Novel role of p66shc in ROS-dependent VEGF signaling and angiogenesis in endothelial cells

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 302, Issue 3, 2012, Pages

  Oshikawa, Jin ^a,c   Kim, Seok Jo ^a,c   Furuta, Eiji ^a,c   Caliceti, Cristiana ^a,c   Chen, Gin Fu ^b,c   McKinney, Ronald D ^a,b,c   Kuhr, Frank ^d   Levitan, Irena ^d   Fukai, Tohru ^b,c   Ushio Fukai, Masuko ^a,c  

^a Center for Lung and Vascular Biology   (United States)

^b Departments of Medicine and Pharmacology   (United States)

^c Center for Cardiovascular Research   (United States)

^d UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Reactive oxygen species; Vascular endothelial growth factor

Indexed keywords

ADAPTOR PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; P66SHC PREOTEIN; RAC1 PROTEIN; REACTIVE OXYGEN METABOLITE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2;

ANGIOGENESIS; ARTICLE; AUTOPHOSPHORYLATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DEPLETION; SIGNAL TRANSDUCTION;

CAVEOLAE; ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MEMBRANE MICRODOMAINS; NEOVASCULARIZATION, PHYSIOLOGIC; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RAC1 GTP-BINDING PROTEIN; REACTIVE OXYGEN SPECIES; SHC SIGNALING ADAPTOR PROTEINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84863063969     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00739.2011     Document Type: Article

References (55)

1. Arany I, Faisal A, Nagamine Y, Safirstein RL. p66Shc inhibits pro-survival epidermal growth factor receptor/ERK signaling during severe oxidative stress in mouse renal proximal tubule cells. J Biol Chem 283: 6110-6117, 2008.
2. Babior BM. The NADPH oxidase of endothelial cells. IUBMB Life 50: 267-269, 2000.
3. Camici GG, Schiavoni M, Francia P, Bachschmid M, Martin-Padura I, Hersberger M, Tanner FC, Pelicci P, Volpe M, Anversa P, Luscher TF, Cosentino F. Genetic deletion of p66(Shc) adaptor protein prevents hyperglycemia-induced endothelial dysfunction and oxidative stress. Proc Natl Acad Sci USA 104: 5217-5222, 2007.
4. Carpi A, Menabo R, Kaludercic N, Pelicci P, Di Lisa F, Giorgio M. The cardioprotective effects elicited by p66(Shc) ablation demonstrate the crucial role of mitochondrial ROS formation in ischemia/reperfusion injury. Biochim Biophys Acta 1787: 774-780, 2009.
5. Chahdi A, Sorokin A. Endothelin-1 couples betaPix to p66Shc: role of betaPix in cell proliferation through FOXO3a phosphorylation and p27kip1 down-regulation independently of Akt. Mol Biol Cell 19: 2609- 2619, 2008.
6. Chen K, Craige SE, Keaney JF. Downstream targets and intracellular compartmentalization in Nox signaling. Antioxid Redox Signal 11: 2467-2480, 2009.
7. Colavitti R, Pani G, Bedogni B, Anzevino R, Borrello S, Waltenberger J, Galeotti T. Reactive oxygen species as downstream mediators of angiogenic signaling by vascular endothelial growth factor receptor-2/ KDR. J Biol Chem 277: 3101-3108, 2002.
8. Cosentino F, Francia P, Camici GG, Pelicci PG, Luscher TF, Volpe M. Final common molecular pathways of aging and cardiovascular disease: role of the p66Shc protein. Arterioscler Thromb Vasc Biol 28: 622-628, 2008.
9. Ebrahimian TG, Heymes C, You D, Blanc-Brude O, Mees B, Waeckel L, Duriez M, Vilar J, Brandes RP, Levy BI, Shah AM, Silvestre JS. NADPH oxidase-derived overproduction of reactive oxygen species impairs postischemic neovascularization in mice with type 1 diabetes. Am J Pathol 169: 719-728, 2006.
10. Fadini GP, Ceolotto G, Pagnin E, de Kreutzenberg S, Avogaro A. At the crossroads of longevity and metabolism: the metabolic syndrome and life span determinant pathways. Aging Cell 10: 10-17.
11. Finkel T. Signal transduction by reactive oxygen species in non-phago-cytic cells. J Leukoc Biol 65: 337-340, 1999.
12. Foschi M, Franchi F, Han J, La Villa G, Sorokin A. Endothelin-1 induces serine phosphorylation of the adaptor protein p66Shc and its association with 14-3-3 protein in glomerular mesangial cells. J Biol Chem 276: 26640-26647, 2001.
13. Francia P, delli Gatti C, Bachschmid M, Martin-Padura I, Savoia C, Migliaccio E, Pelicci PG, Schiavoni M, Luscher TF, Volpe M, Cosen-tino F. Deletion of p66shc gene protects against age-related endothelial dysfunction. Circulation 110: 2889-2895, 2004.
14. Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, Pinton P, Rizzuto R, Bernardi P, Paolucci F, Pelicci PG. Electron transfer between cyto-chrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122: 221-233, 2005.
15. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 86: 494-501, 2000.
16. Guo J, Gertsberg Z, Ozgen N, Steinberg SF. p66Shc links alpha1-adrenergic receptors to a reactive oxygen species-dependent AKT-FOXO3A phosphorylation pathway in cardiomyocytes. Circ Res 104: 660-669, 2009.
17. Haddad P, Dussault S, Groleau J, Turgeon J, Michaud SE, Menard C, Perez G, Maingrette F, Rivard A. Nox2-containing NADPH oxidase deficiency confers protection from hindlimb ischemia in conditions of increased oxidative stress. Arterioscler Thromb Vasc Biol 29: 1522-1528, 2009.
18. Hu Y, Wang X, Zeng L, Cai DY, Sabapathy K, Goff SP, Firpo EJ, Li B. ERK phosphorylates p66shcA on Ser36 and subsequently regulates p27kip1 expression via the Akt-FOXO3a pathway: implication of p27kip1 in cell response to oxidative stress. Mol Biol Cell 16: 3705-3718, 2005.
19. Ikeda S, Ushio-Fukai M, Zuo L, Tojo T, Dikalov S, Patrushev NA, Alexander RW. Novel role of ARF6 in vascular endothelial growth factor-induced signaling and angiogenesis. Circ Res 96: 467-475, 2005.
20. Kao AW, Waters SB, Okada S, Pessin JE. Insulin stimulates the phosphorylation of the 66- and 52-kilodalton Shc isoforms by distinct pathways. Endocrinology 138: 2474-2480, 1997.
21. Kaplan N, Urao N, Furuta E, Kim SJ, Razvi M, Nakamura Y, McKinney RD, Poole LB, Fukai T, Ushio-Fukai M. Localized cysteine sulfenic acid formation by vascular endothelial growth factor: role in endothelial cell migration and angiogenesis. Free Radic Res 45: 1124-1135, 2011.
22. Khanday FA, Santhanam L, Kasuno K, Yamamori T, Naqvi A, Dericco J, Bugayenko A, Mattagajasingh I, Disanza A, Scita G, Irani K. Sos-mediated activation of rac1 by p66shc. J Cell Biol 172: 817-822, 2006.
23. Labrecque L, Royal I, Surprenant DS, Patterson C, Gingras D, Beliveau R. Regulation of vascular endothelial growth factor receptor-2 activity by caveolin-1 and plasma membrane cholesterol. Mol Biol Cell 14: 334-347, 2003.
24. Lamalice L, Houle F, Jourdan G, Huot J. Phosphorylation of tyrosine 1214 on VEGFR2 is required for VEGF-induced activation of Cdc42 upstream of SAPK2/p38. Oncogene 23: 434-445, 2004.
25. Li PL, Gulbins E. Lipid rafts and redox signaling. Antioxid Redox Signal 9: 1411-1415, 2007.
26. Migliaccio E, Giorgio M, Mele S, Pelicci G, Reboldi P, Pandolfi PP, Lanfrancone L, Pelicci PG. The p66shc adaptor protein controls oxida-tive stress response and life span in mammals. Nature 402: 309-313, 1999.
27. Naldini A, Morena E, Pucci A, Pellegrini M, Baldari CT, Pelicci PG, Presta M, Ribatti D, Carraro F. The adaptor protein p66Shc is a positive regulator in the angiogenic response induced by hypoxic T cells. J Leukoc Biol 87: 365-369, 2010.
28. Napoli C, Martin-Padura I, de Nigris F, Giorgio M, Mansueto G, Somma P, Condorelli M, Sica G, De Rosa G, Pelicci P. 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 USA 100: 2112-2116, 2003.
29. Nemoto S, Combs CA, French S, Ahn BH, Fergusson MM, Balaban RS, Finkel T. The mammalian longevity-associated gene product p66shc regulates mitochondrial metabolism. J Biol Chem 281: 10555-10560, 2006.
30. Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 295: 2450-2452, 2002.
31. Okada S, Kao AW, Ceresa BP, Blaikie P, Margolis B, Pessin JE. The 66-kDa Shc isoform is a negative regulator of the epidermal growth factor-stimulated mitogen-activated protein kinase pathway. J Biol Chem 272: 28042-28049, 1997.
32. Oshikawa J, Urao N, Kim HW, Kaplan N, Razvi M, McKinney R, Poole LB, Fukai T, Ushio-Fukai M. Extracellular SOD-derived H2O2 promotes VEGF signaling in caveolae/lipid rafts and postischemic angio-genesis in mice. PLos One 5: e10189, 2010.
33. Pani G. P66SHC and ageing: ROS and TOR? Aging (Albany, NY) 2: 514-518, 2010.
34. Pelicci G, Lanfrancone L, Grignani F, McGlade J, Cavallo F, Forni G, Nicoletti I, Grignani F, Pawson T, Pelicci PG. A novel transforming protein (SHC) with an SH2 domain is implicated in mitogenic signal transduction. Cell 70: 93-104, 1992.
35. Pinton P, Rimessi A, Marchi S, Orsini F, Migliaccio E, Giorgio M, Contursi C, Minucci S, Mantovani F, Wieckowski MR, Del Sal G, Pelicci PG, Rizzuto R. Protein kinase C beta and prolyl isomerase 1 regulate mitochondrial effects of the life-span determinant p66Shc. Science 315: 659-663, 2007.
36. Ranieri SC, Fusco S, Panieri E, Labate V, Mele M, Tesori V, Ferrara AM, Maulucci G, De Spirito M, Martorana GE, Galeotti T, Pani G. Mammalian life-span determinant p66shcA mediates obesity-induced insulin resistance. Proc Natl Acad Sci USA 107: 13420-13425, 2010.
37. Rhee SG, Bae YS, Lee SR, Kwon J. Hydrogen peroxide: a key messenger that modulates protein phosphorylation through cysteine oxidation. Sci STKE 2000: PE1, 2000.
38. Song KS, Li S, Okamoto T, Quilliam LA, Sargiacomo M, Lisanti MP. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J Biol Chem 271: 9690-9697, 1996.
39. Sun L, Xiao L, Nie J, Liu FY, Ling GH, Zhu XJ, Tang WB, Chen WC, Xia YC, Zhan M, Ma MM, Peng YM, Liu H, Liu YH, Kanwar YS. p66Shc mediates high-glucose and angiotensin II-induced oxidative stress renal tubular injury via mitochondrial-dependent apoptotic pathway. Am J Physiol Renal Physiol 299: F1014-F1025, 2010.
40. Takahashi T, Yamaguchi S, Chida K, Shibuya M. A single autophos-phorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. EMBO J 20: 2768-2778, 2001.
41. Terada LS. Specificity in reactive oxidant signaling: think globally, act locally. J Cell Biol 174: 615-623, 2006.
42. Tojo T, Ushio-Fukai M, Yamaoka-Tojo M, Ikeda S, Patrushev NA, Alexander RW. Role of gp91phox (Nox2)-containing NAD(P)H oxidase in angiogenesis in response to hindlimb ischemia. Circulation 111: 2347-2355, 2005.
43. Tomilov AA, Bicocca V, Schoenfeld RA, Giorgio M, Migliaccio E, Ramsey JJ, Hagopian K, Pelicci PG, Cortopassi GA. Decreased super-oxide production in macrophages of long-lived p66Shc knock-out mice. J Biol Chem 285: 1153-1165.
44. Tonks NK. Redox redux: revisiting PTPs and the control of cell signaling. Cell 121: 667-670, 2005.
45. Urao N, Inomata H, Razvi M, Kim HW, Wary K, McKinney R, Fukai T,Ushio-Fukai M. Role of nox2-based NADPH oxidase in bone marrow and progenitor cell function involved in neovascularization induced by hindlimb ischemia. Circ Res 103: 212-220, 2008.
46. Ushio-Fukai M. Compartmentalization of redox signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal 11: 1289-1299, 2009.
47. Ushio-Fukai M. Localizing NADPH oxidase-derived ROS. Sci STKE 2006: re8, 2006.
48. Ushio-Fukai M. VEGF signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal 9: 731-739, 2007.
49. Ushio-Fukai M, Tang Y, Fukai T, Dikalov SI, Ma Y, Fujimoto M, Quinn MT, Pagano PJ, Johnson C, Alexander RW. Novel role of gp91(phox)-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis. Circ Res 91: 1160-1167, 2002.
50. Veeramani S, Yuan TC, Lin FF, Lin MF. Mitochondrial redox signaling by p66Shc is involved in regulating androgenic growth stimulation of human prostate cancer cells. Oncogene 27: 5057-5068, 2008.
51. Wang Y, Zang QS, Liu Z, Wu Q, Maass D, Dulan G, Shaul PW, Melito L, Frantz DE, Kilgore JA, Williams NS, Terada LS, Nwariaku FE. Regulation of VEGF induced endothelial cell migration by mitochon-drial reactive oxygen species. Am J Physiol Cell Physiol 301: C695-C704, 2011.
52. Yamaoka-Tojo M, Ushio-Fukai M, Hilenski L, Dikalov SI, Chen YE, Tojo T, Fukai T, Fujimoto M, Patrushev NA, Wang N, Kontos CD, Bloom GS, Alexander RW. IQGAP1, a novel vascular endothelial growth factor receptor binding protein, is involved in reactive oxygen species-dependent endothelial migration and proliferation. Circ Res 95: 276-283, 2004.
53. Yang B, Oo TN, Rizzo V. Lipid rafts mediate H2O2 prosurvival effects in cultured endothelial cells. FASEB J 20: 1501-1503, 2006.
54. Zaccagnini G, Martelli F, Fasanaro P, Magenta A, Gaetano C, Di Carlo A, Biglioli P, Giorgio M, Martin-Padura I, Pelicci PG, Capo-grossi MC. p66ShcA modulates tissue response to hindlimb ischemia. Circulation 109: 2917-2923, 2004.
55. Zhang AY, Yi F, Zhang G, Gulbins E, Li PL. Lipid raft clustering and redox signaling platform formation in coronary arterial endothelial cells. Hypertension 47: 74-80, 2006.