Consecutive pharmacological activation of PKA and PKC mimics the potent cardioprotection of temperature preconditioning

Cardiovascular Research

Volumn 88, Issue 2, 2010, Pages 324-333

  Khaliulin, Igor ^a   Parker, Joanna E ^a   Halestrap, Andrew P ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Ischaemia; Mitochondria; Preconditioning; Protein kinase A; Protein kinase C

Indexed keywords

ADENOSINE; CHELERYTHRINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLYCOGEN; ISOPRENALINE; LACTATE DEHYDROGENASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PROTEIN KINASE C; SOTALOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; CONDITIONING; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME RELEASE; GLYCOGEN ANALYSIS; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; HEART PROTECTION; HEMODYNAMICS; ISOLATED HEART; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CARBONYLATION; RAT; SIGNAL TRANSDUCTION; TEMPERATURE;

ADENOSINE; ADRENERGIC BETA-AGONISTS; ADRENERGIC BETA-ANTAGONISTS; ANIMALS; CARDIOTONIC AGENTS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; ENZYME ACTIVATORS; GLYCOGEN; GLYCOGEN SYNTHASE KINASE 3; HEMODYNAMICS; ISOPROTERENOL; L-LACTATE DEHYDROGENASE; MALE; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; PERFUSION; PHOSPHORYLATION; PROTEIN CARBONYLATION; PROTEIN KINASE C; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; SIGNAL TRANSDUCTION; TEMPERATURE; TIME FACTORS; VENTRICULAR FUNCTION, LEFT;

EID: 77958112074     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq190     Document Type: Article

References (38)

1. Depre C, Taegtmeyer H. Metabolic aspects of programmed cell survival and cell death in the heart. Cardiovasc Res 2000;45:538-548.
2. Khaliulin I, Clarke SJ, Lin H, ParkerJE, Suleiman MS, Halestrap AP. Temperature pre-conditioning ofisolated rat hearts\a potent cardioprotective mechanism involving a reduction in oxidative stress and inhibition of the mitochondrial permeability tran-sition pore. J Physiol 2007;581:1147-1161.
3. Clarke SJ, Khaliulin I, Das M, ParkerJE, Heesom KJ, Halestrap AP. Inhibition of mito-chondrial permeability transition pore opening by ischemic preconditioning is prob-ably mediated by reduction of oxidative stress rather than mitochondrial protein phosphorylation. Circ Res 2008;102:1082-1090.
4. Lochner A, Genade S, Tromp E, Podzuweit T, Moolman JA. Ischemic preconditioning and the ß-adrenergic signal transduction pathway. Circulation 1999;100:958-966.
5. Yellon DM, Dana A. The preconditioning phenomenon: a tool for the scientist or a clinical reality? Circ Res 2000;87:543-550.
6. Javadov SA, Clarke S, Das M, Griffiths EJ, Lim KH, Halestrap AP. Ischaemic precondi-tioning inhibits opening of mitochondrial permeability transition pores in the reper-fused rat heart. J Physiol 2003;549:513-524.
7. Cohen MV, Downey JM. Adenosine: Trigger and mediator of cardioprotection. Basic Res Cardiol 2008;103:203-215.
8. Hausenloy DJ, Mocanu MM, Yellon DM. Cross-talk between the survival kinases during early reperfusion: its contribution to ischemic preconditioning. Cardiovasc Res 2004;63:305-312.
9. Passonneau JV, Lauderdale VR. A comparison ofthree methods of glycogen measure-ment in tissues. Anal Biochem 1974;60:405-412.
10. Khaliulin I, Schneider A, Houminer E, BormanJB, Schwalb H. Apomorphine prevents myocardial ischemia/reperfusion-induced oxidative stress in the rat heart. Free Radic Biol Med 2004;37:969-976.
11. Guérard NC, Traebert M, Suter W, Dumotier BM. Selective block of iks plays a sig-nificant role in map triangulation induced by ikr block in isolated rabbit heart. J Pharmacol Toxicol Methods 2008;58:32-40.
12. InserteJ, Garcia-Dorado D, Ruiz-Meana M, Agullo L, Pina P, Soler-Soler J. Ischemic preconditioning attenuates calpain-mediated degradation of structural proteins through a protein kinase A-dependent mechanism. Cardiovasc Res 2004;64:105-114.
13. +] sensitivity by moderate hypothermia in guinea pig isolated hearts. Am J Physiol Heart Circ Physiol 1999;277:H2321-H2332.
14. Brennan JP, Bardswell SC, Burgoyne Jr, Fuller W, Schroder E, Wait R et al. Oxidant-induced activation oftype I protein kinase A is mediated by RI subunit inter-protein disulfide bond formation. J Biol Chem 2006;281:21827- 21836.
15. CamaraAK, Riess ML, Kevin LG, Novalija E, Stowe DF. Hypothermia augments reactive oxygen species detected in the guinea pig isolated perfused heart. Am J Physiol Heart Circ Physiol 2004;286:H1289-H1299.
16. Asimakis GK, Inners-McBride K, Conti VR, Yang CJ. Transient beta adrenergic stimu-lation can precondition the rat heart against postischaemic contractile dysfunction. Cardiovasc Res 1994;28:1726-1734.
17. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H et al. The selectivity of protein kinase inhibitors: a further update. Biochem J 2007;408:297-315.
18. Murphy E. Primary and secondary signaling pathways in early preconditioning that converge on the mitochondria to produce cardioprotection. Circ Res 2004;94:7-16.
19. Heusch G. No risk, no..cardioprotection? A critical perspective. Cardiovasc Res 2009;84:173-175.
20. Krieg T, Qin Q, McIntosh EC, Cohen MV, Downey JM. Ach and adenosine activate pi3-kinase in rabbit hearts through transactivation of receptor tyrosine kinases. Am J Physiol Heart Circ Physiol 2002;283:H2322-H2330.
21. Fang N-X,Yao Y-T, Shi C-X, Li L-H. Attenuation of ischemia-reperfusion injurybysevo-flurane postconditioning involves protein kinase B and glycogen synthase kinase 3 beta activation in isolated rat hearts. Mol Biol Rep;doi: 10.1007/s11033-010-0030-5. Published online ahead ofprint 10 March 2010.
22. Neely Jr, Grotyohann LW. Role ofglycolytic products in damage to ischemic myo-cardium. Dissociation of adenosine triphosphate levels and recovery of function of reperfused ischemic hearts. Circ Res 1984;55:816-824.
23. Cross HR, Opie LH, Radda GK, Clarke K. Isa high glycogen content beneficialor detri-mental to the ischemic rat heart? A controversy resolved. Circ Res 1996;78:482-491.
24. Halestrap AP, Pasdois P. The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta 2009;1787:1402-1415.
25. El-Ani D,Zimlichman R, Mashiach Y, Shainberg A. Adenosine and TNF-α exert similar inotropic effect on heart cultures, suggesting a cardioprotective mechanism against hypoxia. Life Sci 2007;81:803-813.
26. Nagasaka S, Katoh H, Niu CF, Matsui S, Urushida T, Satoh H et al. Protein kinase A catalytic subunit alters cardiac mitochondrial redox state and membrane potential via the formation of reactive oxygen species. Circ J 2007;71:429-436.
27. Wallukat G. The ß-adrenergic receptors. Herz 2002;27:683-690.
28. Novalija E, Kevin LG, Camara AK, Bosnjak ZJ, Kampine JP, Stowe DF. Reactive oxygen species precede the epsilon isoform of protein kinase c in the anesthetic precondi-tioning signaling cascade. Anesthesiology 2003;99:421-428.
29. + and delay of ischemia-induced electrical uncoupling in preconditioned rabbit ventricular myo-cardium. Cardiovasc Res 1999;44:101-112.
30. Townsend PA, Davidson SM, Clarke SJ, Khaliulin I, Carroll CJ, Scarabelli TM et al. Uro-cortin prevents mitochondrial permeability transition in response to reperfusion injury indirectly by reducing oxidative stress. Am J Physiol Heart Circ Physiol 2007; 293:H928-H938.
31. Baines CP, Song C-X,Zheng Y-T, Wang G-W, ZhangJ,Wang O-L et al. Protein kinase Cε interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 2003;92:873-880.
32. +-dependent cell survival and death. Mol Cell 2009;33:377-388.
33. Malhotra A, Begley R, Kang BPS, Rana I, Liu J, Yang G et al. PKC-ε-dependent survival signals in diabetic hearts. Am J Physiol Heart Circ Physiol 2005;289:H1343-H1350.
34. Prpic V, Spencer TL, Bygrave FL. Stable enhancement of calcium retention in mito-chondria isolated from rat liver after the administration of glucagon to the intact animal. Biochem J 1978;176:705-714.
35. Taylor WM, Prpic V, Exton JH, Bygrave FL. Stable changes to calcium fluxes in mito-chondria isolated from rat livers perfused with alpha-adrenergic agonists and with glu-cagon. Biochem J 1980;188:443-450.
36. Hughes BP, Barritt GJ. Effects of glucagon and N6O2′- dibutyryladenosine 3′:5′-cyclic monophosphate on calcium transport in isolated rat liver mitochondria. Biochem J 1978;176:295-304.
37. Armston AE, Halestrap AP. Glucagon treatment of rats inhibits the accumulation of lysophospholipids by liver mitochondria during preparation and subsequent incu-bation. Biosci Rep 1984;4:903-908.
38. Van Kuijk FJGM, Sevanian A, Handelman GJ, Dratz EA. A new role for phospholipase A2: protection of membranes from peroxidation damage. Trends Biochem Sci 1987;12: 31-34.