Uncoupling protein 3 mediates H2O2 preconditioning-afforded cardioprotection through the inhibition of MPTP opening

Cardiovascular Research

Volumn 105, Issue 2, 2015, Pages 192-202

  Chen, Yixiong ^a   Liu, Jinlong ^a   Zheng, Yanjun ^a   Wang, Jinxi ^a   Wang, Zhihua ^a   Gu, Shanshan ^a   Tan, Jiliang ^a   Jing, Qing ^a   Yang, Huangtian ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

H2O2 preconditioning; Ischaemia reperfusion; Mitochondria; MPTP Hearts; Uncoupling protein 3

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; ADENINE NUCLEOTIDE TRANSLOCASE; ATRACTYLOSIDE; GLYCOGEN SYNTHASE KINASE 3BETA; HYDROGEN PEROXIDE; LACTATE DEHYDROGENASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN 3; WORTMANNIN; CARRIER PROTEIN; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL SURVIVAL; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; ENZYME RELEASE; HEART FUNCTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE CONTRACTILITY; HEART PERFUSION; HEART PROTECTION; IMMUNOPRECIPITATION; ISCHEMIC PRECONDITIONING; MALE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; RAT; REPERFUSION INJURY; UPREGULATION; ANIMAL; DRUG EFFECTS; HEART MITOCHONDRION; HEART MUSCLE CELL; METABOLISM; MYOCARDIAL REPERFUSION INJURY; SPRAGUE DAWLEY RAT;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; HYDROGEN PEROXIDE; ION CHANNELS; ISCHEMIC PRECONDITIONING; MALE; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MITOCHONDRIAL PROTEINS; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; PHOSPHATIDYLINOSITOL 3-KINASES; RATS, SPRAGUE-DAWLEY;

EID: 84922435398     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvu256     Document Type: Article

References (49)

1. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 2008;88:581-609.
2. Vanden Hoek TL, Shao Z, Li C, Schumacker PT, Becker LB. Mitochondrial electron transport can become a significant source of oxidative injury in cardiomyocytes. J Mol Cell Cardiol 1997;29:2441-2450.
3. Becker LB. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc Res 2004;61:461-470.
4. Stone D, rley-Usmar V, Smith DR, O'Leary V. Hypoxia-reoxygenation induced increase in cellular Ca2+ in myocytes and perfused hearts: the role of mitochondria. J Mol Cell Cardiol 1989;21:963-973.
5. 2+ overload reduces myocardial injury induced by ischemia and reperfusion. Acta Pharmacol Sin 2006;27:911-918.
6. Gao H, Chen L, Yang HT. Activation of alpha1B-adrenoceptors alleviates ischemia/reperfusion injury by limitation of mitochondrial Ca2+ overload in cardiomyocytes. Cardiovasc Res 2007;75:584-595.
7. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009;417: 1-13.
8. Rigoulet M, Yoboue ED, Devin A. Mitochondrial ROS generation and its regulation: mechanisms involved in H(2)O(2) signaling. Antioxid Redox Signal 2011;14:459-468.
9. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, andROS:amito-chondrial love-hate triangle. Am J Physiol Cell Physiol 2004;287:C817-C833.
10. Javadov S, Karmazyn M, Escobales N. Mitochondrial permeability transition pore opening as a promising therapeutic target in cardiac diseases. J Pharmacol Exp Ther 2009;330:670-678.
11. Szabo I, De PV, Zoratti M. The mitochondrial permeability transition pore may comprise VDAC molecules. II. The electrophysiological properties of VDAC are compatible with those of the mitochondrial megachannel. FEBS Lett 1993;330:206-210.
12. Woodfield K, Ruck A, Brdiczka D, Halestrap AP. Direct demonstrationofaspecific interaction between cyclophilin-D and the adenine nucleotide translocase confirmstheirrole in the mitochondrial permeability transition. Biochem J 1998;336:287-290.
13. Miura T, Tanno M. The mPTP and its regulatory proteins:final common targets of signalling pathways for protection against necrosis. Cardiovasc Res 2012;94:181-189.
14. Hausenloy DJ, Maddock HL, Baxter GF, Yellon DM. Inhibiting mitochondrial permeability transition pore opening: a new paradigm for myocardial preconditioning? Cardiovasc Res 2002;55:534-543.
15. Halestrap AP, Clarke SJ, Javadov SA. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res 2004;61: 372-385.
16. Hausenloy DJ, Lim SY, Ong SG, Davidson SM, Yellon DM. Mitochondrial cyclophilin-D as a critical mediator of ischaemic preconditioning. Cardiovasc Res 2010;88:67-74.
17. Chinopoulos C, Szabadkai G. What makes you can also break you, Part III: mitochondrial permeability transition pore formation by an uncoupling channel within the C-subunit ring of the F1FO ATP synthase? Front Oncol 2014;4:235.
18. Karch J, Molkentin JD. Identifying the components of the elusive mitochondrial permeability transition pore. Proc Natl Acad Sci USA 2014;111:10396-10397.
19. Giorgio V, von Stockum S, Antoniel M, Fabbro A, Fogolari F, Forte M, Glick GD, Petronilli V, Zoratti M, Szabo I, Lippe G, Bernardi P. Dimers of mitochondrial ATP syn-thase form the permeability transition pore. Proc Natl Acad Sci USA 2013;110: 5887-5892.
20. Ricquier D, Bouillaud F. The uncoupling protein homologues: UCP1, UCP2, UCP3, StUCP and AtUCP. Biochem J 2000;345:161-179.
21. Teshima Y, Akao M, Jones SP, Marban E. Uncoupling protein-2 overexpression inhibits mitochondrial death pathway in cardiomyocytes. Circ Res 2003;93:192-200.
22. Essop MF, Razeghi P, McLeod C, Young ME, Taegtmeyer H, Sack MN. Hypoxia-induced decrease of UCP3 gene expression in rat heart parallels metabolic gene switching but fails to affect mitochondrial respiratory coupling. Biochem Biophys Res Commun 2004; 314:561-564.
23. Hoshovs'ka I, Lisovyi OO, Shymans'ka TV, Sahach VF. UCP2 and UCP3 gene expression, heart function and oxygen cost of myocardial work changes during aging and ischemia-reperfusion. Fiziol Zh 2009;55:26-36.
24. McLeod CJ, Aziz A, Hoyt RF Jr, McCoy JP Jr, Sack MN. Uncoupling proteins 2 and 3 function in concert to augment tolerance to cardiac ischemia. J Biol Chem 2005;280: 33470-33476.
25. Hoerter J, Gonzalez-Barroso MD, Couplan E, Mateo P, Gelly C, Cassard-Doulcier AM, Diolez P, Bouillaud F. Mitochondrial uncoupling protein1expressedinthe heartoftrans-genic mice protects against ischemic-reperfusion damage. Circulation 2004;110: 528-533.
26. Ozcan C, Palmeri M, Horvath TL, Russell KS, Russell RR. Role of uncoupling protein 3 in ischemia-reperfusion injury, arrhythmias, and preconditioning. Am J Physiol Heart Circ Physiol 2013;304:1192-1200.
27. Perrino C, Schiattarella GG, Sannino A, Pironti G, Petretta MP, Cannavo A, Gargiulo G, Ilardi F, Magliulo F, Franzone A, Carotenuto G, Serino F, Altobelli GG, Cimini V, Cuocolo A, Lombardi A, Goglia F, Indolfi C, Trimarco B, Esposito G. Genetic deletion of uncoupling protein 3 exaggerates apoptotic cell death in the ischemic heart leading to heart failure. J Am Heart Assoc 2013;2:e000086.
28. Hausenloy DJ, Wynne AM, Yellon DM. Ischemic preconditioning targets the reperfusion phase. Basic Res Cardiol 2007;102:445-452.
29. Yang X, Cohen MV, Downey JM. Mechanism of cardioprotection by early ischemic preconditioning. Cardiovasc Drugs Ther 2010;24:225-234.
30. Miyawaki H, Wang Y, Ashraf M. Oxidant stress with hydrogen peroxide attenuates calcium paradox injury: role of protein kinase C and ATP-sensitive potassium channel. Cardiovasc Res 1998;37:691-699.
31. Yaguchi Y, Satoh H, Wakahara N, Katoh H, Uehara A, Terada H, Fujise Y, Hayashi H. Protective effects of hydrogen peroxide against ischemia/reperfusion injury in perfused rat hearts. Circ J 2003;67:253-258.
32. Wang ZH, Chen YX, Zhang CM, Wu L, Yu Z, Cai XL, Guan Y, Zhou ZN, Yang HT.Inter-mittent hypobaric hypoxia improves postischemic recovery of myocardial contractile function via redox signaling during early reperfusion. Am J Physiol Heart Circ Physiol 2011;301:1695-1705.
33. Wang ZH, Liu JL, Wu L, Yu Z, Yang HT. Concentration-dependent wrestling between detrimental and protective effects of H2O2 during myocardial ischemia/reperfusion. Cell Death Dis 2014;5:e1297.
34. Heusch G, Boengler K, Schulz R.Inhibitionofmitochondrial permeability transition pore opening: the Holy Grail of cardioprotection. Basic Res Cardiol 2010;105:151-154.
35. Su CC, Yang JY, Leu HB, Chen Y, Wang PH. Mitochondrial Akt-regulated mitochondrial apoptosis signaling in cardiac muscle cells. Am J Physiol Heart Circ Physiol 2012;302: 716-723.
36. Juhaszova M, Zorov DB, Kim SH, Pepe S, Fu Q, Fishbein KW, Ziman BD, Wang S, Ytrehus K, Antos CL, Olson EN, Sollott SJ. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest 2004;113:1535-1549.
37. Davidson SM, Hausenloy D, Duchen MR, Yellon DM. Signalling via the reperfusion injury signalling kinase (RISK) pathway links closure of the mitochondrial permeability transition pore to cardioprotection. Int J Biochem Cell Biol 2006;38:414-419.
38. Lu XY, Chen L, Cai XL, Yang HT. Overexpression of heat shock protein 27 protects against ischaemia/reperfusion-induced cardiac dysfunction via stabilization of troponin I and T. Cardiovasc Res 2008;79:500-508.
39. Cordeiro JM, Howlett SE, Ferrier GR. Simulated ischaemia and reperfusion in isolated guinea pig ventricular myocytes. Cardiovasc Res 1994;28:1794-1802.
40. Chen L, Lu XY, Li J, Fu JD, Zhou ZN, Yang HT. Intermittent hypoxia protects cardiomyo-cytes against ischemia-reperfusion injury-induced alterations in Ca2+ homeostasis and contraction via the sarcoplasmic reticulum and Na+/Ca2+ exchange mechanisms. Am J Physiol Cell Physiol 2006;290:1221-1229.
41. Trollinger DR, Cascio WE, Lemasters JJ. Mitochondrial calcium transients in adult rabbit cardiac myocytes: inhibition by ruthenium red and artifacts caused by lysosomal loading of Ca(2+)-indicating fluorophores. Biophys J 2000;79:39-50.
42. Levraut J, Iwase H, Shao ZH, Vanden Hoek TL, Schumacker PT. Cell death during ischemia: relationshipto mitochondrial depolarization and ROS generation. Am J Physiol Heart Circ Physiol 2003;284:549-558.
43. Hanninen SL, Ronkainen JJ, Leskinen H, Tavi P. Mitochondrial uncoupling downregulates calsequestrin expression and reducesSR Ca2+ storesincardiomyocytes. Cardiovasc Res 2010;88:75-82.
44. Matsushima S, Kuroda J, Ago T, Zhai P, Ikeda Y, Oka S, Fong GH, Tian R, Sadoshima J. Broad suppression of NADPH oxidase activity exacerbates ischemia/reperfusion injury through inadvertent downregulation of hypoxia-inducible factor-1alpha and upregulation of peroxisome proliferator-activated receptor-alpha. Circ Res 2013;112: 1135-1149.
45. Glancy B, Balaban RS. Role of mitochondrial Ca2+ in the regulation of cellular energetics. Biochemistry 2012;51:2959-2973.
46. Senese R, Valli V, Moreno M, Lombardi A, Busiello RA, Cioffi F, Silvestri E, Goglia F, Lanni A, de Lange P. Uncoupling protein 3 expression levels influence insulin sensitivity, fatty acid oxidation, and related signaling pathways. Pflugers Arch 2011;461:153-164.
47. Sack MN. Mitochondrial depolarization and the role of uncoupling proteins in ischemia tolerance. Cardiovasc Res 2006;72:210-219.
48. Holmuhamedov EL, Wang L, Terzic A. ATP-sensitive K+ channel openers prevent Ca2+ overload in rat cardiac mitochondria. J Physiol 1999;519(Pt 2):347-360.
49. Brennan JP, Southworth R, Medina RA, Davidson SM, Duchen MR, Shattock MJ. Mitochondrial uncoupling, with low concentration FCCP, induces ROS-dependent car-dioprotection independent of KATP channel activation. Cardiovasc Res 2006;72: 313-321.