Insulin suppresses ischemic preconditioning-mediated cardioprotection through Akt-dependent mechanisms

Journal of Molecular and Cellular Cardiology

Volumn 64, Issue , 2013, Pages 20-29

  Fullmer, Tanner M ^a   Pei, Shaobo ^a   Zhu, Yi ^a   Sloan, Crystal ^a   Manzanares, Robert ^a   Henrie, Brandon ^a   Pires, Karla M ^a   Cox, James E ^a   Abel, E Dale ^a   Boudina, Sihem ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

Cardioprotection; Insulin; Insulin signaling; Ischemia; Reperfusion

Indexed keywords

GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3BETA; INSULIN; INSULIN RECEPTOR; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EX VIVO STUDY; HEART INFARCTION SIZE; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PERFUSION; HEART PROTECTION; ISCHEMIC PRECONDITIONING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALIA; MUS;

CARDIOPROTECTION; INSULIN; INSULIN SIGNALING; ISCHEMIA; REPERFUSION;

ANIMALS; CARDIOTONIC AGENTS; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; INSULIN; ISCHEMIC PRECONDITIONING, MYOCARDIAL; LACTIC ACID; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASES; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 84884310168     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.08.005     Document Type: Article

References (51)

1. Kannel W.B., McGee D.L. Diabetes and cardiovascular disease. The Framingham Study. JAMA 1979, 241:2035-2038.
2. Turner R., Cull C., Holman R. United Kingdom Prospective Diabetes Study 17: a 9-year update of a randomized, controlled trial on the effect of improved metabolic control on complications in non-insulin-dependent diabetes mellitus. Ann Intern Med 1996, 124:136-145.
3. Aguilar D., Solomon S.D., Kober L., Rouleau J.L., Skali H., McMurray J.J., et al. Newly diagnosed and previously known diabetes mellitus and 1-year outcomes of acute myocardial infarction: the VALsartan In Acute myocardial iNfarcTion (VALIANT) trial. Circulation 2004, 110:1572-1578.
4. Stevens R.J., Coleman R.L., Adler A.I., Stratton I.M., Matthews D.R., Holman R.R. Risk factors for myocardial infarction case fatality and stroke case fatality in type 2 diabetes: UKPDS 66. Diabetes Care 2004, 27:201-207.
5. Edwards R.J., Saurin A.T., Rakhit R.D., Marber M.S. Therapeutic potential of ischaemic preconditioning. Br J Clin Pharmacol 2000, 50:87-97.
6. Yellon D.M., Downey J.M. Preconditioning the myocardium: from cellular physiology to clinical cardiology. Physiol Rev 2003, 83:1113-1151.
7. Kloner R.A., Rezkalla S.H. Preconditioning, postconditioning and their application to clinical cardiology. Cardiovasc Res 2006, 70:297-307.
8. Murry C.E., Jennings R.B., Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 1986, 74:1124-1136.
9. Vogt A.M., Htun P., Kluge A., Zimmermann R., Schaper W. Insulin-like growth factor-II delays myocardial infarction in experimental coronary artery occlusion. Cardiovasc Res 1997, 33:469-477.
10. Jonassen A.K., Sack M.N., Mjos O.D., Yellon D.M. Myocardial protection by insulin at reperfusion requires early administration and is mediated via Akt and p70s6 kinase cell-survival signaling. Circ Res 2001, 89:1191-1198.
11. Fuglesteg B.N., Tiron C., Jonassen A.K., Mjos O.D., Ytrehus K. Pretreatment with insulin before ischaemia reduces infarct size in Langendorff-perfused rat hearts. Acta Physiol (Oxf) 2009, 195:273-282.
12. Peoples-Sheps M.D., Siegel E., Suchindran C.M., Origasa H., Ware A., Barakat A. Characteristics of maternal employment during pregnancy: effects on low birthweight. Am J Public Health 1991, 81:1007-1012.
13. Anselmino M., Ohrvik J., Malmberg K., Standl E., Ryden L. Glucose lowering treatment in patients with coronary artery disease is prognostically important not only in established but also in newly detected diabetes mellitus: a report from the Euro Heart Survey on Diabetes and the Heart. Eur Heart J 2008, 29:177-184.
14. Barmpouletos D., Stavens G., Ahlberg A.W., Katten D.M., O'Sullivan D.M., Heller G.V. Duration and type of therapy for diabetes: impact on cardiac risk stratification with stress electrocardiographic-gated SPECT myocardial perfusion imaging. J Nucl Cardiol 2010, 17:1041-1049.
15. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 1998, 352:837-853.
16. Mellbin L.G., Malmberg K., Norhammar A., Wedel H., Ryden L. The impact of glucose lowering treatment on long-term prognosis in patients with type 2 diabetes and myocardial infarction: a report from the DIGAMI 2 trial. Eur Heart J 2008, 29:166-176.
17. Bouhidel O., Pons S., Souktani R., Zini R., Berdeaux A., Ghaleh B. Myocardial ischemic postconditioning against ischemia-reperfusion is impaired in ob/ob mice. Am J Physiol Heart Circ Physiol 2008, 295:H1580-H1586.
18. Cook S.A., Varela-Carver A., Mongillo M., Kleinert C., Khan M.T., Leccisotti L., et al. Abnormal myocardial insulin signalling in type 2 diabetes and left-ventricular dysfunction. Eur Heart J 2010, 31:100-111.
19. Shimizu I., Minamino T., Toko H., Okada S., Ikeda H., Yasuda N., et al. Excessive cardiac insulin signaling exacerbates systolic dysfunction induced by pressure overload in rodents. J Clin Invest 2010, 120:1506-1514.
20. Okamoto H., Nakae J., Kitamura T., Park B.C., Dragatsis I., Accili D. Transgenic rescue of insulin receptor-deficient mice. J Clin Invest 2004, 114:214-223.
21. Belke D.D., Betuing S., Tuttle M.J., Graveleau C., Young M.E., Pham M., et al. Insulin signaling coordinately regulates cardiac size, metabolism, and contractile protein isoform expression. J Clin Invest 2002, 109:629-639.
22. Shiojima I., Sato K., Izumiya Y., Schiekofer S., Ito M., Liao R., et al. Disruption of coordinated cardiac hypertrophy and angiogenesis contributes to the transition to heart failure. J Clin Invest 2005, 115:2108-2118.
23. Passonneau J.V., Lauderdale V.R. A comparison of three methods of glycogen measurement in tissues. Anal Biochem 1974, 60:405-412.
24. Tsang A., Hausenloy D.J., Mocanu M.M., Carr R.D., Yellon D.M. Preconditioning the diabetic heart: the importance of Akt phosphorylation. Diabetes 2005, 54:2360-2364.
25. Kunuthur S.P., Mocanu M.M., Hemmings B.A., Hausenloy D.J., Yellon D.M. The Akt1 isoform is an essential mediator of ischemic preconditioning. J Cell Mol Med 2011, 16:1739-1749.
26. Shioi T., McMullen J.R., Kang P.M., Douglas P.S., Obata T., Franke T.F., et al. Akt/protein kinase B promotes organ growth in transgenic mice. Mol Cell Biol 2002, 22:2799-2809.
27. Zhao Z.Q., Corvera J.S., Halkos M.E., Kerendi F., Wang N.P., Guyton R.A., et al. Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 2003, 285:H579-H588.
28. Tosaki A., Pali T., Droy-Lefaix M.T. Effects of Ginkgo biloba extract and preconditioning on the diabetic rat myocardium. Diabetologia 1996, 39:1255-1262.
29. Tosaki A., Engelman D.T., Engelman R.M., Das D.K. The evolution of diabetic response to ischemia/reperfusion and preconditioning in isolated working rat hearts. Cardiovasc Res 1996, 31:526-536.
30. Kersten J.R., Toller W.G., Gross E.R., Pagel P.S., Warltier D.C. Diabetes abolishes ischemic preconditioning: role of glucose, insulin, and osmolality. Am J Physiol Heart Circ Physiol 2000, 278:H1218-H1224.
31. Ravingerova T., Stetka R., Pancza D., Ulicna O., Ziegelhoffer A., Styk J. Susceptibility to ischemia-induced arrhythmias and the effect of preconditioning in the diabetic rat heart. Physiol Res 2000, 49:607-616.
32. Ghosh S., Standen N.B., Galinianes M. Failure to precondition pathological human myocardium. J Am Coll Cardiol 2001, 37:711-718.
33. Lee T.M., Chou T.F. Impairment of myocardial protection in type 2 diabetic patients. J Clin Endocrinol Metab 2003, 88:531-537.
34. Kristiansen S.B., Lofgren B., Stottrup N.B., Khatir D., Nielsen-Kudsk J.E., Nielsen T.T., et al. Ischaemic preconditioning does not protect the heart in obese and lean animal models of type 2 diabetes. Diabetologia 2004, 47:1716-1721.
35. Sivaraman V., Hausenloy D.J., Wynne A.M., Yellon D.M. Preconditioning the diabetic human myocardium. J Cell Mol Med 2010, 14:1740-1746.
36. Drenger B., Ostrovsky I.A., Barak M., Nechemia-Arbely Y., Ziv E., Axelrod J.H. Diabetes blockade of sevoflurane postconditioning is not restored by insulin in the rat heart: phosphorylated signal transducer and activator of transcription 3- and phosphatidylinositol 3-kinase-mediated inhibition. Anesthesiology 2011, 114:1364-1372.
37. Cleveland J.C., Meldrum D.R., Cain B.S., Banerjee A., Harken A.H. Oral sulfonylurea hypoglycemic agents prevent ischemic preconditioning in human myocardium. Two paradoxes revisited. Circulation 1997, 96:29-32.
38. Sena S., Hu P., Zhang D., Wang X., Wayment B., Olsen C., et al. Impaired insulin signaling accelerates cardiac mitochondrial dysfunction after myocardial infarction. J Mol Cell Cardiol 2009, 46:910-918.
39. Baines C.P., Wang L., Cohen M.V., Downey J.M. Myocardial protection by insulin is dependent on phosphatidylinositol 3-kinase but not protein kinase C or KATP channels in the isolated rabbit heart. Basic Res Cardiol 1999, 94:188-198.
40. Tong H., Imahashi K., Steenbergen C., Murphy E. Phosphorylation of glycogen synthase kinase-3beta during preconditioning through a phosphatidylinositol-3-kinase-dependent pathway is cardioprotective. Circ Res 2002, 90:377-379.
41. Vigneron F., Dos Santos P., Lemoine S., Bonnet M., Tariosse L., Couffinhal T., et al. GSK-3beta at the crossroads in the signalling of heart preconditioning: implication of mTOR and Wnt pathways. Cardiovasc Res 2011, 90:49-56.
42. Nishino Y., Webb I.G., Davidson S.M., Ahmed A.I., Clark J.E., Jacquet S., et al. Glycogen synthase kinase-3 inactivation is not required for ischemic preconditioning or postconditioning in the mouse. Circ Res 2008, 103:307-314.
43. Zhu Y., Pereira R.O., O'Neill B.T., Riehle C., Ilkun O., Wende A.R., et al. Cardiac PI3K-Akt impairs insulin-stimulated glucose uptake independent of mTORC1 and GLUT4 translocation. Mol Endocrinol 2013, 27:172-184.
44. Kunuthur S.P., Milliken P.H., Gibson C.L., Suckling C.J., Wadsworth R.M. Tetrahydrobiopterin analogues with NO-dependent pulmonary vasodilator properties. Eur J Pharmacol 2011, 650:371-377.
45. Hughes K., Nikolakaki E., Plyte S.E., Totty N.F., Woodgett J.R. Modulation of the glycogen synthase kinase-3 family by tyrosine phosphorylation. EMBO J 1993, 12:803-808.
46. Neely J.R., Grotyohann L.W. Role of glycolytic products in damage to ischemic myocardium. Dissociation of adenosine triphosphate levels and recovery of function of reperfused ischemic hearts. Circ Res 1984, 55:816-824.
47. Soares P.R., de Albuquerque C.P., Chacko V.P., Gerstenblith G., Weiss R.G. Role of preischemic glycogen depletion in the improvement of postischemic metabolic and contractile recovery of ischemia-preconditioned rat hearts. Circulation 1997, 96:975-983.
48. Depre C., Vanoverschelde J.L., Taegtmeyer H. Glucose for the heart. Circulation 1999, 99:578-588.
49. Moreno-Sanchez R., Hernandez-Esquivel L., Rivero-Segura N.A., Marin-Hernandez A., Neuzil J., Ralph S.J., et al. Reactive oxygen species are generated by the respiratory complex II-evidence for lack of contribution of the reverse electron flow in complex I. FEBS J 2013, 280:927-938.
50. Symons J.D., McMillin S.L., Riehle C., Tanner J., Palionyte M., Hillas E., et al. Contribution of insulin and Akt1 signaling to endothelial nitric oxide synthase in the regulation of endothelial function and blood pressure. Circ Res 2009, 104:1085-1094.
51. Liu B., el Alaoui-Talibi Z., Clanachan A.S., Schulz R., Lopaschuk G.D. Uncoupling of contractile function from mitochondrial TCA cycle activity and MVO2 during reperfusion of ischemic hearts. Am J Physiol 1996, 270:H72-H80.