Phosphorylation of phosphatidylinositol-3-kinase-protein kinase B and extracellular signal-regulated kinases 1/2 mediate reoxygenation-induced cardioprotection during hypoxia

Experimental Biology and Medicine

Volumn 235, Issue 3, 2010, Pages 401-410

  Milano, Giuseppina ^a   Von Segesser, Ludwig K ^a   Morel, Sandrine ^b   Joncic, Ana ^a   Bianciardi, Paola ^c   Vassalli, Giuseppe ^a,d   Samaja, Michele ^c  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c UNIVERSITY OF MILAN   (Italy)

^d DIVISION OF CARDIOLOGY   (Switzerland)

Author keywords

Chronic hypoxia; Hypoxic preconditioning; Ischemia reperfusion; Langendorff perfusion; LY 294002; PD 98059; Reoxygenation; UO 126

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; TETRAZOLIUM; UO 126;

AMBIENT AIR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; DISEASE MODEL; ENZYME ACTIVATION; HEART INFARCTION SIZE; HEART MUSCLE ISCHEMIA; HEART PERFUSION; HEART PROTECTION; HEART VENTRICLE ENDDIASTOLIC PRESSURE; IN VIVO STUDY; MALE; NONHUMAN; PROTEIN PHOSPHORYLATION; RAT; REOXYGENATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANOXIA; CHROMONES; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FLAVONOIDS; MALE; MORPHOLINES; OXYGEN; PERFUSION; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY;

RATTUS;

EID: 77950210575     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1258/ebm.2009.009153     Document Type: Article

References (34)

1. Milano G, Corno A, Lippa S, von Segesser L, Samaja M. Chronic and intermittent hypoxia induce different degrees of myocardial tolerance to hypoxia-induced dysfunction. Exp Biol Med 2002;227:389-397
2. +ATP channels. Exp Biol Med (Maywood) 2004;229:1196-1205
3. Morel S, Milano G, Ludunge KM, Corno AF, Samaja M, Fleury S, Bonny C, Kappenberger L, von Segesser LK, Vassalli G. Brief reoxygenation episodes during chronic hypoxia enhance posthypoxic recovery of LV function: role of mitogen-activated protein kinase signaling pathways. Basic Res Cardiol 2006;101:336-345
4. Bianciardi P, Fantacci M, Caretti A, Ronchi R, Milano G, Morel S, von Segesser L, Corno A, Samaja M. Chronic in vivo hypoxia in various organs: hypoxia-inducible factor-1alpha and apoptosis. Biochem Biophys Res Commun 2006;342:875-880
5. Corno AF, Milano G, Morel S, Tozzi P, Genton CY, Samaja M, von Segesser LK. Hypoxia: unique myocardial morphology? J Thorac Cardiovasc Surg 2004;127:1301-1308
6. Hausenloy DJ, Yellon DM. New directions for protecting the heart against ischaemia-reperfusion injury: targeting the reperfusion injury salvage kinase (RISK)-pathway. Cardiovasc Res 2004;61:448-460
7. + when the Griess reaction is used to assay for nitrate. Anal Biochem 1995;224:502-508
8. Darling CE, Jiang R, Maynard M, Whittaker P, Vinten-Johansen J, Przyklenk K. Postconditioning via stuttering reperfusion limits myocardial infarct size in rabbit hearts: role of ERK1/2. Am J Physiol Heart Circ Physiol 2005;289:H1618-26
9. Duncia JV, Santella JB III, Higley CA, Pitts WJ, Wityak J, Frietze WE, Rankin FW, Sun JH, Earl RA, Tabaka AC, Teleha CA, Blom KF, Favata MF, Manos EJ, Daulerio AJ, Stradley DA, Horiuchi K, Copeland RA, Scherle PA, Trzaskos JM, Magolda RL, Trainor GL, Wexler RR, Hobbs FW, Olson RE. MEK inhibitors: the chemistry and biological activity of U0126, its analogs, and cyclization products. Bioorg Med Chem Lett 1998;8:2839-2844
10. Bailey DM, Davies B, Young IS. Intermittent hypoxic training: implications for lipid peroxidation induced by acute normoxic exercise in active men. Clin Sci (Lond) 2001;101:465-475
11. Mukherjee S, Lekli I, Das M, Azzi A, Das DK. Cardioprotection with alpha-tocopheryl phosphate: Amelioration of myocardial ischemia reperfusion injury is linked with its ability to generate a survival signal through Akt activation. Biochim Biophys Acta 2008;1782:498-503
12. Milano G, Corno AF, Lippa S, Von Segesser LK, Samaja M. Chronic and intermittent hypoxia induce different degrees of myocardial tolerance to hypoxia-induced dysfunction. Exp Biol Med (Maywood) 2002;227:389-397
13. Mik EG, Ince C, Eerbeek O, Heinen A, Stap J, Hooibrink B, Schumacher CA, Balestra GM, Johannes T, Beek JF, Nieuwenhuis AF, van Horssen P, Spaan JA, Zuurbier CJ. Mitochondrial oxygen tension within the heart. J Mol Cell Cardiol 2009;46:943-951
14. Stenslokken KO, Rutkovskiy A, Kaljusto ML, Hafstad AD, Larsen TS, Vaage J. Inadvertent phosphorylation of survival kinases in isolated perfused hearts: a word of caution. Basic Res Cardiol 2009;104:412-423
15. Manalo DJ, Rowan A, Lavoie T, Natarajan L, Kelly BD, Ye SQ, Garcia JG, Semenza GL. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood 2005;105:659-669
16. Caretti A, Morel S, Milano G, Fantacci M, Bianciardi P, Ronchi R, Vassalli G, von Segesser LK, Samaja M. Heart HIF-1alpha and MAP kinases during hypoxia: are they associated in vivo? Exp Biol Med (Maywood) 2007;232:887-894
17. Martinive P, Defresne F, Quaghebeur E, Daneau G, Crokart N, Gregoire V, Gallez B, Dessy C, Feron O. Impact of cyclic hypoxia on HIF-1alpha regulation in endothelial cells - new insights for anti-tumor treatments. FEBS J 2009;276:509-518
18. Lee SD, Kuo WW, Lin JA, Chu YF, Wang CK, Yeh YL, Wang SG, Liu JY, Chang MH, Huang CY. Effects of long-term intermittent hypoxia on mitochondrial and Fas death receptor dependent apoptotic pathways in rat hearts. Int J Cardiol 2006;116:348-356
19. Xu D, Patten RD, Force T, Kyriakis JM. Gene 33/RALT is induced by hypoxia in cardiomyocytes, where it promotes cell death by suppressing phosphatidylinositol 3-kinase and extracellular signal-regulated kinase survival signaling. Mol Cell Biol 2006;26:5043-5054
20. Kwon DS, Kwon CH, Kim JH, Woo JS, Jung JS, Kim YK. Signal transduction of MEK/ERK and PI3K/Akt activation by hypoxia/reoxygenation in renal epithelial cells. Eur J Cell Biol 2006;85:1189-1199
21. Miki T, Miura T, Tanno M, Nishihara M, Naitoh K, Sato T, Takahashi A, Shimamoto K. Impairment of cardioprotective PI3K-Akt signaling by post-infarct ventricular remodeling is compensated by an ERK-mediated pathway. Basic Res Cardiol 2007;102:163-170
22. 2 prosurvival effects in cultured endothelial cells. FASEB J 2006;20:1501-1503
23. Uchiyama T, Engelman RM, Maulik N, Das DK. Role of Akt signaling in mitochondrial survival pathway triggered by hypoxic preconditioning. Circulation 2004;109:3042-3049
24. Budisavljevic MN, Hodge L, Barber K, Fulmer JR, Durazo-Arvizu RA, Self SE, Kuhlmann M, Raymond JR, Greene EL. Oxidative stress in the pathogenesis of experimental mesangial proliferative glomerulonephritis. Am J Physiol Renal Physiol 2003;285:F1138-48
25. Wang X, McCullough KD, Franke TF, Holbrook NJ. Epidermal growth factor receptor-dependent Akt activation by oxidative stress enhances cell survival. J Biol Chem 2000;275:14624-14631
26. Shao Z, Bhattacharya K, Hsich E, Park L, Walters B, Germann U, Wang YM, Kyriakis J, Mohanlal R, Kuida K, Namchuk M, Salituro F, Yao YM, Hou WM, Chen X, Aronovitz M, Tsichlis PN, Bhattacharya S, Force T, Kilter H. c-Jun N-terminal kinases mediate reactivation of Akt and cardiomyocyte survival after hypoxic injury in vitro and in vivo. Circ Res 2006;98:111-118
27. Kilic E, Kilic U, Soliz J, Bassetti CL, Gassmann M, Hermann DM. Brain-derived erythropoietin protects from focal cerebral ischemia by dual activation of ERK-1/-2 and Akt pathways. FASEB J 2005;19:2026-2028
28. Ravingerova T, Matejikova J, Neckar J, Andelova E, Kolar F. Differential role of PI3K/Akt pathway in the infarct size limitation and antiarrhythmic protection in the rat heart. Mol Cell Biochem 2007;297:111-120
29. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999;399:601-605
30. Caretti A, Bianciardi P, Ronchi R, Fantacci M, Guazzi M, Samaja M. Phosphodiesterase-5 inhibition abolishes neuron apoptosis induced by chronic hypoxia independently of hypoxia-inducible factor-1alpha signaling. Exp Biol Med (Maywood) 2008;233:1222-1230
31. Nagy N, Shiroto K, Malik G, Huang CK, Gaestel M, Abdellatif M, Tosaki A, Maulik N, Das DK. Ischemic preconditioning involves dual cardio-protective axes with p38MAPK as upstream target. J Mol Cell Cardiol 2007;42:981-990
32. Oudit GY, Sun H, Kerfant BG, Crackower MA, Penninger JM, Backx PH. The role of phosphoinositide-3 kinase and PTEN in cardiovascular physiology and disease. J Mol Cell Cardiol 2004;37:449-471
33. Hu Y, Chen X, Pan TT, Neo KL, Lee SW, Khin ES, Moore PK, Bian JS. Cardioprotection induced by hydrogen sulfide preconditioning involves activation of ERK and PI3K/Akt pathways. Pflugers Arch 2008;455:607-616
34. Schulz R, Belosjorow S, Gres P, Jansen J, Michel MC, Heusch G. p38 MAP kinase is a mediator of ischemic preconditioning in pigs. Cardiovasc Res 2002;55:690-700