Caspase and calpain function in cell death: Bridging the gap between apoptosis and necrosis

Annals of Clinical Biochemistry

Volumn 42, Issue 6, 2005, Pages 415-431

  Harwood, Steven M ^a   Yaqoob, Muhammad M ^a   Allen, David A ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALPAIN; CASPASE; DEATH RECEPTOR; PROTEINASE;

APOPTOSIS; AUTOLYSIS; CELL DEATH; CELL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVITY; FLOW CYTOMETRY; IMMUNOHISTOCHEMISTRY; MITOCHONDRION; NECROSIS; OXIDATIVE STRESS; PATHOLOGY; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; REVIEW; STRESS; WESTERN BLOTTING;

APOPTOSIS; BIOLOGICAL MARKERS; CALPAIN; CASPASES; ENZYME ACTIVATION; HUMANS; MODELS, BIOLOGICAL; NECROSIS; PROTEIN ISOFORMS;

EID: 27844595293     PISSN: 00045632     EISSN: 00045632     Source Type: Journal    
DOI: 10.1258/000456305774538238     Document Type: Review

References (128)

1. Padanilam BJ. Cell death induced by acute renal injury: a perspective on the contributions of apoptosis and necrosis. Am J Physiol Renal Physiol 2003; 284: F608-27
2. Degterev A, Boyce M, Yuan J. A decade of caspases. Oncogene 2003; 22: 8543-67
3. Wang KKW. Calpain and caspases: can you tell the difference? Trends Neurosci 2000; 23: 20-6
4. Park M, Helip-Wooley A, Thoene J. Lysosomal cystine storage augments apoptosis in cultured human fibroblasts and renal tubular epithelial cells. J Am Nephrol 2002; 13: 2878-87
5. Guicciardi ME, Leist M, Gores GJ. Lysosomes in cell death. Oncogene 2004; 23: 2881-90
6. Glading A, Chang P, Lauffenburger DA, Wells A. Epidermal growth factor receptor activation of calpain is required for fibroblast motility and occurs via an ERK/MAP kinase signaling pathway. J Biol Chem 2000; 275: 2390-8
7. Glading A, Uberall F, Keyse SM, Lauffenburger DA, Wells A. Membrane proximal ERK signaling is required for m-calpain activation downstream of epidermal growth factor receptor signaling. J Biol Chem 2001; 276: 23341-8
8. Glading A, Bodnar RJ, Reynolds IJ, et al. Epidermal growth factor activates m-calpain (calpain II), at least in part, by extracellular signal-regulated kinase-mediated phosphorylation. Mol Cell Biol 2004; 24: 2499-512
9. Wei Y, Fox T, Chambers SP, Sintchak J, Coll JT, Golec JM. The structures of caspases-1, -3, -7 and -8 reveal the basis for substrate in inhibitor selectivity. Chem Biol 2000; 7: 423-32
10. Goll DE, Thompson VF, LI H, Wei W, Cong J. The calpain system. Physiol Rev 2003; 83: 731-801
11. Fischer H, Koenig U, Eckhart L, Tschachler E. Human caspase 12 has acquired deleterious mutations. Biochem Biophys Res Commun 2002; 293: 722-6
12. Saleh M, Vaillancourt JP, Graham RK, et al. Differential modulation of endotoxin responsiveness by human caspase-12 polymorphisms. Nature 2004; 429: 75-9
13. Mamoune A, Luo J-H, Lauffenburger W. Calpain-2 as a target for limiting cancer invasion. Cancer Res 2003; 63: 4632-40
14. Jonges LE, Nagelkerke JF, Ensink NG, et al. Caspase-3 activity as a prognostic factor in colorectal carcinoma. Lab Invest 2001; 81: 681-8
15. Proskuryakov SY, Konoplyannikov AG, Gabai VL. Necrosis: a specific form of programmed cell death? Exp Cell Res 2003; 283: 1-16
16. Lozupone F, Lugini L, Matarrese P, et al. Identification and relevance of the CD95-binding domain in N-terminal region of ezrin. J Biol Chem 2004; 279: 9199-207
17. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase-8 mediates the mitochondrial damage in the Fas pathways of apoptosis. Cell 1998; 94: 491-501
18. Chandrasekar B, Vemula K, Surabhi RM, et al. Activation of intrinsic and extrinsic proapoptotic signalling pathways in interleukin-18-mediated human cardiac endothelial cell death. J Biol Chem 2004; 279: 20221-33
19. Hakem R, Hakem A, Duncan GS, et al. Differential requirement for caspase-9 in apoptotic pathways in vivo. Cell 1998; 94: 339-52
20. Marsden VS, O'Connor L, O'Reilly LA, et al. Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature 2002; 419: 634-7
21. Chai J, Du C, Wu JW, Kyin S, Wang X, Shi Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature 2000; 406: 855-62
22. Robertson JD, Gogvadze V, Kropotov A, Vakifahmetoglu H, Zhivotovsky B, Orrenius S. Processed caspase-2 can induce mitochondrial-mediated apoptosis independently of its enzyme activity. EMBO Rep 2004; 5: 643-8
23. Lieberman J, Fan Z. Nuclear war: the granzyme A-bomb. Cur Opin Immunol 2003; 15: 553-9
24. Zeiss CJ. The apoptosis - necrosis continuum: insights from genetically altered mice. Vet Pathol 2003; 40: 481-95
25. Ueda N, Walker PD, Hsu S, Shah SV. Activation of a 15-kDa endonuclease in hypoxia/reoxygenation injury without morphologic features of apoptosis. Proc Natl Acad Sci USA 1995; 92: 7202-6
26. Ueda N, Shah SV. Tubular cell damage in acute renal failure - apoptosis, necrosis, or both. Nephrol Dial Transplant 2000; 15: 318-23
27. Meli E, Pangallo M, Picca R, Baronti R, Moroni F, Pellegrini-Giampietro DE. Differential role of poly(ADP-ribose) polymerase-1 in apoptotic and necrotic neuronal death induced by mild or intense NMDA exposure in vitro. Mol Cell Neurosci 2004; 25: 172-80
28. Xiao AY, Wei L, Xia S, Rothman S, Yu SP. Ionic mechanism of ouabain-induced concurrent apoptosis and necrosis in individual cultured cortical neurons. J Neurosci 2002; 22: 1350-62
29. Borutaite V, Brown GC. Nitric oxide induces apoptosis via hydrogen peroxide, but necrosis via energy and thiol depletion. Free Radic Biol Med 2003; 35: 1457-68
30. Rabkin SW, Kong JY. Lovastatin-induced cardiac toxicity involves both oncotic and apoptotic cell death with the apoptotic component blunted by both caspase-2 and caspase-3 inhibitors. Toxicol Appl Pharmacol 2003; 193: 346-55
31. Nicotera P, Leist M, Ferrando-May E. Apoptosis and necrosis: different execution of the same death. Biochem Soc Symp 1999; 66: 69-73
32. Wang X, Ryter SW, Dai C, et al. Necrotic cell death in response to oxidant stress involves the activation of apoptogenic caspase-8/bid pathway. J Biol Chem 2003; 278: 29184-91
33. Kim J-S, He L, Lemasters JJ. Mitochondrial permeability transition; a common pathway to necrosis and apoptosis. Biochem Biophys Res Commun 2003; 304: 463-70
34. Lockshin RA, Zakeri Z. Caspase-independent cell deaths. Cur Opin Cell Biol 2002; 14: 727-33
35. Jaattela M, Tschopp J. Caspase-independent cell death in T lymphocytes. Nat Immunol 2003; 4: 416-23
36. Ray SK, Wilford GG, Ali SF, Banik NL. Calpain upregulation in spinal cords of mice with 1-methyl-4-phenyl-1,2,3,6,-tetrahydro-pyridine (MPTP)-induced Parkinson's disease. Ann NY Acad Sci 2000; 914: 275-83
37. Chera B, Schaecher KE, Rocchini A, et al. Calpain upregulation and neuron death in spinal cord of MPTP-induced parkinsonism in mice. Ann NY Acad Sci 2002; 965: 274-80
38. Crocker SJ, Smith PD, Jackson-Lewis V, et al. Inhibition of calpains prevents neuronal and behavioural deficits in an MPTP mouse model of Parkinson's disease. J Neurosci 2003; 23: 4081-91
39. Tsuji T, Shimohama S, Kimura J, Shimizu K. m-Calpain (calcium-activated neutral proteinase) in Alzheimer's disease brains. Neurosci Lett 1998; 248: 109-12
40. Battaglia F, Trinchese F, Liu S, Walter S, Nixon RA, Arancio O. Calpain inhibitors, a treatment for Alzheimer's disease: position paper. J Mol Neurosci 2003; 20: 357-62
41. Canu N, Calissano P. In vitro cultured neurons for molecular studies correlating apoptosis and events related to Alzheimer disease. Cerebellum 2003; 2: 270-8
42. Veeranna, Kaji T, Boland B, et al. Calpain mediates calcium-induced activation of the Erk1,2 MAPK pathway and cytoskeletal phosphorylation in neurons. Relevance to Alzheimer's disease. Am J Pathol 2004; 165: 795-805
43. Shields DC, Schaecher KE, Saido TC, Banik NL. A putative mechanism of demyelination in multiple sclerosis by a proteolytic enzyme, calpain. Proc Natl Acad Sci USA 1999; 96: 11486-91
44. Schaecher KE, Shields DC, Banik NL. Mechanism of myelin breakdown in experimental demyelination: a putative role for calpain. Neurochem Res 2001; 26: 731-7
45. Richard I, Broux O, Allamand V, Fougerousse F, Chiannilkulchai N, Bourg N. Mutations in the proteolytic enzyme calpain 3 cause limb-girdle muscular dystrophy type 2A. Cell 1995; 81: 27-40
46. Richard I, Roudaut C, Marchand S, et al. Loss of calpain 3 proteolytic activity leads to muscular dystrophy and to apoptosis-associated IκBα/nuclear factor κB pathway perturbation in mice. J Cell Biol 2000; 151: 1583-90
47. Fougerousse F, Gonin P, Durand M, Richard I, Raymackers JM. Force impairment in calpain 3-deficient mice is not correlated with mechanical disruption. Muscle Nerve 2003; 27: 616-23
48. Ray SK, Hogan EL, Banik NL. Calpain in the pathophysiology of spinal cord injury: neuroprotection with calpain inhibitors. Brain Res Brain Res Rev 2003; 42: 169-85
49. Ray SK, Matzelle DD, Sribnick EA, Guyton MK, Wingrave JM, Banik NL. Calpain inhibitor prevented apoptosis and maintained transcription of proteolipid protein and myelin basic protein genes in rat spinal cord injury. J Chem Neuroanat 2003; 26: 119-24
50. Sandmann S, Prenzel F, Shaw L, Schauer R, Unger T. Activity profile of calpains I and II in chronically infarcted rat myocardium - influence of the calpain inhibitor CAL 9961. Br J Pharmacol 2002; 135: 1951-8
51. Chatterjee PK, Brown PA, Cuzzocrea S, et al. Calpain inhibitor-I reduces renal ischemia/reperfusion injury in the rat. Kidney Int 2001; 59: 2073-83
52. Pike BR, Flint J, Dave JR, et al. Accumulation of calpain and caspase-3 proteolytic fragments of brain-derived αII-spectrin in cerebral spinal fluid after middle cerebral artery occlusion in rats. J Cereb Blood Flow Metab 2004; 24: 98-106
53. 2+-calpain and caspase-3 dependent pathway. Pharmacol Res 2003; 48: 571-8
54. Emgard M, Hallin U, Karlsson J, Bahr BA, Brundin P, Blomgren K. Both apoptosis and necrosis occur early after intracerebral grafting of ventral mesencephalic tissue: a role for protease action. J Neurochem 2003; 86: 1223-32
55. Jayanthi S, Deng X, Noailles PA, Ladenhein B, Cadet JL. Methamphetamine induces neuronal apoptosis via cross-talks between endoplasmic reticulum and mitochondria-dependent death cascades. FASEB J 2004; 18: 238-51
56. Liu X, Vleet TV, Schnellmann RG. The role of calpain in oncotic cell death. Annu Rev Pharmacol Toxicol 2004; 44: 349-70
57. Gil-Parrado S, Fernandex-Montalvan A, Assfalg-Machleidt I, et al. lonomycin-activated calpain triggers apoptosis. J Biol Chem 2002; 277: 27217-26
58. Mandic A, Viktorsson K, Strandberg L, et al. Calpain-mediated Bid cleavage and calpain-independent Bak modulation: two separate pathways in cisplatin-induced apoptosis. Mol Cell Biol 2002; 22: 3003-13
59. Ding WX, Shen HM, Ong CN. Calpain activation after mitochondrial permeability transition in microcystin-induced cell death in rat hepatocytes. Biochem Biophys Res Commun 2002; 291: 321-31
60. Blomgren K, Zhu C, Wang X, et al. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia - ischemia. J Biol Chem 2001; 276: 10191-8
61. Nakagawa T, Zhu H, Morishima N, et al. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-β. Nature 2000; 403: 98-103
62. Wang KKW, Posmantur R, Nadimpalli R, et al. Caspase-mediated fragmentation of calpain inhibitor protein calpastatin during apoptosis. Arch Biochem Biophys 1998; 356: 187-96
63. Porn-Ares MI, Samali A, Orrenius S. Cleavage of the calpain inhibitor calpastatin during apoptosis. Cell Death Differ 1998; 5: 1028-33
64. Kato M, Nonaka T, Maki M, Kikuchi H, Imajoh-Ohmi S. Caspases cleave the amino-terminal calpain inhibitory unit of calpastatin during apoptosis in human Jurkat T cells. J Biochem 2000; 127: 297-305
65. Neumar RW, Xu YA, Gada H, Guttman RP, Siman R. Cross-talk between calpain and caspase proteolytic systems during neuronal apoptosis. J Biol Chem 2003; 278: 14162-7
66. Ruiz-Vela A, Gonzalez de Buitrago G, Martinez-A C. Implication of calpain in caspase activation during B cell clonal deletion. EMBO J 1999; 18: 4988-58
67. Chua BT, Guo K, Peng L. Direct cleavage by the calcium-activated protease calpain can lead to inactivation of caspases. J Biol Chem 2000; 275: 5131-5
68. Nakagawa T, Yuan J. Cross-talk between two cysteine protease families: activation of caspase-12 by calpain in apoptosis. J Cell Biol 2000; 150: 887-94
69. Barnoy S, Kosower NS. Caspase-1-induced calpastatin degradation in myoblast differentiation and fusion: cross-talk between the caspase and calpain systems. FEBS Lett 2003; 546: 213-17
70. Hwang SY, Paik S, Park SH, et al. N-phenethyl-2-phenylacetamide isolated from Xenorhabdus nematophilus induces apoptosis through caspase activation and calpain-mediated Bax cleavage in U937 cells. Int J Oncol 2003; 22: 151-7
71. Altznauer F, Conus S, Cavalli A, Folkers G, Simon HU. Caspase-1 regulates Bax and subsequent Smac-dependent caspase-3 activation in neutrophil apoptosis. J Biol Chem 2004; 279: 5947-57
72. Kobayashi S, Yamashita K, Takeoka T, et al. Calpain-mediated X-linked inhibitor of apoptosis degradation in neutrophil apoptosis and its impairment in chronic neutrophilic leukemia. J Biol Chem 2002; 277: 33968-77
73. Rutkowski DT, Kaufman RJ. A trip to the ER: coping with stress. Trends Cell Biol 2004; 14: 20-8
74. Allen DA, Harwood SM, Varagunam M, Raftery MJ, Yaqoob MM. High glucose-induced oxidative stress causes apoptosis in proximal tubular epithelial cells and is mediated by multiple caspases. FASEB J 2003; 17: 908-10
75. Mack A, Furmann C, Hacker G. Detection of caspase-activation in intact lymphoid cells using standard caspase substrates and inhibitors. J Immunol Methods 2000; 241: 19-31
76. Smolewski P, Grabarek J, Halicka HD, Darzynkiewicz Z. Assay of caspase activation in situ combined with probing plasma membrane integrity to detect three distinct stages of apoptosis. J Immunol Methods 2002; 265: 111-21
77. Ormerod MG. Using flow cytometry to follow the apoptotic cascade. Redox Rep 2001; 6: 275-87
78. Tuschl H, Schwab CE. Flow cytometric methods used as screening tests for basal toxicity of chemicals. Toxicol In vitro 2004; 18: 483-31
79. He L, Wu X, Meylan F, et al. Monitoring caspase activity in living cells using fluorescent proteins and flow cytometry. Am J Pathol 2004; 164: 1901-13
80. Harwood SM, Allen DA, Chesser AMS, New DI, Raftery MY, Yaqoob MM. Calpain is activated in experimental uremia: is calpain a mediator of uremia-induced myocardial injury? Kid Int 2003; 63: 866-77
81. Tompa P, Schad E, Friedrich P. A sensitive and continuous fluorometric activity assay using a natural substrate. Microtubule-associated protein 2. Methods Mol Biol 2000; 144: 137-41
82. Rosser BG, Powers SP, Gores GJ. Calpain activity increases in hepatocytes following addition of ATP. J Biol Chem 1993; 268: 23593-300
83. Rosser BG, Gores GJ. Cellular in vivo assay calpain activity using a fluorescent substrate. Application to study of anoxic liver injury. Methods Mol Biol 2000; 144: 245-59
84. Komatsu N, Nakauchi H, Miwa A, et al. Establishment and characterization of a leukemic cell line and megakaryocytic features: dependency on granulocyte-macrophage colony-stimulating factor, interleukin 3, or erythropoietin for growth and survival. Cancer Res 1991; 51: 341-8
85. 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
86. Lindberg C, Eriksson C, Van Dam AM, Winblad B, Schultzberg M. Neuronal expression of caspase-1 immunoreactivity in the rat central nervous system. J Neuroimmunol 2004; 146: 99-113
87. Rami A, Volkmann T, Schoninger S, et al. 2-Adrenergic receptor responsiveness of the calpain-calpastatin system and attenuation of neuronal death in rat hippocampus after transient global ischemia. Neurosci Res 2003; 47: 373-82
88. Sandmann S, Spormann J, Prenzel F, Shaw L, Linger T. Calcium channel blockade limits transcriptional, translational and function up-regulation of the cardiac calpain system after myocardial infarction. Eur J Pharmacol 2002; 453: 99-109
89. Limaye PB, Apte UM, Shankar K, Bucci TJ, Warbritton A, Mehendale HM. Calcium released from dying hepatocytes mediates progression of acute liver injury induced by model hepatotoxicants. Toxicol Appl Pharmacol 2003; 191: 211-26
90. Weber H, Hopp HH, Wagner ACC, et al. Expression and regulation of calpain in rat pancreatic acinar cells. Pancreas 2002; 24: 63-74
91. Edelstein CL. Calpain activity in rat renal proximal tubules. An in vitro assay. Methods Mol Biol 2000; 144: 233-8
92. Hampton MB, Stemenkovic I, Winterbourn CC. Interaction with substrate sensitise caspase-3 to inactivation by hydrogen peroxide. FEBS Lett 2002; 517: 229-32
93. Guttmann RP, Johnson GVW. Oxidative stress inhibits calpain activity in situ. J Biol Chem 1998; 273: 13331-8
94. 2-terminal kinase pathway in H9c2 cardiac muscle cells. J Mol Cell Cardiol 1998; 30: 1789-801
95. Li H, Thompson VF, Goll DE. Effects of autolysis on properties of μ- and m-calpain. Biochim et Biophys Acta Mol Cell Res 2004; 1691:91-103
96. Watanabe M, Hitomi M, van der Wee K, et al. The pros and cons of apoptosis assays for use in the study of cells, tissues, and organs. Microsc Microanal 2002; 8: 375-91
97. Schultz DR, Harrington Jr WJ. Apoptosis: programmed cell death at a molecular level. Semin Arthritis Rheum 2003; 6: 345-69
98. Biswas S, Harris F, Singh J, Phoenix DA. The in vitro retardation of porcine cataractogenesis by the calpain inhibitor, SJA6017. Mol Cell Biochem 2004; 261: 169-73
99. Harris F, Chatfield L, Singh J, Phoenix DA. Role of calpains in diabetes mellitus: a mini review. Mol Cell Biochem 2004; 261: 161-7
100. Huang Y, Wang KKW. The calpain family and human disease. Trends Mol Med 2001; 7: 355-62
101. McDonald MC, Mota-Filipe H, Paul A, et al. Calpain inhibitor I reduces the activation of nuclear factor-β and organ injury/dysfunction in hemorrhagic shock. FASEB J 2001; 15: 171-86
102. Rios-Doria J, Kuefer R, Ethier SP, Day ML. Cleavage of β-catenin by calpain in prostate and mammary tumour cells. Cancer Res 2004; 64: 7237-40
103. Lakshmikuttyamma A, Selvakumar P, Kanthan R, Kanthan SC, Sharma RK. Overexpression of m-calpain in human colorectal adenocarcinomas. Cancer Epidemiol Biomarkers Prev 2004; 13: 1604-9
104. Gonzalez A, Lopez B, Ravassa S, et al. Stimulation of cardiac apoptosis in essential hypertension. Hypertension 2002; 39: 75-80
105. Sharif M, Whitehouse A, Sharman P, Parry M, Adams M. Increased apoptosis in human osteoarthritic cartridge corresponds to reduced cell density and expression of caspase-3. Arthritis Rheum 2004; 50: 507-15
106. Anwar S, Ambros RA, Jennings TA, et al. Expression of cysteine protease protein 32 in prostatic adrenocarcinoma correlates with tumor grade. Arch Pathol Lab Med 2004; 128: 649-52
107. Isobe N, Onodera H, Mori A, et al. Caspase-3 expression in human gastric carcinoma and its clinical significance. Oncology 2004; 66: 201-9
108. Mohr S. Potential new strategies to prevent the development of diabetic retinopathy. Expert Opin Investig Drugs 2004; 13: 189-98
109. Valentino KL, Gutierrez M, Sanchez R, Winship MJ, Shapiro DA. First clinical trial of a novel caspase inhibitor: anti-apoptotic caspase inhibitor, IDN-6556, improves liver enzymes. Int J Clin Pharmacol Ther 2003; 41: 441-9
110. Shimohama S, Tanino H, Fujimoto S. Changes in caspase expression in Alzheimer's disease: comparison and development and aging. Biochem Biophys Res Commun 1999; 256: 381-4
111. Quo H, Albrecht S, Bourdeau M, Petzke T, Bergeron C, LeBlanc AC. Active caspase-6 and caspase-6-cleaved tau in neuropil threads, neuritic plaques, and neurofibrillary tangles of Alzheimer's disease. Am J Pathol 2004; 165: 523-31
112. Cribbs DH, Poon WW, Rissman RA, Blurton-Jones M. Caspase-mediated degeneration in Alzheimer's disease. Am J Pathol 2004; 165: 353-5
113. Schmeck B, Gross R, N'Guessan PD, et al. Streptococcus pneumoniae-induced caspase 6-dependent apoptosis in lung epithelium. Infect Immun 2004; 72: 4940-7
114. Silman R, McIntosh TK, Soltesz KM, et al. Proteins released from degenerating neurons are surrogate markers for acute brain damage. Neurobiol Dis 2004; 16: 311-20
115. Berdowska I. Cysteine proteases as disease markers. Clin Chim Acta 2004; 342: 41-69
116. Jedeszko C, Sloane BF. Cysteine cathepsins in human cancer. Biol Chem 2004; 385: 1017-27
117. Tappel A. Lysosomal enzymes and initiation of breast cancer. Med Hypotheses 2005; 64: 288-9
118. Lang T, Willinger U, Holzer G. Soluble cathepsin-L: a marker of bone resorption and bone density? J Lab Clin Med 2004; 144: 163-6
119. Yoo NJ, Lee JW, Kim YJ, et al. Loss of caspase-2, -6 and -7 expression in gastric cancers. APMIS 2004; 112: 330-5
120. Byrd JC, Kitada S, Flinn IW, et al. The mechanism of tumor cell clearance by rituximab in vivo in patients with B-cell chronic lymphocytic leukaemia: evidence of caspase activation and apoptosis induction. Blood 2002; 99: 1038-43
121. Linder S, Havelka AM, Ueno T, Shoshan MC. Determining tumor apoptosis and necrosis in patient serum using cytokeratin 18 as a biomarker. Cancer lett 2004; 214: 1-9
122. Bantel H, Lugering A, Heidemann J, et al. Detection of apoptotic caspase activation in sera from patients with chronic HCV infection is associated with fibrotic liver injury. Hepatology 2004; 40: 1078-87
123. 2+-mediated, calpain/caspase-12-dependent apoptosis in breast cancer cells. Biochem Biophys Res Commun 2004; 321: 462-7
124. Cox NJ, Hayes MG, Roe CA, Tsuchiya T, Bell GI. Linkage of calpain 10 to type 2 diabetes. Diabetes 2004; 53: S19-25
125. Chen Y, Kittles R, Zhou J, et al. Calpain-10 gene polymorphisms and type 2 diabetes in West Africans: The African American diabetes mellitus (AADM) study. Ann Epidemiol 2005; 15: 153-9
126. Harwood SM, Allen DA, Raftery MJ, Yaqoob MM. Calpain is a mediator of myocardial injury in experimental uremia: is it activated by endogenous ouabain? Kid Int 2003; 84: S177-80
127. Lockshin RA, Zakeri Z. Apoplosis, autophagy, and more. Int J Biochem Cell Biol 2004; 36: 2405-19
128. Guimaraes CA, Linden R. Programmed cell death. Apoptosis and alternative deathstyles. Eur J Biochem 2004; 271: 1638-50