Involvement of Cyclophilin D and calcium in isoflurane-induced preconditioning

Anesthesiology

Volumn 123, Issue 6, 2015, Pages 1374-1384

  Teixeira, Geoffrey ^a   Chiari, Pascal ^a,b   Fauconnier, Jeremy ^c   Abrial, Maryline ^a   Couture Lepetit, Elisabeth ^a   Harisseh, Rania ^a   Pillot, Bruno ^a   Lacampagne, Alain ^c   Tourneur, Yves ^a   Gharib, Abdallah ^a   Ovize, Michel ^a,b  

^a UNIVERSITÉ LYON 1   (France)

^b LOUIS PRADEL HOSPITAL   (France)

^c INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLOPHILIN D; CYCLOSPORIN A; ISOFLURANE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); ROTENONE; CALCIUM; CYCLOPHILIN; INHALATION ANESTHETIC AGENT;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; HEART INFARCTION SIZE; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART PROTECTION; ION TRANSPORT; MALE; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL MEMBRANE POTENTIAL; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REOXYGENATION; REPERFUSION INJURY; SARCOPLASMIC RETICULUM; ANIMAL; DRUG EFFECTS; HEART INFARCTION PREVENTION; KNOCKOUT MOUSE; METABOLISM; PATHOPHYSIOLOGY;

ANESTHETICS, INHALATION; ANIMALS; CALCIUM; CYCLOPHILINS; ELECTRON TRANSPORT COMPLEX I; ISCHEMIC PRECONDITIONING, MYOCARDIAL; ISOFLURANE; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MYOCARDIAL REPERFUSION INJURY;

EID: 84947487337     PISSN: 00033022     EISSN: 15281175     Source Type: Journal    
DOI: 10.1097/ALN.0000000000000876     Document Type: Article

References (49)

1. Hillis LD, Smith PK, Anderson JL, Bittl JA, Bridges CR, Byrne JG, Cigarroa JE, Disesa VJ, Hiratzka LF, Hutter AM Jr, Jessen ME, Keeley EC, Lahey SJ, Lange RA, London MJ, Mack MJ, Patel MR, Puskas JD, Sabik JF, Selnes O, Shahian DM, Trost JC, Winniford MD, 2011 ACCF/AHA Guideline for Coronary Artery Bypass Graft Surgery: A report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. Circulation 2011 124 e652 735
2. Fleisher LA, Beckman JA, Brown KA, Calkins H, Chaikof E, Fleischmann KE, Freeman WK, Froehlich JB, Kasper EK, Kersten JR, Riegel B, Robb JF, Smith SC Jr, Jacobs AK, Adams CD, Anderson JL, Antman EM, Buller CE, Creager MA, Ettinger SM, Faxon DP, Fuster V, Halperin JL, Hiratzka LF, Hunt SA, Lytle BW, Nishimura R, Ornato JP, Page RL, Tarkington LG, Yancy CW, ACC/AHA 2007 guidelines on perioperative cardiovascular evaluation and care for noncardiac surgery: A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the 2002 Guidelines on Perioperative Cardiovascular Evaluation for Noncardiac Surgery): Developed in collaboration with the American Society of Echocardiography, American Society of Nuclear Cardiology, Heart Rhythm Society, Society of Cardiovascular Anesthesiologists, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, and Society for Vascular Surgery. Circulation 2007 116 1971 96
3. Crompton M, Andreeva L, On the involvement of a mitochondrial pore in reperfusion injury. Basic Res Cardiol 1993 88 513 23
4. Di Lisa F, Carpi A, Giorgio V, Bernardi P, The mitochondrial permeability transition pore and cyclophilin D in cardioprotection. Biochim Biophys Acta 2011 1813 1316 22
5. Halestrap AP, Pasdois P, The role of the mitochondrial permeability transition pore in heart disease. Biochim Biophys Acta 2009 1787 1402 15
6. Zorov DB, Juhaszova M, Yaniv Y, Nuss HB, Wang S, Sollott SJ, Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovasc Res 2009 83 213 25
7. Halestrap AP, Calcium, mitochondria and reperfusion injury: A pore way to die. Biochem Soc Trans 2006 34 (pt 2) 232 7
8. Baines CP, Kaiser RA, Purcell NH, Blair NS, Osinska H, Hambleton MA, Brunskill EW, Sayen MR, Gottlieb RA, Dorn GW, Robbins J, Molkentin JD, Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005 434 658 62
9. Gomez L, Paillard M, Thibault H, Derumeaux G, Ovize M, Inhibition of GSK3beta by postconditioning is required to prevent opening of the mitochondrial permeability transition pore during reperfusion. Circulation 2008 117 2761 8
10. Skyschally A, Schulz R, Heusch G, Cyclosporine A at reperfusion reduces infarct size in pigs. Cardiovasc Drugs Ther 2010 24 85 7
11. Piot C, Croisille P, Staat P, Thibault H, Rioufol G, Mewton N, Elbelghiti R, Cung TT, Bonnefoy E, Angoulvant D, Macia C, Raczka F, Sportouch C, Gahide G, Finet G, André-Fouët X, Revel D, Kirkorian G, Monassier JP, Derumeaux G, Ovize M, Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 2008 359 473 81
12. Chiari P, Angoulvant D, Mewton N, Desebbe O, Obadia JF, Robin J, Farhat F, Jegaden O, Bastien O, Lehot JJ, Ovize M, Cyclosporine protects the heart during aortic valve surgery. A nesthesiology 2014 121 232 8
13. Ruiz-Meana M, Fernandez-Sanz C, Garcia-Dorado D, The SR-mitochondria interaction: A new player in cardiac pathophysiology. Cardiovasc Res 2010 88 30 9
14. Abdallah Y, Kasseckert SA, Iraqi W, Said M, Shahzad T, Erdogan A, Neuhof C, Gündüz D, Schlüter KD, Tillmanns H, Piper HM, Reusch HP, Ladilov Y, Interplay between Ca2+ cycling and mitochondrial permeability transition pores promotes reperfusion-induced injury of cardiac myocytes. J Cell Mol Med 2011 15 2478 85
15. Yaniv Y, Spurgeon HA, Lyashkov AE, Yang D, Ziman BD, Maltsev VA, Lakatta EG, Crosstalk between mitochondrial and sarcoplasmic reticulum Ca2+ cycling modulates cardiac pacemaker cell automaticity. PLoS One 2012 7 e37582
16. Teixeira G, Abrial M, Portier K, Chiari P, Couture-Lepetit E, Tourneur Y, Ovize M, Gharib A, Synergistic protective effect of cyclosporin A and rotenone against hypoxia-reoxygenation in cardiomyocytes. J Mol Cell Cardiol 2013 56 55 62
17. Kersten JR, Orth KG, Pagel PS, Mei DA, Gross GJ, Warltier DC, Role of adenosine in isoflurane-induced cardioprotection. A nesthesiology 1997 86 1128 39
18. Chiari PC, Bienengraeber MW, Pagel PS, Krolikowski JG, Kersten JR, Warltier DC, Isoflurane protects against myocardial infarction during early reperfusion by activation of phosphatidylinositol-3-kinase signal transduction: Evidence for anesthetic-induced postconditioning in rabbits. A nesthesiology 2005 102 102 9
19. Tanaka K, Ludwig LM, Kersten JR, Pagel PS, Warltier DC, Mechanisms of cardioprotection by volatile anesthetics. A nesthesiology 2004 100 707 21
20. Landoni G, Greco T, Biondi-Zoccai G, Nigro Neto C, Febres D, Pintaudi M, Pasin L, Cabrini L, Finco G, Zangrillo A, Anaesthetic drugs and survival: A Bayesian network meta-analysis of randomized trials in cardiac surgery. Br J Anaesth 2013 111 886 96
21. Hanley PJ, ter Keurs HE, Cannell MB, Excitation-contraction coupling in the heart and the negative inotropic action of volatile anesthetics. A nesthesiology 2004 101 999 1014
22. Hannon JD, Cody MJ, Effects of volatile anesthetics on sarcolemmal calcium transport and sarcoplasmic reticulum calcium content in isolated myocytes. A nesthesiology 2002 96 1457 64
23. Tampo A, Hogan CS, Sedlic F, Bosnjak ZJ, Kwok WM, Accelerated inactivation of cardiac L-type calcium channels triggered by anaesthetic-induced preconditioning. Br J Pharmacol 2009 156 432 43
24. Hanley PJ, Ray J, Brandt U, Daut J, Halothane, isoflurane and sevoflurane inhibit NADH:ubiquinone oxidoreductase (complex I) of cardiac mitochondria. J Physiol 2002 544 (pt 3) 687 93
25. Hirata N, Shim YH, Pravdic D, Lohr NL, Pratt PF Jr, Weihrauch D, Kersten JR, Warltier DC, Bosnjak ZJ, Bienengraeber M, Isoflurane differentially modulates mitochondrial reactive oxygen species production via forward versus reverse electron transport flow: Implications for preconditioning. A nesthesiology 2011 115 531 40
26. De Paulis D, Chiari P, Teixeira G, Couture-Lepetit E, Abrial M, Argaud L, Gharib A, Ovize M, Cyclosporine A at reperfusion fails to reduce infarct size in the in vivo rat heart. Basic Res Cardiol 2013 108 379
27. Schinzel AC, Takeuchi O, Huang Z, Fisher JK, Zhou Z, Rubens J, Hetz C, Danial NN, Moskowitz MA, Korsmeyer SJ, Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci USA 2005 102 12005 10
28. Obame FN, Plin-Mercier C, Assaly R, Zini R, Dubois-Randé JL, Berdeaux A, Morin D, Cardioprotective effect of morphine and a blocker of glycogen synthase kinase 3 beta, SB216763 [3-(2,4-dichlorophenyl)-4(1-methyl-1H-indol-3-yl)-1H-pyrrole-2,5-dione], via inhibition of the mitochondrial permeability transition pore. J Pharmacol Exp Ther 2008 326 252 8
29. Janicki PK, Erskine WA, James MF, High-performance liquid chromatographic method for the direct determination of the volatile anaesthetics halothane, isoflurane and enflurane in water and in physiological buffer solutions. J Chromatogr 1990 518 250 3
30. Schaller S, Paradis S, Ngoh GA, Assaly R, Buisson B, Drouot C, Ostuni MA, Lacapere JJ, Bassissi F, Bordet T, Berdeaux A, Jones SP, Morin D, Pruss RM, TRO40303, a new cardioprotective compound, inhibits mitochondrial permeability transition. J Pharmacol Exp Ther 2010 333 696 706
31. Maack C, Cortassa S, Aon MA, Ganesan AN, Liu T, O'Rourke B, Elevated cytosolic Na+ decreases mitochondrial Ca2+ uptake during excitation-contraction coupling and impairs energetic adaptation in cardiac myocytes. Circ Res 2006 99 172 82
32. Fauconnier J, Lacampagne A, Rauzier JM, Vassort G, Richard S, Ca2+-dependent reduction of IK1 in rat ventricular cells: A novel paradigm for arrhythmia in heart failure? Cardiovasc Res 2005 68 204 12
33. Halestrap AP, Clarke SJ, Javadov SA, Mitochondrial permeability transition pore opening during myocardial reperfusion-A target for cardioprotection. Cardiovasc Res 2004 61 372 85
34. Ruiz-Meana M, Inserte J, Fernandez-Sanz C, Hernando V, Miro-Casas E, Barba I, Garcia-Dorado D, The role of mitochondrial permeability transition in reperfusion-induced cardiomyocyte death depends on the duration of ischemia. Basic Res Cardiol 2011 106 1259 68
35. Lemasters JJ, Theruvath TP, Zhong Z, Nieminen AL, Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta 2009 1787 1395 401
36. Ruiz-Meana M, Abellán A, Miró-Casas E, Garcia-Dorado D, Opening of mitochondrial permeability transition pore induces hypercontracture in Ca2+ overloaded cardiac myocytes. Basic Res Cardiol 2007 102 542 52
37. Stadnicka A, Marinovic J, Ljubkovic M, Bienengraeber MW, Bosnjak ZJ, Volatile anesthetic-induced cardiac preconditioning. J Anesth 2007 21 212 9
38. Sedlic F, Sepac A, Pravdic D, Camara AK, Bienengraeber M, Brzezinska AK, Wakatsuki T, Bosnjak ZJ, Mitochondrial depolarization underlies delay in permeability transition by preconditioning with isoflurane: Roles of ROS and Ca2+. Am J Physiol Cell Physiol 2010 299 C506 15
39. Agarwal B, Stowe DF, Dash RK, Bosnjak ZJ, Camara AK, Mitochondrial targets for volatile anesthetics against cardiac ischemia-reperfusion injury. Front Physiol 2014 5 341
40. Li B, Chauvin C, De Paulis D, De Oliveira F, Gharib A, Vial G, Lablanche S, Leverve X, Bernardi P, Ovize M, Fontaine E, Inhibition of complex I regulates the mitochondrial permeability transition through a phosphate-sensitive inhibitory site masked by cyclophilin D. Biochim Biophys Acta 2012 1817 1628 34
41. Ludwig LM, Tanaka K, Eells JT, Weihrauch D, Pagel PS, Kersten JR, Warltier DC, Preconditioning by isoflurane is mediated by reactive oxygen species generated from mitochondrial electron transport chain complex III. Anesth Analg 2004 99 1308 15
42. Agarwal B, Camara AK, Stowe DF, Bosnjak ZJ, Dash RK, Enhanced charge-independent mitochondrial free Ca(2+) and attenuated ADP-induced NADH oxidation by isoflurane: Implications for cardioprotection. Biochim Biophys Acta 2012 1817 453 65
43. Agarwal B, Dash RK, Stowe DF, Bosnjak ZJ, Camara AK, Isoflurane modulates cardiac mitochondrial bioenergetics by selectively attenuating respiratory complexes. Biochim Biophys Acta 2014 1837 354 65
44. Ljubkovic M, Mio Y, Marinovic J, Stadnicka A, Warltier DC, Bosnjak ZJ, Bienengraeber M, Isoflurane preconditioning uncouples mitochondria and protects against hypoxia-reoxygenation. Am J Physiol Cell Physiol 2007 292 C1583 90
45. Davies LA, Gibson CN, Boyett MR, Hopkins PM, Harrison SM, Effects of isoflurane, sevoflurane, and halothane on myofilament Ca2+ sensitivity and sarcoplasmic reticulum Ca2+ release in rat ventricular myocytes. A nesthesiology 2000 93 1034 44
46. Terentyev D, Viatchenko-Karpinski S, Gyorke I, Terentyeva R, Gyorke S, Protein phosphatases decrease sarcoplasmic reticulum calcium content by stimulating calcium release in cardiac myocytes. J Physiol 2003 552 (pt 1) 109 18
47. Piper HM, Abdallah Y, Kasseckert S, Schlüter KD, Sarcoplasmic reticulum-mitochondrial interaction in the mechanism of acute reperfusion injury. Viewpoint. Cardiovasc Res 2008 77 234 6
48. Paillard M, Tubbs E, Thiebaut PA, Gomez L, Fauconnier J, Da Silva CC, Teixeira G, Mewton N, Belaidi E, Durand A, Abrial M, Lacampagne A, Rieusset J, Ovize M, Depressing mitochondria-reticulum interactions protects cardiomyocytes from lethal hypoxia-reoxygenation injury. Circulation 2013 128 1555 65
49. Elrod JW, Wong R, Mishra S, Vagnozzi RJ, Sakthievel B, Goonasekera SA, Karch J, Gabel S, Farber J, Force T, Brown JH, Murphy E, Molkentin JD, Cyclophilin D controls mitochondrial pore-dependent Ca(2+) exchange, metabolic flexibility, and propensity for heart failure in mice. J Clin Invest 2010 120 3680 7