Role of PI3Kα and sarcolemmal ATP-sensitive potassium channels in epoxyeicosatrienoic acid mediated cardioprotection

Journal of Molecular and Cellular Cardiology

Volumn 53, Issue 1, 2012, Pages 43-52

  Batchu, Sri N ^a   Chaudhary, Ketul R ^a   El Sikhry, Haitham ^a   Yang, Wei ^a   Light, Peter E ^a   Oudit, Gavin Y ^a   Seubert, John M ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

EET; PI3K and Ischemia Reperfusion; PmKATP channel

Indexed keywords

14,15 EPOXY 5,8,11 ICOSATRIENOIC ACID; 2 (4 HYDROXYPHENYL) 4 MORPHOLINOPYRIDO[3',2':4,5]FURO[3,2 D]PYRIMIDINE; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CALCINEURIN; CALCIUM; CASPASE 3; HEPOXILIN A; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR6.2; PHOSPHATIDYLINOSITOL 3 KINASE; WORTMANNIN;

ANIMAL CELL; ANIMAL TISSUE; ANOXIA; ARTICLE; CALCIUM CELL LEVEL; CELL PROTECTION; CONTROLLED STUDY; DENSITOMETRY; ENZYME ACTIVITY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; REOXYGENATION; REPERFUSION INJURY; TISSUE LEVEL;

8,11,14-EICOSATRIENOIC ACID; ANIMALS; ANOXIA; CALCIUM; CARDIOTONIC AGENTS; CELL LINE; CLASS IA PHOSPHATIDYLINOSITOL 3-KINASE; HEART; ISOENZYMES; KATP CHANNELS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; SARCOLEMMA;

MUS;

EID: 84861989657     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2012.04.008     Document Type: Article

References (40)

1. Saluja I., Song D., O'Regan M.H., Phillis J.W. Role of phospholipase A2 in the release of free fatty acids during ischemia-reperfusion in the rat cerebral cortex. Neurosci Lett 1997, 233:97-100.
2. Roman R.J. P-450 metabolites of arachidonic acid in the control of cardiovascular function. Physiol Rev 2002, 82:131-185.
3. Batchu S.N., Law E., Brocks D.R., Falck J.R., Seubert J.M. Epoxyeicosatrienoic acid prevents postischemic electrocardiogram abnormalities in an isolated heart model. J Mol Cell Cardiol 2009, 46:67-74.
4. Seubert J., Yang B., Bradbury J.A., Graves J., Degraff L.M., Gabel S., et al. Enhanced postischemic functional recovery in CYP2J2 transgenic hearts involves mitochondrial ATP-sensitive K+ channels and p42/p44 MAPK pathway. Circ Res 2004, 95:506-514.
5. Seubert J.M., Sinal C.J., Graves J., DeGraff L.M., Bradbury J.A., Lee C.R., et al. Role of soluble epoxide hydrolase in postischemic recovery of heart contractile function. Circ Res 2006, 99:442-450.
6. Dhanasekaran A., Gruenloh S.K., Buonaccorsi J.N., Zhang R., Gross G.J., Falck J.R., et al. Multiple antiapoptotic targets of the PI3K/Akt survival pathway are activated by epoxyeicosatrienoic acids to protect cardiomyocytes from hypoxia/anoxia. Am J Physiol Heart Circ Physiol 2008, 294:724-735.
7. Gross G.J., Hsu A., Falck J.R., Nithipatikom K. Mechanisms by which epoxyeicosatrienoic acids (EETs) elicit cardioprotection in rat hearts. J Mol Cell Cardiol 2007, 42:687-691.
8. Lu T., Hoshi T., Weintraub N.L., Spector A.A., Lee H.C. Activation of ATP-sensitive K(+) channels by epoxyeicosatrienoic acids in rat cardiac ventricular myocytes. J Physiol 2001, 537:811-827.
9. Gumina R.J., Pucar D., Bast P., Hodgson D.M., Kurtz C.E., Dzeja P.P., et al. Knockout of Kir6.2 negates ischemic preconditioning-induced protection of myocardial energetics. Am J Physiol Heart Circ Physiol 2003, 284:2106-2113.
10. Suzuki M., Sasaki N., Miki T., Sakamoto N., Ohmoto-Sekine Y., Tamagawa M., et al. Role of sarcolemmal K(ATP) channels in cardioprotection against ischemia/reperfusion injury in mice. J Clin Invest 2002, 194:509-516.
11. Baczko I., Giles W.R., Light P.E. Pharmacological activation of plasma-membrane KATP channels reduces reoxygenation-induced Ca(2+) overload in cardiac myocytes via modulation of the diastolic membrane potential. Br J Pharmacol 2004, 141:1059-1067.
12. Yao Z., Cavero I., Gross G.J. Activation of cardiac KATP channels: an endogenous protective mechanism during repetitive ischemia. Am J Physiol 1993, 264:495-504.
13. Cantley L.C. The phosphoinositide 3-kinase pathway. Science 2002, 296:1655-1657.
14. Oudit G.Y., Penninger J.M. Cardiac regulation by phosphoinositide 3-kinases and PTEN. Cardiovasc Res 2009, 82:250-260.
15. Plum L., Ma X., Hampel B., Balthasar N., Coppari R., Munzberg H., et al. Enhanced PIP3 signaling in POMC neurons causes KATP channel activation and leads to diet-sensitive obesity. J Clin Invest 2006, 116:1886-1901.
16. Yano N., Tseng A., Zhao T.C., Robbins J., Padbury J.F., Tseng Y.T. Temporally controlled overexpression of cardiac-specific PI3Kalpha induces enhanced myocardial contractility - a new transgenic model. Am J Physiol Heart Circ Physiol 2008, 295:1690-1694.
17. Ban K., Cooper A.J., Samuel S., Bhatti A., Patel M., Izumo S., et al. Phosphatidylinositol 3-kinase gamma is a critical mediator of myocardial ischemic and adenosine-mediated preconditioning. Circ Res 2008, 103:643-653.
18. Crackower M.A., Oudit G.Y., Kozieradzki I., Sarao R., Sun H., Sasaki T., et al. Regulation of myocardial contractility and cell size by distinct PI3K-PTEN signaling pathways. Cell 2002, 110:737-749.
19. Guo D., Kassiri Z., Basu R., Chow F.L., Kandalam V., Damilano F., et al. Loss of PI3Kgamma enhances cAMP-dependent MMP remodeling of the myocardial N-cadherin adhesion complexes and extracellular matrix in response to early biomechanical stress. Circ Res 2010, 107:1275-1289.
20. Batchu S., Lee S., Qadhi R., Chaudhary K., El-Sikhry H., Kodela R. Cardioprotective effect of a dual acting epoxyeicosatrienoic acid analogue towards ischaemia reperfusion injury. Br J Pharmacol 2010, 162:897-907.
21. Lakshmikuttyamma A., Selvakumar P., Kakkar R., Kanthan R., Wang R., Sharma R.K. Activation of calcineurin expression in ischemia-reperfused rat heart and in human ischemic myocardium. J Cell Biochem 2003, 90:987-997.
22. Wang H.G., Pathan N., Ethell I.M., Krajewski S., Yamaguchi Y., Shibasaki F., et al. Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 1999, 284:339-343.
23. Tahara S., Fukuda K., Kodama H., Kato T., Miyoshi S., Ogawa S. Potassium channel blocker activates extracellular signal-regulated kinases through Pyk2 and epidermal growth factor receptor in rat cardiomyocytes. J Am Coll Cardiol 2001, 38:1554-1563.
24. Hansson M.J., Mansson R., Morota S., Uchino H., Kallur T., Sumi T., et al. Calcium-induced generation of reactive oxygen species in brain mitochondria is mediated by permeability transition. Free Radic Biol Med 2008, 45:284-294.
25. Bodiga S., Zhang R., Jacobs D.E., Larsen B.T., Tampo A., Manthati V.L., et al. Protective actions of epoxyeicosatrienoic acid: dual targeting of cardiovascular PI3K and KATP channels. J Mol Cell Cardiol 2009, 46:978-988.
26. Katragadda D., Batchu S.N., Cho W.J., Chaudhary K.R., Falck J.R., Seubert J.M. Epoxyeicosatrienoic acids limit damage to mitochondrial function following stress in cardiac cells. J Mol Cell Cardiol 2009, 46:867-875.
27. Pretorius L., Owen K.L., McMullen J.R. Role of phosphoinositide 3-kinases in regulating cardiac function. Front Biosci 2009, 14:14. 2221-9.
28. Naga Prasad S.V., Esposito G., Mao L., Koch W.J., Rockman H.A. Gbetagamma-dependent phosphoinositide 3-kinase activation in hearts with in vivo pressure overload hypertrophy. J Biol Chem 2000, 275:4693-4698.
29. Vanhaesebroeck B., Leevers S.J., Ahmadi K., Timms J., Katso R., Driscoll P.C., et al. Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 2001, 70:535-602.
30. Alloatti G., Montrucchio G., Lembo G., Hirsch E. Phosphoinositide 3-kinase gamma: kinase-dependent and -independent activities in cardiovascular function and disease. Biochem Soc Trans 2004, 32:383-386.
31. Luo J., McMullen J.R., Sobkiw C.L., Zhang L., Dorfman A.L., Sherwood M.C., et al. Class IA phosphoinositide 3-kinase regulates heart size and physiological cardiac hypertrophy. Mol Cell Biol 2005, 25:9491-9502.
32. Braz J.C., Gill R.M., Corbly A.K., Jones B.D., Jin N., Vlahos C.J., et al. Selective activation of PI3Kalpha/Akt/GSK-3beta signalling and cardiac compensatory hypertrophy during recovery from heart failure. Eur J Heart Fail 2009, 11:739-748.
33. Fan Q.W., Weiss W.A. Isoform specific inhibitors of PI3 kinase in glioma. Cell Cycle 2006, 5:2301-2305.
34. Lu T., Ye D., Wang X., Seubert J.M., Graves J.P., Bradbury J.A., et al. Cardiac and vascular KATP channels in rats are activated by endogenous epoxyeicosatrienoic acids through different mechanisms. J Physiol 2006, 575:627-644.
35. Cukras C.A., Jeliazkova I., Nichols C.G. Structural and functional determinants of conserved lipid interaction domains of inward rectifying Kir6.2 channels. J Gen Physiol 2002, 119:581-591.
36. Hawkins P.T., Anderson K.E., Davidson K., Stephens L.R. Signalling through Class I PI3Ks in mammalian cells. Biochem Soc Trans 2006, 34:647-662.
37. Yuan T.L., Cantley L.C. PI3K pathway alterations in cancer: variations on a theme. Oncogene 2008, 27:5497-5510.
38. Lu T., VanRollins M., Lee H.C. Stereospecific activation of cardiac ATP-sensitive K(+) channels by epoxyeicosatrienoic acids: a structural determinant study. Mol Pharmacol 2002, 62:1076-1083.
39. Marinovic J., Ljubkovic M., Stadnicka A., Bosnjak Z.J., Bienengraeber M. Role of sarcolemmal ATP-sensitive potassium channel in oxidative stress-induced apoptosis: mitochondrial connection. Am J Physiol Heart Circ Physiol 2008, 294:1317-1325.
40. Hayabuchi Y., Willars G.B., Standen N.B., Davies N.W. Insulin-like growth factor-I inhibits rat arterial K(ATP) channels through pI 3-kinase. Biochem Biophys Res Commun 2008, 374:742-746.