Role of PI3K in myocardial ischaemic preconditioning: mapping pro-survival cascades at the trigger phase and at reperfusion

Journal of Cellular and Molecular Medicine

Volumn 22, Issue 2, 2018, Pages 926-935

  Rossello, Xavier ^a   Riquelme, Jaime A ^a,b   Davidson, Sean M ^a   Yellon, Derek M ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CHILE   (Chile)

Author keywords

cardioprotection; ischaemia reperfusion injury; ischaemic preconditioning; RISK pathway; SAFE pathway

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; STAT3 PROTEIN; WORTMANNIN; PROTEIN KINASE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEART INFARCTION PREVENTION; HEART INFARCTION SIZE; HEART MUSCLE REPERFUSION; ISOLATED HEART; MALE; MOUSE; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; NONHUMAN; PI3K/AKT SIGNALING; PROTEIN ANALYSIS; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; METABOLISM; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SURVIVAL ANALYSIS;

ANIMALS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GLYCOGEN SYNTHASE KINASE 3 BETA; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MALE; MICE, INBRED C57BL; MYOCARDIAL REPERFUSION INJURY; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; SURVIVAL ANALYSIS;

EID: 85040973020     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/jcmm.13394     Document Type: Article

References (42)

1. Ibáñez B, Heusch G, Ovize M, et al. Evolving therapies for myocardial ischemia/reperfusion injury. J Am Coll Cardiol. 2015; 65: 1454–71.
2. Hausenloy DJ, Garcia-Dorado D, Bøtker HE, et al. Novel targets and future strategies for acute cardioprotection: position Paper of the European Society of Cardiology Working Group on Cellular Biology of the Heart. Cardiovasc Res. 2017; 113: 564–85.
3. Murry CE, Jennings RB, Reimer KA. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation. 1986; 74: 1124–36.
4. Hausenloy DJ, Barrabes JA, Botker HE, et al. Ischaemic conditioning and targeting reperfusion injury: a 30 year voyage of discovery. Basic Res Cardiol. 2016; 111: 70. https://www.ncbi.nlm.nih.gov/pubmed/27766474
5. Bromage DI, Pickard JMJ, Rossello X, et al. Remote ischaemic conditioning reduces infarct size in animal in vivo models of ischaemia-reperfusion injury: a systematic review and meta-analysis. Cardiovasc Res. 2016; 113: 288–97.
6. Yellon DM, Alkhulaifi AM, Pugsley WB. Preconditioning the human myocardium. Lancet. 1993; 342: 276–7.
7. Hausenloy DJ, Yellon DM. Ischaemic conditioning and reperfusion injury. Nat Rev Cardiol. 2016; 13: 193–209.
8. Hausenloy DJ, Yellon DM. Preconditioning and postconditioning: united at reperfusion. Pharmacol Ther. 2007; 116: 173–91.
9. Lecour S, Suleman N, Deuchar GA, et al. Pharmacological preconditioning with tumor necrosis factor-alpha activates signal transducer and activator of transcription-3 at reperfusion without involving classic prosurvival kinases (Akt and extracellular signal-regulated kinase). Circulation. 2005; 112: 3911–8.
10. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007; 357: 1121–35.
11. Kunuthur SP, Mocanu MM, Hemmings BA, et al. The Akt1 isoform is an essential mediator of ischaemic preconditioning. J Cell Mol Med. 2012; 16: 1739–49.
12. Hausenloy DJ, Mocanu MM, Yellon DM. Cross-talk between the survival kinases during early reperfusion: its contribution to ischemic preconditioning. Cardiovasc Res. 2004; 63: 305–12.
13. Suleman N, Somers S, Smith R, et al. Dual activation of STAT-3 and Akt is required during the trigger phase of ischaemic preconditioning. Cardiovasc Res. 2008; 79: 127–33.
14. Somers SJ, Frias M, Lacerda L, et al. Interplay between SAFE and RISK pathways in sphingosine-1-phosphate-induced cardioprotection. Cardiovasc Drugs Ther. 2012; 26: 227–37.
15. Mocanu MM, Bell RM, Yellon DM. PI3 kinase and not p42/p44 appears to be implicated in the protection conferred by ischemic preconditioning. J Mol Cell Cardiol. 2002; 34: 661–8.
16. Rossello X, Hall AR, Bell RM, et al. Characterization of the langendorff perfused isolated mouse heart model of global ischemia-reperfusion injury: impact of ischemia and reperfusion length on infarct size and LDH release. J Cardiovasc Pharmacol Ther. 2015; 21: 286–95.
17. Rossello X, Burke N, Stoppe C, et al. Exogenous administration of recombinant MIF at physiological concentrations failed to attenuate infarct size in a langendorff perfused isolated mouse heart model. Cardiovasc Drugs Ther. 2016; 30: 445–53.
18. Jonassen AK, Sack MN, Mjøs OD, et al. Myocardial protection by insulin at reperfusion requires early administration and is mediated via Akt and p70s6 kinase cell-survival signaling. Circ Res. 2001; 89: 1191–8.
19. Hausenloy DJ, Duchen MR, Yellon DM. Inhibiting mitochondrial permeability transition pore opening at reperfusion protects against ischaemia-reperfusion injury. Cardiovasc Res. 2003; 60: 617–25.
20. Hausenloy DJ, Tsang A, Mocanu MM, et al. Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol Heart Circ Physiol. 2005; 288: H971–6.
21. Curtis MJ, Bond RA, Spina D, et al. Experimental design and analysis and their reporting: new guidance for publication in BJP. Br J Pharmacol. 2015; 172: 3461–71.
22. Klein HH, Puschmann S, Schaper J, et al. Vircho archiv a the mechanism of the tetrazolium reaction in identifying experimental myocardial infarction. Virchows Arch. 1981; 393: 287–97.
23. Nishino Y, Webb IG, Davidson SM, et al. Glycogen synthase kinase-3 inactivation is not required for ischemic preconditioning or postconditioning in the mouse. Circ Res. 2008; 103: 307–14.
24. Mocanu MM, Yellon DM. PTEN, the Achilles’ heel of myocardial ischaemia/reperfusion injury? Br J Pharmacol. 2007; 150: 833–8.
25. Oudit GY, Penninger JM. Cardiac regulation by phosphoinositide 3-kinases and PTEN. Cardiovasc Res. 2009; 82: 250–60.
26. Heusch G, Musiolik J, Kottenberg E, et al. STAT5 activation and cardioprotection by remote ischemic preconditioning in humans novelty and significance. Circ Res. 2012; 110: 111–5.
27. Yellon DM, Downey JM. Preconditioning the myocardium : from cellular physiology to clinical cardiology. Physiol Rev. 2003; 83: 1113–51.
28. Solenkova NV, Solodushko V, Cohen MV, et al. Endogenous adenosine protects preconditioned heart during early minutes of reperfusion by activating Akt. Am J Physiol Heart Circ Physiol. 2006; 290: H441–9.
29. Heusch G. Molecular basis of cardioprotection: signal transduction in ischemic pre-, post-, and remote conditioning. Circ Res. 2015; 116: 674–99.
30. Davidson SM, Hausenloy D, Duchen MR, et al. Signalling via the reperfusion injury signalling kinase (RISK) pathway links closure of the mitochondrial permeability transition pore to cardioprotection. Int J Biochem Cell Biol. 2006; 38: 414–9.
31. Datta K, Bellacosa A, Chan TO, et al. Akt is a direct target of the phosphatidylinositol 3-kinase. Activation by growth factors, v-src and v-Ha-ras, in Sf9 and mammalian cells. J Biol Chem. 1996; 271: 30835–9.
32. Tong H, Imahashi K, Steenbergen C, et al. Phosphorylation of glycogen synthase kinase-3beta during preconditioning through a phosphatidylinositol-3-kinase–dependent pathway is cardioprotective. Circ Res. 2002; 90: 377–9.
33. Juhaszova M, Zorov DB, Kim S-H, et al. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest. 2004; 113: 1535–49.
34. Fan WJ, Vuuren D, Genade S, et al. Kinases and phosphatases in ischaemic preconditioning: a re-evaluation. Basic Res Cardiol. 2010; 105: 495–511.
35. Cai Z, Semenza GL. PTEN activity is modulated during ischemia and reperfusion: involvement in the induction and decay of preconditioning. Circ Res. 2005; 97: 1351–9.
36. Mensah K, Mocanu MM, Yellon DM. Failure to protect the myocardium against ischemia/reperfusion injury after chronic atorvastatin treatment is recaptured by acute atorvastatin treatment: a potential role for phosphatase and tensin homolog deleted on chromosome ten? J Am Coll Cardiol. 2005; 45: 1287–91.
37. Ruan H, Li J, Ren S, et al. Inducible and cardiac specific PTEN inactivation protects ischemia/reperfusion injury. J Mol Cell Cardiol. 2009; 46: 193–200.
38. Siddall HK, Warrell CE, Yellon DM, et al. Ischemia-reperfusion injury and cardioprotection: investigating PTEN, the phosphatase that negatively regulates PI3K, using a congenital model of PTEN haploinsufficiency. Basic Res Cardiol. 2008; 103: 560–8.
39. Boengler K, Hilfiker-Kleiner D, Heusch G, et al. Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res Cardiol. 2010; 105: 771–85.
40. Pfeffer LM, Mullersman JE, Pfeffer SR, et al. STAT3 as an adapter to couple phosphatidylinositol 3-kinase to the IFNAR1 chain of the type I interferon receptor. Science. 1997; 276: 1418–20.
41. Zhang X, Shan P, Alam J, et al. Carbon monoxide differentially modulates STAT1 and STAT3 and inhibits apoptosis via a phosphatidylinositol 3-kinase/Akt and p38 kinase-dependent STAT3 pathway during anoxia-reoxygenation injury. J Biol Chem. 2005; 280: 8714–21.
42. Stensløkken K-O, Rutkovskiy A, Kaljusto M-L, et al. Inadvertent phosphorylation of survival kinases in isolated perfused hearts: a word of caution. Basic Res Cardiol. 2009; 104: 412–23.