Cyclosporine A at reperfusion fails to reduce infarct size in the in vivo rat heart

Basic Research in Cardiology

Volumn 108, Issue 5, 2013, Pages

  De Paulis, Damien ^a   Chiari, Pascal ^a,b   Teixeira, Geoffrey ^a   Couture Lepetit, Elisabeth ^a   Abrial, Maryline ^a   Argaud, Laurent ^a,c   Gharib, Abdallah ^a   Ovize, Michel ^a,b  

^a UNIVERSITÉ LYON 1   (France)

^b LOUIS PRADEL HOSPITAL   (France)

^c EDOUARD HERRIOT HOSPITAL   (France)

Author keywords

Complex I; Cyclophilin D; MPTP; Postconditioning; Preconditioning

Indexed keywords

CYCLOSPORIN A; HYDROGEN PEROXIDE; ISOFLURANE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE);

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HEART HEMODYNAMICS; HEART INFARCTION; HEART INFARCTION SIZE; HEART PROTECTION; IN VIVO STUDY; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; MALE; MITOCHONDRIAL PERMEABILITY; NONHUMAN; OXIDATIVE PHOSPHORYLATION; RAT; REPERFUSION INJURY;

EID: 84881450484     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-013-0379-4     Document Type: Article

References (48)

1. Argaud L, Gateau-Roesch O, Muntean D, Chalabreysse L, Loufouat J, Robert D, Ovize M (2005) Specific inhibition of the mitochondrial permeability transition prevents lethal reperfusion injury. J Mol Cell Cardiol 38:367-374. doi: 10.1016/j.yjmcc.2004.12.001 (Pubitemid 40215206)
2. Argaud L, Prigent AF, Chalabreysse L, Loufouat J, Lagarde M, Ovize M (2004) Ceramide in the antiapoptotic effect of ischemic preconditioning. Am J Physiol Heart Circ Physiol 286:H246-H251. doi: 10.1152/ajpheart.00638.2003
3. Bhayana V, Alto LE, Dhalla NS (1980) Effects of pentobarbital and pentothal on rat heart contractile force and oxidative phosphorylation activities. Gen Pharmacol 11:375-377 (Pubitemid 10076547)
4. Boengler K, Hilfiker-Kleiner D, Heusch G, Schulz R (2010) Inhibition of permeability transition pore opening by mitochondrial STAT3 and its role in myocardial ischemia/reperfusion. Basic Res Cardiol 105:771-785. doi: 10.1007/s00395-010-0124-1
5. Bopassa JC, Ferrera R, Gateau-Roesch O, Couture-Lepetit E, Ovize M (2006) PI 3-kinase regulates the mitochondrial transition pore in controlled reperfusion and postconditioning. Cardiovasc Res 69:178-185. doi: 10.1016/j.cardiores.2005.07.014 (Pubitemid 41814821)
6. Boveris A, Cadenas E (1975) Mitochondrial production of superoxide anions and its relationship to the antimycin insensitive respiration. FEBS Lett 54:311-314
7. Chen Q, Moghaddas S, Hoppel CL, Lesnefsky EJ (2006) Reversible blockade of electron transport during ischemia protects mitochondria and decreases myocardial injury following reperfusion. J Pharmacol Exp Ther 319:1405-1412. doi: 10.1124/jpet.106.110262
8. Chiari PC, Bienengraeber MW, Pagel PS, Krolikowski JG, Kersten JR, Warltier DC (2005) Isoflurane protects against myocardial infarction during early reperfusion by activation of phosphatidylinositol-3-kinase signal transduction: evidence for anesthetic-induced postconditioning in rabbits. Anesthesiology 102:102-109 (Pubitemid 40082846)
9. Dow J, Kloner RA (2007) Postconditioning does not reduce myocardial infarct size in an in vivo regional ischemia rodent model. J Cardiovasc Pharmacol Ther 12:153-163. doi: 10.1177/1074248407300897 (Pubitemid 46836328)
10. Fabiato A (1982) Calcium release in skinned cardiac cells: variations with species, tissues, and development. Fed Proc 41:2238-2244 (Pubitemid 12048931)
11. Fontaine E, Eriksson O, Ichas F, Bernardi P (1998) Regulation of the permeability transition pore in skeletal muscle mitochondria. Modulation by electron flow through the respiratory chain complex i. J Biol Chem 273:12662-12668 (Pubitemid 28240645)
12. Ge ZD, Pravdic D, Bienengraeber M, Pratt PF Jr, Auchampach JA, Gross GJ, Kersten JR, Warltier DC (2010) Isoflurane postconditioning protects against reperfusion injury by preventing mitochondrial permeability transition by an endothelial nitric oxide synthase-dependent mechanism. Anesthesiology 112:73-85. doi: 10.1097/ALN.0b013e3181c4a607
13. Gomez L, Paillard M, Price M, Chen Q, Teixeira G, Spiegel S, Lesnefsky EJ (2011) A novel role for mitochondrial sphingosine-1-phosphate produced by sphingosine kinase-2 in PTP-mediated cell survival during cardioprotection. Basic Res Cardiol 106:1341-1353. doi: 10.1007/s00395-011-0223-7
14. Gomez L, Thibault H, Gharib A, Dumont JM, Vuagniaux G, Scalfaro P, Derumeaux G, Ovize M (2007) Inhibition of mitochondrial permeability transition improves functional recovery and reduces mortality following acute myocardial infarction in mice. Am J Physiol Heart Circ Physiol 293:H1654-H1661. doi: 10.1152/ajpheart.01378.2006 (Pubitemid 47367212)
15. Hanley PJ, Ray J, Brandt U, Daut J (2002) Halothane, isoflurane and sevoflurane inhibit NADH:ubiquinone oxidoreductase (complex I) of cardiac mitochondria. J Physiol 544:687-693 (Pubitemid 35355950)
16. Hausenloy DJ, Lim SY, Ong SG, Davidson SM, Yellon DM (2010) Mitochondrial cyclophilin-D as a critical mediator of ischaemic preconditioning. Cardiovasc Res 88:67-74. doi: 10.1093/cvr/cvq113
17. Hausenloy DJ, Yellon DM (2007) Preconditioning and postconditioning: united at reperfusion. Pharmacol Ther 116:173-191. doi: 10.1016/j.pharmthera. 2007.06.005 (Pubitemid 47451505)
18. Heusch G, Boengler K, Schulz R (2008) Cardioprotection: nitric oxide, protein kinases, and mitochondria. Circulation 118:1915-1919. doi: 10.1161/CIRCULATIONAHA.108.805242
19. Heusch G, Boengler K, Schulz R (2010) Inhibition of mitochondrial permeability transition pore opening: the Holy Grail of cardioprotection. Basic Res Cardiol 105:151-154. doi: 10.1007/s00395-009-0080-9
20. Heusch G, Musiolik J, Gedik N, Skyschally A (2011) Mitochondrial STAT3 activation and cardioprotection by ischemic postconditioning in pigs with regional myocardial ischemia/reperfusion. Circ Res 109:1302-1308. doi: 10.1161/CIRCRESAHA.111.255604
21. Hirata N, Shim YH, Pravdic D, Lohr NL, Pratt PF Jr, Weihrauch D, Kersten JR, Warltier DC, Bosnjak ZJ, Bienengraeber M (2011) Isoflurane differentially modulates mitochondrial reactive oxygen species production via forward versus reverse electron transport flow: implications for preconditioning. Anesthesiology 115:531-540. doi: 10.1097/ALN.0b013e31822a2316
22. Ichas F, Mazat JP (1998) From calcium signaling to cell death: two conformations for the mitochondrial permeability transition pore. Switching from low- to high-conductance state. Biochim Biophys Acta 1366:33-50 (Pubitemid 28467021)
23. Iliodromitis EK, Georgiadis M, Cohen MV, Downey JM, Bofilis E, Kremastinos DT (2006) Protection from post-conditioning depends on the number of short ischemic insults in anesthetized pigs. Basic Res Cardiol 101:502-507. doi: 10.1007/s00395-006-0606-3 (Pubitemid 44637866)
24. Janssen M, van der Meer P, de Jong JW (1993) Antioxidant defences in rat, pig, guinea pig, and human hearts: comparison with xanthine oxidoreductase activity. Cardiovasc Res 27:2052-2057 (Pubitemid 23357353)
25. Kaljusto ML, Mori T, Mohammad Husain Rizvi S, Galagudza M, Frantzen ML, Valen G, Vaage J (2006) Postconditioning in rats and mice. Scand Cardiovasc J 40:334-341. doi: 10.1080/14017430601007587 (Pubitemid 44803885)
26. Kersten JR, Schmeling TJ, Pagel PS, Gross GJ, Warltier DC (1997) Isoflurane mimics ischemic preconditioning via activation of K(ATP) channels: reduction of myocardial infarct size with an acute memory phase. Anesthesiology 87:361-370 (Pubitemid 27435379)
27. Kin H, Zhao ZQ, Sun HY, Wang NP, Corvera JS, Halkos ME, Kerendi F, Guyton RA, Vinten-Johansen J (2004) Postconditioning attenuates myocardial ischemia-reperfusion injury by inhibiting events in the early minutes of reperfusion. Cardiovasc Res 62:74-85. doi: 10.1016/j.cardiores.2004.01.006 (Pubitemid 38326813)
28. Kottenberg E, Thielmann M, Bergmann L, Heine T, Jakob H, Heusch G, Peters J (2012) Protection by remote ischemic preconditioning during coronary artery bypass graft surgery with isoflurane but not propofol - a clinical trial. Acta Anaesthesiol Scand 56:30-38. doi: 10.1111/j.1399-6576.2011.02585.x
29. Kuznetsov AV, Veksler V, Gellerich FN, Saks V, Margreiter R, Kunz WS (2008) Analysis of mitochondrial function in situ in permeabilized muscle fibers, tissues and cells. Nat Protoc 3:965-976. doi: 10.1038/nprot.2008.61 (Pubitemid 351818685)
30. Li B, Chauvin C, De Paulis D, De Oliveira F, Gharib A, Vial G, Lablanche S, Leverve X, Bernardi P, Ovize M, Fontaine E (2012) Inhibition of complex I regulates the mitochondrial permeability transition through a phosphate-sensitive inhibitory site masked by cyclophilin D. Biochim Biophys Acta 1817:1628-1634. doi: 10.1016/j.bbabio.2012.05.011
31. Liu L, Zhu J, Brink PR, Glass PS, Rebecchi MJ (2011) Age-associated differences in the inhibition of mitochondrial permeability transition pore opening by cyclosporine A. Acta Anaesthesiol Scand 55:622-630. doi: 10.1111/j.1399-6576.2011.02421.x
32. Loschen G, Azzi A, Richter C, Flohe L (1974) Superoxide radicals as precursors of mitochondrial hydrogen peroxide. FEBS Lett 42:68-72
33. Paillard M, Gomez L, Augeul L, Loufouat J, Lesnefsky EJ, Ovize M (2009) Postconditioning inhibits mPTP opening independent of oxidative phosphorylation and membrane potential. J Mol Cell Cardiol 46:902-909. doi: 10.1016/j.yjmcc. 2009.02.017
34. 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, Andre-Fouet X, Revel D, Kirkorian G, Monassier JP, Derumeaux G, Ovize M (2008) Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 359:473-481. doi: 10.1056/NEJMoa071142
35. Piriou V, Chiari P, Gateau-Roesch O, Argaud L, Muntean D, Salles D, Loufouat J, Gueugniaud PY, Lehot JJ, Ovize M (2004) Desflurane-induced preconditioning alters calcium-induced mitochondrial permeability transition. Anesthesiology 100:581-588 (Pubitemid 38268876)
36. Pratt PF Jr, Wang C, Weihrauch D, Bienengraeber MW, Kersten JR, Pagel PS, Warltier DC (2006) Cardioprotection by volatile anesthetics: new applications for old drugs? Curr Opin Anaesthesiol 19:397-403. doi: 10.1097/01.aco. 0000236139.31099.b5 (Pubitemid 44048261)
37. Pravdic D, Sedlic F, Mio Y, Vladic N, Bienengraeber M, Bosnjak ZJ (2009) Anesthetic-induced preconditioning delays opening of mitochondrial permeability transition pore via protein kinase C-epsilon-mediated pathway. Anesthesiology 111:267-274. doi: 10.1097/ALN.0b013e3181a91957
38. Sedlic F, Pravdic D, Hirata N, Mio Y, Sepac A, Camara AK, Wakatsuki T, Bosnjak ZJ, Bienengraeber M (2010) Monitoring mitochondrial electron fluxes using NAD(P)H-flavoprotein fluorometry reveals complex action of isoflurane on cardiomyocytes. Biochim Biophys Acta 1797:1749-1758. doi: 10.1016/j.bbabio.2010. 07.009
39. Skyschally A, Schulz R, Heusch G (2010) Cyclosporine A at reperfusion reduces infarct size in pigs. Cardiovasc Drugs Ther 24:85-87. doi: 10.1007/s10557-010-6219-y
40. Skyschally A, van Caster P, Iliodromitis EK, Schulz R, Kremastinos DT, Heusch G (2009) Ischemic postconditioning: experimental models and protocol algorithms. Basic Res Cardiol 104:469-483. doi: 10.1007/s00395-009-0040-4
41. Staat P, Rioufol G, Piot C, Cottin Y, Cung TT, L'Huillier I, Aupetit JF, Bonnefoy E, Finet G, Andre-Fouet X, Ovize M (2005) Postconditioning the human heart. Circulation 112:2143-2148. doi: 10.1161/CIRCULATIONAHA.105.558122 (Pubitemid 41475808)
42. Stewart S, Lesnefsky EJ, Chen Q (2009) Reversible blockade of electron transport with amobarbital at the onset of reperfusion attenuates cardiac injury. Transl Res 153:224-231. doi: 10.1016/j.trsl.2009.02.003
43. Tanaka K, Weihrauch D, Kehl F, Ludwig LM, LaDisa JF Jr, Kersten JR, Pagel PS, Warltier DC (2002) Mechanism of preconditioning by isoflurane in rabbits: a direct role for reactive oxygen species. Anesthesiology 97:1485-1490 (Pubitemid 35417447)
44. Tang XL, Sato H, Tiwari S, Dawn B, Bi Q, Li Q, Shirk G, Bolli R (2006) Cardioprotection by postconditioning in conscious rats is limited to coronary occlusions <45 min. Am J Physiol Heart Circ Physiol 291:H2308-H2317. doi: 10.1152/ajpheart.00479.2006
45. Teixeira G, Abrial M, Portier K, Chiari P, Couture-Lepetit E, Tourneur Y, Ovize M, Gharib A (2013) Synergistic protective effect of cyclosporin A and rotenone against hypoxia-reoxygenation in cardiomyocytes. J Mol Cell Cardiol 56:55-62. doi: 10.1016/j.yjmcc.2012.11.023
46. Tsutsumi YM, Yokoyama T, Horikawa Y, Roth DM, Patel HH (2007) Reactive oxygen species trigger ischemic and pharmacological postconditioning: in vivo and in vitro characterization. Life Sci 81:1223-1227. doi: 10.1016/j.lfs.2007. 08.031 (Pubitemid 47513165)
47. Yellon DM, Hausenloy DJ (2007) Myocardial reperfusion injury. N Engl J Med 357:1121-1135. doi: 10.1056/NEJMra071667 (Pubitemid 47443217)
48. Zhao ZQ, Corvera JS, Halkos ME, Kerendi F, Wang NP, Guyton RA, Vinten-Johansen J (2003) Inhibition of myocardial injury by ischemic postconditioning during reperfusion: comparison with ischemic preconditioning. Am J Physiol Heart Circ Physiol 285:H579-H588. doi: 10.1152/ajpheart.01064.2002