Calpains, mitochondria, and apoptosis

Cardiovascular Research

Volumn 96, Issue 1, 2012, Pages 32-37

  Smith, Matthew A ^a   Schnellmann, Rick G ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Calpains; Cardiovascular system; Mitochondria

Indexed keywords

CALPAIN; CALPAIN 1; CALPAIN 2; CASPASE 3; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOTHELIUM CELL; ENZYME ACTIVATION; HEART MUSCLE ISCHEMIA; HUMAN; KIDNEY DISEASE; KIDNEY TUBULE CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SMOOTH MUSCLE FIBER;

ANIMALS; APOPTOSIS; CALCIUM; CALPAIN; ENDOTHELIAL CELLS; HUMANS; KIDNEY; MITOCHONDRIA; MYOCARDIUM; MYOCYTES, SMOOTH MUSCLE;

EID: 84866685475     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs163     Document Type: Review

References (113)

1. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 2003; 83:731-801.
2. Dayton WR, Reville WJ, Goll DE, Stromer MH. A calcium(2+) ion-activated protease possibly involved in myofibrillar protein turnover. Partial characterization of the purified enzyme. Biochemistry 1976;15:2159-2167.
3. Dayton WR, Goll DE, Zeece MG, Robson RM, Reville WJ. A Ca2+ ion-activated protease possibly involved in myofibrillar protein turnover. Purification from porcine muscle. Biochemistry 1976;15:2150-2158.
4. Futai E, Kubo T, Sorimachi H, Suzuki K, Maeda T. Molecular cloning of PalBH, a mammalian homologue of the Aspergillus atypical calpain PalB. Biochim Biophys Acta 2001; 1517:316-319.
5. Lee H-J, Tomioka S, Kinbara K, Masumoto H, Jeong S-Y, Sorimachi H et al. Characterization of a human digestive tract-specific calpain, nCL-4, expressed in the baculovirus system. Arch Biochem Biophys 1999;362:22-31.
6. Liu K, Li L, Cohen SN. Antisense RNA-mediated deficiency of the calpain protease, nCL-4, in NIH3T3 cells is associated with neoplastic transformation and tumorigenesis. J Biol Chem 2000;275:31093-31098.
7. Ma H, Fukiage C, Kim YH, Duncan MK, Reed NA, Shih M et al. Characterization and expression of calpain 10. J Biol Chem 2001;276:28525-28531.
8. Matena K, Boehm T, Dear TN. Genomic organization of MouseCapn5andCapn6- Genes confirms that they are a distinct calpain subfamily. Genomics 1998;48: 117-120.
9. Sorimachi H, Imajoh-Ohmi S, Emori Y, Kawasaki H, Ohno S, Minami Y et al. Molecular cloning of a novel mammalian calcium-dependent protease distinct from both mand mu-types. Specific expression of the mRNA in skeletal muscle. J Biol Chem 1989; 264:20106-20111.
10. Dear N, Matena K, Vingron M, Boehm T. A new subfamily of vertebrate calpains lacking a calmodulin-like domain: implications for calpain regulation and evolution. Genomics 1997;45:175-184.
11. Sorimachi H, Ishiura S, Suzuki K. A novel tissue-specific calpain species expressed predominantly in the stomach comprises two alternative splicing products with and without Ca(2+)-binding domain. J Biol Chem 1993;268:19476-19482.
12. Dear TN, Boehm T. Identification and characterization of two novel calpain large subunit genes. Gene 2001;274:245-252.
13. Dear TN, Mö ller A, Boehm T. CAPN11: a calpain with high mRNA levels in testis and located on chromosome 6. Genomics 1999;59:243-247.
14. Dear TN, Meier NT, Hunn M, Boehm T. Gene structure, chromosomal localization, and expression pattern of Capn12, a new member of the calpain large subunit gene family. Genomics 2000;68:152-160.
15. Kamei M, Webb GC, Young IG, Campbell HD. SOLH, a human homologue of the Drosophila melanogaster small optic lobes gene is a member of the calpain and zincfinger gene families and maps to human chromosome 16p13.3 near CATM (Cataract with Microphthalmia). Genomics 1998;51:197-206.
16. Suzuki K, Hata S, Kawabata Y, Sorimachi H. Structure, activation, and biology of calpain. Diabetes 2004;53:S12-S18.
17. Zatz M, Starling A. Calpains and disease. N Engl J Med 2005;352:2413-2423.
18. Arrington DD, Van Vleet TR, Schnellmann RG. Calpain 10: a mitochondrial calpain and its role in calcium-induced mitochondrial dysfunction. Am J Physiol Cell Physiol 2006;291:C1159-C1171.
19. Reverter D, Braun M, Fernandez-Catalan C, Strobl S, Sorimachi H, Bode W. Flexibility analysis and structure comparison of two crystal forms of calcium-free human m-calpain. Biol Chem 2002;383:1415-1422.
20. Moldoveanu T, Hosfield CM, Lim D, Elce JS, Jia Z, Davies PL. A Ca2+ switch aligns the active site of calpain. Cell 2002;108:649-660.
21. Tompa P, Emori Y, Sorimachi H, Suzuki K, Friedrich P. Domain III of calpain is a Ca2+-regulated phospholipid-binding domain. Biochem Biophys Res Commun 2001; 280:1333-1339.
22. Hayashi M, Suzuki H, Kawashima S, Saido TC, Inomata M. The behavior of calpaingenerated N-and C-terminal fragments of talin in integrin-mediated signaling pathways. Arch Biochem Biophys 1999;371:133-141.
23. Strobl S, Fernandez-Catalan C, Braun M, Huber R, Masumoto H, Nakagawa K et al. The crystal structure of calcium-free human m-calpain suggests an electrostatic switch mechanism for activation by calcium. Proc Natl Acad Sci USA 2000;97: 588-592.
24. Sorimachi H, Ishiura S, Suzuki K. Structure and physiological function of calpains. Biochem J 1997;328:721-732.
25. Kinbara K, Sorimachi H, Ishiura S, Suzuki K. Muscle-specific calpain, p94, interacts with the extreme C-terminal region of connectin, a unique region flanked by two immunoglobulin C2 motifs. Arch Biochem Biophys 1997;342:99-107.
26. Friedrich P, Papp H, Halasy K, Farkas A, Farkas B, Tompa P et al. Differential distribution of calpain small subunit 1 and 2 in rat brain. Eur J Neurosci 2004;19: 1819-1825.
27. Ma H, Nakajima E, Shih M, Azuma M, Shearer TR. Expression of calpain small subunit 2 in mammalian tissues. Curr Eye Res 2004;29:337-347.
28. Zimmerman U-JP, Boring L, Pak UH, Mukerjee N, Wang KKW. The calpain small subunit gene is essential: its inactivation results in embryonic lethality. IUBMB Life 2000;50:63-68.
29. Sorimachi H, Suzuki K. The structure of calpain. J Biochem 2001;129:653-664.
30. Geesink GH, Nonneman D, Koohmaraie M. An improved purification protocol for heart and skeletal muscle calpastatin reveals two isoforms resulting from alternative splicing. Arch Biochem Biophys 1998;356:19-24.
31. Parr T, Sensky PL, Bardsley RG, Buttery PJ. Calpastatin expression in porcine cardiac and skeletal muscle and partial gene structure. Arch Biochem Biophys 2001;395:1-13.
32. Takano J, Watanabe M, Hitomi K, Maki M. Four types of calpastatin isoforms with distinct amino-terminal sequences are specified by alternative first exons and differentially expressed in mouse tissues. J Biochem 2000;128:83-92.
33. Kawasaki H, Emori Y, Imajoh-Ohmi S, Minami Y, Suzuki K. Identification and characterization of inhibitory sequences in four repeating domains of the endogenous inhibitor for calcium-dependent protease. J Biochem 1989;106:274-281.
34. 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.
35. Michiels C. Endothelial cell functions. J Cell Physiol 2003;196:430-443.
36. Rodgers G, Cong J, Goll D, Kane W. Activation of coagulation factor V by calciumdependent proteinase. Biochim Biophys Acta 1987;929:263-270.
37. Hayashi M, Kasai Y, Kawashima S. Preferential localization of calcium-activated neutral protease in epithelial tissues. Biochem Biophys Res Commun 1987;148: 567-574.
38. Fujitani K, Kambayashi J-i, Sakon M, Ohmi SI, Kawashima S-i, Yukawa M et al. Identification of m-, m-calpains and calpastatin and capture of m-calpain activation in endothelial cells. J Cell Biochem 1997;66:197-209.
39. Carragher NO, Frame MC. Calpain: a role in cell transformation and migration. Int J Biochem Cell Biol 2002;34:1539-1543.
40. Glading A, Lauffenburger DA,Wells A. Cutting to the chase: calpain proteases in cell motility. Trends Cell Biol 2002;12:46-54.
41. Perrin BJ, Amann KJ, Huttenlocher A. Proteolysis of cortactin by calpain regulates membrane protrusion during cell migration. Mol Biol Cell 2006;17:239-250.
42. Qiu K, Su Y, Block E. Use of recombinant calpain-2 siRNA adenovirus to assess calpain-2 modulation of lung endothelial cell migration and proliferation. Mol Cell Biochem 2006;292:69-78.
43. Ma H, Tochigi A, Shearer TR, Azuma M. Calpain inhibitor SNJ-1945 attenuates events prior to angiogenesis in cultured human retinal endothelial cells. J Ocul Pharmacol Ther 2009;25:409-414.
44. Mo X-G, Chen Q-W, Li X-S, Zheng M-M, Ke D-Z, Deng W et al. Suppression of NHE1 by small interfering RNA inhibits HIF-1a-induced angiogenesis in vitro via modulation of calpain activity. Microvasc Res 2011;81:160-168.
45. Letavernier B, Zafrani L, Nassar D, Perez J, Levi C, Bellocq A et al. Calpains contribute to vascular repair in rapidly progressive form of glomerulonephritis: potential role of their externalization. Arterioscler Thromb Vasc Biol 2012;32:335-342.
46. Hoang MV, Nagy J, Fox JEB, Senger DR. Moderation of calpain activity promotes neovascular integration and lumen formation during VEGF-induced pathological angiogenesis. PLoS One 2010;5:e13612.
47. Gonscherowski V, Becker BF, Moroder L, Motrescu E, Gil-Parrado S, Gloe T et al. Calpains: a physiological regulator of the endothelial barrier? Am J Physiol Heart Circ Physiol 2006;290:H2035-H2042.
48. Scalia R, Gong Y, Berzins B, Freund B, Feather D, Landesberg G et al. A novel role for calpain in the endothelial dysfunction induced by activation of angiotensin II type 1 receptor signaling/novelty and significance. Circ Res 2011;108:1102-1111.
49. Kang H, Kwak H-I, Kaunas R, Bayless KJ. Fluid shear stress and sphingosine 1-phosphate activate calpain to promote membrane type 1 matrix metalloproteinase (MT1-MMP) membrane translocation and endothelial invasion into threedimensional collagen matrices. J Biol Chem 2011;286:42017-42026.
50. Vindis C, Elbaz M, Escargueil-Blanc I, Augé N, Heniquez A, Thiers J-C et al. Two distinct calcium-dependent mitochondrial pathways are involved in oxidized LDL-induced apoptosis. Arterioscler Thromb Vasc Biol 2005;25:639-645.
51. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 2003;4:552-565.
52. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J 1999;341:233-249.
53. Kroemer G, Reed JC. Mitochondrial control of cell death. Nat Med 2000;6:513-519.
54. Bernardi P, Petronilli V, Di Lisa F, Forte M. A mitochondrial perspective on cell death. Trends Biochem Sci 2001;26:112-117.
55. Henry-Mowatt J, Dive C, Martinou J-C, James D. Role of mitochondrial membrane permeabilization in apoptosis and cancer. Oncogene 2004;23:2850-2860.
56. Zhao Y, Ding W-x, Qian T, Watkins S, Lemasters JJ, Yin X-m. Bid activates multiple mitochondrial apoptotic mechanisms in primary hepatocytes after death receptor engagement. Gastroenterology 2003;125:854-867.
57. Walter DH, Haendeler J, Galle J, Zeiher AM, Dimmeler S. Cyclosporin A inhibits apoptosis of human endothelial cells by preventing release of cytochrome C from mitochondria. Circulation 1998;98:1153-1157.
58. Pörn-Ares MI, Saido TC, Andersson T, Ares MPS. Oxidized low-density lipoprotein induces calpain-dependent cell death and ubiquitination of caspase 3 in HMEC-1 endothelial cells. Biochem J 2003;374:403-411.
59. Cregan SP, Dawson VL, Slack RS. Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 2004;23:2785-2796.
60. Mallat Z, Tedgui A. Apoptosis in the vasculature: mechanisms and functional importance. Br J Pharmacol 2000;130:947-962.
61. Geng Y-J, Libby P. Progression of atheroma. Arterioscler Thromb Vasc Biol 2002;22: 1370-1380.
62. Song J, Liu K, Yi J, Zhu D, Liu G, Liu B. Luteolin inhibits lysophosphatidylcholine-induced apoptosis in endothelial cells by a calcium/mitocondrion/caspases-dependent pathway. Planta Med 2010;76:433-438.
63. Moshal KS, Singh M, Sen U, Rosenberger DSE, Henderson B, Tyagi N et al. Homocysteine-mediated activation and mitochondrial translocation of calpain regulates MMP-9 in MVEC. Am J Physiol Heart Circ Physiol 2006;291:H2825-H2835.
64. Papatheodorou L, Weiss N. Vascular oxidant stress and inflammation in hyperhomocysteinemia. Antioxid Redox Signal 2007;9:1941-1958.
65. Kar P, Chakraborti T, Samanta K, Chakraborti S. Submitochondrial localization of associated m-calpain and calpastatin. Arch Biochem Biophys 2008;470:176-186.
66. Kar P, Chakraborti T, Samanta K, Chakraborti S. m-Calpain mediated cleavage of the Na +Ca2+ exchanger in isolated mitochondria under A23187 induced Ca2+ stimulation. Arch Biochem Biophys 2009;482:66-76.
67. Hoang MV, Smith LEH, Senger DR. Calpain inhibitors reduce retinal hypoxia in ischemic retinopathy by improving neovascular architecture and functional perfusion. Biochim Biophys Acta 2011;1812:549-557.
68. Tsubokawa T, Yamaguchi-Okada M, Calvert JW, Solaroglu I, Shimamura N, Yata K et al. Neurovascular and neuronal protection by E64d after focal cerebral ischemia in rats. J Neurosci Res 2006;84:832-840.
69. Yadav SS, Sindram D, Perry DK, Clavien P-A. Ischemic preconditioning protects the mouse liver by inhibition of apoptosis through a caspase-dependent pathway. Hepatology 1999;30:1223-1231.
70. Seyfried DM, Veyna R, Han Y, Li K, Tang N, Betts RL et al. A selective cysteine protease inhibitor is non-toxic and cerebroprotective in rats undergoing transient middle cerebral artery ischemia. Brain Res 2001;901:94-101.
71. 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-F738.
72. Waters SL, Sarang SS, Wang KKW, Schnellmann RG. Calpains mediate calcium and chloride influx during the late phase of cell injury. J Pharmacol Exp Ther 1997;283: 1177-1184.
73. Harriman JF, Waters-Williams S, Chu D-L, Powers JC, Schnellmann RG. Efficacy of novel calpain inhibitors in preventing renal cell death. J Pharmacol Exp Ther 2000;294: 1083-1087.
74. Harriman J, Liu X, Aleo M, Machaca K, Schnellmann R. Endoplasmic reticulum Ca2+ signaling and calpains mediate renal cell death. Cell Death Differ 2002;9:734-741.
75. 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.
76. Neumar RW, Xu YA, Gada H, Guttmann RP, Siman R. Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis. J Biol Chem 2003;278: 14162-14167.
77. Chua BT, Guo K, Li P. Direct cleavage by the calcium-activated protease calpain can lead to inactivation of caspases. J Biol Chem 2000;275:5131-5135.
78. Lee W-K, Abouhamed M, Thévenod F. Caspase-dependent and-independent pathways for cadmium-induced apoptosis in cultured kidney proximal tubule cells. Am J Physiol Renal Physiol 2006;291:F823-F832.
79. Nakagawa T, Yuan J. Cross-talk between two cysteine protease families. J Cell Biol 2000;150:887-894.
80. Giguere CJ, Covington MD, Schnellmann RG. Mitochondrial calpain 10 activity and expression in the kidney of multiple species. Biochem Biophys Res Commun 2008;366: 258-262.
81. Shumway SD, Maki M, Miyamoto S. The PEST domain of IkBa is necessary and sufficient for in vitro degradation by m-calpain. J Biol Chem 1999;274:30874-30881.
82. Rogers S, Wells R, Rechsteiner M. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science 1986;234:364-368.
83. Spencer ML, Theodosiou M, Noonan DJ. NPDC-1, a novel regulator of neuronal proliferation, is degraded by the ubiquitin/proteasome system through a PEST degradation motif. J Biol Chem 2004;279:37069-37078.
84. Coca SG. Acute kidney injury in elderly persons. Am J Kidney Dis 2010;56:122-131.
85. Covington MD, Arrington DD, Schnellmann RG. Calpain 10 is required for cell viability and is decreased in the aging kidney. Am J Physiol Renal Physiol 2009;296: F478-F486.
86. Jung K-Y, Dean D, Jiang J, Gaylor S, Griffith WH, Burghardt RC et al. Loss of Ncadherin and a-catenin in the proximal tubules of aging male Fischer 344 rats. Mech Ageing Dev 2004;125:445-453.
87. Horikawa Y, Oda N, Cox NJ, Li X, Orho-Melander M, Hara M et al. Genetic variation in the gene encoding calpain-10 is associated with type 2 diabetes mellitus. Nat Genet 2000;26:163-175.
88. Covington MD, Schnellmann RG. Chronic high glucose downregulates mitochondrial calpain 10 and contributes to renal cell death and diabetes-induced renal injury. Kidney Int 2012;81:391-400.
89. Lin G-d, Chattopadhyay D, Maki M, Wang KKW, Carson M, Jin L et al. Crystal structure of calcium bound domain VI of calpain at 1.9 A resolution and its role in enzyme assembly, regulation, and inhibitor binding. Nat Struct Mol Biol 1997;4:539-547.
90. Todd B, Moore D, Deivanayagam CCS, Lin G-d, Chattopadhyay D, Maki M et al. A Structural model for the inhibition of calpain by calpastatin: crystal structures of the native domain VI of calpain and its complexes with calpastatin peptide and a small molecule inhibitor. J Mol Biol 2003;328:131-146.
91. Rasbach KA, Arrington DD, Odejinmi S, Giguere C, Beeson CC, Schnellmann RG. Identification and optimization of a novel inhibitor of mitochondrial calpain 10. J Med Chem 2008;52:181-188.
92. Leonardo B. Changing patterns of ST elevation myocardial infarction epidemiology. Am Heart J 2010;160:S1-S3.
93. Gao W, Atar D, Liu Y, Perez N, Murphy A, Marban E. Role of troponin I proteolysis in the pathogenesis of stunned myocardium. Circ Res 1997;80:393-399.
94. Iwamoto H, Miura T, Okamura T, Shirakawa K, Iwatate M, Kawamura S et al. Calpain inhibitor-1 reduces infarct size and DNA fragmentation of mycardium in ischemia/reperfused rat heart. J Cardiovasc Pharmacol 1999;33:580-586.
95. Urthaler F, Wolkowicz PE, Digerness SB, Harris KD, Walker AA. MDL-28170, a membrane-permeant calpain inhibitor, attenuates stunning and PKC1 proteolysis in reperfused ferret hearts. Cardiovasc Res 1997;35:60-67.
96. Gao G, Dou QP. N-terminal cleavage of Bax by calpain generates a potent proapoptotic 18-kDa fragment that promotes Bcl-2-independent cytochrome C release and apoptotic cell death. J Cell Biochem 2001;80:53-72.
97. Aguilar HI, Botla R, Arora AS, Bronk SF, Gores GJ. Induction of the mitochondrial permeability transition by protease activity in rats: A mechanism of hepatocyte necrosis. Gastroenterology 1996;110:558-566.
98. Gores GJ, Miyoshi H, Botla R, Aguilar HI, Bronk SF. Induction of the mitochondrial permeability transition as a mechanism of liver injury during cholestasis: a potential role for mitochondrial proteases. Biochim Biophys Acta 1998;1366:167-175.
99. Kohli V, Madden J, Bentley R, Clavien P. Calpain mediates ischemic injury of the liver through modulation of apoptosis and necrosis. Gastroenterology 1999;116:168-178.
100. Wang KKW, Posmantur R, Nadimpalli R, Nath R, Mohan P, Nixon RA et al. Caspasemediated fragmentation of calpain inhibitor protein calpastatin during apoptosis. Arch Biochem Biophys 1998;356:187-196.
101. Trumbeckaite S, Neuhof C, Zierz S, Gellerich FN. Calpain inhibitor (BSF 409425) diminishes ischemia/reperfusion-induced damage of rabbit heart mitochondria. Biochem Pharmacol 2003;65:911-916.
102. 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.
103. Perrin C, Escarnot-Laubriet A, Vergely C, Rochette L. Calpain and caspase-3 inhibitors reduce infarct size and post-ischemic apoptosis in rat heart without modifying contractile recovery. Cell Mol Biol 2003;49:497-505.
104. Kakkar R,Wang X, Radhi JM, Rajala RVS,Wang R, Sharma RK. Decreased expression of high-molecular-weight calmodulin-binding protein and its correlation with apoptosis in ischemia-reperfused rat heart. Cell Calcium 2001;29:59-71.
105. Levine B, Kalman J, Mayer L, Fillit HM, Packer M. Elevated circulating levels of tumor necrosis factor in severe chronic heart failure. New Engl J Med 1990;323:236-241.
106. Aggarwal BB. Signalling pathways of the TNF superfamily: a double-edged sword. Nat Rev Immunol 2003;3:745-756.
107. Bajaj G, Sharma RK. TNF-a-mediated cardiomyocyte apoptosis involves caspase-12 and calpain. Biochem Biophys Res Commun 2006;345:1558-1564.
108. Chen Q, Paillard M, Gomez L, Ross T, Hu Y, Xu A et al. Activation of mitochondrial m-calpain increases AIF cleavage in cardiac mitochondria during ischemia-reperfusion. Biochem Biophys Res Commun 2011;415:533-538.
109. Ozaki T, Yamashita T, Ishiguro S-i. ERp57-associated mitochondrial m-calpain truncates apoptosis-inducing factor. Biochim Biophys Acta 2008;1783:1955-1963.
110. Ye H, Cande C, Stephanou NC, Jiang S, Gurbuxani S, Larochette N et al. DNA binding is required for the apoptogenic action of apoptosis inducing factor. Nat Struct Mol Biol 2002;9:680-684.
111. Joshi A, Bondada V, Geddes JW. Mitochondrial m-calpain is not involved in the processing of apoptosis-inducing factor. Exp Neurol 2009;218:221-227.
112. Wendt A, Thompson V, Goll D. Interaction of calpastatin with calpain: a review. Biol Chem 2004;385:465-472.
113. Ozaki T, Yamashita T, Ishiguro S-i. Mitochondrial m-calpain plays a role in the release of truncated apoptosis-inducing factor from the mitochondria. Biochim Biophys Acta 2009;1793:1848-1859.