The Role of Calpain in Oncotic Cell Death

Annual Review of Pharmacology and Toxicology

Volumn 44, Issue , 2004, Pages 349-370

  Liu, Xiuli ^a   Van Vleet, Terry ^b   Schnellmann, Rick G ^b  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Calcium; Cytoskeleton; Mitochondria; Oncosis; Plasma membrane permeability

Indexed keywords

CALPAIN; CALPASTATIN; CYSTEINE PROTEINASE; CYTOSKELETON PROTEIN;

CELL DEATH; CELL FUNCTION; CELL MEMBRANE PERMEABILITY; CYTOSKELETON; ENZYME SUBSTRATE; HUMAN; ION PERMEABILITY; MITOCHONDRION; NONHUMAN; ONCOTIC PRESSURE; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW;

ADENOSINE TRIPHOSPHATE; ANIMALS; APOPTOSIS; CALCIUM; CALPAIN; HUMANS; MITOCHONDRIA; MODELS, BIOLOGICAL; NECROSIS;

EID: 1342281236     PISSN: 03621642     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.pharmtox.44.101802.121804     Document Type: Review

References (154)

1. Majno G, Joris I. 1995. Apoptosis, oncosis, and necrosis: an overview of cell death. Am. J. Pathol. 146:3-15
2. Levin S, Bucci TJ, Cohen SM, Fix AS, Hardisty JF, et al. 1999. The nomenclature of cell death: recommendations of an ad hoc committee of the society of toxicologic pathologists. Toxicol. Pathol. 27: 484-90
3. Savill JS, Mooney AF, Hughes J. 1997. Apoptosis in acute renal inflammation. In Immunologic Renal Diseases, ed. EG Neilson, WG Couser, pp. 309-29. Philadelphia: Lippincott-Raven
4. Trump BF, Berezesky IK, Chang SH, Phelps PC. 1997. The pathways of cell death: oncosis, apoptosis, and necrosis. Toxicol. Pathol. 25:82-88
5. Lemasters JJ. 1999. Necrapoptosis and the mitochondrial permeability transition: shared pathways to necrosis and apoptosis. Am. J. Physiol. Gastrointest. Liver Physiol. 276:G1-6
6. Arends MJ, Morris RG, Wyllie AH. 1990. Apoptosis: the role of the endonuclease. Am. J. Pathol. 136:593-608
7. 2+. Biochem. Biophys. Res. Commun. 181:915-20
8. Compton MM. 1992. A biochemical hallmark of apoptosis: internucleosomal degradation of the genome. Cancer Metastasis Rev. 11:105-19
9. Moran JH, Schnellmann RG. 1997. Diverse cytoprotectants prevent cell lysis and promote recovery of respiration and ion transport. Biochem. Biophys. Res. Commun. 234:275-77
10. Liu X, Rainey JJ, Harriman JF, Schnellmann RG. 2001. Calpains mediate acute renal cell death: role of autolysis and translocation. Am. J. Physiol. Renal Physiol. 81:F728-38
11. Liu X, Harriman JF, Schnellmann RG. 2002. Cytoprotective properties of novel nonpeptide calpain inhibitors in renal cells. J. Pharmacol. Exp. Ther. 302:88-94
12. Lieberthal W, Menza SA, Levine JS. 1998. Graded ATP depletion can cause necrosis or apoptosis of cultured mouse proximal tubular cells. Am. J. Physiol. Renal Physiol. 274:F315-27
13. Berridge MJ. 1993. Inositol trisphosphate and calcium signaling. Nature 361:315-25
14. Schanne FA, Kane AB, Young EE, Farber JL. 1979. Calcium dependence of toxic cell death: a final common pathway. Science 206:700-2
15. 2+ and mitochondrial membrane potential preceding cell death in hepatocytes. Nature 325:78-81
16. Kobryn CE, Mandel LJ. 1994. Decreased protein phosphorylation induced by anoxia in proximal renal tubules. Am. J. Physiol. Cell Physiol. 267:C1073-79
17. Schnellmann RG, Griffin JM, Sarang SS. 1995. J. Am. Soc. Nephrol. 6:1004 (Abstr.)
18. 2+ signaling and calpains mediate renal cell death. Cell Death Differ. 9:734-41
19. Waters SL, Wong JK, Schnellmann RG. 1997. Depletion of endoplasmic reticulum calcium stores protects against hypoxia-and mitochondrial inhibitor-induced cellular injury and death. Biochem. Biophys. Res. Commun. 240:57-60
20. Guroff G. 1964. A neutral calcium-activated proteinase from the soluble fraction of rat brain. J. Biol. Chem. 239:149-55
21. Huang Y, Wang KK. 2001. The calpain family and human disease. Trends Mol. Med. 7:355-62
22. Sorimachi H, Ishiura S, Suzuki K. 1997. Structure and physiological function of calpains. Biochem. J. 328:721-32
23. Croall DE, Demartino GN. 1991. Calcium-activated neutral protease (calpain) system: structure, function and regulation. Physiol. Rev. 71:813-47
24. Saido TC, Suzuki H, Yamazaki H, Tanoue K, Suzuki K. 1993. In situ capture of tt-calpain activation in platelets. J. Biol. Chem. 268:7422-26
25. Saido TC, Sorimachi H, Suzuki K. 1994. Calpain: new perspectives in molecular diversity and physiological-pathological involvement. FASEB J. 8:814-22
26. Azam M, Andrabi SS, Sahr KE, Kamath L, Kuliopulos A, Chishti AH, et al. 2001. Disruption of the mouse μ-calpain gene reveals an essential role in platelet function. Mol. Cell. Biol. 21:2213-20
27. Arthur JSC, Elce JS, Hegadorn C, Williams K, Greer PA. 2000. Disruption of the murine calpain small subunit gent, capn4: calpain is essential for embryonic development but not for cell growth and division. Mol. Cell. Biol. 20:4474-81
28. Zhang W, Lu Q, Xie ZJ, Mellgren RL. 1997. Inhibition of the growth of WI-38 fibroblasts by benzyloxycarbonyl-Leu-Leu-Tyr diazomethyl ketone: evidence that cleavage of p53 by a calpain-like protease is necessary for G1 to S-phase transition. Oncogene 14:255-63
29. Zhang W, Lane RD, Mellgren RL. 1996. The major calpain isozymes are long-lived proteins. Design of an antisense strategy for calpain depletion in cultured cells. J. Biol. Chem. 271:18825-30
30. Patel Y, Lane MD. 2000. Mitotic clonal expansion during preadipocyte differentiation: calpain-mediated turnover of p27. J. Biol. Chem. 275:17653-60
31. Grynspan F, Griffin WB, Mohan PS, Shea TB, Nixon RA. 1997. Calpains and calpastatin in SH-SY5Y neuroblastoma cells during retinoic acid-induced differentiation and neurite outgrowth: comparison with the human brain calpain system. J. Neurosci. Res. 48:181-91
32. Glading A, Chang P, Lauffenburger DA, Wells A. 2000. Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway. J. Biol. Chem. 275:2390-98
33. Glading A, Uberall F, Keyse SM, Lauffenburger DA, Wells A. 2001. Membrane proximal ERK signaling is required for m-calpain activation downstream of epidermal growth factor receptor signaling. J. Biol. Chem. 276:23341-48
34. Kulkarni S, Saido TC, Suzuki K, Fox JEB. 1999. Calpain mediates integrin-induced signaling at a point upstream of Rho family members. J. Biol. Chem. 274:21265-75
35. Santella L, Kyozuka K, Hoving S, Munchbach M, Quadroni M, et al. 2000. Breakdown of cytoskeletal proteins during meiosis of starfish oocytes and proteolysis induced by calpain. Exp. Cell Res. 259:117-26
36. Schollmeyer JE. 1988. Calpain II involvement in mitosis. Science 240:911-13
37. Goll DE, Thompson VF, Taylor RG, Zalewska T. 1992. Is calpain activity regulated by membranes and autolysis or by calcium and calpastatin? Bioessays 14:549-56
38. Elliget KA, Phelps PC, Trump BF. 1991. HgC12-induced alteration of actin filaments in cultured primary rat proximal tubule epithelial cells labelled with fluorescein phalloidin. Cell Biol. Toxicol. 7:263-80
39. 2 injury to rat kidney proximal tubule epithelial cells. Pathobiology 62:298-310
40. Wilson PD, Hartz, PA. 1991. Mechanisms of cyclosporin A toxicity in defined cultures of renal tubular epithelia: a role for cysteine proteases. Cell Biol. Int. Reports 15:1243-58
41. Bronk SF, Gores GJ. 1993. pH-dependent nonlysosomal proteolysis contributes to lethal anoxic injury of rat hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 264:G744-51
42. Schnellmann RG, Yang X, Cross TJ. 1994. Calpains play a critical role in renal proximal tubule (RPT) cell death. Can. J. Physiol. Pharmacol. 72:602 (Abstr.)
43. Bednarski E, Vanderklish P, Gall C, Saido TC, Bahr BA, et al. 1995. Translational suppression of calpain I reduces NMDA-induced spectrin proteolysis and pathophysiology in cultured hippocampal slices. Brain Res. 694:147-57
44. Choi DW. 1995. Calcium: still centerstage in hypoxic-ischemic neuronal death. Trends Neurosci. 18:58-60
45. Edelstein CL, Wieder ED, Yaqoob MM, Gengaro PE, Burke TJ, et al. 1995. The role of cysteine proteases in hypoxia-induced rat renal proximal tubular injury. Proc. Natl. Acad. Sci. USA 92:7662-66
46. Edelstein CL, Yaqoob MM, Alkhunaizi AM, Gengaro PE, Nemenoff RA, et al. 1996. Modulation of hypoxia-induced calpain activity in rat renal proximal tubules. Kidney Int. 50:1150-57
47. Edelstein CL, Ling H, Gengaro P, Nemenoff RA, Bahr BA, et al. 1997. Effect of glycine on prelethal and postlethal increases in calpain activity in rat renal proximal tubules. Kidney Int. 52:1271-78
48. Edelstein CL, Ling H, Schrier RW. 1997. The nature of renal cell injury. Kidney Int. 51:1341-51
49. Edelstein CL, Shi Y, Schrier RW. 1999. Role of caspases in hypoxia-induced necrosis of rat renal proximal tubules. J. Am. Soc. Nephrol. 10:1940-49
50. Trump BF, Berezesky IK. 1995. Calcium-mediated cell injury and cell death. FASEB J. 9:219-28
51. Miyoshi H, Umeshita K, Sakon M, Imajoh-Ohmi S, Fujitani K, et al. 1996. Calpain activation in plasma membrane bleb formation during tert-butyl hydroperoxide-induced rat hepatocyte injury. Gastroenterology 110:1897-904
52. Yang X, Schnellmann RG. 1996. Proteinases in renal cell death. J. Toxicol. Environ. Health 48:319-32
53. Chen Z-F, Schottler F, Lee KS. 1997. Neuronal recovery after moderate hypoxia is improved by the calpain inhibitor MDL28170. Brain Res. 769:188-92
54. Waters SL, Sarang SS, Wang KKW, Schnellmann RG. 1997. Calpains mediate calcium and chloride influx during the late phase of cell injury. J. Pharmacol. Exp. Ther. 283:1177-84
55. Waters SL, Schnellmann RG. 1998. Examination of the mechanisms of action of diverse cytoprotectants in renal cell death. Toxicol. Pathol. 26:58-63
56. Markgraf CG, Velayo N, Johnson MP, McCarty DR, Medhi S, et al. 1998. Six-hour window of opportunity for calpain inhibition in focal cerebral ischemia in rats. Stroke 29:152-58
57. Schumacher PA, Eubanks JH, Fehlings MG. 1999. Increased calpain I-mediated proteolysis, and preferential loss of dephosphorylated NF200, following traumatic spinal cord injury. Neuroscience 91: 733-44
58. Schumacher PA, Siman RG, Fehlings MG. 2000. Pretreatment with calpain inhibitor CEP-4143 inhibits calpain I activation and cytoskeletal degradation, improves neurological function, and enhances axonal survival after traumatic spinal cord injury. J. Neurochem. 74: 1646-55
59. Edelstein CL. 2000. Calcium-mediated proximal tubular injury-what is the role of cysteine proteases? Nephrol. Dial. Transplant 15:141-44
60. Harriman JF, Waters-Williams S, Chu DL, Powers JC, Schnellmann RG. 2000. Efficacy of novel calpain inhibitors in preventing renal cell death. J. Pharmacol. Exp. Ther. 294:1083-87
61. Yoshida K-I. 2000. Myocardial ischemia-reperfusion injury and proteolysis of fodrin, ankyrin, and calpastatin. Methods Mol. Biol. 144:267-75
62. Chatterjee PK, Brown PA, Cuzzocrea S, Sacharowski K, Stewart KN, et al. 2001. Calpain inhibitor-1 reduces renal ischemia/reperfusion injury in rat. Kidney Int. 59:2073-83
63. Liu X, Schnellmann RG. 2003. Calpain mediates progressive plasma membrane permeability and proteolysis of cytoskeleton-associated paxillin, talin, and vinculin during renal cell death. J. Pharmacol. Exp. Ther. 304:63-70
64. McDonald MC, Mota-Filipe H, Paul A, Cuzzocrea S, Abdelrahman M, et al. 2001. Calpain inhibitor I reduces the activation of nuclear factor-kappaB and organ injury/dysfunction in hemorrhagic shock. FASEB J. 15:171-86
65. Matsumura Y, Saeki E, Otsu K, Morita T, Takeda H, et al. 2001. Intracellular calcium level required for calpain activation in a single myocardial cell. J. Mol. Cell. Cardiol. 33:1133-42
66. Chen M, He H, Zhan S, Krajewski S, Reed JC, et al. 2001. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J. Biol. Chem. 276:30724-28
67. Chen M, Won D-J, Krajewski S, Gottlieb RA. 2002. Calpain and mitochondria in ischemia/reperfusion injury. J. Biol. Chem. 277:29181-86
68. Rami A, Agarwal R, Botez G, Winckler. 2000. μ-Calpain activation, DNA fragmentation, and synergistic effects of caspase and calpain inhibitors in protecting hippocampal neurons from ischemic damage. Brain Res. 866:299-312
69. Blomgren K, Zhu C, Wang X, Karlsson J-S, Leverin A-L, et al. 2001. Synergistic activation of caspase by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis"? J. Biol. Chem. 276:10191-98
70. Melloni E, Michetti M, Salamino F, Minafra R, Pontremoli S. 1996. Modulation of the calpain autoproteolysis by calpastatin and phospholipids. Biochem. Biophys. Res. Commun. 229:193-97
71. 2+-dependent proteolytic system in rat brain: the calpain activator. Biochem. Biophys. Res. Commun. 249:583-88
72. Melloni E, Avema M, Salamino F, Sparatore B, Minafra R, Pontremoni S. 2000. Acyl-CoA-binding protein is a potent m-calpain activator. J. Biol. Chem. 275:82-86
73. Suzuki K, Sorimachi H. 1998. A novel aspect of calpain activation. FEBS Lett. 433:1-4
74. Yoshizawa T, Sorimachi H, Tomioka S, Ishiura S, Suzuki K. 1995. Calpain dissociates into subunits in the presence of calcium ions. Biochem. Biophys. Res. Commun. 208:376-83
75. Michetti M, Salamino F, Tedesco I, Avema M, Minafra R, et al. 1996. Autolysis of human erythrocyte calpain produces two active enzyme forms with different cell localization. FEBS Lett. 392:11-15
76. Michetti M, Salamino F, Minafra R, Melloni E, Pontremoli S. 1997. Calcium-binding properties of human erythrocyte calpain. Biochem. J. 325:721-26
77. Kitagaki H, Tomioka S, Yoshizawa T, Sorimachi H, Saido TC, et al. 2000. Autolysis of calpain large subunit inducing irreversible dissociation of stoichiometric heterodimer of calpain. Biosci. Biotechnol. Biochem. 64:689-95
78. 2+-activated neutral protease is active in the erythrocyte membrane in its nonautolyzed 80-kDa form. J. Biol. Chem. 269:27992-95
79. 2+ requirement, and heterodimer stability in m-calpain. J. Biol. Chem. 272:11268-75
80. Koh TJ, Tidball JG. 2000. Nitric oxide inhibits calpain-mediated proteolysis of talin in skeletal muscle cells. Am. J. Physiol. Cell Physiol. 279:C806-12
81. Fox JEB, Taylor RG, Taffarel M, Boyles JK, Goll DE. 1993. Evidence that activation of platelet calpain is induced as a consequence of binding of adhesive ligand to the integrin, glycoprotein IIb-IIIa. J. Cell Biol. 120:1501-7
82. Zhao X, Posmantur R, Kampfl A, Liu SJ, Wang KK, et al. 1998. Subcellular localization and duration of mu-calpain and m-calpain activity after traumatic brain injury in the rat: a casein zymography study. J. Cerebral Blood Flow Metab. 18:161-67
83. Hewitt KE, Lesiuk HJ, Tauskela JS, Morley P, Durdin JP. 1998. Selective coupling of mu-calpain activation with the NMDA receptor is independent of translocation and autolysis in primary cortical neurons. J. Neurosci. Res. 54:223-32
84. Blomgren K, Kawashima S, Saido TC, Karlsson J-O, Elmered A, Hagberg H. 1995. Fodrin degradation and subcellular distribution of calpains after neonatal rat cerebral hypoxic-ischemia. Brain Res. 684:143-49
85. Blomgren K, Hallin U, Andersson A-L, Puka-Sundvall M, Bahr BA, et al. 1999. Calpastatin is up-regulated in response to hypoxia and is a suicidal substrate to calpain after neonatal cerebral hypoxia-ischemia. J. Biol. Chem. 274:14046-52
86. Shi Y, Melnikov VY, Schrier RW, Edelstein CL. 2000. Downregulation of the calpain inhibitor protein calpastatin by caspases during renal ischemia-reperfusion. Am. J. Physiol. Renal Physiol. 279: F509-17
87. 2+-activated neutral protease. Biochemistry 27:8122-28
88. Cong J, Thompson VF, Goll DE. 2002. Immunoaffinity purification of the calpains. Protein Expr. Purif. 25:283-90
89. Shiraha H, Glading A, Gupta K, Wells A. 1999. IP-10 inhibits epidermal factor-induced motility by decreasing epidermal growth factor receptor-mediated calpain activity. J. Cell Biol. 146:243-53
90. Storer AC, Menard R. 1994. Catalytic mechanism in papain family of cysteine peptidases. Methods Enzymol. 244:486-50
91. Wang KK. 2000. Calpain and caspase: can you tell the difference? Trends Neurosci. 23:20-26
92. Umezawa H, Miyano T, Murakami T, Takita T, Aoyagi T. 1973. Chemistry of enzyme inhibitors of microbial origins. Pure Appl. Chem. 33(1):129-44
93. Tsujinaka T, Kajiwara Y, Kambayashi J, Sakon M, Higuchi N, et al. 1988. Biochem. Biophys. Res. Commun. 153:1201-8
94. Li Z, Patil GS, Golubski ZE, Hori H, Tehrani K, et al. 1993. Peptide α-ketoesters, α-ketoamides and α-ketoacids inhibitors of calpains and other cysteine proteases. J. Med. Chem. 36:3472-80
95. Peet NP, Burkhart JP, Angelastro MR, Giroux EL, Mehdi S, et al. 1990. Synthesis of peptidyl fluoromethyl ketones and peptidyl α-keto esters as inhibitors of porcine pancreatic elastase, human neutrophil elastase, and rat and human neutrophil cathepsin G. J. Med. Chem. 33: 394-407
96. Li Z, Ortega-Vilain A-C, Patil GS, Chu D-L, Foreman JE, et al. 1996. Novel peptidyl α-keto amide inhibitors of calpains and other cysteine proteases. J. Med. Chem. 39:4089-98
97. Dolle RE, Singh J, Whipple D, Osifo IK, Speier G, et al. 1995. Aspartyl alpha-((diphenylphosphinyl)oxy)methyl ketones as novel inhibitors of interleukin-1 beta converting enzyme. Utility of the diphenylphosphinic acid leaving group for the inhibition of cysteine proteases. J. Med. Chem. 38:220-22
98. Wang KK, Nath R, Posner A, Raser KJ, Buroker-Kilgore M, et al. 1996. An alpha-mercaptoacrylic acid derivative is a selective nonpeptide cell-permeable calpain inhibitor and is neuroprotective. Proc. Natl. Acad. Sci. USA 93:6687-92
99. Hanada K, Tamai M, Yamagishi M, Ohmura S, Sawada J, Tanaka I. 1978. Studies on thiol protease inhibitors. Part I. Isolation and characterization of E-64, a new thiol protease inhibitor. Agric. Biol. Chem. 42:523-28
100. Chatterjee S, Ator MA, Bozyczko-Coyne D, Josef K, Wells G, et al. 1997. Synthesis and biological activity of a series of potent fluoromethyl ketone inhibitors of recombinant human calpain I. J. Med. Chem. 40:3820-28
101. Pliura DH, Bonaventura B, Smith RA, Coles PJ, Krantz A. 1992. Comparative behaviour of calpain and cathepsin B toward peptidyl acyloxymethyl ketones, sulphonium methyl ketones and other potential inhibitors of cysteine proteinases. Biochem. J. 288:759-62
102. Crawford C, Mason RW, Wickstrom P, Shaw E. 1988. The design of peptidyldiazomethane inhibitors to distinguish between the cysteine proteinases calpain II, cathepsin L, and cathepsin B. Biochem. J. 253:751-58
103. Creenbaum D, Medzihradszky KF, Burlingame A, Bogyo M. 2000. Epoxide electrophiles as activity-dependent cysteine protease profiling and discovery tools. Chem. Biol. 7:569-81
104. 2+-dependent neutral protease. Arch. Biochem. Biophys. 260:696-704
105. Shim SR, Kook S, Sim JI, Song WK. 2001. Degradation of focal adhesion proteins paxillin and p130cas by caspases or calpains in apoptotic rat-1 and L929 cells. Biochem. Biophys. Res. Commun. 286:601-8
106. Nath R, Davis M, Probert AW, Kupina NC, Ren X, et al. 2000. Processing of cdk5 activator p35 to its truncated form (p25) by calpain in acutely injured neuronal cells. Biochem. Biophys. Res. Commun. 274:16-21
107. Kusakawa G-I, Saito T, Onuki R, Ishiguro K, Kishimoto T, Hisanaga S-I. 2000. Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J. Biol. Chem. 275:17166-72
108. McGinnis KM, Shariat-Madar Z, Gnegy ME. 1998. Cytosolic calmodulin is increased in SK-N-SH human neuroblastoma cells by release of calcium from the intracellular stores. J. Neurochem. 70: 139-46
109. Endo S, Ishiguro S, Tamai M. 1999. Possible mechanism for the decrease of mitochondrial aspartate aminotransferase activity in ischemic and hypoxic retinas. Biochim. Biophys. Acta 1450:385-96
110. Carragher NO, Levkau B, Ross R, Raines EW. 1999. Degraded collagen fragments promote rapid disassembly of smooth muscle focal adhesion that correlates with cleavage of pp 125FAK, paxillin, and Talin. J. Cell Biol. 147:619-29
111. Pike BR, Zhao X, Newcomb JK, Posmantur RM, Wang KK, Hayes RL. 1998. Regional calpain and caspase-3 proteolysis of alpha-spectrin after traumatic brain injury. Neuroreport 9:2437-42
112. Pike BR, Flint J, Dutta S, Johnson E, Wang KK, Hayes RL. 2001. Accumulation of non-erythroid alpha II-spectrin and calpain-cleaved alpha II-spectrin breakdown products in cerebrospinal fluid after traumatic brain injury in rats. J. Neurochem. 78:1297-306
113. Yokota M, Tani E, Tsubuki S, Yamaura I, Nakagaki I, et al. 1999. Calpain inhibitor entrapped in liposome rescues ischemia neuronal damage. Brain Res. 819:8-14
114. De Jongh KS, Colvin AA, Wang KKW, Catterall WA. 1994. Differential proteolysis of the full-length form of the L-type calcium channel a 1 subunit by calpain. J. Neurochem. 63:1558-64
115. 2+-channel. FEBS Lett. 323:229-32
116. 3 receptor subtypes by caspases and calpain during TNFa-induced apoptosis of human T-lymphoma cells. Cell Calcium 27:315-28
117. Miller GW, Schnellmann RG. 1993. A novel low affinity strychnine binding site on renal proximal tubules: role in toxic cell death. Life Sci. 53:1203-9
118. Miller GW, Schnellmann RG. 1995. Inhibitors of renal chloride transport do not block toxicant-induced chloride influx in the proximal tubule. Toxicol. Lett. 76:179-84
119. Waters SL, Schnellmann RG. 1996. Extracellular acidosis and chloride channel inhibitors act in the late phase of cellular injury to prevent death. J. Pharmacol. Exp. Ther. 278:1012-17
120. Reeves WB. 1997. Effects of chloride channel blockers on hypoxic injury in rat proximal tubules. Kidney Int. 51:1529-34
121. Dong Z, Venkatachalam MA, Weinberg JM, Saikumar P, Patel Y. 2001. Protection of ATP-depleted cells by impermeant strychnine derivatives. Am. J. Pathol. 158:1021-28
122. Garza-Quintero R, Weinberg JM, Ortega-Lopez J, Davis JA, Venkatachalam MA. 1993. Conservation of structure in ATP-depleted proximal tubules: role of calcium, polyphosphoinositides, and glycine. Am. J. Physiol. Renal Physiol. 265: F605-23
123. Zahrebelski G, Niemenen A-L, Al-Ghoul K, Qian T, Herman B, Lemasters JJ. 1995. Progression of subcellular changes during chemical hypoxia to cultured rat hepatocytes: a laser scanning confocal microscopic study. Hepatology 21:1361-72
124. Dong Z, Patel Y, Saikumar P, Weinberg JM, Venkatachalam MA. 1998. Development of porous defects in plasma membrane of adenosine triphosphate-depleted Madin-Darby canine kidney cells and its inhibition by glycine. Lab. Invest. 78:657-68
125. Chen J, Liu X, Mandel LJ, Schnellmann RG. 2001. Progressive disruption of the plasma membrane during renal proximal tubule cellular injury. Toxicol. Appl. Pharmacol. 171:1-11
126. Nishimura Y, Lemasters JJ. 2001. Glycine blocks opening of a death channel in cultured hepatic sinusoidal endothelial cells during chemical hypoxia. Cell Death Differ. 8:850-58
127. Chen J. 1997. Reversibility/irreversibility of anoxia-induced plasma membrane permeabilization. J. Am. Soc. Nephrol. 8:585A (Abstr.)
128. Schnellmann RG, Waters-Williams SL. 1998. Proteases in renal cell death: calpains mediate cell death produced by diverse toxicants. Ren. Fail. 20:679-86
129. Seubert P, Lee K, Lynch G. 1989. Ischemia triggers NMDA receptor-linked cytoskeletal proteolysis in hippocampus. Brain Res. 492:366-70
130. Lee KS, Frank S, Vanderklish P, Arai A, Lynch G. 1991. Inhibition of proteolysis protects hippocampal neurons from ischemia. Proc. Natl. Acad. Sci. USA 88: 7233-37
131. Thevananther S, Kolli AH, Devarajan P. 1998. Identification of a novel ankyrin isoform (AnkG190) in kidney and lung that associates with the plasma membrane and binds alpha-Na, K-ATPase. J. Biol. Chem. 273:23952-58
132. Doctor RB, Chen J, Peters LL, Lux SE, Mandel LJ. 1998. Distribution of epithelial ankyrin (Ank3) spliceoforms in renal proximal and distal tubules. Am. J. Physiol. Renal Physiol. 274:F129-38
133. Doctor RB, Bennett V, Mandel LJ. 1993. Degradation of spectrin and ankyrin in the ischemic rat kidney. Am. J. Physiol. Cell Physiol. 264(4 Pt. 1):C1003-13
134. Chen J, Dai J, Grant RL, Doctor RB, Sheetz MP, Mandel LJ. 1997. Loss of cytoskeletal support is not sufficient for anoxic plasma membrane disruption in renal cells. Am. J. Physiol. Cell Physiol. 272:C1319-28
135. Doctor RB, Zhelev DV, Mandel LJ. 1997. Loss of plasma membrane structural support in ATP-depleted renal epithelia. Am. J. Physiol. Cell Physiol. 272:C439-49
136. Bamardi P, Scorrano L, Colonna R, Petronilli V, Di Lisa F. 1999. Mitochondria and cell death: mechanistic aspects and methodological issues. Eur. J. Biochem. 264:687-701
137. Lemasters JJ. 1998. The mitochondrial permeability transition: from biochemical curiosity to pathophysiological mechanism. Gastroenterology 115:783-87
138. Hunter DR, Haworth RA, Southard JH. 1976. Relationship between configuration, function, and permeability in calcium-treated mitochondria. J. Biol. Chem. 251:5069-77
139. 2+-induced large amplitude swelling of liver and heart mitochondria by cyclosporine is probably caused by the inhibitor binding to mitochondrialmatrix peptidyl-prolyl cis-trans isomerase and preventing it interacting with the adenine nucleotide translocase. Biochem. J. 268:153-60
140. Halestrap AP, Kerr PM, Javadov S, Woodfield KY. 1998. Elucidating the molecular mechanism of the permeability transition pore and its role in reperfusion injury of the heart. Biochim. Biophys. Acta 1366:79-94
141. Zoratti M, Szabo I. 1995. The mitochondrial permeability transition. Biochim. Biophys. Acta 1241:139-76
142. Beutner G, Ruck A, Riede B, Welte W, Brdiczka D. 1996. Complexes between kinases, mitochondrial porin and adenylate translocator in rat brain resemble the permeability transition pore. FEBS Lett. 396:189-95
143. 2+ and collapse of mitochondrial potential in anoxic, but not hypoxic, rat proximal tubules. J. Am. Soc. Nephrol. 7:2348-56
144. Aguilar HI, Botla R, Arora AS, Bronk SF, Gores GJ. 1996. Induction of the mitochondrial permeability transition by protease activity in rats: a mechanism of hepatocyte necrosis. Gastroenterology 110:558-66
145. Van Vleet TR, Schnellmann RG. 2002. Identification of mitochondrial calpain-like activity during mitochondrial dysfunction. ToxicolSci. 66(Suppl. 1):LB144 (Abstr.)
146. Van Vleet TR, Schnellmann RG. 2002. Mitochondrial calpain-like activity mediates Ca2+-induced mitochondrial dysfunction. J. Am. Soc. Nephrol. 13(Suppl.): 138A (Abstr.)
147. Gores GJ, Miyoshi H, Botla R, Aguilar HI, Bronk SF. 1998. Induction of the mitochondrial permeability transition as a mechanism of liver injury during cholestasis: a potential role for mitochondrial protease. Biochim. Biophys. Acta 1366:167-75
148. Gao G, Dou QP. 2000. 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. 80:53-72
149. Wood DE, Newcomb EW. 2000. Cleavage of Bax enhances its cell death function. Exp. Cell. Res. 256:375-82
150. Nakagawa T, Yuan J. 2000. Cross-talk between two cysteine protease families. Activation of caspase-12 by calpain in apoptosis. J. Cell. Biochem. 150:887-94
151. Shimizu S, Konishi A, Kodama T, Tsujimoto Y. 2000. BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc. Natl. Acad. Sci. USA 97:3100-5
152. Kohli V, Gao W, Camargo CA Jr, Clavien PA. 1997. Calpain is a mediator of preservation-reperfusion injury in rat liver transplantation. Proc. Natl. Acad. Sci. USA 94:9354-59
153. Kohli V, Madden JF, Bentley RC, Clavien PA. 1999. Calpain mediates ischemic injury of the liver through modulation of apoptosis and necrosis. Gastroenterology 116:168-78
154. Hong S-C, Goto Y, Lanzino G, Soleau S, Kassell NF, et al. 1994. Neuroprotection with a calpain inhibitor in a model of focal cerebral ischemia. Stroke 25:663-69