Griendling KK. Reactive oxygen species, NADPH oxidases, and hypertension. Hypertension. 2010; 56: 325-330.
2. Luo Z, Teerlink T, Griendling K, Aslam S, Welch WJ and Wilcox CS. Angiotensin II and NADPH oxidase increase ADMA in vascular smooth muscle cells. Hypertension. 2010; 56: 498-504.
3. Frey RS, Ushio-Fukai M and Malik AB. NADPH oxidasedependent signaling in endothelial cells: role in physiology and pathophysiology. Antioxidants & redox signaling. 2009; 11: 791-810.
4. Drummond GR, Selemidis S, Griendling KK and Sobey CG. Combating oxidative stress in vascular disease: NADPH oxidases as therapeutic targets. Nature reviews. Drug discovery. 2011; 10: 453-471.
5. Vivekananthan DP, Penn MS, Sapp SK, Hsu A, and Topol EJ. Use of antioxidant vitamins for the prevention of cardiovascular disease: meta-analysis of randomised trials. Lancet. 2003; 361:2017-2023.
6. Virtamo J, Rapola JM, Ripatti S, Heinonen OP, Taylor PR, Albanes D,and Huttunen JK. Effect of vitamin E and beta carotene on the incidence of primary nonfatal myocardial infarction and fatal coronary heart disease. Arch Intern Med. 1998; 158: 668-675.
7. Rapola JM, Virtamo J, Ripatti S, Haukka JK, Huttunen JK, Albanes D, Taylor RR, and Heinonen PO. Effects of alpha tocopherol and beta carotene supplements on symptoms, progression, and prognosis of angina pectoris. Heart. 1998; 79: 454-458.
8. Hegele RA. Angiotensin-converting enzyme (ACE) inhibition in the secondary prevention of vascular disease: the Heart Outcomes Prevention Evaluation (HOPE) Trial and its substudies. Curr Atheroscler Rep. 2000; 2: 361-362.
9. Abid MR, Spokes KC, Shih SCand Aird WC. NADPH oxidase activity selectivelymodulates vascular endothelial growth factor signaling pathways. The Journal of biological chemistry. 2007; 282: 35373-35385.
10. Feng J, Damrauer SM, Lee M, Sellke FW, Ferran C and Abid MR. Endothelium dependent coronary vasodilatation requires NADPH oxidase-derived reactive oxygen species. Arteriosclerosis, thrombosis, and vascular biology. 2010; 30: 1703-1710.
11. Zhang Q, Malik P, Pandey D, Gupta S, Jagnandan D, Belin de Chantemele E, Banfi B, Marrero MB, Rudic RD, Stepp DW, and Fulton DJ. Paradoxical activation of endothelial nitric oxide synthase by NADPH oxidase. Arteriosclerosis, thrombosis, and vascular biology. 2008; 28: 1627-1633.
12. Ushio-Fukai M, Tang Y, Fukai T, Dikalov SI, Ma Y, Fujimoto M, Quinn MT, Pagano PJ, Johnson C, and Alexander RW. Novel role of gp91(phox)-containing NAD(P)H oxidase in vascularendothelial growth factor-induced signaling and angiogenesis. Circulation research. 2002; 91: 1160-1167.
13. Sawada N, Salomone S, Kim HH, Kwiatkowski DJ, and Liao JK. Regulation of endothelial nitric oxide synthase and postnatal angiogenesis by Rac1. Circulation research. 2008; 103: 360-368.
14. Craige SM, Chen K, Pei Y, Li C, Huang X, Chen C, Shibata R, Sato K, Walsh K, and Keaney, Jr JF. NADPH oxidase 4 promotes endothelial angiogenesis through endothelial nitric oxide synthase activation. Circulation. 2011; 124: 731-740.
15. Cai H, Li Z, SDikalov S, Holland SM, Hwang J, Jo H, Dudley, Jr. SC, and Harrison DG. NAD(P)H oxidase-derived hydrogen peroxide mediates endothelial nitric oxide production in response to angiotensin II. The Journal of biological chemistry. 2002; 277: 48311-48317.
16. Ray R, Murdoch CE, Wang M, Santos CX, Zhang M, Alom- Ruiz S, Anilkumar N, Ouattara A, Cave AC, Walker SJ, Grieve DJ, Charles RL, Eaton P, Brewer AC, and Shah AM. Endothelial Nox4 NADPH oxidase enhances vasodilatation and reduces blood pressure in vivo. Arteriosclerosis, thrombosis, and vascular biology. 2011; 31: 1368 1376.
17. Krotz F, Engelbrecht B, Buerkle MA, Bassermann F, Bridell H, Gloe T, JDuyster J, Pohl U, and Sohn HY. The tyrosine phosphatase, SHP-1, is a negative regulator of endothelial superoxide formation. Journal of the American College of Cardiology. 2005; 45: 1700-1706.
18. Lee M, Choy WC, and Abid MR. Direct sensing of endothelial oxidants by vascular endothelial growth factor receptor-2 and c- Src. PloS one. 2011; 6: e28454.
19. Mungai PT, Waypa GB, Jairaman A, Prakriya M, Dokic D, Ball MK,and Schumacker PT. Hypoxia triggers AMPK activation through reactive oxygen species-mediated activation of calcium release-activated calcium channels. Molecular and cellular biology. 2011; 31: 3531-3545.
20. Mackenzie RM, Salt IP, Miller WH, Logan A, Ibrahim HA, Degasperi A, Dymott JA, Hamilton CA, Murphy MP, Delles C, and Dominiczak AF. Mitochondrial reactive oxygen species enhance MP-activated protein kinase activation in the endothelium of patients with coronary artery disease and diabetes. Clinical science. 2013; 124: 403-411.
21. Wang Q, Liang B, Shirwany NA, and Zou MH. 2-Deoxy-Dglucose treatment of endothelial cells induces autophagy by reactive oxygen species-mediated activation of the AMPactivated protein kinase. PloS one. 2011; 6: e17234.
22. Lee M, Hwang JT, Lee HJ, Jung SN, Kang I, Chi SG, Kim SS, and Ha J. AMP-activated protein kinase activity is critical for hypoxiainducible factor-1 transcriptional activity and its target gene expression under hypoxic conditions in DU145 cells. The Journal of biological chemistry. 2003; 278: 39653-39661.
23. Dixit M, Bess E, Fisslthaler B, Hartel FV, Noll T, Busse R, and IFleming I. Shear stress-induced activation of the AMP-activated protein kinase regulates FoxO1a and angiopoietin-2 in endothelial cells. Cardiovascular research. 2008; 77: 160-168.
24. Cardaci S, Filomeni G, and Ciriolo MR. Redox implications of AMPK-mediated signal transduction beyond energetic clues. Journal of cell science. 2012; 125: 2115-2125.
25. Kimura S, Noda T, and Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy. 2007; 3: 452-460.
26. Abid MR, Tsai JC, Spokes KC, Deshpande SS, Irani K, and Aird WC. Vascular endothelial growth factor induces manganesesuperoxide dismutase expression in endothelial cells by a Rac1- regulated NADPH oxidase-dependent mechanism. FASEB journal: official publication of the Federation of American Societies for Experimental Biology. 2001; 15: 2548-2550.
27. Bayraktutan U, Blayney L, and Shah AM. Molecular characterization and localization of the NAD(P)H oxidase components gp91-phox and p22-phox in endothelial cells. Arteriosclerosis, thrombosis, and vascular biology. 2000; 20: 1903-1911.
28. Arbiser JL, Petros J, Klafter R, Govindajaran B, McLaughlin ER, Brown LF, Cohen C, Moses M, Kilroy S, Arnold RS, and Lambeth. JD Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proceedings of the National Academy of Sciences of the United States of America. 2002; 99: 715-720.
29. Bengtsson M SH, Gulluyan LM, Dusting GJ, and Drummond GR. Novel isoforms of NADPH oxidase in vascular physiology and pathophysiology. Clinical and experimental pharmacology & physiology. 2003; 30: 849-854.
30. Ago T, Kitazono T, Ooboshi H, Iyama T, Han YH, Takada J, Wakisaka M, Ibayashi S, Utsumi H,and Iida M. Nox4 as the major catalytic component of an endothelial NAD(P)H oxidase. Circulation. 2004; 109: 227-233.
31. BelAiba RS, Djordjevic T, Petry A, Diemer K, Bonello S, Banfi B, Hess J, Pogrebniak A, Bickel C,and Gorlach A. NOX5 variants are functionally active in endothelial cells. Free radical biology & medicine. 2007; 42: 446-459.
32. Van Buul JD, Fernandez-Borja M, Anthony EC, and Hordijk PL. Expression and localization of NOX2 and NOX4 in primary human endothelial cells. Antioxidants & redox signaling. 2005; 7: 308-317.
33. Thomas SR, Chen K, and Keaney, Jr. JF. Hydrogen peroxide activates endothelial nitric-oxide synthase through coordinated phosphorylation and dephosphorylation via a phosphoinositide 3-kinase-dependent signaling pathway. The Journal of biological chemistry. 2002; 277: 6017-6024.
34. Cai H, Davis ME, Drummond GR, and Harrison DG. Induction of endothelial NO synthase by hydrogen peroxide via a Ca(2+)/calmodulin-dependent protein kinase II/janus kinase 2- dependent pathway. Arteriosclerosis, thrombosis, and vascular biology. 2001; 21: 1571-1576.
35. Schroder K, Zhang M, Benkhoff S, Mieth A, Pliquett R, Kosowski J, Kruse C,Luedike P, Michaelis UR, Weissmann N,Dimmeler S, Shah AM,and Brandes RP. Nox4 is a protective reactive oxygen species generating vascular NADPH oxidase. Circulation research. 2012; 110: 1217-1225.
36. Bendall JK, Rinze R, Adlam D, Tatham AL, de Bono J, Wilson N, Volpi E, and Channon KM. Endothelial Nox2 overexpression potentiates vascular oxidative stress and hemodynamic response to angiotensin II: studies in endothelial-targeted Nox2 transgenic mice. Circulation research. 2007; 100: 1016-1025.
37. Zhang Q, Malik P, Pandey D, Gupta S, Jagnandan D, Belin de Chantemele E, Banfi B, Marrero MB, Rudic RD, Stepp DW, and Fulton DJ. Paradoxical activation of endothelial nitric oxide synthase by NADPH oxidase. Arterioscler Thromb Vasc Biol. 2008; 28: 1627-1633.
38. Sarbassov DD, Ali SM, and Sabatini DM. Growing roles for the mTOR pathway. Current opinion in cell biology. 2005; 17: 596- 603.
39. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, and Sadoshima J. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circulation research. 2007; 100: 914-922.
40. Hariharan N, Zhai P, and Sadoshima J. Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxidants & redox signaling. 2011; 14: 2179-2190.
41. Gems D and Guardia YD. Alternative Perspectives on Aging in Caenorhabditis elegans: Reactive Oxygen Species or Hyperfunction? Antioxidants & redox signaling. 2012.
42. Blagosklonny MV. Aging: ROS or TOR. Cell cycle. 2008; 7: 3344-3354.
43. Blagosklonny MV. Hormesis does not make sense except in the light of TOR-driven aging. Aging. 2011; 3: 1051-62.
44. Sessa, W.C. eNOS at a glance. Journal of cell science. 2004; 117: 2427-2429.
45. Chen ZP, Mitchelhill KI, Michell BJ, Stapleton D, Rodriguez-Crespo I, Witters LA, Power DA, Ortiz de Montellano PR, and Kemp BE. AMP-activated protein kinase phosphorylation of endothelial NO synthase. FEBS letters. 1999; 443: 285-289.
46. Morrow VA, Foufelle F, Connell JM, Petrie JR, Gould GW, and Salt IP. Direct activation of AMP-activated protein kinase stimulates nitric-oxide synthesis in human aortic endothelial cells. The Journal of biological chemistry. 2003; 278: 31629-31639.
47. Hardie DG. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy.Nature reviews. Molecular cell biology. 2007; 8: 774-785.
48. Fisslthaler B and Fleming I. Activation and signaling by the AMP-activated protein kinase in endothelial cells. Circulation research. 2009; 105: 114-127.
49. Stahmann N, Woods A, Carling D, and Heller R. Thrombin activates AMP-activated protein kinase in endothelial cells via a pathway involving Ca2+/calmodulin-dependent protein kinase kinase beta. Molecular and cellular biology. 2006; 26: 5933-5945.
50. Goirand F, Solar M, Athea Y, Viollet B, Mateo P, Fortin D, Leclerc J, Hoerter J, Ventura-Clapier R, and Garnier A. Activation of AMP kinase alpha1 subunit induces aortic vasorelaxation in mice. The Journal of physiology. 2007; 581: 1163-1671.
51. Katakam PV, Ujhelyi MR, Hoenig M,and Miller AW. Metformin improves vascular function in insulin-resistant rats. Hypertension. 2000; 35: 108-112.
52. Sartoretto JL, Melo GA, Carvalho MH, Nigro D, Passaglia RT, Scavone C, Cuman RK, and Fortes ZB. Metformin treatment restores the altered microvascular reactivity in neonatal streptozotocin-induced diabetic rats increasing NOS activity, but not NOS expression. Life sciences. 2005; 77: 2676-2689.
53. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewi Ks, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, et al. Resveratrol improves health and survival of mice on a high-calorie diet. Nature. 2006; 444: 337-342.
54. Phung TL, Ziv K, Dabydeen D, Eyiah-Mensah G, Riveros M, Perruzzi C, Sun J, Monahan-Earley RA, Shiojima I, Nagy JA, Lin MI, Walsh K, Dvorak AM, Briscoe DM, Neeman M, Sessa WC, et al. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell. 2006; 10: 159-170.
55. Abid MR., Yano K, Guo S, Patel VI, Shrikhande G, Spokes KC, Ferran C, and Aird WC. Forkhead transcription factors inhibit vascular smooth muscle cell proliferation and neointimal hyperplasia. J Biol Chem. 2005; 280: 29864-29873.
56. Mukai Y, Rikitake Y, Shiojima I, Wolfrum S, Satoh M, Takeshita K, Hiroi Y, Salomone S, Kim HH, Benjamin LE, Walsh K and Liao JK. Decreased vascular lesion formation in mice with inducible endothelial-specific expression of protein kinase Akt. J Clin Invest. 2006; 116: 334-343.
57. Griendling KK, Minieri CA, Ollerenshaw JD, and Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circulation research. 1994; 74: 1141-1148.
58. Abid MR, Guo S, Minami T, Spokes KC, Ueki K, Skurk C, Walsh K, and Aird WC. Vascular endothelial growth factor activates PI3K/Akt/forkhead signaling in endothelial cells. Arteriosclerosis, thrombosis, and vascular biology. 2004; 24: 294-300.