Middle age aggravates myocardial ischemia through surprising upholding of complex II activity, oxidative stress, and reduced coronary perfusion

Age

Volumn 33, Issue 3, 2011, Pages 321-336

  Mourmoura, Evangelia ^a,b   Leguen, Marie ^a,b   Dubouchaud, Hervé ^a,b   Couturier, Karine ^a,b   Vitiello, Damien ^a,b   Lafond, Jean Luc ^c   Richardson, Melanie ^d   Leverve, Xavier ^a,b   Demaison, Luc ^a,b,e  

^a INSERM   (France)

^b UNIV GRENOBLE ALPES   (France)

^c GRENOBLE UNIVERSITY HOSPITAL   (France)

^d UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^e CENTRE DES SCIENCES DU GOÛT ET DE L ALIMENTATION   (France)

Author keywords

Ischemia; Myocardial aging; Oxidative stress; Respiratory chain complexes

Indexed keywords

5,10 METHYLENETETRAHYDROFOLATE REDUCTASE (FADH2); ACONITATE HYDRATASE; ADENOSINE TRIPHOSPHATE; FUMARATE HYDRATASE; HYDROGEN PEROXIDE; LIPID; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUCCINATE DEHYDROGENASE (UBIQUINONE);

ADULT ANIMAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR EFFECT; CELL ISOLATION; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; DISEASE ASSOCIATION; DISEASE EXACERBATION; ENZYME ACTIVITY; HEART CONTRACTION; HEART MITOCHONDRION; HEART MUSCLE ISCHEMIA; HEART MUSCLE METABOLISM; HEART MUSCLE OXYGEN CONSUMPTION; HEART MUSCLE REPERFUSION; LIPID MEMBRANE; MALE; MICROENVIRONMENT; MIDDLE AGED; NONHUMAN; OXIDATIVE STRESS; RAT;

EID: 85027942037     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-010-9186-0     Document Type: Article

References (71)

1. Amrani M, Chester AH, Jayakumar J, Yacoub MH (1996) Aging reduces postischemic recovery of coronary endo-thelial function. J Thorac Cardiovasc Surg 111:238-245 (Pubitemid 26035192)
2. Azhar G, Gao W, Liu L, Wei JY (1999) Ischemia-reperfusion in the adultmouseheart: influenceofage. Exp Gerontol34:699-714
3. Batandier C, Leverve X, Fontaine E (2004) Opening of the mitochondrial permeability transition pore induces reactive oxygen species production at the level of the respiratory chain complex I. J Biol Chem 279:17197-17204 (Pubitemid 38560477)
4. Besse S, Tanguy S, Riou B, Boucher F, Bulteau AL, Le Page C, Swynghedauw B, de Liris J (2001) Coronary and aortic vasoreactivity protection with endothelin receptor antago-nist, bosentan, after ischemia and hypoxia in aged rats. Eur J Pharmacol 432:167-175 (Pubitemid 34003598)
5. Besse S, Tanguy S, Boucher F, Le Page C, Rozenberg S, Riou B, Liris J, Swynghedaw B (2004) Cardioprotection with cariporide, a sodium-proton exchanger inhibitor, after prolonged ischemia and reperfusion in senescent rats. Exp Gerontol 39:1307-1314 (Pubitemid 39360371)
6. Besse S, Bulteau AL, Boucher F, Riou B, Swynghedauw B, de Liris J (2006) Antioxidant treatment prevents cardiac protein oxidation after ischemia-reperfusion and improves myocardial function and coronary perfusion in senescent hearts. J Physiol Pharmacol 57:541-552 (Pubitemid 46096104)
7. Boengler K, Konietzka I, Buechert A, Heinen Y, Garcia-Dorado D, Heusch G, Schulz R (2007) Loss of ischemic preconditioning's cardioprotection in aged mouse hearts is associated with reduced gap junctional and mitochon-drial levels of connexin 43. Am J Physiol Heart Circ Physiol 292:H1764-H1769 (Pubitemid 46572399)
8. Capel F, Rimbert V, Lioger D, Diot A, Rousset P, Mirand PP, Boirie Y, Morio B, Mosoni L (2005) Due to reverse electron transfer, mitochondrial H2O2 release increases with age in human vastus lateralis muscle although oxidative capacity is preserved. Mech Ageing Dev 126:505-511 (Pubitemid 40269294)
9. Chen YR, Chen CL, Pfeiffer DR, Zweier JL (2007) Mitochon-drial complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation. J Biol Chem 282:32640-32654 (Pubitemid 350159288)
10. Chen CL, Chen J, Rawale S, Varadharaj S, Kaumaya PP, Zweier JL, Chen YR (2008) Protein tyrosine nitration of the flavin subunit is associated with oxidative modification of mitochondrial complex II in the post-ischemic myocar-dium. J Biol Chem 283:27991-28003
11. Crabtree MJ, Tatham AL, Al-Wakeel Y, Warrick N, Hale AB, Cai S, Channon KM, Alp NJ (2009) Quantitative regulation of intracellular endothelial nitric-oxide synthase (e NOS) coupling by both tetrahydrobiopterin-e NOS stoi-chiometry and biopterin redox status: insights from cells with tet-regulated GTP cyclohydrolase I expression. J Biol Chem 284:1136-1144
12. Crestanello JA, Doliba NM, Doliba NM, Babsky AM, Niborii K, Osbakken MD, Whitman GJ (2002) Effect of coen-zyme Q10 supplementation on mitochondrial function after myocardial ischemia reperfusion. J Surg Res 102:221-228 (Pubitemid 34969471)
13. Demaison L, Moreau D, Vergely-Vandriesse C, Grégoire S, Degois M, Rochette L (2001) Effects of dietary polyun-saturated fatty acids and hepatic steatosis on the function-ing of isolated working rat heart under normoxic conditions and during post-ischemic reperfusion. Mol Cell Biochem 224:103-116 (Pubitemid 32962656)
14. Faloona GR, Srere PA (1969) Escherichia coli citrate synthase. Purification and the effect of potassium on some proper-ties. Biochemistry 8:4497-4503
15. Fannin SW, Lesnefsky EJ, Slabe TJ, Hassan MO, Hoppel CL (1999) Aging selectively decreases oxidative capacity in rat heart interfibrillar mitochondria. Arch Biochem Bio-phys 372:399-407 (Pubitemid 30026794)
16. Gao F, Christopher TA, Lopez BL, Friedman E, Cai G, Ma XL (2000) Mechanism of decreased adenosine protection in reperfusion injury of aging rats. Am J Physiol Heart Circ Physiol 279:H329-H338 (Pubitemid 30616677)
17. Gardner PR, Nguyen DD, White CW (1994) Aconitase is a sensitive and critical target of oxygen poisoning in cultured mammalian cells and in rat lungs. Proc Natl Acad Sci USA 91:12248-12252 (Pubitemid 24368642)
18. Gnaiger E (2001) Oxygen solubility in experimental media. Oroboros Bioenergetics Newsletter 6(3):1-6
19. Goodwin AT, Amrani M, Marchbank AJ, Gray CC, Jayakumar J, Yacoub MH (1999) Coronary vasoconstriction to endothelin-1 increases with age before and after ischaemia andreperfusion. Cardiovasc Res 41:554-562 (Pubitemid 29130619)
20. Hansford RG, Tsuchiya N, Pepe S (1999) Mitochondria in heart ischaemia and aging. Biochem Soc Symp 66:141-147 (Pubitemid 129639029)
21. Headrick JP (1998) Aging impairs functional, metabolic and ionic recovery from ischemia-reperfusion and hypoxia-reoxygenation. J Mol Cell Cardiol 30:1415-1430 (Pubitemid 28345042)
22. Hoppel CL, Moghaddas S, Lesnefsky EJ (2002) Interfibrillar cardiac mitochondrial complex III defects in the aging rat heart. Biogerontology 3:41-44
23. Hu A, Jiao X, Gao E, Li Y, Sharifi-Azad S, Grunwald Z, Ma XL, Sun JZ (2008) Tonic beta-adrenergic drive provokes proinflammatory and proapoptotic changes in aging mouse heart. Rejuvenation Res 11:215-226 (Pubitemid 351271637)
24. Jahangir A, Ozcan C, Holmuhamedov EL, Terzic A (2001) Increased calcium vulnerability of senescent cardiac mitochondria: protective role for a mitochondrial potassi-um channel opener. Mech Ageing Dev 122:1073-1086 (Pubitemid 32520992)
25. Juhaszova M, Rabuel C, Zorov DB, Lakatta EG, Sollott SJ (2005) Protection in the aged heart: preventing the heat-break ofold age? Cardiovasc Res 66:233-244
26. Kakarla P, Vadluri G, Reddy KS, Leeuwenburgh C (2005) Vulnerability of the mid aged rat myocardium to the age-induced oxidative stress: influence of exercise training on antioxidant defense system. Free Radic Res 39:1211-1217 (Pubitemid 41601423)
27. Krähenbühl S, Talos C, Wiesmann U, Hoppel CL (1994) Development and evaluation of a spectrophotometric assay for complex III in isolated mitochondria, tissues and fibroblasts: application to mitochondrial encephalo-myopathies. Clin Chim Acta 230:177-187 (Pubitemid 24319743)
28. Kramer KA, Oglesbee D, Hartman SJ, Huey J, Anderson B, Magera MJ, Matern D, Rinaldo P, Robinson BH, Cameron JM, Hahn SH (2005) Automated spectrophotometric analysis ofmitochondrial respiratory chain complex enzyme activities in cultured skin fibroblasts. Clin Chem 51:2110-2116 (Pubitemid 41532627)
29. Lacraz G, Couturier K, Taleux N, Servais S, Sibille B, Letexier D, Guigas B, Dubouchaud H, Leverve X, Favier R (2008) Liver mitochondrial properties from the obesity-resistant Lou/C rat. Int J Obes (Lond) 32:629-638 (Pubitemid 351536019)
30. Lakatta EG, Sollott SJ, Pepe S (2001) The old heart: operating on the edge. Novartis Found Symp 235:172-196
31. Lakomkin VL, Korkina OV, Tsyplenkova VG, Timoshin AA, Ruuge EK, Kapel'ko VI (2002) The protective action of ubiquinone at ischemia and reperfusion. Kardiologiia 42:51-55
32. Leichtweis S, Leeuwenburgh C, Bejma J, Ji LL (2001) Aged rat hearts are not more susceptible to ischemia-reperfusion injury in vivo: role of glutathione. Mech Ageing Dev 122:503-518 (Pubitemid 32280797)
33. Lesfnefsky EJ, Hoppel CL (2003) Ischemia-reperfusion injury in the aged heart: role of mitochondria. Arch Biochem Biophys 420:287-297 (Pubitemid 37491113)
34. Lesnefsky EJ, Hoppel CL (2008) Cardiolipin as an oxidative target in cardiac mitochondria in the aged heart. Biochim Biophys Acta 1777:1020-1027
35. Lesnefsky EJ, Gudz TI, Moghaddas S, Migita CT, Ikeda-Saito M, Turkaly PJ, Hoppel CL (2001a) Aging decreases electron transport complex III activity in heart interfibrillar mitochondria by alteration of the cytochrome c binding site. J Mol Cell Cardiol 33:37-47
36. Lesnefsky EJ, Gudz TI, Migita CT, Ikeda-Saito M, Hassan MO, Turkaly PJ, Hoppel CL (2001b) Ischemic injury to mito-chondrial electron transport in the aging heart: damage to the iron-sulfur protein subunit of electron transport complex III. Arch Biochem Biophys 385:117-128 (Pubitemid 32988989)
37. Lesnefsky EJ, Minkler P, Hoppel CL (2009) Enhanced modification of cardiolipin during ischemia in the aged heart. J Mol Cell Cardiol 46:1008-1015
38. Martin C, Dubouchaud H, Mosoni L, Chardigny JM, Oudot A, Fontaine E, Vergely C, Keriel C, Rochette L, Leverve X, Demaison L (2007) Abnormalities of mitochondrial functioning can partly explain the metabolic disorders encountered in sarcopenic gastrocnemius. Aging Cell 6:165-177 (Pubitemid 46455061)
39. Maulik N, Yoshida T, Engelman RM, Bagchi D, Otani H, Das DK (2000) Dietary coenzyme Q(10) supplement renders swine hearts resistant to ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 278:H1084-H1090 (Pubitemid 30235483)
40. Miro O, Barrientos A, Alonso JR, Casademont J, Jarreta D, Urbano-Marquez A, Cardellach F (1999) Effects of general anaesthetic procedures on mitochondrial function of human skeletal muscle. Eur J Pharmacol 55:35-41 (Pubitemid 29144097)
41. Miyata H, Lakatta EG, Stern MD, Silverman HS (1992) Relation of mitochondrial and cytosolic free calcium to cardiac myocyte recovery after exposure to anoxia. Circ Res 71:605-613
42. Nagy K, Takacs IE, Pankucsi C (1996) Age-dependence offree radical-induced oxidative damage in ischemic-reperfused rat heart. Arch Gerontol Geriatr 22:297-309 (Pubitemid 26165250)
43. +) exchanger inhibitor HOE642 offers myoprotection in senescent myocardium independent of ischemic precondi-tioning mechanisms. Eur Surg Res 34:244-250 (Pubitemid 34665177)
44. Nakamura K, Al-Ruzzeh S, Chester AH, Dewar A, Rothery S, Severs NJ, Yacoub MH, Amrani M (2003) Age-related changes in the protective effect of chronic administration of L-arginine on post-ischemic recovery of endothelial function. Eur J Cardiothorac Surg 23:626-632 (Pubitemid 36411894)
45. Oudot A, Martin C, Busseuil D, Vergely C, Demaison L, Rochette L (2006) NADPH oxydases are in part respon-sible for increased cardiovascular superoxide production during aging. Free Radic Biol Med 40:2214-2222 (Pubitemid 43922397)
46. Paradies G, Petrosillo G, Pistolese M, Di Venosa N, Federici A, Ruggiero FM (2004) Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ Res 94:53-59 (Pubitemid 38064098)
47. Pasdois P, Beauvoit B, Tariosse L, Vinassa B, Bonoron-Adèle S, Santos PD (2006) Mito K(ATP)-dependent changes in mitochondrial volume and in complex II activity during ischemic and pharmacological preconditioning of Langendorff-perfused rat heart. J Bioenerg Biomembr 38:101-112
48. Pepe S, Tsuchiya N, Lakatta EG, Hansford RG (1999) PUFA and aging modulate cardiac mitochondrial membrane lipid composition and Ca2+ activation of PDH. Am J Physiol 276:H149-H158 (Pubitemid 29065633)
49. Polewczyk A, Janion M, Gasior M, Gierlotka M (2008) Myocardial infarction in the elderly Clinical and thera-peutic differences. Kardiol Pol 66:166-172
50. Ramani K, Lust WD, Wittingham TS, Lesnefsky EJ (1996) ATP catabolism and adenosine generation during ischemia in the aging heart. Mech Ageing Dev 89:113-124 (Pubitemid 26248834)
51. Ruiz-Meana M, Rodriguez-Sinovas A, Cabestrero A, Boengler K, Heusch G, Garcia-Dorado D (2008) Mitochondrial connexin 43 as a new player in the pathophysiology of myocardial ischaemia-reperfusion injury. Cardiovasc Res 77:325-333 (Pubitemid 351197646)
52. Sahach VF, Vavilova HL, Rudyk OV, Dobrovol's'ky FV, Shymans'ka TV, Miedviediev OS (2007) Inhibition of mitochondrial permeability transition pore is one of the mechanisms of cardioprotective effect of coenzyme Q10. Fiziol Zh 53:35-42
53. Sentex E, Laurent A, Martine L, Grégoire S, Rochette L, Demaison L (1999) Calcium-and ADP-magnesium-induced respiratory uncoupling in isolated cardiac mito-chondria: influence of cyclosporine A. Mol Cell Biochem 202:73-84 (Pubitemid 30099740)
54. Simm A, Friedrich I, Scheubel RJ, Gursinsky T, Silber RE, Bartling B (2008) Age dependency of the cariporide-mediated cardio-protection after simulated ischemia in isolated human atrial heart muscles. Exp Gerontol 43:691-699
55. Sniecinski R, Liu H (2004) Reduced efficacy of volatile anesthetic preconditioning with advanced age in isolated ratmyocardium. Anesthesiology 100:589-597 (Pubitemid 38268877)
56. + after ischemia. J Mol Cell Cardiol 29:3081-3089 (Pubitemid 27510774)
57. + imbalance. Cardio-vasc Res 41:594-602 (Pubitemid 29130623)
58. Timoshchuk SV, Vavilova HL, Strutyns'ka NA, Talanov SA, Petukhov DM, Kuchmenko OB, Donchenko HV, Sahach VF (2009) Cardioprotective action of coenzyme Q in conditions of its endogenous synthesis activation in cardiac ischemia-reperfusion in old rats. Fiziol Zh 55:58-63
59. Timoshin AA, Lakomkin VL, Gubkin AA, Ruuge EK (2003) Effect of coenzyme Q10on free radical centers in isolated rat myocardium tissue. Biofizika 48:717-721
60. Tsukube T, Mc Cully JD, Federman M, Krukenkamp IB, Levitsky S (1996) Developmental differences in cytosolic calcium accumulation associated with surgically induced global ischemia: optimization of cardioplegic protection and mechanism of action. J Thorac Cardiovasc Surg 112:175-184 (Pubitemid 26268985)
61. Turan N, Csonka C, Csont T, Giricz Z, Fodor G, Bencsik P, Gyongyosi M, Cakici I, Ferdinandy P (2006) The role of peroxynitrite in chemical preconditioning with 3-nitropropionic acid in rat hearts. Cardiovasc Res 70:384-390
62. Veitch K, Hue L (1994) Flunarizine and cinnarizine inhibit complexes I and II: possible implication for Parkinsonism. Mol Pharmacol 45:158-163 (Pubitemid 24042295)
63. Verma DD, Hartner WC, Thakkar V, Levchenko TS, Torchilin VP (2007) Protective effect of coenzyme Q10-loaded liposomes on the myocardium in rabbits with an acute experimental myocardial infarction. Pharm Res 24:2131-2137 (Pubitemid 47493570)
64. Wei Y Sowers JR, Nistala R, Gong H, Uptergrove GM, Clark SE, Morris EM, Szary N, Manrique C, Stump CS (2006) Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J Biol Chem 281:35137-35146 (Pubitemid 46036553)
65. Willems L, Garnham B, Headrick JP (2003) Aging-related changes in myocardial purine metabolism and ischemic tolerance. Exp Gerontol 38:1169-1177 (Pubitemid 37324428)
66. Willems L, Zatta A, Holmgren K, Ashton KJ, Headrick JP (2005) Age-related changes in ischemic tolerance in male and female mouse hearts. J Mol Cell Cardiol 38:245-256 (Pubitemid 40215194)
67. Wojtovich AP, Brookes PS (2008) The endogenous mitochon-drial complex II inhibitor malonate regulates mitochondri-al ATP-sensitive potassium channels: implications for ischemic preconditioning. Biochim Biophys Acta 1777:882-889
68. Xia Z, Godin DV, Ansley DM (2003) Propofol enhances ischemic tolerance of middle-aged rat hearts: effects on 15-F(2t)-isoprostane formation and tissue antioxidant capacity Cardiovasc Res 59:113-121
69. (2+) exchange inhibitor, KB-R7943, protects ischemic reperfused aged Fischer 344 rat hearts: considerable strain difference in the sensitivity to KB-R7943. Cardiovasc Res 52:397-406 (Pubitemid 33153102)
70. Zhang S, Yang JH, Yu F, Zhao J, Jiang P, Chang L, Tang C, Xu J (2006) Protective role of 3-nitro-N-methyl-salicylamide on isolated rat heart during 4 hours of cold storage and reperfusion. Transplant Proc 38:1247-1252
71. Zorov DB, Juhaszova M, Sollott SJ (2006) Mitochondrial ROS-induced ROS release: an update and review. Biochim Biophys Acta 1757:509-517