Acute hyperglycemia abolishes cardioprotection by remote ischemic perconditioning

Cardiovascular Diabetology

Volumn 14, Issue 1, 2015, Pages

  Baranyai, Tamás ^a   Nagy, Csilla Terézia ^a   Koncsos, Gábor ^a   Onódi, Zsófia ^a   Károlyi Szabó, Melinda ^a   Makkos, András ^a   Varga, Zoltán V ^a   Ferdinandy, Péter ^a,b   Giricz, Zoltán ^a,b  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b PHARMAHUNGARY GROUP   (Hungary)

Author keywords

Acute hyperglycemia; Autophagy; Ischemia reperfusion injury; Nitrosative stress; Remote ischemic conditioning

Indexed keywords

BECLIN 1; MAMMALIAN TARGET OF RAPAMYCIN; MEMBRANE PROTEIN; PROTEIN ATG7; PROTEIN KINASE B; PROTEIN P62; PROTEIN S6; PROTEIN ULK1; UNCLASSIFIED DRUG; 3-NITROTYROSINE; APOPTOSIS REGULATORY PROTEIN; ATG7 PROTEIN, RAT; AUTOPHAGY RELATED PROTEIN 7; BECN1 PROTEIN, RAT; HEAT SHOCK PROTEIN; SEQUESTOSOME 1; SERINE THREONINE PROTEIN KINASE ULK1; SIGNAL PEPTIDE; SQSTM1 PROTEIN, RAT; TARGET OF RAPAMYCIN KINASE; TYROSINE; UBIQUITIN PROTEIN LIGASE; ULK1 PROTEIN, RAT;

ACUTE DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; BLOOD VESSEL OCCLUSION; CARDIOVASCULAR FUNCTION; CONTROLLED STUDY; CORONARY ARTERY OCCLUSION; DETERIORATION; DISEASE DURATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; FEMORAL ARTERY OCCLUSION; FEMORAL VEIN OCCLUSION; GLUCOSE BLOOD LEVEL; HEART ARRHYTHMIA; HEART INFARCTION SIZE; HEART PROTECTION; HEART RATE; HYPERGLYCEMIA; IMMUNOBLOTTING; LEFT ANTERIOR DESCENDING CORONARY ARTERY; MALE; MEAN ARTERIAL PRESSURE; NITRATIVE STRESS; NONHUMAN; OSMOLARITY; PROTEIN TARGETING; RAT; REMOTE ISCHEMIC PERCONDITIONING; REPERFUSION; ANALOGS AND DERIVATIVES; ANIMAL; ARRHYTHMIAS, CARDIAC; COMPLICATION; HEART INFARCTION; HEART INFARCTION PREVENTION; METABOLISM; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; PATHOLOGY; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; WISTAR RAT;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; ARRHYTHMIAS, CARDIAC; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 7; AUTOPHAGY-RELATED PROTEIN-1 HOMOLOG; BECLIN-1; HEAT-SHOCK PROTEINS; HYPERGLYCEMIA; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; SEQUESTOSOME-1 PROTEIN; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TOR SERINE-THREONINE KINASES; TYROSINE; UBIQUITIN-ACTIVATING ENZYMES;

EID: 84947573799     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/s12933-015-0313-1     Document Type: Article

References (52)

1. Heusch G, Botker HE, Przyklenk K, Redington A, Yellon D. Remote ischemic conditioning. J Am Coll Cardiol. 2015;65(2):177-95. doi: 10.1016/j.jacc.2014.10.031.
2. Ferdinandy P, Hausenloy DJ, Heusch G, Baxter GF, Schulz R. Interaction of risk factors, comorbidities, and comedications with ischemia/reperfusion injury and cardioprotection by preconditioning, postconditioning, and remote conditioning. Pharmacol Rev. 2014;66(4):1142-74. doi: 10.1124/pr.113.008300.
3. Gaspar A, Leite-Moreira AF. Remote cardiac ischemic conditioning: underlying mechanisms and clinical applications. Revista portuguesa de cirurgia cardio-toracica e vascular: orgao oficial da Sociedade Portuguesa de Cirurgia Cardio-Toracica e Vasc. 2012;19(4):183-90.
4. Xu J, Sun S, Lu X, Hu X, Yang M, Tang W. Remote ischemic pre- and postconditioning improve postresuscitation myocardial and cerebral function in a rat model of cardiac arrest and resuscitation. Crit Care Med. 2015;43(1):e12-8. doi: 10.1097/CCM.0000000000000684.
5. Hausenloy DJ, Candilio L, Evans R, Ariti C, Jenkins DP, Kolvekar S, et al. Remote ischemic preconditioning and outcomes of cardiac surgery. New Engl J Med. 2015;373(15):1408-17. doi: 10.1056/NEJMoa1413534.
6. Salie R, Huisamen B, Lochner A. High carbohydrate and high fat diets protect the heart against ischaemia/reperfusion injury. Cardiovasc Diabetol. 2014;13:109. doi: 10.1186/s12933-014-0109-8.
7. Hausenloy DJ, Whittington HJ, Wynne AM, Begum SS, Theodorou L, Riksen N, et al. Dipeptidyl peptidase-4 inhibitors and GLP-1 reduce myocardial infarct size in a glucose-dependent manner. Cardiovasc Diabetol. 2013;12:154. doi: 10.1186/1475-2840-12-154.
8. Kiss A, Tratsiakovich Y, Gonon AT, Fedotovskaya O, Lanner JT, Andersson DC, et al. The role of arginase and rho kinase in cardioprotection from remote ischemic perconditioning in non-diabetic and diabetic rat in vivo. PLoS One. 2014;9(8):e104731. doi: 10.1371/journal.pone.0104731.
9. Xu X, Zhou Y, Luo S, Zhang W, Zhao Y, Yu M, et al. Effect of remote ischemic preconditioning in the elderly patients with coronary artery disease with diabetes mellitus undergoing elective drug-eluting stent implantation. Angiology. 2014;65(8):660-6. doi: 10.1177/0003319713507332.
10. Wei CH, Litwin SE. Hyperglycemia and adverse outcomes in acute coronary syndromes: is serum glucose the provocateur or innocent bystander? Diabetes. 2014;63(7):2209-12. doi: 10.2337/db14-0571.
11. Timmer JR, Hoekstra M, Nijsten MW, van der Horst IC, Ottervanger JP, Slingerland RJ, et al. Prognostic value of admission glycosylated hemoglobin and glucose in nondiabetic patients with ST-segment-elevation myocardial infarction treated with percutaneous coronary intervention. Circulation. 2011;124(6):704-11. doi: 10.1161/CIRCULATIONAHA.110.985911.
12. Kehl F, Krolikowski JG, Mraovic B, Pagel PS, Warltier DC, Kersten JR. Hyperglycemia prevents isoflurane-induced preconditioning against myocardial infarction. Anesthesiology. 2002;96(1):183-8.
13. Kersten JR, Schmeling TJ, Orth KG, Pagel PS, Warltier DC. Acute hyperglycemia abolishes ischemic preconditioning in vivo. Am J Physiol. 1998;275(2 Pt 2):H721-5.
14. Clarke SJ, McCormick LM, Dutka DP. Optimising cardioprotection during myocardial ischaemia: targeting potential intracellular pathways with glucagon-like peptide-1. Cardiovasc Diabetol. 2014;13:12. doi: 10.1186/1475-2840-13-12.
15. Gottlieb RA, Finley KD, Mentzer RM Jr. Cardioprotection requires taking out the trash. Basic Res Cardiol. 2009;104(2):169-80. doi: 10.1007/s00395-009-0011-9.
16. Godar RJ, Ma X, Liu H, Murphy JT, Weinheimer CJ, Kovacs A, et al. Repetitive stimulation of autophagy-lysosome machinery by intermittent fasting preconditions the myocardium to ischemia-reperfusion injury. Autophagy. 2015;11(9):1537-60. doi: 10.1080/15548627.2015.1063768.
17. Van der Mieren G, Nevelsteen I, Vanderper A, Oosterlinck W, Flameng W, Herijgers P. Angiotensin-converting enzyme inhibition and food restriction restore delayed preconditioning in diabetic mice. Cardiovasc Diabetol. 2013;12:36. doi: 10.1186/1475-2840-12-36.
18. Giricz Z, Gorbe A, Pipis J, Burley DS, Ferdinandy P, Baxter GF. Hyperlipidaemia induced by a high-cholesterol diet leads to the deterioration of guanosine-3',5'-cyclic monophosphate/protein kinase G-dependent cardioprotection in rats. Br J Pharmacol. 2009;158(6):1495-502. doi: 10.1111/j.1476-5381.2009.00424.x.
19. Curtis MJ, Walker MJ. Quantification of arrhythmias using scoring systems: an examination of seven scores in an in vivo model of regional myocardial ischaemia. Cardiovasc Res. 1988;22(9):656-65.
20. Matsuo T, Izumori K. Effects of dietary D-psicose on diurnal variation in plasma glucose and insulin concentrations of rats. Biosci Biotechnol Biochem. 2006;70(9):2081-5.
21. Sciarretta S, Volpe M, Sadoshima J. Mammalian target of rapamycin signaling in cardiac physiology and disease. Circ Res. 2014;114(3):549-64. doi: 10.1161/CIRCRESAHA.114.302022.
22. Sloth AD, Schmidt MR, Munk K, Schmidt M, Pedersen L, Sorensen HT, et al. Impact of cardiovascular risk factors and medication use on the efficacy of remote ischaemic conditioning: post hoc subgroup analysis of a randomised controlled trial. BMJ Open. 2015;5(4):e006923. doi: 10.1136/bmjopen-2014-006923.
23. Mapanga RF, Joseph D, Symington B, Garson KL, Kimar C, Kelly-Laubscher R, et al. Detrimental effects of acute hyperglycaemia on the rat heart. Acta Physiol. 2014;210(3):546-64. doi: 10.1111/apha.12184.
24. Schmidt MR, Stottrup NB, Contractor H, Hyldebrandt JA, Johannsen M, Pedersen CM, et al. Remote ischemic preconditioning with-but not without-metabolic support protects the neonatal porcine heart against ischemia-reperfusion injury. Int J Cardiol. 2014;170(3):388-93. doi: 10.1016/j.ijcard.2013.11.020.
25. Kersten JR, Montgomery MW, Ghassemi T, Gross ER, Toller WG, Pagel PS, et al. Diabetes and hyperglycemia impair activation of mitochondrial K(ATP) channels. Am J Physiol Heart Circ Physiol. 2001;280(4):H1744-50.
26. Raphael J, Gozal Y, Navot N, Zuo Z. Hyperglycemia inhibits anesthetic-induced postconditioning in the rabbit heart via modulation of phosphatidylinositol-3-kinase/Akt and endothelial nitric oxide synthase signaling. J Cardiovasc Pharmacol. 2010;55(4):348-57. doi: 10.1097/FJC.0b013e3181d26583.
27. Weber NC, Goletz C, Huhn R, Grueber Y, Preckel B, Schlack W, et al. Blockade of anaesthetic-induced preconditioning in the hyperglycaemic myocardium: the regulation of different mitogen-activated protein kinases. Eur J Pharmacol. 2008;592(1-3):48-54. doi: 10.1016/j.ejphar.2008.07.010.
28. Alburquerque-Bejar JJ, Barba I, Inserte J, Miro-Casas E, Ruiz-Meana M, Poncelas M, et al. Combination therapy with remote ischaemic conditioning and insulin or exenatide enhances infarct size limitation in pigs. Cardiovasc Res. 2015;107(2):246-54. doi: 10.1093/cvr/cvv171.
29. Li H, Liu Z, Wang J, Wong GT, Cheung CW, Zhang L, et al. Susceptibility to myocardial ischemia reperfusion injury at early stage of type 1 diabetes in rats. Cardiovasc Diabetol. 2013;12:133. doi: 10.1186/1475-2840-12-133.
30. Ferdinandy P, Szilvassy Z, Horvath LI, Csont T, Csonka C, Nagy E, et al. Loss of pacing-induced preconditioning in rat hearts: role of nitric oxide and cholesterol-enriched diet. J Mol Cell Cardiol. 1997;29(12):3321-33. doi: 10.1006/jmcc.1997.0557.
31. Gorbe A, Varga ZV, Kupai K, Bencsik P, Kocsis GF, Csont T, et al. Cholesterol diet leads to attenuation of ischemic preconditioning-induced cardiac protection: the role of connexin 43. Am J Physiol Heart Circ Physiol. 2011;300(5):H1907-13. doi: 10.1152/ajpheart.01242.2010.
32. Giricz Z, Lalu MM, Csonka C, Bencsik P, Schulz R, Ferdinandy P. Hyperlipidemia attenuates the infarct size-limiting effect of ischemic preconditioning: role of matrix metalloproteinase-2 inhibition. J Pharmacol Exp Ther. 2006;316(1):154-61. doi: 10.1124/jpet.105.091140.
33. Ceriello A, Quagliaro L, D'Amico M, Di Filippo C, Marfella R, Nappo F, et al. Acute hyperglycemia induces nitrotyrosine formation and apoptosis in perfused heart from rat. Diabetes. 2002;51(4):1076-82.
34. Varga ZV, Giricz Z, Liaudet L, Hasko G, Ferdinandy P, Pacher P. Interplay of oxidative, nitrosative/nitrative stress, inflammation, cell death and autophagy in diabetic cardiomyopathy. Biochim Biophys Acta. 2015;1852(2):232-42. doi: 10.1016/j.bbadis.2014.06.030.
35. Chen HH, Mekkaoui C, Cho H, Ngoy S, Marinelli B, Waterman P, et al. Fluorescence tomography of rapamycin-induced autophagy and cardioprotection in vivo. Circ Cardiovasc Imaging. 2013;6(3):441-7. doi: 10.1161/CIRCIMAGING.112.000074.
36. Sciarretta S, Zhai P, Shao D, Maejima Y, Robbins J, Volpe M, et al. Rheb is a critical regulator of autophagy during myocardial ischemia: pathophysiological implications in obesity and metabolic syndrome. Circulation. 2012;125(9):1134-46. doi: 10.1161/CIRCULATIONAHA.111.078212.
37. Rohailla S, Clarizia N, Sourour M, Sourour W, Gelber N, Wei C, et al. Acute, delayed and chronic remote ischemic conditioning is associated with downregulation of mTOR and enhanced autophagy signaling. PLoS One. 2014;9(10):e111291. doi: 10.1371/journal.pone.0111291.
38. Shafique E, Choy WC, Liu Y, Feng J, Cordeiro B, Lyra A, et al. Oxidative stress improves coronary endothelial function through activation of the pro-survival kinase AMPK. Aging. 2013;5(7):515-30.
39. Wei WB, Hu X, Zhuang XD, Liao LZ, Li WD. GYY4137, a novel hydrogen sulfide-releasing molecule, likely protects against high glucose-induced cytotoxicity by activation of the AMPK/mTOR signal pathway in H9c2 cells. Mol Cell Biochem. 2014;389(1-2):249-56. doi: 10.1007/s11010-013-1946-6.
40. Yeshao W, Gu J, Peng X, Nairn AC, Nadler JL. Elevated glucose activates protein synthesis in cultured cardiac myocytes. Metab Clin Exp. 2005;54(11):1453-60. doi: 10.1016/j.metabol.2005.05.010.
41. Heusch G. Molecular basis of cardioprotection: signal transduction in ischemic pre-, post-, and remote conditioning. Circ Res. 2015;116(4):674-99. doi: 10.1161/CIRCRESAHA.116.305348.
42. Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K. Akt promotes survival of cardiomyocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation. 2000;101(6):660-7.
43. Matsui T, Tao J, del Monte F, Lee KH, Li L, Picard M, et al. Akt activation preserves cardiac function and prevents injury after transient cardiac ischemia in vivo. Circulation. 2001;104(3):330-5.
44. Moreira JB, Wohlwend M, Alves MN, Wisloff U, Bye A. A small molecule activator of AKT does not reduce ischemic injury of the rat heart. J Transl Med. 2015;13:76. doi: 10.1186/s12967-015-0444-x.
45. 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(4):H1580-6. doi: 10.1152/ajpheart.00379.2008.
46. Cook SA, Matsui T, Li L, Rosenzweig A. Transcriptional effects of chronic Akt activation in the heart. J Biol Chem. 2002;277(25):22528-33. doi: 10.1074/jbc.M201462200.
47. Fullmer TM, Pei S, Zhu Y, Sloan C, Manzanares R, Henrie B, et al. Insulin suppresses ischemic preconditioning-mediated cardioprotection through Akt-dependent mechanisms. J Mol Cell Cardiol. 2013;64:20-9. doi: 10.1016/j.yjmcc.2013.08.005.
48. Dibble CC, Cantley LC. Regulation of mTORC1 by PI3 K signaling. Trends Cell Biol. 2015;25(9):545-55. doi: 10.1016/j.tcb.2015.06.002.
49. Varma S, Lal BK, Zheng R, Breslin JW, Saito S, Pappas PJ, et al. Hyperglycemia alters PI3 k and Akt signaling and leads to endothelial cell proliferative dysfunction. Am J Physiol Heart Circ Physiol. 2005;289(4):H1744-51. doi: 10.1152/ajpheart.01088.2004.
50. Gross ER, Hsu AK, Gross GJ. Diabetes abolishes morphine-induced cardioprotection via multiple pathways upstream of glycogen synthase kinase-3beta. Diabetes. 2007;56(1):127-36. doi: 10.2337/db06-0907.
51. Huang C, Yitzhaki S, Perry CN, Liu W, Giricz Z, Mentzer RM Jr, et al. Autophagy induced by ischemic preconditioning is essential for cardioprotection. J Cardiovasc Transl Res. 2010;3(4):365-73. doi: 10.1007/s12265-010-9189-3.
52. Giricz Z, Mentzer RM Jr, Gottlieb RA. Autophagy, myocardial protection, and the metabolic syndrome. J Cardiovasc Pharmacol. 2012;60(2):125-32. doi: 10.1097/FJC.0b013e318256ce10.