Differential regulation of eEF2 and p70S6K by AMPKalpha2 in heart

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 6, 2013, Pages 780-790

  Demeulder, Bénédicte ^a   Zarrinpashneh, Elham ^a   Ginion, Audrey ^a   Viollet, Benoit ^b,c,d   Hue, Louis ^a   Rider, Mark H ^a   Vanoverschelde, Jean Louis ^a,e   Beauloye, Christophe ^a,e   Horman, Sandrine ^a   Bertrand, Luc ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b INSTITUT COCHIN   (France)

^c CNRS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e CLINIQUES UNIVERSITAIRES SAINT LUC   (Belgium)

Author keywords

AMPK; EEF2; Myocardial ischemia; P70S6K; PKB Akt; Protein synthesis

Indexed keywords

AMP ACTIVATED PROTEIN KINASE ALPHA 1; AMP ACTIVATED PROTEIN KINASE ALPHA 2; ELONGATION FACTOR; EUKARYOTIC ELONGATION FACTOR 2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN P70 RIBOSOMAL PROTEIN S6; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CATALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME ACTIVITY; EX VIVO STUDY; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; INHIBITION KINETICS; MOUSE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEIN TARGETING; RAT; REGULATORY MECHANISM;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CARRIER PROTEINS; ENZYME ACTIVATION; MICE; MICE, KNOCKOUT; MUSCLE PROTEINS; MYOCARDIAL ISCHEMIA; MYOCARDIUM; PEPTIDE ELONGATION FACTOR 2; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EUKARYOTA; MAMMALIA; MUS; RAPTORES;

EID: 84875489311     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.02.015     Document Type: Article

References (56)

1. Proud C.G. Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem. J. 2007, 403:217-234.
2. Kaul G., Pattan G., Rafeequi T. Eukaryotic elongation factor-2 (eEF2): its regulation and peptide chain elongation. Cell Biochem. Funct. 2011, 29:227-234.
3. Wang L., Wang X., Proud C.G. Activation of mRNA translation in rat cardiac myocytes by insulin involves multiple rapamycin-sensitive steps. Am. J. Physiol. Heart Circ. Physiol. 2000, 278:H1056-H1068.
4. Bertrand L., Horman S., Beauloye C., Vanoverschelde J.L. Insulin signalling in the heart. Cardiovasc. Res. 2008, 79:238-248.
5. Wang X., Proud C.G. mTORC1 signaling: what we still don't know. J. Mol. Cell Biol. 2011, 3:206-220.
6. Inoki K., Li Y., Zhu T., Wu J., Guan K.L. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell Biol. 2002, 4:648-657.
7. Goncharova E.A., Goncharov D.A., Eszterhas A., Hunter D.S., Glassberg M.K., Yeung R.S., Walker C.L., Noonan D., Kwiatkowski D.J., Chou M.M., Panettieri R.A., Krymskaya V.P. Tuberin regulates p70 S6 kinase activation and ribosomal protein S6 phosphorylation. A role for the TSC2 tumor suppressor gene in pulmonary lymphangioleiomyomatosis (LAM). J. Biol. Chem. 2002, 277:30958-30967.
8. Tee A.R., Fingar D.C., Manning B.D., Kwiatkowski D.J., Cantley L.C., Blenis J. Tuberous sclerosis complex-1 and -2 gene products function together to inhibit mammalian target of rapamycin (mTOR)-mediated downstream signaling. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13571-13576.
9. Shah O.J., Anthony J.C., Kimball S.R., Jefferson L.S. 4E-BP1 and S6K1: translational integration sites for nutritional and hormonal information in muscle. Am. J. Physiol. Endocrinol. Metab. 2000, 279:E715-E729.
10. Horman S., Beauloye C., Vertommen D., Vanoverschelde J.L., Hue L., Rider M.H. Myocardial ischemia and increased heart work modulate the phosphorylation state of eukaryotic elongation factor-2. J. Biol. Chem. 2003, 278:41970-41976.
11. Beauloye C., Bertrand L., Krause U., Marsin A.S., Dresselaers T., Vanstapel F., Vanoverschelde J.L., Hue L. No-flow ischemia inhibits insulin signaling in heart by decreasing intracellular pH. Circ. Res. 2001, 88:513-519.
12. Crozier S.J., Vary T.C., Kimball S.R., Jefferson L.S. Cellular energy status modulates translational control mechanisms in ischemic-reperfused rat hearts. Am. J. Physiol. Heart Circ. Physiol. 2005, 289:H1242-H1250.
13. Kim A.S., Miller E.J., Wright T.M., Li J., Qi D., Atsina K., Zaha V., Sakamoto K., Young L.H. A small molecule AMPK activator protects the heart against ischemia-reperfusion injury. J. Mol. Cell. Cardiol. 2011, 51:24-32.
14. Poole-Wilson P.A. Regulation of intracellular pH in the myocardium; relevance to pathology. Mol. Cell. Biochem. 1989, 89:151-155.
15. Kudo N., Barr A.J., Barr R.L., Desai S., Lopaschuk G.D. High rates of fatty acid oxidation during reperfusion of ischemic hearts are associated with a decrease in malonyl-CoA levels due to an increase in 5'-AMP-activated protein kinase inhibition of acetyl-CoA carboxylase. J. Biol. Chem. 1995, 270:17513-17520.
16. Viollet B., Lantier L., Devin-Leclerc J., Hebrard S., Amouyal C., Mounier R., Foretz M., Andreelli F. Targeting the AMPK pathway for the treatment of Type 2 diabetes. Front. Biosci. 2009, 14:3380-3400.
17. Beauloye C., Bertrand L., Horman S., Hue L. AMPK activation, a preventive therapeutic target in the transition from cardiac injury to heart failure. Cardiovasc. Res. 2011, 90:224-233.
18. Hardie D.G. AMP-activated protein kinase as a drug target. Annu. Rev. Pharmacol. Toxicol. 2007, 47:185-210.
19. Young L.H., Li J., Baron S.J., Russell R.R. AMP-activated protein kinase: a key stress signaling pathway in the heart. Trends Cardiovasc. Med. 2005, 15:110-118.
20. Bolster D.R., Crozier S.J., Kimball S.R., Jefferson L.S. AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J. Biol. Chem. 2002, 277:23977-23980.
21. Dubbelhuis P.F., Meijer A.J. Hepatic amino acid-dependent signaling is under the control of AMP-dependent protein kinase. FEBS Lett. 2002, 521:39-42.
22. Horman S., Browne G., Krause U., Patel J., Vertommen D., Bertrand L., Lavoinne A., Hue L., Proud C., Rider M. Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr. Biol. 2002, 12:1419-1423.
23. Krause U., Bertrand L., Hue L. Control of p70 ribosomal protein S6 kinase and acetyl-CoA carboxylase by AMP-activated protein kinase and protein phosphatases in isolated hepatocytes. Eur. J. Biochem. 2002, 269:3751-3759.
24. Browne G.J., Finn S.G., Proud C.G. Stimulation of the AMP-activated protein kinase leads to activation of eukaryotic elongation factor 2 kinase and to its phosphorylation at a novel site, serine 398. J. Biol. Chem. 2004, 279:12220-12231.
25. Chan A.Y., Soltys C.L., Young M.E., Proud C.G., Dyck J.R. Activation of AMP-activated protein kinase inhibits protein synthesis associated with hypertrophy in the cardiac myocyte. J. Biol. Chem. 2004, 279:32771-32779.
26. Chan A.Y., Dyck J.R. Activation of AMP-activated protein kinase (AMPK) inhibits protein synthesis: a potential strategy to prevent the development of cardiac hypertrophy. Can. J. Physiol. Pharmacol. 2005, 83:24-28.
27. Chan A.Y., Dolinsky V.W., Soltys C.L., Viollet B., Baksh S., Light P.E., Dyck J.R. Resveratrol inhibits cardiac hypertrophy via AMP-activated protein kinase and Akt. J. Biol. Chem. 2008, 283:24194-24201.
28. Gwinn D.M., Shackelford D.B., Egan D.F., Mihaylova M.M., Mery A., Vasquez D.S., Turk B.E., Shaw R.J. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol. Cell 2008, 30:214-226.
29. Roca H., Varsos Z.S., Pienta K.J. CCL2 is a negative regulator of AMP-activated protein kinase to sustain mTOR complex-1 activation, survivin expression, and cell survival in human prostate cancer PC3 cells. Neoplasia 2009, 11:1309-1317.
30. Inoki K., Zhu T., Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 2003, 115:577-590.
31. Ginion A., Auquier J., Benton C.R., Mouton C., Vanoverschelde J.L., Hue L., Horman S., Beauloye C., Bertrand L. Inhibition of the mTOR/p70S6K pathway is not involved in the insulin-sensitizing effect of AMPK on cardiac glucose uptake. Am. J. Physiol. Heart Circ. Physiol. 2011, 301:H469-H477.
32. Viollet B., Andreelli F., Jorgensen S.B., Perrin C., Geloen A., Flamez D., Mu J., Lenzner C., Baud O., Bennoun M., Gomas E., Nicolas G., Wojtaszewski J.F., Kahn A., Carling D., Schuit F.C., Birnbaum M.J., Richter E.A., Burcelin R., Vaulont S. The AMP-activated protein kinase alpha2 catalytic subunit controls whole-body insulin sensitivity. J. Clin. Invest. 2003, 111:91-98.
33. Zarrinpashneh E., Carjaval K., Beauloye C., Ginion A., Mateo P., Pouleur A.C., Horman S., Vaulont S., Hoerter J., Viollet B., Hue L., Vanoverschelde J.L., Bertrand L. Role of the {alpha}2-isoform of AMP-activated protein kinase in the metabolic response of the heart to no-flow ischemia. Am. J. Physiol. Heart Circ. Physiol. 2006, 291:H2875-H2883.
34. Carvajal K., Zarrinpashneh E., Szarszoi O., Joubert F., Athea Y., Mateo P., Gillet B., Vaulont S., Viollet B., Bigard X., Bertrand L., Ventura-Clapier R., Hoerter J.A. Dual cardiac contractile effects of the alpha2-AMPK deletion in low-flow ischemia and reperfusion. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H3136-H3147.
35. Athea Y., Viollet B., Mateo P., Rousseau D., Novotova M., Garnier A., Vaulont S., Wilding J.R., Grynberg A., Veksler V., Hoerter J., Ventura-Clapier R. AMP-activated protein kinase {alpha}2 deficiency affects cardiac cardiolipin homeostasis and mitochondrial function. Diabetes 2007, 56:786-794.
36. Zarrinpashneh E., Beauloye C., Ginion A., Pouleur A.C., Havaux X., Hue L., Viollet B., Vanoverschelde J.L., Bertrand L. AMPKalpha2 counteracts the development of cardiac hypertrophy induced by isoproterenol. Biochem. Biophys. Res. Commun. 2008, 376:677-681.
37. Bertrand L., Ginion A., Beauloye C., Hebert A.D., Guigas B., Hue L., Vanoverschelde J.L. AMPK activation restores the stimulation of glucose uptake in an in vitro model of insulin-resistant cardiomyocytes via the activation of protein kinase B. Am. J. Physiol. Heart Circ. Physiol. 2006, 291:H239-H250.
38. Marsin A.S., Bertrand L., Rider M.H., Deprez J., Beauloye C., Vincent M.F., Van den Berghe G., Carling D., Hue L. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 2000, 10:1247-1255.
39. Bertrand L., Alessi D.R., Deprez J., Deak M., Viaene E., Rider M.H., Hue L. Heart 6-phosphofructo-2-kinase activation by insulin results from Ser-466 and Ser-483 phosphorylation and requires 3-phosphoinositide-dependent kinase-1, but not protein kinase B. J. Biol. Chem. 1999, 274:30927-30933.
40. Sanchez Canedo C., Demeulder B., Ginion A., Bayascas J.R., Balligand J.L., Alessi D.R., Vanoverschelde J.L., Beauloye C., Hue L., Bertrand L. Activation of the cardiac mTOR/p70(S6K) pathway by leucine requires PDK1 and correlates with PRAS40 phosphorylation. Am. J. Physiol. Endocrinol. Metab. 2010, 298:E761-E769.
41. Rosner M., Siegel N., Valli A., Fuchs C., Hengstschlager M. mTOR phosphorylated at S2448 binds to raptor and rictor. Amino Acids 2010, 38:223-228.
42. Chiang G.G., Abraham R.T. Phosphorylation of mammalian target of rapamycin (mTOR) at Ser-2448 is mediated by p70S6 kinase. J. Biol. Chem. 2005, 280:25485-25490.
43. Copp J., Manning G., Hunter T. TORC-specific phosphorylation of mammalian target of rapamycin (mTOR): phospho-Ser2481 is a marker for intact mTOR signaling complex 2. Cancer Res. 2009, 69:1821-1827.
44. Wang X., Li W., Parra J.L., Beugnet A., Proud C.G. The C terminus of initiation factor 4E-binding protein 1 contains multiple regulatory features that influence its function and phosphorylation. Mol. Cell. Biol. 2003, 23:1546-1557.
45. Wang X., Beugnet A., Murakami M., Yamanaka S., Proud C.G. Distinct signaling events downstream of mTOR cooperate to mediate the effects of amino acids and insulin on initiation factor 4E-binding proteins. Mol. Cell. Biol. 2005, 25:2558-2572.
46. Beauloye C., Marsin A.S., Bertrand L., Krause U., Hardie D.G., Vanoverschelde J.L., Hue L. Insulin antagonizes AMP-activated protein kinase activation by ischemia or anoxia in rat hearts, without affecting total adenine nucleotides. FEBS Lett. 2001, 505:348-352.
47. Liu L., Cash T.P., Jones R.G., Keith B., Thompson C.B., Simon M.C. Hypoxia-induced energy stress regulates mRNA translation and cell growth. Mol. Cell 2006, 21:521-531.
48. Dorovkov M.V., Pavur K.S., Petrov A.N., Ryazanov A.G. Regulation of elongation factor-2 kinase by pH. Biochemistry 2002, 41:13444-13450.
49. Noga A.A., Soltys C.L., Barr A.J., Kovacic S., Lopaschuk G., Dyck J.R. Expression of an active LKB1 complex in cardiac myocytes results in decreased protein synthesis associated with phenylephrine-induced hypertrophy. Am. J. Physiol. Heart Circ. Physiol. 2007, 292:H1460-H1469.
50. Jorgensen S.B., Viollet B., Andreelli F., Frosig C., Birk J.B., Schjerling P., Vaulont S., Richter E.A., Wojtaszewski J.F. Knockout of the alpha2 but not alpha1 5'-AMP-activated protein kinase isoform abolishes 5-aminoimidazole-4-carboxamide-1-beta-4-ribofuranosidebut not contraction-induced glucose uptake in skeletal muscle. J. Biol. Chem. 2004, 279:1070-1079.
51. Zhang P., Hu X., Xu X., Fassett J., Zhu G., Viollet B., Xu W., Wiczer B., Bernlohr D.A., Bache R.J., Chen Y. AMP activated protein kinase-alpha2 deficiency exacerbates pressure-overload-induced left ventricular hypertrophy and dysfunction in mice. Hypertension 2008, 52:918-924.
52. Mounier R., Lantier L., Leclerc J., Sotiropoulos A., Pende M., Daegelen D., Sakamoto K., Foretz M., Viollet B. Important role for AMPKalpha1 in limiting skeletal muscle cell hypertrophy. FASEB J. 2009, 23:2264-2273.
53. McMullen J.R., Shioi T., Zhang L., Tarnavski O., Sherwood M.C., Dorfman A.L., Longnus S., Pende M., Martin K.A., Blenis J., Thomas G., Izumo S. Deletion of ribosomal S6 kinases does not attenuate pathological, physiological, or insulin-like growth factor 1 receptor-phosphoinositide 3-kinase-induced cardiac hypertrophy. Mol. Cell. Biol. 2004, 24:6231-6240.
54. Sakamoto K., Zarrinpashneh E., Budas G.R., Pouleur A.C., Dutta A., Prescott A.R., Vanoverschelde J.L., Ashworth A., Jovanovic A., Alessi D.R., Bertrand L. Deficiency of LKB1 in heart prevents ischemia-mediated activation of AMPKalpha2 but not AMPKalpha1. Am. J. Physiol. Endocrinol. Metab. 2006, 290:E780-E788.
55. Russell R.R., Li J., Coven D.L., Pypaert M., Zechner C., Palmeri M., Giordano F.J., Mu J., Birnbaum M.J., Young L.H. AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. J. Clin. Invest. 2004, 114:495-503.
56. Saha A.K., Xu X.J., Lawson E., Deoliveira R., Brandon A.E., Kraegen E.W., Ruderman N.B. Downregulation of AMPK accompanies leucine- and glucose-induced increases in protein synthesis and insulin resistance in rat skeletal muscle. Diabetes 2010, 59:2426-2434.