Rheb is a critical regulator of autophagy during myocardial ischemia: Pathophysiological implications in obesity and metabolic syndrome

Circulation

Volumn 125, Issue 9, 2012, Pages 1134-1146

  Sciarretta, Sebastiano ^a,b   Zhai, Peiyong ^a   Shao, Dan ^a   Maejima, Yasuhiro ^a   Robbins, Jeffrey ^c   Volpe, Massimo ^b,d   Condorelli, Gianluigi ^e   Sadoshima, Junichi ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b IRCCS NEUROMED   (Italy)

^c CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

apoptosis; ischemia; obesity; signal transduction

Indexed keywords

ADENOSINE TRIPHOSPHATE; AUTOPHAGY PROTEIN 7; CELL PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; RHEB PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOPHAGY; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; GENE ACTIVATION; GENE OVEREXPRESSION; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; IN VITRO STUDY; LIPID DIET; METABOLIC SYNDROME X; MOUSE; NONHUMAN; OBESITY; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; AUTOPHAGY; CELL SURVIVAL; CELLS, CULTURED; DIETARY FATS; ENDOPLASMIC RETICULUM STRESS; ENERGY METABOLISM; GLUCOSE; METABOLIC SYNDROME X; MICE; MICE, KNOCKOUT; MONOMERIC GTP-BINDING PROTEINS; MYOCARDIAL ISCHEMIA; MYOCYTES, CARDIAC; NEUROPEPTIDES; OBESITY; RATS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84857914471     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.078212     Document Type: Article

References (35)

1. Velagaleti RS, Pencina MJ, Murabito JM, Wang TJ, Parikh NI, D'Agostino RB, Levy D, Kannel WB, Vasan RS. Long-term trends in the incidence of heart failure after myocardial infarction. Circulation. 2008; 118:2057-2062.
2. Inoki K, Ouyang H, Zhu T, Lindvall C, Wang Y, Zhang X, Yang Q, Bennett C, Harada Y, Stankunas K, Wang CY, He X, MacDougald OA, You M, Williams BO, Guan KL. TSC2 integrates Wnt and energy signals via a coordinated phosphorylation by AMPK and GSK3 to regulate cell growth. Cell. 2006;126:955-968. (Pubitemid 44310775)
3. Aspuria PJ, Sato T, Tamanoi F. The TSC/Rheb/TOR signaling pathway in fission yeast and mammalian cells: temperature sensitive and constitutive active mutants of TOR. Cell Cycle. 2007;6:1692-1695. (Pubitemid 47327919)
4. Karassek S, Berghaus C, Schwarten M, Goemans CG, Ohse N, Kock G, Jockers K, Neumann S, Gottfried S, Herrmann C, Heumann R, Stoll R. Ras homolog enriched in brain (Rheb) enhances apoptotic signaling. J Biol Chem. 2010;285:33979-33991.
5. Babcock JT, Quilliam LA. Rheb/mTOR Activation and regulation in cancer: novel treatment strategies beyond rapamycin. Curr Drug Targets. 2011;12:1223-1231.
6. Ma D, Bai X, Zou H, Lai Y, Jiang Y. Rheb GTPase controls apoptosis by regulating interaction of FKBP38 with Bcl-2 and Bcl-XL. J Biol Chem. 2010;285:8621-8627.
7. Inoki K, Li Y, Xu T, Guan KL. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 2003;17: 1829-1834. (Pubitemid 36944560)
8. Sengupta S, Peterson TR, Sabatini DM. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell. 2010;40:310-322.
9. Zhang D, Contu R, Latronico MV, Zhang JL, Rizzi R, Catalucci D, Miyamoto S, Huang K, Ceci M, Gu Y, Dalton ND, Peterson KL, Guan KL, Brown JH, Chen J, Sonenberg N, Condorelli G. MTORC1 regulates cardiac function and myocyte survival through 4E-BP1 inhibition in mice. J Clin Invest. 2010;120:2805-2816.
10. Buss SJ, Muenz S, Riffel JH, Malekar P, Hagenmueller M, Weiss CS, Bea F, Bekeredjian R, Schinke-Braun M, Izumo S, Katus HA, Hardt SE. Beneficial effects of Mammalian target of rapamycin inhibition on left ventricular remodeling after myocardial infarction. J Am Coll Cardiol. 2009;54:2435-2446.
11. Song X, Kusakari Y, Xiao CY, Kinsella SD, Rosenberg MA, Scherrer- Crosbie M, Hara K, Rosenzweig A, Matsui T. mTOR attenuates the inflammatory response in cardiomyocytes and prevents cardiac dysfunction in pathological hypertrophy. Am J Physiol Cell Physiol. 2010; 299:C1256-C1266.
12. Flegal KM, Carroll MD, Ogden CL, Curtin LR. Prevalence and trends in obesity among US adults, 1999-2008. JAMA. 2010;303:235-241.
13. Clavijo LC, Pinto TL, Kuchulakanti PK, Torguson R, Chu WW, Satler LF, Kent KM, Suddath WO, Pichard AD, Waksman R. Metabolic syndrome in patients with acute myocardial infarction is associated with increased infarct size and in-hospital complications. Cardiovasc Revasc Med. 2006;7:7-11.
14. Zeller M, Steg PG, Ravisy J, Laurent Y, Janin-Manificat L, L'Huillier I, Beer JC, Oudot A, Rioufol G, Makki H, Farnier M, Rochette L, Verges B, Cottin Y. Prevalence and impact of metabolic syndrome on hospital outcomes in acute myocardial infarction. Arch Intern Med. 2005;165: 1192-1198. (Pubitemid 40720745)
15. Abdulla J, Kober L, Abildstrom SZ, Christensen E, James WP, Torp- Pedersen C. Impact of obesity as a mortality predictor in high-risk patients with myocardial infarction or chronic heart failure: a pooled analysis of five registries. Eur Heart J. 2008;29:594-601.
16. du Toit EF, Smith W, Muller C, Strijdom H, Stouthammer B, Woodiwiss AJ, Norton GR, Lochner A. Myocardial susceptibility to ischemicreperfusion injury in a prediabetic model of dietary-induced obesity. Am J Physiol Heart Circ Physiol. 2008;294:H2336-H2343.
17. Khamzina L, Veilleux A, Bergeron S, Marette A. Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-linked insulin resistance. Endocrinology. 2005;146:1473-1481. (Pubitemid 40289337)
18. Um SH, D'Alessio D, Thomas G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab. 2006;3:393-402. (Pubitemid 43811780)
19. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, 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. Circ Res. 2007;100:914-922. (Pubitemid 46555697)
20. Zhai P, Sciarretta S, Galeotti J, Volpe M, Sadoshima J. Differential roles of GSK-3β during myocardial ischemia and ischemia/reperfusion. Circ Res. 2011;109:502-511.
21. Ravikumar B, Futter M, Jahreiss L, Korolchuk VI, Lichtenberg M, Luo S, Massey DC, Menzies FM, Narayanan U, Renna M, Jimenez-Sanchez M, Sarkar S, Underwood B, Winslow A, Rubinsztein DC. Mammalian macroautophagy at a glance. J Cell Sci. 2009;122:1707-1711.
22. Yang L, Li P, Fu S, Calay ES, Hotamisligil GS. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 2010;11:467-478.
23. Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC. Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J Biol Chem. 2007; 282:5641-5652. (Pubitemid 47093730)
24. Hamacher-Brady A, Brady NR, Gottlieb RA. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem. 2006;281:29776-29787. (Pubitemid 44536987)
25. Romero-Corral A, Montori VM, Somers VK, Korinek J, Thomas RJ, Allison TG, Mookadam F, Lopez-Jimenez F. Association of bodyweight with total mortality and with cardiovascular events in coronary artery disease: a systematic review of cohort studies. Lancet. 2006;368: 666-678. (Pubitemid 44223694)
26. Aronson D, Nassar M, Goldberg T, Kapeliovich M, Hammerman H, Azzam ZS. The impact of body mass index on clinical outcomes after acute myocardial infarction. Int J Cardiol. 2010;145:476-480.
27. Wang CY, Kim HH, Hiroi Y, Sawada N, Salomone S, Benjamin LE, Walsh K, Moskowitz MA, Liao JK. Obesity increases vascular senescence and susceptibility to ischemic injury through chronic activation of Akt and mTOR. Sci Signal. 2009;2:ra11.
28. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature. 2004;431:200-205. (Pubitemid 39243474)
29. 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 U S A. 2010;107:13420-13425.
30. Drake JC, Alway SE, Hollander JM, Williamson DL. AICAR treatment for 14 days normalizes obesity-induced dysregulation of TORC1 signaling and translational capacity in fasted skeletal muscle. Am J Physiol Regul Integr Comp Physiol. 2010;299:R1546-R1554.
31. Rivas DA, Yaspelkis BB, III, Hawley JA, Lessard SJ. Lipid-induced mTOR activation in rat skeletal muscle reversed by exercise and 5′- aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside. J Endocrinol. 2009;202:441-451.
32. Glazer HP, Osipov RM, Clements RT, Sellke FW, Bianchi C. Hypercholesterolemia is associated with hyperactive cardiac mTORC1 and mTORC2 signaling. Cell Cycle. 2009;8:1738-1746.
33. Sung MM, Koonen DP, Soltys CL, Jacobs RL, Febbraio M, Dyck JR. Increased CD36 expression in middle-aged mice contributes to obesityrelated cardiac hypertrophy in the absence of cardiac dysfunction. J Mol Med (Berl). 2011;89:459-469.
34. Turdi S, Kandadi MR, Zhao J, Huff AF, Du M, Ren J. Deficiency in AMP-activated protein kinase exaggerates high fat diet-induced cardiac hypertrophy and contractile dysfunction. J Mol Cell Cardiol. 2011;50: 712-722.
35. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 2004;18:1926-1945. (Pubitemid 39071573)