Cyclosporine A normalizes mitochondrial coupling, reactive oxygen species production, and inflammation and partially restores skeletal muscle maximal oxidative capacity in experimental aortic cross-clamping

Journal of Vascular Surgery

Volumn 57, Issue 4, 2013, Pages

  Pottecher, Julien ^a,b   Guillot, Max ^b,c   Belaidi, Elise ^d   Charles, Anne Laure ^a,b   Lejay, Anne ^a,b   Gharib, Abdallah ^d   Diemunsch, Pierre ^a,b   Geny, Bernard ^a,b  

^a UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c HÔPITAL DE HAUTEPIERRE   (France)

^d UNIVERSITÉ LYON 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CYCLOPHILIN D; CYCLOSPORIN A; CYTOCHROME C OXIDASE; HYDROETHIDINE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); UBIQUINOL CYTOCHROME C REDUCTASE;

ANAEROBIC METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CLAMPING; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG BLOOD LEVEL; GASTROCNEMIUS MUSCLE; HEART MUSCLE; IMMUNOHISTOCHEMISTRY; MALE; MITOCHONDRIAL RESPIRATION; MYOSITIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPERFUSION INJURY; SKELETAL MUSCLE; WESTERN BLOTTING;

EID: 84875412748     PISSN: 07415214     EISSN: 10976809     Source Type: Journal    
DOI: 10.1016/j.jvs.2012.09.020     Document Type: Article

References (45)

1. R.E. Lovegrove, M. Javid, T.R. Magee, and R.B. Galland A meta-analysis of 21,178 patients undergoing open or endovascular repair of abdominal aortic aneurysm Br J Surg 95 2008 677 684
2. Z.A. Ali, C.J. Callaghan, E. Lim, A.A. Ali, S.A. Reza Nouraei, and A.M. Akthar Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial Circulation 116 2007 I98 I105
3. C.C. Miller III, M.A. Villa, J. Sutton, D. Lau, K. Keyhani, and A.L. Estrera Serum myoglobin and renal morbidity and mortality following thoracic and thoraco-abdominal aortic repair: does rhabdomyolysis play a role? Eur J Vasc Endovasc Surg 37 2009 388 394
4. D.B. Zorov, M. Juhaszova, and S.J. Sollott Mitochondrial ROS-induced ROS release: an update and review Biochim Biophys Acta 1757 2006 509 517
5. T.P. Tran, H. Tu, Pipinos II, R.L. Muelleman, H. Albadawi, and Y.-L. Li Tourniquet-induced acute ischemia-reperfusion injury in mouse skeletal muscles: involvement of superoxide Eur J Pharmacol 650 2011 328 334
6. S. Javadov, M. Karmazyn, and N. Escobales Mitochondrial permeability transition pore opening as a promising therapeutic target in cardiac diseases J Pharmacol Exp Ther 330 2009 670 678
7. Z. Mansour, J. Bouitbir, A.L. Charles, S. Talha, M. Kindo, and J. Pottecher Remote and local ischemic preconditioning equivalently protects rat skeletal muscle mitochondrial function during experimental aortic cross-clamping J Vasc Surg 55 2012 497 505
8. A.L. Charles, A.S. Guilbert, J. Bouitbir, P. Goette-Di Marco, I. Enache, and J. Zoll Effect of postconditioning on mitochondrial dysfunction in experimental aortic cross-clamping Br J Surg 98 2011 511 516
9. Z. Mansour, A.L. Charles, J. Bouitbir, J. Pottecher, M. Kindo, and J.-P. Mazzucotelli Remote and local ischemic postconditioning further impaired skeletal muscle mitochondrial function after ischemia-reperfusion J Vasc Surg 56 2012 774 782
10. H.Y. Chen, J.A. Navia, S. Shafique, and G.S. Kassab Fluid-structure interaction in aortic cross-clamping: implications for vessel injury J Biomech 43 2010 221 227
11. M. Cour, L. Gomez, N. Mewton, M. Ovize, and L. Argaud Postconditioning: from the bench to bedside J Cardiovasc Pharmacol Ther 16 2011 117 130
12. D.B. Zorov, M. Juhaszova, Y. Yaniv, H.B. Nuss, S. Wang, and S.J. Sollott Regulation and pharmacology of the mitochondrial permeability transition pore Cardiovasc Res 83 2009 213 225
13. V. Giorgio, M.E. Soriano, E. Basso, E. Bisetto, G. Lippe, and M.A. Forte Cyclophilin D in mitochondrial pathophysiology Biochim Biophys Acta 1797 2010 1113 1118
14. A.S. Farivar, B.C. Mackinnon-Patterson, A.D. Barnes, A.S. McCourtie, and M.S. Mulligan Cyclosporine modulates the response to hypoxia-reoxygenation in pulmonary artery endothelial cells Ann Thorac Surg 79 2005 1010 1016
15. I.M. Askar, and M. Bozkurt Protective effects of immunosuppressants and steroids against ischemia-reperfusion injury in cremaster muscle flap at microcirculatory level Microsurgery 22 2002 361 366
16. D.R. Eisinger, and A.G. Sheil A comparison of the effects of cyclosporin A and standard agents on primary wound healing in the rat Surg Gynecol Obstet 160 1985 135 138
17. E. Noll, J. Bouitbir, O. Collange, J. Zoll, A.L. Charles, and F. Thaveau Local but not systemic capillary lactate is a reperfusion biomarker in experimental acute limb ischaemia Eur J Vasc Endovasc Surg 7 2012 1 2
18. D.R. Luke, L.J. Brunner, and K. Vadiei Bioavailability assessment of cyclosporine in the rat. Influence of route of administration Drug Metab Dispos 18 1990 158 162
19. P.G. Sullivan, A.G. Rabchevsky, R.R. Hicks, T.R. Gibson, A. Fletcher-Turner, and S.W. Scheff Dose-response curve and optimal dosing regimen of cyclosporin A after traumatic brain injury in rats Neuroscience 101 2000 289 295
20. C. Piot, P. Croisille, P. Staat, H. Thibault, G. Rioufol, and N. Mewton Effect of cyclosporine on reperfusion injury in acute myocardial infarction N Engl J Med 359 2008 473 481
21. F.W. Blaisdell The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review Cardiovasc Surg 10 2002 620 630
22. P. Eckert, and K. Schnackerz Ischemic tolerance of human skeletal muscle Ann Plast Surg 26 1991 77 84
23. F. Dick, J. Li, M.-N. Giraud, C. Kalka, J. Schmidli, and H. Tevaearai Basic control of reperfusion effectively protects against reperfusion injury in a realistic rodent model of acute limb ischemia Circulation 118 2008 1920 1928
24. F. Beyersdorf, and C. Schlensak Controlled reperfusion after acute and persistent limb ischemia Semin Vasc Surg 22 2009 52 57
25. F. Thaveau, J. Zoll, O. Rouyer, N. Chafke, J.G. Kretz, and F. Piquard Ischemic preconditioning specifically restores complexes I and II activities of the mitochondrial respiratory chain in ischemic skeletal muscle J Vasc Surg 46 2007 541 547
26. S.E. McAllister, H. Ashrafpour, N. Cahoon, N. Huang, M.A. Moses, and P.C. Neligan Postconditioning for salvage of ischemic skeletal muscle from reperfusion injury: efficacy and mechanism Am J Physiol Regul Integr Comp Physiol 295 2008 R681 R689
27. H. Sanchez, X. Bigard, V. Veksler, B. Mettauer, E. Lampert, and J. Lonsdorfer Immunosuppressive treatment affects cardiac and skeletal muscle mitochondria by the toxic effect of vehicle J Mol Cell Cardiol 32 2000 323 331
28. G.C. Brown, and V. Borutaite Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols Biochim Biophys Acta 1658 2004 44 49
29. Y. Liu, G. Fiskum, and D. Schubert Generation of reactive oxygen species by the mitochondrial electron transport chain J Neurochem 80 2002 780 787
30. J. Zoll, B. N'Guessan, F. Ribera, E. Lampert, D. Fortin, and V. Veksler Preserved response of mitochondrial function to short-term endurance training in skeletal muscle of heart transplant recipients J Am Coll Cardiol 42 2003 126 132
31. H. Sanchez, J. Zoll, X. Bigard, V. Veksler, B. Mettauer, and E. Lampert Effect of cyclosporin A and its vehicle on cardiac and skeletal muscle mitochondria: relationship to efficacy of the respiratory chain Br J Pharmacol 133 2001 781 788
32. F. Piquard, B. Geny, H. Hardy, N. Chakfe, B. Mettauer, and A. Charloux Lack of acute cyclosporine nephrotoxicity in late heart-transplant recipients J Heart Lung Transplant 19 2000 507 509
33. K. Csukly, A. Ascah, J. Matas, P.F. Gardiner, E. Fontaine, and Y. Burelle Muscle denervation promotes opening of the permeability transition pore and increases the expression of cyclophilin D J Physiol 574 2006 319 327
34. T. Nakagawa, S. Shimizu, T. Watanabe, O. Yamaguchi, K. Otsu, and H. Yamagata Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death Nature 434 2005 652 658
35. T. Sayd, M. Morzel, C. Chambon, M. Franck, P. Figwer, and C. Larzul Proteome analysis of the sarcoplasmic fraction of pig semimembranosus muscle: implications on meat color development J Agric Food Chem 54 2006 2732 2737
36. H.S. Kim, J. Raskova, D. Degiannis, and K. Raska Effects of cyclosporine and rapamycin on immunoglobulin production by preactivated human B cells Clin Exp Immunol 96 1994 508 512
37. G.J. Nabel A transformed view of cyclosporine Nature 397 1999 471 472
38. C.E. Ganote, and S.C. Armstrong Effects of CCCP-induced mitochondrial uncoupling and cyclosporin A on cell volume, cell injury and preconditioning protection of isolated rabbit cardiomyocytes J Mol Cell Cardiol 35 2003 749 759
39. R. Badalzadeh, M. Mohammadi, M. Najafi, N. Ahmadiasl, S. Farajnia, and H. Ebrahimi The additive effects of ischemic postconditioning and cyclosporine-A on nitric oxide activity and functions of diabetic myocardium injured by ischemia/reperfusion J Cardiovasc Pharmacol Ther 17 2012 181 189
40. X.-S. Guo, Y.-Z. Li, X.-H. Liu, Z.-Y. Zhang, F.-Y. Liu, and C. Hu W- Calcineurin mediates the protective effect of postconditioning on skeletal muscle Shock 36 2011 312 316
41. S. Dikalov, K.K. Griendling, and D.G. Harrison Measurement of reactive oxygen species in cardiovascular studies Hypertension 49 2007 717 727
42. A. Mulsch, M. Oelze, S. Kloss, H. Mollnau, A. Topfer, and A. Smolenski Effects of in vivo nitroglycerin treatment on activity and expression of the guanylyl cyclase and cGMP-dependent protein kinase and their downstream target vasodilator-stimulated phosphoprotein in aorta Circulation 103 2001 2188 2194
43. Z. Mansour, A.L. Charles, J. Bouitbir, J. Pottecher, M. Kindo, and J.P. Mazzucotelli Remote and local ischemic post-conditioning further impaired skeletal muscle mitochondrial function after ischemia-reperfusion J Vasc Surg 56 2012 774 782
44. M. Paillard, L. Gomez, L. Augeul, J. Loufouat, E.J. Lesnefsky, and M. Ovize Postconditioning inhibits mPTP opening independent of oxidative phosphorylation and membrane potential J Mol Cell Cardiol 46 2009 902 909
45. 2+-induced opening of the permeability transition pore differs in mitochondria from glycolytic and oxidative muscles Am J Physiol Regul Integr Comp Physiol 295 2008 R659 R668