P66Shc links α1-adrenergic receptors to a reactive oxygen species-dependent AKT-FOXO3A phosphorylation pathway in cardiomyocytes

Circulation Research

Volumn 104, Issue 5, 2009, Pages 660-669

  Guo, Jianfen ^a   Gertsberg, Zoya ^a   Ozgen, Nazira ^a   Steinberg, Susan F ^a  

^a Columbia University ^*  (United States)

Author keywords

1 adrenergic receptors; AKT; P66Shc; Protein kinase C; ROS

Indexed keywords

ALPHA 1 ADRENERGIC RECEPTOR; BIM 1 PROTEIN; BIM PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1B; EPIDERMAL GROWTH FACTOR RECEPTOR; MANGANESE SUPEROXIDE DISMUTASE; PROTEIN KINASE B; PROTEIN KINASE C EPSILON; PROTEIN KINASE C GAMMA; PROTEIN P66; PROTEIN P66SHC; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; DOXORUBICIN; EGFR PROTEIN, RAT; FORKHEAD TRANSCRIPTION FACTOR; FOXO3A PROTEIN, RAT; GLYCOGEN SYNTHASE KINASE 3; NORADRENALIN; PROTEIN KINASE C DELTA; PROTEIN SHC; SHC1 PROTEIN, RAT; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; CAVEOLA; CELL GROWTH; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE REPRESSION; HEART MUSCLE CELL; MUSCLE HYPERTROPHY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; ANIMAL; APOPTOSIS; CARDIOMEGALY; CELL CULTURE; CELL ENLARGEMENT; DRUG EFFECT; ENZYMOLOGY; GENETIC TRANSDUCTION; GENETICS; METABOLISM; NEWBORN; PATHOLOGY; PHOSPHORYLATION; RNA INTERFERENCE; TIME; WISTAR RAT;

ANIMALS; ANIMALS, NEWBORN; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; CARDIOMEGALY; CAVEOLAE; CELL ENLARGEMENT; CELLS, CULTURED; DOXORUBICIN; FORKHEAD TRANSCRIPTION FACTORS; GLYCOGEN SYNTHASE KINASE 3; MYOCYTES, CARDIAC; NOREPINEPHRINE; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN KINASE C-DELTA; PROTEIN KINASE C-EPSILON; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, ADRENERGIC, ALPHA-1; RNA INTERFERENCE; RNA, SMALL INTERFERING; SHC SIGNALING ADAPTOR PROTEINS; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSDUCTION, GENETIC;

EID: 63649159307     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.186288     Document Type: Article

References (31)

1. Aronow BJ, Toyokawa T, Canning A, Haghighi K, Delling U, Kranias E, Molkentin JD, Dorn GW. Divergent transcriptional responses to independent genetic causes of cardiac hypertrophy. Physiol Genomics. 2001; 6:19-28.
2. Sabri A, Muske G, Zhang H, Pak E, Darrow A, Andrade-Gordon P, Steinberg SF. Signaling properties and functions of two distinct cardiomyocyte protease-activated receptors. Circ Res. 2000;86:1054-1061.
3. Shiojima I, Walsh K. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev. 2006;20: 3347-3365.
4. Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science. 2002;295:2450-2452.
5. Rybin VO, Xu X, Lisanti MP, Steinberg SF. Differential targeting of -adrenergic receptor subtypes and adenylyl cyclase to cardiomyocyte caveolae. J Biol Chem. 2000;275:41447-41457.
6. Rybin VO, Xu X, Steinberg SF. Activated protein kinase C isoforms target to cardiomyocyte caveolae. Circ Res. 1999;84:980-988.
7. Rybin VO, Sabri A, Short J, Braz JC, Molkentin JD, Steinberg SF. Cross regulation of nPKC isoform function in cardiomyocytes. J Biol Chem. 2003;278:14555-14564.
8. Yamamori T, White AR, Mattagajasingh I, Khanday FA, Haile A, Qi B, Jeon BH, Bugayenko A, Kasuno K, Berkowitz DE, Irani K. p66shc regulates endothelial NO production and endothelium-dependent vasorelaxation: implications for age-associated vascular dysfunction. J Mol Cell Cardiol. 2005;39:992-995.
9. Obreztchikova M, Elouardighi H, Ho M, Wilson BA, Gertsberg Z, Steinberg SF. Distinct signaling functions for SHC isoforms in the heart. J Biol Chem. 2006;281:20194-20204.
10. Yang B, Oo TN, Rizzo V. Lipid rafts mediate H2O2 prosurvival effects in cultured endothelial cells. FASEB J. 2006;20:1501-1503.
11. Xiao L, Pimentel DR, Wang J, Singh K, Colucci WS, Sawyer DB. Role of reactive oxygen species and NAD(P)H oxidase in -1-adrenoceptor signaling in adult rat cardiac myocytes. Am J Physiol. 2002;282: C926-C934.
12. 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-- and prolyl isomerase 1 regulate mitochondrial effects of the life-span determinant p66Shc. Science. 2007; 315:659-663.
13. Ni YG, Berenji K, Wang N, Oh M, Sachan N, Dey A, Cheng J, Lu G, Morris DJ, Castrillon DH, Gerard RD, Rothermel BA, Hill JA. Foxo transcription factors blunt cardiac hypertrophy by inhibiting calcineurin signaling. Circulation. 2006;114:1159-1168.
14. Stahl M, Dijkers PF, Kops GJPL, Lens SMA, Coffer PJ, Burgering BMT, Medema RH. The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J Immunol. 2002;168: 5042-15031
15. Hauck L, Harms C, Rohne J, Gertz K, Dietz R, Endres M, von Harsdorf R. Protein kinase CK2 links extracellular growth factor signaling with the control of p27(Kip1) stability in the heart. Nat Med. 2008;14:315-324.
16. Skurk C, Izumiya Y, Maatz H, Razeghi P, Shiojima I, Sandri M, Sato K, Zeng L, Schiekofer S, Pimentel D, Lecker S, Taegtmeyer H, Goldberg AL, Walsh K. The FOXO3a transcription factor regulates cardiac myocyte size downstream of AKT signaling. J Biol Chem. 2005;280: 20814-20823.
17. Orsini F, Migliaccio E, Moroni M, Contursi C, Raker VA, Piccini D, Martin-Padura I, Pelliccia G, Trinei M, Bono M, Puri C, Tacchetti C, Ferrini M, Mannucci R, Nicoletti I, Lanfrancone L, Giorgio M, Pelicci PG. The life span determinant p66Shc localizes to mitochondria where it associates with mitochondrial heat shock protein 70 and regulates transmembrane potential. J Biol Chem. 2004;279:25689-25695.
18. 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 cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell. 2005;122:221-233.
19. 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. 2006;281:10555-10560.
20. Soltoff SP. Rottlerin: an inappropriate and ineffective inhibitor of PKC. Trends Pharmacol Sci. 2007;28:453-458.
21. Polak P, Hall MN. mTORC2 Caught in a SINful Akt. Dev Cell. 2006; 11:433-434.
22. Graiani G, Lagrasta C, Migliaccio E, Spillmann F, Meloni M, Madeddu P, Quaini F, Padura IM, Lanfrancone L, Pelicci P, Emanueli C. Genetic deletion of the p66Shc adaptor protein protects from angiotensin II-induced myocardial damage. Hypertension. 2005;46:433-440.
23. Rota M, LeCapitaine N, Hosoda T, Boni A, De Angelis A, Padin-Iruegas ME, Esposito G, Vitale S, Urbanek K, Casarsa C, Giorgio M, Luscher TF, Pelicci PG, Anversa P, Leri A, Kajstura J. Diabetes promotes cardiac stem cell aging and heart failure, which are prevented by deletion of the p66Shc gene. Circ Res. 2006;99:42-52.
24. Finetti F, Pellegrini M, Ulivieri C, Savino MT, Paccagnini E, Ginanneschi C, Lanfrancone L, Pellicci PG, Baldari CT. The proapoptotic and antimitogenic protein p66SHC acts as a negative regulator of lymphocyte activation and autoimmunity. Blood. 2008;111:5017-5027.
25. Andoh T, Lee SY, Chiueh CC. Preconditioning regulation of bcl-2 and p66shc by human NOS1 enhances tolerance to oxidative stress. FASEB J. 2000;14:2144-2146.
26. Zaccagnini G, Martelli F, Fasanaro P, Magenta A, Gaetano C, Di Carlo A, Biglioli P, Giorgio M, Martin-Padura I, Pelicci PG, Capogrossi MC. p66ShcA modulates tissue response to hindlimb ischemia. Circulation. 2004;109:2917-2923.
27. 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 U S A. 2003;100:2112-2116.
28. Francia P, delli Gatti C, Bachschmid M, Martin-Padura I, Savoia C, Migliaccio E, Pelicci PG, Schiavoni M, Luscher TF, Volpe M, Cosentino F. Deletion of p66shc gene protects against age-related endothelial dysfunction. Circulation. 2004;110:2889-2895.
29. Pellegrini M, Finetti F, Petronilli V, Ulivieri C, Giusti F, Lupetti P, Giorgio M, Pelicci PG, Bernardi P, Baldari CT. p66SHC promotes T cell apoptosis by inducing mitochondrial dysfunction and impaired Ca2 homeostasis. Cell Death Differ. 2007;14:338-347.
30. Petti LM, Ricciardi EC, Page HJ, Porter KA. Transforming signals resulting from sustained activation of PDGF- receptor in mortal human fibroblasts. J Cell Sci. 2008;121:1172-1182.
31. Sansone P, Storci G, Giovannini C, Pandolfi S, Pianetti S, Taffurelli M, Santini D, Ceccarelli C, Chieco P, Bonafe M. p66Shc/Notch-3 interplay controls self-renewal and hypoxia survival in human stem/progenitor cells of the mammary gland expanded in vitro as mammospheres. Stem Cells. 2007;25:807-815.