Contribution of calpains to myocardial ischaemia/reperfusion injury

Cardiovascular Research

Volumn 96, Issue 1, 2012, Pages 23-31

  Inserte, Javier ^a   Hernando, Victor ^a   Garcia Dorado, David ^a  

^a HOSPITAL UNIVERSITARI VALL D HEBRON   (Spain)

Author keywords

Calcium; Calpains; Ischaemia; Necrosis; Reperfusion

Indexed keywords

[1 [(1 FORMYL 2 PHENYLETHYL)CARBAMOYL] 2 METHYLPROPYL]CARBAMIC ACID BENZYL ESTER; A 790523; CALCIUM; CALPAIN; CALPASTATIN; CARDIOVASCULAR AGENT; LEUPEPTIN; MUSCLE PROTEIN; UNCLASSIFIED DRUG;

CALCIUM TRANSPORT; CELL DEATH; DRUG MECHANISM; ENZYME ACTIVATION; HEART MUSCLE CELL; HUMAN; IONIC STRENGTH; ISCHEMIC POSTCONDITIONING; ISCHEMIC PRECONDITIONING; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; REPERFUSION INJURY; REVIEW; SARCOLEMMA;

ANIMALS; CALCIUM; CALPAIN; ENZYME ACTIVATION; HUMANS; MYOCARDIAL ISCHEMIA; MYOCARDIAL REPERFUSION INJURY;

EID: 84866645505     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs232     Document Type: Review

References (126)

1. Zatz M, Starling A. Calpains and disease. N Engl J Med 2005;352:2413-2423.
2. Bulliard C, Marmy N, Dreyer JL. Effects of plasma membrane oxidoreductases on Ca2+ mobilization and protein phosphorylation in rat brain synaptosomes. J Bioenerg Biomembr 1990;22:645-662.
3. Ruiz-Meana M, Garcia-Dorado D, Julia M, Inserte J, Siegmund B, Ladilov Y et al. Protective effect of HOE642, a selective blocker of Na+-H+ exchange, against the development of rigor contracture in rat ventricular myocytes. Exp Physiol 2000;85: 17-25.
4. Siegmund B, Ladilov YV, Piper HM. Importance of sodium for recovery of calcium control in reoxygenated cardiomyocytes. Am J Physiol 1994;267:H506-H513.
5. Miyamae M, Camacho SA, Weiner MW, Figueredo VM. Attenuation of postischemic reperfusion injury is related to prevention of [Ca2+]m overload in rat hearts. Am J Physiol 1996;271:H2145-H2153.
6. Marban E, Kitakaze M, Kusuoka H, Porterfield JK, Yue DT, Chacko VP. Intracellular free calcium concentration measured with 19F NMR spectroscopy in intact ferret hearts. Proc Natl Acad Sci USA 1987;84:6005-6009.
7. Blaustein MP, Lederer WJ. Sodium/calcium exchange: its physiological implications. Physiol Rev 1999;79:763-854.
8. Ohtsuka M, Takano H, Suzuki M, Zou Y, Akazawa H, Tamagawa M et al. Role of Na+-Ca2+ exchanger in myocardial ischemia/reperfusion injury: evaluation using a heterozygous Na+-Ca2+ exchanger knockout mouse model. Biochem Biophys Res Commun 2004;314:849-853.
9. Tani M, Neely JR. Role of intracellular Na+ in Ca2+ overload and depressed recovery of ventricular function of reperfused ischemic rat hearts. Possible involvement of H+-Na+ and Na+-Ca2+ exchange. Circ Res 1989;65:1045-1056.
10. Imahashi K, Pott C, Goldhaber JI, Steenbergen C, Philipson KD, Murphy E. Cardiacspecific ablation of the Na+-Ca2+ exchanger confers protection against ischemia/reperfusion injury. Circ Res 2005;97:916-921.
11. Maddaford TG, Dibrov E, Hurtado C, Pierce GN. Reduced expression of the Na +Ca2+ exchanger in adult cardiomyocytes via adenovirally delivered shRNA results in resistance to simulated ischemic injury. Am J Physiol Heart Circ Physiol 2010;298: H360-H366.
12. Murphy E, Perlman M, London RE, Steenbergen C. Amiloride delays the ischemia-induced rise in cytosolic free calcium. Circ Res 1991;68:1250-1258.
13. Hartmann M, Decking UK. Blocking Na+-H+ exchange by cariporide reduces Na+-overload in ischemia and is cardioprotective. J Mol Cell Cardiol 1999;31:1985-1995.
14. Williams IA, Xiao XH, Ju YK, Allen DG. The rise of [Na+]i during ischemia and reperfusion in the rat heart-underlying mechanisms. Pflugers Arch 2007;454: 903-912.
15. ten Hove M, Jansen MA, Nederhoff MG, Van Echteld CJ. Combined blockade of the Na+ channel and the Na +H+ exchanger virtually prevents ischemic Na+ overload in rat hearts. Mol Cell Biochem 2007;297:101-110.
16. Chen X, Zhang X, Kubo H, Harris DM, Mills GD, Moyer J et al. Ca2+ influx-induced sarcoplasmic reticulum Ca2+ overload causes mitochondrial- dependent apoptosis in ventricular myocytes. Circ Res 2005;97:1009-1017.
17. Sun J, Picht E, Ginsburg KS, Bers DM, Steenbergen C, Murphy E. Hypercontractile female hearts exhibit increased S-nitrosylation of the L-type Ca2+ channel alpha1 subunit and reduced ischemia/reperfusion injury. Circ Res 2006;98:403-411.
18. Imahashi K, Kusuoka H, Hashimoto K, Yoshioka J, Yamaguchi H, Nishimura T. Intracellular sodium accumulation during ischemia as the substrate for reperfusion injury. Circ Res 1999;84:1401-1406.
19. Shintani-Ishida K, Yoshida K. Ischemia induces phospholamban dephosphorylation via activation of calcineurin, PKC-alpha, and protein phosphatase 1, thereby inducing calcium overload in reperfusion. Biochim Biophys Acta 2011;1812:743-751.
20. Vila-Petroff M, Salas MA, Said M, Valverde CA, Sapia L, Portiansky E et al. CaMKII inhibition protects against necrosis and apoptosis in irreversible ischemia-reperfusion injury. Cardiovasc Res 2007;73:689-698.
21. Vila-Petroff M, Mundina-Weilenmann C, Lezcano N, Snabaitis AK, Huergo MA, Valverde CA et al. Ca(2+)/calmodulin-dependent protein kinase II contributes to intracellular pH recovery from acidosis via Na(+)/H(+) exchanger activation. J Mol Cell Cardiol 2010;49:106-112.
22. Inserte J, Ruiz-Meana M, Rodriguez-Sinovas A, Barba I, Garcia-Dorado D. Contribution of delayed intracellular pH recovery to ischemic postconditioning protection. Antioxid Redox Signal 2011;14:923-939.
23. Farkas A, Tompa P, Friedrich P. Revisiting ubiquity and tissue specificity of human calpains. Biol Chem 2003;384:945-949.
24. Ilian MA, Gilmour RS, Bickerstaffe R. Quantification of ovine and bovine calpain I, calpain II, and calpastatin mRNA by ribonuclease protection assay. J Anim Sci 1999; 77:853-864.
25. Sandmann S, Yu M, Unger T. Transcriptional and translational regulation of calpain in the rat heart after myocardial infarction-effects of AT(1) and AT(2) receptor antagonists and ACE inhibitor. Br J Pharmacol 2001;132:767-777.
26. Molinari M, Carafoli E. Calpain: a cytosolic proteinase active at the membranes. J Membr Biol 1997;156:1-8.
27. Hood JL, Brooks WH, Roszman TL. Subcellular mobility of the calpain/calpastatin network: an organelle transient. Bioessays 2006;28:850-859.
28. Melloni E, Averna M, Salamino F, Sparatore B, Minafra R, Pontremoli S. Acyl-CoA-binding protein is a potent m-calpain activator. J Biol Chem 2000;275: 82-86.
29. Shulga N, Pastorino JG. Acyl coenzyme A-binding protein augments bid-induced mitochondrial damage and cell death by activating mu-calpain. J Biol Chem 2006; 281:30824-30833.
30. Matsumura Y, Saeki E, Otsu K, Morita T, Takeda H, Kuzuya T et al. Intracellular calcium level required for calpain activation in a single myocardial cell. J Mol Cell Cardiol 2001;33:1133-1142.
31. Steenbergen C, Murphy E, Levy L, London RE. Elevation in cytosolic free calcium concentration early in myocardial ischemia in perfused rat heart. Circ Res 1987;60: 700-707.
32. Steenbergen C, Perlman ME, London RE, Murphy E. Mechanism of preconditioning. Ionic alterations. Circ Res 1993;72:112-125.
33. Griffiths EJ, Ocampo CJ, Savage JS, Rutter GA, Hansford RG, Stern MD et al. Mitochondrial calcium transporting pathways during hypoxia and reoxygenation in single rat cardiomyocytes. Cardiovasc Res 1998;39:423-433.
34. Yoshida K, Yamasaki Y, Kawashima S. Calpain activity alters in rat myocardial subfractions after ischemia or reperfusion. Biochim Biophys Acta 1993;1182:215-220.
35. Yoshida K, Inui M, Harada K, Saido TC, Sorimachi Y, Ishihara T et al. Reperfusion of rat heart after brief ischemia induces proteolysis of calspectin (nonerythroid spectrin or fodrin) by calpain. Circ Res 1995;77:603-610.
36. Urthaler F, Wolkowicz PE, Digerness SB, Harris KD, Walker AA. MDL-28170, a membrane-permeant calpain inhibitor, attenuates stunning and PKC epsilon proteolysis in reperfused ferret hearts. Cardiovasc Res 1997;35:60-67.
37. Neuhof C, Fabiunke V, Deibele K, Speth M, Moller A, Lubisch Wet al. Reduction of myocardial infarction by calpain inhibitors A-705239 and A-705253 in isolated perfused rabbit hearts. Biol Chem 2004;385:1077-1082.
38. Inserte J, Garcia-Dorado D, Ruiz-Meana M, Agullo L, Pina P, Soler-Soler J. Ischemic preconditioning attenuates calpain-mediated degradation of structural proteins through a protein kinase A-dependent mechanism. Cardiovasc Res 2004;64:105-114.
39. Gilchrist JS, Cook T, Abrenica B, Rashidkhani B, Pierce GN. Extensive autolytic fragmentation of membranous versus cytosolic calpain following myocardial ischemia-reperfusion. Can J Physiol Pharmacol 2010;88:584-594.
40. Hernando V, Inserte J, Sartorio CL, Parra VM, Poncelas-Nozal M, Garcia-Dorado D. Calpain translocation and activation as pharmacological targets during myocardial ischemia/reperfusion. J Mol Cell Cardiol 2010;49:271-279.
41. Donkor IO. Calpain inhibitors: a survey of compounds reported in the patent and scientific literature. Expert Opin Ther Pat 2011;21:601-636.
42. Iizuka K, Kawaguchi H, Yasuda H, Kitabatake A. The role of calcium activated neutral protease on myocardial cell injury in hypoxia. Jpn Heart J 1992;33:707-715.
43. Atsma DE, Bastiaanse EM, Jerzewski A, Van der Valk LJ, Van der Laarse A. Role of calcium-activated neutral protease (calpain) in cell death in cultured neonatal rat cardiomyocytes during metabolic inhibition. Circ Res 1995;76:1071-1078.
44. Matsumura Y, Saeki E, Inoue M, Hori M, Kamada T, Kusuoka H. Inhomogeneous disappearance of myofilament-related cytoskeletal proteins in stunned myocardium of guinea pig. Circ Res 1996;79:447-454.
45. Zhao X, Newcomb JK, Posmantur RM, Wang KK, Pike BR, Hayes RL. pH dependency of mu-calpain and m-calpain activity assayed by casein zymography following traumatic brain injury in the rat. Neurosci Lett 1998;247:53-57.
46. Kendall TL, Koohmaraie M, Arbona JR, Williams SE, Young LL. Effect of pH and ionic strength on bovine m-calpain and calpastatin activity. J Anim Sci 1993;71:96-104.
47. Liu X, Rainey JJ, Harriman JF, Schnellmann RG. Calpains mediate acute renal cell death: role of autolysis and translocation. Am J Physiol Renal Physiol 2001;281: F728-738.
48. Spencer MJ, Tidball JG. Calpain translocation during muscle fiber necrosis and regeneration in dystrophin-deficient mice. Exp Cell Res 1996;226:264-272.
49. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 2003; 83:731-801.
50. Shiraha H, Glading A, Chou J, Jia Z, Wells A. Activation of m-calpain (calpain II) by epidermal growth factor is limited by protein kinase A phosphorylation of m-calpain. Mol Cell Biol 2002;22:2716-2727.
51. Glading A, Bodnar RJ, Reynolds IJ, Shiraha H, Satish L, Potter DA et al. Epidermal growth factor activates m-calpain (calpain II), at least in part, by extracellular signalregulated kinase-mediated phosphorylation. Mol Cell Biol 2004;24:2499-2512.
52. McClelland P, Adam LP, Hathaway DR. Identification of a latent Ca2 +calmodulin dependent protein kinase II phosphorylation site in vascular calpain II. J Biochem 1994; 115:41-46.
53. Hausenloy DJ, Yellon DM. Survival kinases in ischemic preconditioning and postconditioning. Cardiovasc Res 2006;70:240-253.
54. Takano E, Yumoto N, Kannagi R, Murachi T. Molecular diversity of calpastatin in mammalian organs. Biochem Biophys Res Commun 1984;122:912-917.
55. Takano E, Maki M, Mori H, Hatanaka M, Marti T, Titani K et al. Pig heart calpastatin: identification of repetitive domain structures and anomalous behavior in polyacrylamide gel electrophoresis. Biochemistry 1988;27:1964-1972.
56. Mellgren RL, Lane RD, Mericle MT. The binding of large calpastatin to biologic membranes is mediated in part by interaction of an amino terminal region with acidic phospholipids. Biochim Biophys Acta 1989;999:71-77.
57. Salamino F, De Tullio R, Michetti M, Mengotti P, Melloni E, Pontremoli S. Modulation of calpastatin specificity in rat tissues by reversible phosphorylation and dephosphorylation. Biochem Biophys Res Commun 1994;199:1326-1332.
58. Sorimachi Y, Harada K, Saido TC, Ono T, Kawashima S, Yoshida K. Downregulation of calpastatin in rat heart after brief ischemia and reperfusion. J Biochem 1997;122: 743-748.
59. Cong M, Thompson VF, Goll DE, Antin PB. The bovine calpastatin gene promoter and a new N-terminal region of the protein are targets for cAMP-dependent protein kinase activity. J Biol Chem 1998;273:660-666.
60. Pedrozo Z, Sanchez G, Torrealba N, Valenzuela R, Fernandez C, Hidalgo C et al. Calpains and proteasomes mediate degradation of ryanodine receptors in a model of cardiac ischemic reperfusion. Biochim Biophys Acta 2010;1802:356-362.
61. Michetti M, Salamino F, Melloni E, Pontremoli S. Reversible inactivation of calpain isoforms by nitric oxide. Biochem Biophys Res Commun 1995;207:1009-1014.
62. Koh TJ, Tidball JG. Nitric oxide inhibits calpain-mediated proteolysis of talin in skeletal muscle cells. Am J Physiol Cell Physiol 2000;279:C806-C812.
63. Chohan PK, Singh RB, Dhalla NS, Netticadan T. L-Arginine administration recovers sarcoplasmic reticulum function in ischemic reperfused hearts by preventing calpain activation. Cardiovasc Res 2006;69:152-163.
64. Norberg E, Gogvadze V, Vakifahmetoglu H, Orrenius S, Zhivotovsky B. Oxidative modification sensitizes mitochondrial apoptosis-inducing factor to calpain-mediated processing. Free Radic Biol Med 2010;48:791-797.
65. Sahara S, Yamashima T. Calpain-mediated Hsp70.1 cleavage in hippocampal CA1 neuronal death. Biochem Biophys Res Commun 2010;393:806-811.
66. Hamilton KL, Quindry JC, French JP, Staib J, Hughes J, Mehta JL et al. MnSOD antisense treatment and exercise-induced protection against arrhythmias. Free Radic Biol Med 2004;37:1360-1368.
67. Khaliulin I, Schneider A, Houminer E, Borman JB, Schwalb H. Apomorphine-induced myocardial protection is due to antioxidant and not adrenergic/dopaminergic effects. Free Radic Biol Med 2006;40:1713-1720.
68. Murphy E, Steenbergen C. Gender-based differences in mechanisms of protection in myocardial ischemia-reperfusion injury. Cardiovasc Res 2007;75:478-486.
69. Nadtochiy SM, Burwell LS, Brookes PS. Cardioprotection and mitochondrial Snitrosation: effects of S-nitroso-2-mercaptopropionyl glycine (SNO-MPG) in cardiac ischemia-reperfusion injury. J Mol Cell Cardiol 2007;42:812-825.
70. Khalil PN, Neuhof C, Huss R, Pollhammer M, Khalil MN, Neuhof H et al. Calpain inhibition reduces infarct size and improves global hemodynamics and left ventricular contractility in a porcine myocardial ischemia/reperfusion model. Eur J Pharmacol 2005;528:124-131.
71. Chen Q, Paillard M, Gomez L, Ross T, Hu Y, Xu A et al. Activation of mitochondrial mu-calpain increases AIF cleavage in cardiac mitochondria during ischemia-reperfusion. Biochem Biophys Res Commun 2011;415:533-538.
72. Shan L, Li J, Wei M, Ma J, Wan L, Zhu W et al. Disruption of Rac1 signaling reduces ischemia-reperfusion injury in the diabetic heart by inhibiting calpain. Free Radic Biol Med 2010;49:1804-1814.
73. Maekawa A, Lee JK, Nagaya T, Kamiya K, Yasui K, Horiba M et al. Overexpression of calpastatin by gene transfer prevents troponin I degradation and ameliorates contractile dysfunction in rat hearts subjected to ischemia/reperfusion. J Mol Cell Cardiol 2003;35:1277-1284.
74. Ruiz-Meana M, Garcia-Dorado D, Gonzalez MA, Barrabes JA, Soler-Soler J. Effect of osmotic stress on sarcolemmal integrity of isolated cardiomyocytes following transient metabolic inhibition. Cardiovasc Res 1995;30:64-69.
75. Armstrong SC, Latham CA, Shivell CL, Ganote CE. Ischemic loss of sarcolemmal dystrophin and spectrin: correlation with myocardial injury. J Mol Cell Cardiol 2001; 33:1165-1179.
76. Piper HM, Garcia-Dorado D, Ovize M. A fresh look at reperfusion injury. Cardiovasc Res 1998;38:291-300.
77. Post JA, Verkleij AJ, Langer GA. Organization and function of sarcolemmal phospholipids in control and ischemic/reperfused cardiomyocytes. J Mol Cell Cardiol 1995;27: 749-760.
78. Ganote C, Armstrong S. Ischaemia and the myocyte cytoskeleton: review and speculation. Cardiovasc Res 1993;27:1387-1403.
79. Iizuka K, Kawaguchi H, Kitabatake A. Effects of thiol protease inhibitors on fodrin degradation during hypoxia in cultured myocytes. J Mol Cell Cardiol 1993;25: 1101-1109.
80. Wang KK. Calpain and caspase: can you tell the difference? Trends Neurosci 2000;23: 20-26.
81. Kawada T, Masui F, Tezuka A, Ebisawa T, Kumagai H, Nakazawa M et al. A novel scheme of dystrophin disruption for the progression of advanced heart failure. Biochim Biophys Acta 2005;1751:73-81.
82. Liu X, Schnellmann RG. Calpain mediates progressive plasma membrane permeability and proteolysis of cytoskeleton-associated paxillin, talin, and vinculin during renal cell death. J Pharmacol Exp Ther 2003;304:63-70.
83. Jordan C, Puschel B, Koob R, Drenckhahn D. Identification of a binding motif for ankyrin on the alpha-subunit of Na+,K+-ATPase. J Biol Chem 1995;270: 29971-29975.
84. Rubtsov AM, Lopina OD. Ankyrins. FEBS Lett 2000;482:1-5.
85. Inserte J, Garcia-Dorado D, Hernando V, Soler-Soler J. Calpain-mediated impairment of Na +K+-ATPase activity during early reperfusion contributes to cell death after myocardial ischemia. Circ Res 2005;97:465-473.
86. Li ZP, Burke EP, Frank JS, Bennett V, Philipson KD. The cardiac Na+-Ca2+ exchanger binds to the cytoskeletal protein ankyrin. J Biol Chem 1993;268:11489-11491.
87. Kar P, Chakraborti T, Samanta K, Chakraborti S. mu-Calpain mediated cleavage of the Na +Ca2+ exchanger in isolated mitochondria under A23187 induced Ca2+ stimulation. Arch Biochem Biophys 2009;482:66-76.
88. Inserte J, Garcia-Dorado D, Ruiz-Meana M, Padilla F, Barrabes JA, Pina P et al. Effect of inhibition of Na +Ca2+ exchanger at the time of myocardial reperfusion on hypercontracture and cell death. Cardiovasc Res 2002;55:739-748.
89. Singh RB, Chohan PK, Dhalla NS, Netticadan T. The sarcoplasmic reticulum proteins are targets for calpain action in the ischemic-reperfused heart. J Mol Cell Cardiol 2004;37:101-110.
90. French JP, Quindry JC, Falk DJ, Staib JL, Lee Y, Wang KK et al. Ischemia-reperfusion-induced calpain activation and SERCA2a degradation are attenuated by exercise training and calpain inhibition. Am J Physiol Heart Circ Physiol 2006;290: H128-H136.
91. Chen M, Won DJ, Krajewski S, Gottlieb RA. Calpain and mitochondria in ischemia/reperfusion injury. J Biol Chem 2002;277:29181-29186.
92. Chen M, He H, Zhan S, Krajewski S, Reed JC, Gottlieb RA. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J Biol Chem 2001;276:30724-30728.
93. Polster BM, Basanez G, Etxebarria A, Hardwick JM, Nicholls DG. Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J Biol Chem 2005;280:6447-6454.
94. Kar P, Samanta K, Shaikh S, Chowdhury A, Chakraborti T, Chakraborti S. Mitochondrial calpain system: an overview. Arch Biochem Biophys 2010;495:1-7.
95. Smith MA, Schnellmann RG. Mitochondrial calpain 10 is degraded by Lon protease after oxidant injury. Arch Biochem Biophys 2012;517:144-152.
96. Barta J, Toth A, Edes I, Vaszily M, Papp JG, Varro A et al. Calpain-1-sensitive myofibrillar proteins of the human myocardium. Mol Cell Biochem 2005;278:1-8.
97. Feng HZ, Biesiadecki BJ, Yu ZB, Hossain MM, Jin JP. Restricted N-terminal truncation of cardiac troponin T: a novel mechanism for functional adaptation to energetic crisis. J Physiol 2008;586:3537-3550.
98. Zhang Z, Biesiadecki BJ, Jin JP. Selective deletion of the NH2-terminal variable region of cardiac troponin T in ischemia reperfusion by myofibril-associated mu-calpain cleavage. Biochemistry 2006;45:11681-11694.
99. Papp Z, van der Velden J, Stienen GJ. Calpain-I induced alterations in the cytoskeletal structure and impaired mechanical properties of single myocytes of rat heart. Cardiovasc Res 2000;45:981-993.
100. Blunt BC, Creek AT, Henderson DC, Hofmann PA. H2O2 activation of HSP25/27 protects desmin from calpain proteolysis in rat ventricular myocytes. Am J Physiol Heart Circ Physiol 2007;293:H1518-H1525.
101. 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.
102. Kishimoto A, Mikawa K, Hashimoto K, Yasuda I, Tanaka S, Tominaga M et al. Limited proteolysis of protein kinase C subspecies by calcium-dependent neutral protease (calpain). J Biol Chem 1989;264:4088-4092.
103. Kang MY, Zhang Y, Matkovich SJ, Diwan A, Chishti AH, Dorn GW 2nd. Receptorindependent cardiac protein kinase Calpha activation by calpain-mediated truncation of regulatory domains. Circ Res 2010;107:903-912.
104. Lakshmikuttyamma A, Selvakumar P, Sharma AR, Anderson DH, Sharma RK. In vitro proteolytic degradation of bovine brain calcineurin by m-calpain. Neurochem Res 2004;29:1913-1921.
105. Lakshmikuttyamma A, Selvakumar P, Kakkar R, Kanthan R, Wang R, Sharma RK. Activation of calcineurin expression in ischemia-reperfused rat heart and in human ischemic myocardium. J Cell Biochem 2003;90:987-997.
106. Wang KK, Villalobo A, Roufogalis BD. Calmodulin-binding proteins as calpain substrates. Biochem J 1989;262:693-706.
107. Tremper-Wells B, Vallano ML. Nuclear calpain regulates Ca2+-dependent signaling via proteolysis of nuclear Ca2 +calmodulin-dependent protein kinase type IV in cultured neurons. J Biol Chem 2005;280:2165-2175.
108. Hajimohammadreza I, Raser KJ, Nath R, Nadimpalli R, Scott M, Wang KK. Neuronal nitric oxide synthase and calmodulin-dependent protein kinase IIalpha undergo neurotoxin-induced proteolysis. J Neurochem 1997;69:1006-1013.
109. Yoshimura Y, Nomura T, Yamauchi T. Purification and characterization of active fragment of Ca2 +calmodulin-dependent protein kinase II from the post-synaptic density in the rat forebrain. J Biochem 1996;119:268-273.
110. Matsumura Y, Kusuoka H, Inoue M, Hori M, Kamada T. Protective effect of the protease inhibitor leupeptin against myocardial stunning. J Cardiovasc Pharmacol 1993;22: 135-142.
111. Donkor IO. A survey of calpain inhibitors. Curr Med Chem 2000;7:1171-1188.
112. Neuhof C, Gotte O, Trumbeckaite S, Attenberger M, Kuzkaya N, Gellerich F et al. A novel water-soluble and cell-permeable calpain inhibitor protects myocardial and mitochondrial function in postischemic reperfusion. Biol Chem 2003;384: 1597-1603.
113. Neuhof C, Fabiunk V, Speth M, Moller A, Fritz F, Tillmanns H et al. Reduction of myocardial infarction by postischemic administration of the calpain inhibitor A-705253 in comparison to the Na +H+ exchange inhibitor Cariporide in isolated perfused rabbit hearts. Biol Chem 2008;389:1505-1512.
114. Yoshikawa Y, Zhang GX, Obata K, Ohga Y, Matsuyoshi H, Taniguchi S et al. Cardioprotective effects of a novel calpain inhibitor SNJ-1945 for reperfusion injury after cardioplegic cardiac arrest. Am J Physiol Heart Circ Physiol 2010;298: H643-H651.
115. Galvez AS, Diwan A, Odley AM, Hahn HS, Osinska H, Melendez JG et al. Cardiomyocyte degeneration with calpain deficiency reveals a critical role in protein homeostasis. Circ Res 2007;100:1071-1078.
116. Inserte J, Garcia-Dorado D, Hernando V, Barba I, Soler-Soler J. Ischemic preconditioning prevents calpain-mediated impairment of Na +K+-ATPase activity during early reperfusion. Cardiovasc Res 2006;70:364-373.
117. Imajoh S, Aoki K, Ohno S, Emori Y, Kawasaki H, Sugihara H et al. Molecular cloning of the cDNA for the large subunit of the high-Ca2+-requiring form of human Ca2+-activated neutral protease. Biochemistry 1988;27:8122-8128.
118. Lochner A, Genade S, Tromp E, Podzuweit T, Moolman JA. Ischemic preconditioning and the beta-adrenergic signal transduction pathway. Circulation 1999;100: 958-966.
119. 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 2004;110:51-57.
120. Cohen MV, Yang XM, Downey JM. The pH hypothesis of postconditioning: staccato reperfusion reintroduces oxygen and perpetuates myocardial acidosis. Circulation 2007;115:1895-1903.
121. Inserte J, Barba I, Hernando V, Garcia-Dorado D. Delayed recovery of intracellular acidosis during reperfusion prevents calpain activation and determines protection in postconditioned myocardium. Cardiovasc Res 2009;81:116-122.
122. Inserte J, Barba I, Poncelas-Nozal M, Hernando V, Agullo L, Ruiz-Meana M et al. cGMP/PKG pathway mediates myocardial postconditioning protection in rat hearts by delaying normalization of intracellular acidosis during reperfusion. J Mol Cell Cardiol 2011;50:903-909.
123. Inserte J, Barrabes JA, Hernando V, Garcia-Dorado D. Orphan targets for reperfusion injury. Cardiovasc Res 2009;83:169-178.
124. Hanna RA, Campbell RL, Davies PL. Calcium-bound structure of calpain and its mechanism of inhibition by calpastatin. Nature 2008;456:409-412.
125. Moldoveanu T, Gehring K, Green DR. Concerted multi-pronged attack by calpastatin to occlude the catalytic cleft of heterodimeric calpains. Nature 2008;456: 404-408.
126. Singh RB, Dhalla NS. Ischemia reperfusion-induced changes in sarcolemmal Na +K+-ATPase are due to the activation of calpain in the heart. Can J Physiol Pharmacol 2010; 88:388-397.