The end-effectors of preconditioning protection against myocardial cell death secondary to ischemia-reperfusion

Cardiovascular Research

Volumn 70, Issue 2, 2006, Pages 274-285

  Garcia Dorado, David ^a   Rodriguez Sinovas, Antonio ^a   Ruiz Meana, Marisol ^a   Inserte, Javier ^a   Agulló, Luis ^a   Cabestrero, Alberto ^a  

^a HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

Calpain; cGMP; Connexin43; GSK3beta; Hypercontracture; Mitochondrial permeability transition; Myocardial infarction; PKG

Indexed keywords

2 (2,4 DICHLOROPHENYL) 3 (1 METHYL 3 INDOLYL)MALEIMIDE; ADRENOMEDULLIN; CALCINEURIN INHIBITOR; CALPAIN; CALPASTATIN; CASPASE INHIBITOR; CONNEXIN 43; CYCLOPHILIN; CYCLOSPORIN A; DIAZOXIDE; GLYCOGEN SYNTHASE KINASE 3 INHIBITOR; GLYCOGEN SYNTHASE KINASE 3BETA INHIBITOR; LITHIUM; MITOCHONDRIAL PERMEABILITY TRANSITION PORE INHIBITOR; OPIATE; SANGLYPHERIN; UNCLASSIFIED DRUG; URODILATIN;

CAUSE OF DEATH; CYTOSKELETON; GAP JUNCTION; HEART INFARCTION PREVENTION; HEART MUSCLE CELL; HEART MUSCLE ISCHEMIA; HEART PROTECTION; ISCHEMIC PRECONDITIONING; ISOLATED HEART; MOUSE STRAIN; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; RAT STRAIN; REPERFUSION INJURY; REVIEW;

CALCIUM; CELL DEATH; HUMANS; ION CHANNEL GATING; ISCHEMIC PRECONDITIONING, MYOCARDIAL; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; SARCOPLASMIC RETICULUM;

EID: 33646073794     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cardiores.2006.02.011     Document Type: Review

References (111)

1. Murry C.E., Jennings R.B., and Reimer K.A. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium. Circulation 74 (1986) 1124-1136
2. Halestrap A.P., Clarke S.J., and Javadov S.A. Mitochondrial permeability transition pore opening during myocardial reperfusion-a target for cardioprotection. Cardiovasc Res 61 (2004) 372-385
3. Piper H.M., Garcia-Dorado D., and Ovize M. A fresh look at reperfusion injury. Cardiovasc Res 38 (1998) 291-300
4. Piper H.M., Abdallah Y., and Schafer C. The first minutes of reperfusion: a window of opportunity for cardioprotection. Cardiovasc Res 61 (2004) 365-371
5. Garcia-Dorado D., Theroux P., Duran J.M., Solares J., Alonso J., Sanz E., et al. Selective inhibition of the contractile apparatus. A new approach to modification of infarct size, infarct composition, and infarct geometry during coronary artery occlusion and reperfusion. Circulation 85 (1992) 1160-1174
6. Sebbag L., Verbinski S.G., Reimer K.A., and Jennings R.B. Protection of ischemic myocardium in dogs using intracoronary 2,3-butanedione monoxime (BDM). J Mol Cell Cardiol 35 (2003) 165-176
7. Schlack W., Uebing A., Schafer M., Bier F., Schafer S., Piper H.M., et al. Regional contractile blockade at the onset of reperfusion reduces infarct size in the dog heart. Pflugers Arch 428 (1994) 134-141
8. +-ATPase activity during early reperfusion contributes to cell death after myocardial ischemia. Circ Res 97 (2005) 465-473
9. Siegmund B., Klietz T., Schwartz P., and Piper H.M. Temporary contractile blockade prevents hypercontracture in anoxic-reoxygenated cardiomyocytes. Am J Physiol 260 (1991) H426-H435
10. Inserte J., Garcia-Dorado D., Ruiz-Meana M., Padilla F., Barrabes J.A., Pina P., et al. Effect of inhibition of Na(+)/Ca(2+) exchanger at the time of myocardial reperfusion on hypercontracture and cell death. Cardiovasc Res 55 (2002) 739-748
11. 2+ exchanger in reoxygenation-induced cardiomyocyte injury. Cardiovasc Res 51 (2001) 241-250
12. Ladilov Y., Efe O., Schafer C., Rother B., Kasseckert S., Abdallah Y., et al. Reoxygenation-induced rigor-type contracture. J Mol Cell Cardiol 35 (2003) 1481-1490
13. Inserte J., Garcia-Dorado D., Ruiz-Meana M., Agullo L., Pina P., and Soler-Soler J. Ischemic preconditioning attenuates calpain-mediated degradation of structural proteins through a protein kinase A-dependent mechanism. Cardiovasc Res 64 (2004) 105-114
14. Garcia-Dorado D., Rodriguez-Sinovas A., and Ruiz-Meana M. Gap junction-mediated spread of cell injury and death during myocardial ischemia-reperfusion. Cardiovasc Res 61 (2004) 386-401
15. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 341 (1999) 233-249
16. + and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem 276 (2001) 2571-2575
17. Javadov S.A., Clarke S., Das M., Griffiths E.J., Lim K.H., and Halestrap A.P. Ischaemic preconditioning inhibits opening of mitochondrial permeability transition pores in the reperfused rat heart. J Physiol 549 (2003) 513-524
18. Griffiths E.J., and Halestrap A.P. Mitochondrial non-specific pores remain closed during cardiac ischaemia, but open upon reperfusion. Biochem J 307 (1995) 93-98
19. Baines C.P., Kaiser R.A., Purcell N.H., Blair N.S., Osinska H., Hambleton M.A., et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434 (2005) 658-662
20. 2+-overloaded cultured rat cardiomyocytes. Am J Physiol 274 (1998) H2085-H2093
21. Siegmund B., Koop A., Klietz T., Schwartz P., and Piper H.M. Sarcolemmal integrity and metabolic competence of cardiomyocytes under anoxia-reoxygenation. Am J Physiol 258 (1990) H285-H291
22. 2+ influx in reperfusion injury of metabolically inhibited cardiac myocytes. Cardiovasc Res 67 (2005) 291-300
23. Suleiman M.S., Halestrap A.P., and Griffiths E.J. Mitochondria: a target for myocardial protection. Pharmacol Ther 89 (2001) 29-46
24. Periasamy M. Calcineurin and the heartbeat, an evolving story. J Mol Cell Cardiol 34 (2002) 259-262
25. Bandyopadhyay A., Shin D.W., Ahn J.O., and Kim D.H. Calcineurin regulates ryanodine receptor/Ca(2+)-release channels in rat heart. Biochem J 352 (2000) 61-70
26. Schinzel A.C., Takeuchi O., Huang Z., Fisher J.K., Zhou Z., Rubens J., et al. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc Natl Acad Sci U S A 102 (2005) 12005-12010
27. Hausenloy D.J., Tsang A., Mocanu M.M., and Yellon D.M. Ischemic preconditioning protects by activating prosurvival kinases at reperfusion. Am J Physiol Heart Circ Physiol 288 (2005) H971-H976
28. Garcia-Dorado D., Ruiz-Meana M., and Barrabes J.A. Does preconditioning reduce lethal mechanical reperfusion injury?. In: Wainwright C.L., and Parratt J.R. (Eds). Myocardial Preconditioning (1996), Springer-Verlag, Heidelberg 19-34
29. Salloum F.N., Ockaili R.A., Wittkamp M., Marwaha V., and Kukreja R.C. Erectile dysfunction drug Vardenafil limits myocardial infarction when given either as a preconditioning mimetic or at reperfusion in rabbits. Circulation 112 (2005) II-499 (Abstract)
30. Costa A.D., Garlid K.D., West I.C., Lincoln T.M., Downey J.M., Cohen M.V., et al. Protein kinase G transmits the cardioprotective signal from cytosol to mitochondria. Circ Res 97 (2005) 329-336
31. Agullo L., Garcia-Dorado D., Escalona N., Inserte J., Ruiz-Meana M., Barrabes J.A., et al. Hypoxia and acidosis impair cGMP synthesis in microvascular coronary endothelial cells. Am J Physiol Heart Circ Physiol 283 (2002) H917-H925
32. Agullo L., Garcia-Dorado D., Escalona N., Ruiz-Meana M., Inserte J., and Soler-Soler J. Effect of ischemia on soluble and particulate guanylyl cyclase-mediated cGMP synthesis in cardiomyocytes. Am J Physiol Heart Circ Physiol 284 (2003) H2170-H2176
33. Agullo L., Garcia-Dorado D., Escalona N., Ruiz-Meana M., Mirabet M., Inserte J., et al. Membrane association of nitric oxide-sensitive guanylyl cyclase in cardiomyocytes. Cardiovasc Res 68 (2005) 65-74
34. Padilla F., Garcia-Dorado D., Agullo L., Inserte J., Paniagua A., Mirabet S., et al. l-Arginine administration prevents reperfusion-induced cardiomyocyte hypercontracture and reduces infarct size in the pig. Cardiovasc Res 46 (2000) 412-420
35. Inserte J., Garcia-Dorado D., Agullo L., Paniagua A., and Soler-Soler J. Urodilatin limits acute reperfusion injury in the isolated rat heart. Cardiovasc Res 45 (2000) 351-359
36. Agullo L., Garcia-Dorado D., Inserte J., Paniagua A., Pyrhonen P., Llevadot J., et al. l-Arginine limits myocardial cell death secondary to hypoxia-reoxygenation by a cGMP-dependent mechanism. Am J Physiol 276 (1999) H1574-H1580
37. Lochner A., Marais E., Du T.E., and Moolman J. Nitric oxide triggers classic ischemic preconditioning. Ann N Y Acad Sci 962 (2002) 402-414
38. Lochner A., Genade S., Tromp E., Opie L., Moolman J., Thomas S., et al. Role of cyclic nucleotide phosphodiesterases in ischemic preconditioning. Mol Cell Biochem 186 (1998) 169-175
39. Sabine B., Willenbrock R., Haase H., Karczewski P., Wallukat G., Dietz R., et al. Cyclic GMP-mediated phospholamban phosphorylation in intact cardiomyocytes. Biochem Biophys Res Commun 214 (1995) 75-80
40. Abdallah Y., Gkatzoflia A., Piper H.M., Zoga E., Walther S., Kasseckert S., et al. Mechanism of cGMP-mediated protection in a cellular model of myocardial reperfusion injury. Cardiovasc Res 66 (2005) 123-131
41. 2+ in intact cardiac myocytes. Circ Res 74 (1994) 970-978
42. Bolz S.S., Vogel L., Sollinger D., Derwand R., de Wit C., Loirand G., et al. Nitric oxide-induced decrease in calcium sensitivity of resistance arteries is attributable to activation of the myosin light chain phosphatase and antagonized by the RhoA/Rho kinase pathway. Circulation 107 (2003) 3081-3087
43. 2+ sensitization of contraction in vascular smooth muscle. J Biol Chem 275 (2000) 21722-21729
44. Chen M., Won D.J., Krajewski S., and Gottlieb R.A. Calpain and mitochondria in ischemia/reperfusion injury. J Biol Chem 277 (2002) 29181-29186
45. Ajamieh H., Merino N., Candelario-Jalil E., Menendez S., Martinez-Sanchez G., Re L., et al. Similar protective effect of ischaemic and ozone oxidative preconditionings in liver ischaemia/reperfusion injury. Pharmacol Res 45 (2002) 333-339
46. Armstrong S.C., Shivell L.C., and Ganote C.E. Sarcolemmal blebs and osmotic fragility as correlates of irreversible ischemic injury in preconditioned isolated rabbit cardiomyocytes. J Mol Cell Cardiol 33 (2001) 149-160
47. Imahashi K., Kusuoka H., Hashimoto K., Yoshioka J., Yamaguchi H., and Nishimura T. Intracellular sodium accumulation during ischemia as the substrate for reperfusion injury. Circ Res 84 (1999) 1401-1406
48. Imahashi K., Nishimura T., Yoshioka J., and Kusuoka H. Role of intracellular Na(+) kinetics in preconditioned rat heart. Circ Res 88 (2001) 1176-1182
49. +-ATPase activity reduces the infarct size-limiting effect of preconditioning in rabbit hearts. Circulation 96 (1997) 599-604
50. +,K(+)-ATPase and Ca(2+)-ATPase activities in multi-cycle ischemic preconditioning in rabbit hearts. Eur J Cardiothorac Surg 26 (2004) 981-987
51. Chen M., He H., Zhan S., Krajewski S., Reed J.C., and Gottlieb R.A. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J Biol Chem 276 (2001) 30724-30728
52. Polster B.M., Basanez G., Etxebarria A., Hardwick J.M., and Nicholls D.G. Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J Biol Chem 280 (2005) 6447-6454
53. Cong J., Thompson V.F., and Goll D.E. Immunoaffinity purification of the calpains. Protein Expr Purif 25 (2002) 283-290
54. 2+-activated neutral protease. Biochemistry 27 (1988) 8122-8128
55. Shiraha H., Glading A., Gupta K., and Wells A. IP-10 inhibits epidermal growth factor-induced motility by decreasing epidermal growth factor receptor-mediated calpain activity. J Cell Biol 146 (1999) 243-254
56. Lochner A., Genade S., Tromp E., Podzuweit T., and Moolman J.A. Ischemic preconditioning and the beta-adrenergic signal transduction pathway. Circulation 100 (1999) 958-966
57. Sanada S., Asanuma H., Tsukamoto O., Minamino T., Node K., Takashima S., et al. Protein kinase A as another mediator of ischemic preconditioning independent of protein kinase C. Circulation 110 (2004) 51-57
58. Garcia-Dorado D., Inserte J., Ruiz-Meana M., Gonzalez M.A., Solares J., Julia M., et al. Gap junction uncoupler heptanol prevents cell-to-cell progression of hypercontracture and limits necrosis during myocardial reperfusion. Circulation 96 (1997) 3579-3586
59. Rodriguez-Sinovas A., Garcia-Dorado D., Ruiz-Meana M., and Soler-Soler J. Enhanced effect of gap junction uncouplers on macroscopic electrical properties of reperfused myocardium. J Physiol 559 (2004) 245-257
60. Ruiz-Meana M., Garcia-Dorado D., Hofstaetter B., Piper H.M., and Soler-Soler J. Propagation of cardiomyocyte hypercontracture by passage of Na(+) through gap junctions. Circ Res 85 (1999) 280-287
61. Garcia-Dorado D., and Ruiz-Meana M. Propagation of cell death during myocardial reperfusion. News Physiol Sci 15 (2000) 326-330
62. Krysko D.V., Leybaert L., Vandenabeele P., and D'Herde K. Gap junctions and the propagation of cell survival and cell death signals. Apoptosis 10 (2005) 459-469
63. Cruciani V., and Mikalsen S.O. Connexins, gap junctional intercellular communication and kinases. Biol Cell 94 (2002) 433-443
64. Lampe P.D., and Lau A.F. Regulation of gap junctions by phosphorylation of connexins. Arch Biochem Biophys 384 (2000) 205-215
65. Garcia-Dorado D., Ruiz-Meana M., Padilla F., Rodriguez-Sinovas A., and Mirabet M. Gap junction-mediated intercellular communication in ischemic preconditioning. Cardiovasc Res 55 (2002) 456-465
66. Jain S.K., Schuessler R.B., and Saffitz J.E. Mechanisms of delayed electrical uncoupling induced by ischemic preconditioning. Circ Res 92 (2003) 1138-1144
67. Miura T., Ohnuma Y., Kuno A., Tanno M., Ichikawa Y., Nakamura Y., et al. Protective role of gap junctions in preconditioning against myocardial infarction. Am J Physiol Heart Circ Physiol 286 (2003) H214-H221
68. Schulz R., Gres P., Skyschally A., Duschin A., Belosjorow S., Konietzka I., et al. Ischemic preconditioning preserves connexin 43 phosphorylation during sustained ischemia in pig hearts in vivo. FASEB J 17 (2003) 1355-1357
69. John S., Cesario D., and Weiss J.N. Gap junctional hemichannels in the heart. Acta Physiol Scand 179 (2003) 23-31
70. Contreras J.E., Sanchez H.A., Eugenin E.A., Speidel D., Theis M., Willecke K., et al. Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc Natl Acad Sci U S A 99 (2002) 495-500
71. John S.A., Kondo R., Wang S.Y., Goldhaber J.I., and Weiss J.N. Connexin-43 hemichannels opened by metabolic inhibition. J Biol Chem 274 (1999) 236-240
72. Saez J.C., Retamal M.A., Basilio D., Bukauskas F.F., and Bennett M.V. Connexin-based gap junction hemichannels: gating mechanisms. Biochim Biophys Acta 1711 (2005) 215-224
73. Quist A.P., Rhee S.K., Lin H., and Lal R. Physiological role of gap-junctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J Cell Biol 148 (2000) 1063-1074
74. Stout C.E., Costantin J.L., Naus C.C., and Charles A.C. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 277 (2002) 10482-10488
75. Sanz E., Garcia D.D., Oliveras J., Barrabes J.A., Gonzalez M.A., Ruiz-Meana M., et al. Dissociation between anti-infarct effect and anti-edema effect of ischemic preconditioning. Am J Physiol 268 (1995) H233-H241
76. Kevelaitis E., Peynet J., Mouas C., Launay J.M., and Menasche P. Opening of potassium channels: the common cardioprotective link between preconditioning and natural hibernation?. Circulation 99 (1999) 3079-3085
77. Schulz R., and Heusch G. Connexin 43 and ischemic preconditioning. Cardiovasc Res 62 (2004) 335-344
78. Lin J.H., Yang J., Liu S., Takano T., Wang X., Gao Q., et al. Connexin mediates gap junction-independent resistance to cellular injury. J Neurosci 23 (2003) 430-441
79. Harris A.L. Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 34 (2001) 325-472
80. Przyklenk K., Maynard M., Darling C.E., and Whittaker P. Pretreatment with d-myo-inositol trisphosphate reduces infarct size in rabbit hearts: role of inositol trisphosphate receptors and gap junctions in triggering protection. J Pharmacol Exp Ther 314 (2005) 1386-1392
81. Daleau P., Boudriau S., Michaud M., Jolicoeur C., and Kingma Jr. J.G. Preconditioning in the absence or presence of sustained ischemia modulates myocardial Cx43 protein levels and gap junction distribution. Can J Physiol Pharmacol 79 (2001) 371-378
82. Schwanke U., Konietzka I., Duschin A., Li X., Schulz R., and Heusch G. No ischemic preconditioning in heterozygous connexin43-deficient mice. Am J Physiol Heart Circ Physiol 283 (2002) H1740-H1742
83. Schwanke U., Li X., Schulz R., and Heusch G. No ischemic preconditioning in heterozygous connexin 43-deficient mice-a further in vivo study. Basic Res Cardiol 98 (2003) 181-182
84. Li X., Heinzel F.R., Boengler K., Schulz R., and Heusch G. Role of connexin 43 in ischemic preconditioning does not involve intercellular communication through gap junctions. J Mol Cell Cardiol 36 (2004) 161-163
85. Ping P., Song C., Zhang J., Guo Y., Cao X., Li R.C., et al. Formation of protein kinase C(epsilon)-Lck signaling modules confers cardioprotection. J Clin Invest 109 (2002) 499-507
86. Boengler K., Dodoni G., Rodriguez-Sinovas A., Cabestrero A., Ruiz-Meana M., Gres P., et al. Connexin 43 in cardiomyocyte mitochondria and its increase by ischemic preconditioning. Cardiovasc Res 67 (2005) 234-244
87. Rodriguez-Sinovas A., Cabestrero A., Morente M., Ruiz-Meana M., Miro E., Boengler K., et al. Translocation of connexin43 to mitochondria during ischemic preconditioning involves HSP90-TOM mechanism. Circulation 112 (2005) II-229 (Abstract)
88. Heinzel F.R., Luo Y., Li X., Boengler K., Buechert A., Garcia-Dorado D., et al. Impairment of diazoxide-induced formation of reactive oxygen species and loss of cardioprotection in connexin 43 deficient mice. Circ Res 97 (2005) 583-586
89. Hausenloy D.J., Maddock H.L., Baxter G.F., and Yellon D.M. Inhibiting mitochondrial permeability transition pore opening: a new paradigm for myocardial preconditioning?. Cardiovasc Res 55 (2002) 534-543
90. 2+-induced mitochondrial permeability transition. Cardiovasc Res 61 (2004) 115-122
91. Griffiths E.J., Ocampo C.J., Savage J.S., Stern M.D., and Silverman H.S. Protective effects of low and high doses of cyclosporin A against reoxygenation injury in isolated rat cardiomyocytes are associated with differential effects on mitochondrial calcium levels. Cell Calcium 27 (2000) 87-95
92. Hausenloy D.J., Yellon D.M., Mani-Babu S., and Duchen M.R. Preconditioning protects by inhibiting the mitochondrial permeability transition. Am J Physiol Heart Circ Physiol 287 (2004) H841-H849
93. Juhaszova M., Zorov D.B., Kim S.H., Pepe S., Fu Q., Fishbein K.W., et al. Glycogen synthase kinase-3beta mediates convergence of protection signaling to inhibit the mitochondrial permeability transition pore. J Clin Invest 113 (2004) 1535-1549
94. Weiss J.N., Korge P., Honda H.M., and Ping P. Role of the mitochondrial permeability transition in myocardial disease. Circ Res 93 (2003) 292-301
95. Das M., Parker J.E., and Halestrap A.P. Matrix volume measurements challenge the existence of diazoxide/glibencamide-sensitive KATP channels in rat mitochondria. J Physiol 547 (2003) 893-902
96. Hanley P.J., and Daut J. K(ATP) channels and preconditioning: a re-examination of the role of mitochondrial K(ATP) channels and an overview of alternative mechanisms. J Mol Cell Cardiol 39 (2005) 17-50
97. Penzo D., Petronilli V., Angelin A., Cusan C., Colonna R., Scorrano L., et al. Arachidonic acid released by phospholipase A(2) activation triggers Ca(2+)-dependent apoptosis through the mitochondrial pathway. J Biol Chem 279 (2004) 25219-25225
98. Pap M., and Cooper G.M. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 273 (1998) 19929-19932
99. Chin P.C., Majdzadeh N., and D'Mello S.R. Inhibition of GSK3beta is a common event in neuroprotection by different survival factors. Brain Res Mol Brain Res 137 (2005) 193-201
100. Loberg R.D., Vesely E., and Brosius III F.C. Enhanced glycogen synthase kinase-3beta activity mediates hypoxia-induced apoptosis of vascular smooth muscle cells and is prevented by glucose transport and metabolism. J Biol Chem 277 (2002) 41667-41673
101. Tong H., Imahashi K., Steenbergen C., and Murphy E. Phosphorylation of glycogen synthase kinase-3beta during preconditioning through a phosphatidylinositol-3-kinase-dependent pathway is cardioprotective. Circ Res 90 (2002) 377-379
102. Gross E.R., Hsu A.K., and Gross G.J. Opioid-induced cardioprotection occurs via glycogen synthase kinase beta inhibition during reperfusion in intact rat hearts. Circ Res 94 (2004) 960-966
103. Yin H., Chao L., and Chao J. Adrenomedullin protects against myocardial apoptosis after ischemia/reperfusion through activation of Akt-GSK signaling. Hypertension 43 (2004) 109-116
104. Barandon L., Dufourcq P., Costet P., Moreau C., Allieres C., Daret D., et al. Involvement of FrzA/sFRP-1 and the Wnt/frizzled pathway in ischemic preconditioning. Circ Res 96 (2005) 1299-1306
105. Meijer L., Flajolet M., and Greengard P. Pharmacological inhibitors of glycogen synthase kinase 3. Trends Pharmacol Sci 25 (2004) 471-480
106. Piantadosi C.A., Tatro L.G., and Whorton A.R. Nitric oxide and differential effects of ATP on mitochondrial permeability transition. Nitric Oxide 6 (2002) 45-60
107. Kim J.S., Ohshima S., Pediaditakis P., and Lemasters J.J. Nitric oxide protects rat hepatocytes against reperfusion injury mediated by the mitochondrial permeability transition. Hepatology 39 (2004) 1533-1543
108. Wang G., Liem D.A., Vondriska T.M., Honda H.M., Korge P., Pantaleon D.M., et al. Nitric oxide donors protect murine myocardium against infarction via modulation of mitochondrial permeability transition. Am J Physiol Heart Circ Physiol 288 (2005) H1290-H1295
109. Brookes P.S., Salinas E.P., Darley-Usmar K., Eiserich J.P., Freeman B.A., Darley-Usmar V.M., et al. Concentration-dependent effects of nitric oxide on mitochondrial permeability transition and cytochrome c release. J Biol Chem 275 (2000) 20474-20479
110. Davidson S.M., and Duchen M.R. Effects of NO on mitochondrial function in cardiomyocytes: pathophysiological relevance. Cardiovasc Res (2006) 10.1016/j.cardiores.2006.01.019 in press
111. Zhang S.Z., Gao Q., Cao C.M., Bruce I.C., and Xia Q. Involvement of the mitochondrial calcium uniporter in cardioprotection by ischemic preconditioning. Life Sci 78 (2006) 738-745