Ca2+-dependent proteases in ischemic neuronal death. A conserved 'calpain-cathepsin cascade' from nematodes to primates

Cell Calcium

Volumn 36, Issue 3-4, 2004, Pages 285-293

  Yamashima, Tetsumori ^a  

^a KANAZAWA UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCE   (Japan)

Author keywords

Calpain; Calpain cathepsin hypothesis; Caspase; Cathepsin; Hippocampus; Ischemic neuronal death

Indexed keywords

ALOXISTATIN ACID; ASPARTIC PROTEINASE; CA 074; CALCIUM ION; CALPAIN; CASPASE 3; CASPASE INHIBITOR; CATHEPSIN; CATHEPSIN B; CATHEPSIN D; CATHEPSIN H; CATHEPSIN L; CYSTEINE PROTEINASE; LYSOSOME ENZYME; N (3 CARBOXYOXIRANE 2 CARBONYL)ISOLEUCYLPROLINE; NEUROPROTECTIVE AGENT; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; BRAIN ISCHEMIA; BRAIN NERVE CELL; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME SUBSTRATE; HUMAN; NEMATODE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PRIMATE; PRIORITY JOURNAL; RETROSPECTIVE STUDY; REVIEW; ANIMAL; CAENORHABDITIS ELEGANS; CELL DEATH; ENZYMOLOGY; HAPLORHINI; NERVE CELL; PATHOLOGY; PHYSIOLOGY;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; NEMATODA; PRIMATES; RODENTIA;

ALZHEIMER DISEASE; ANIMALS; BRAIN ISCHEMIA; CAENORHABDITIS ELEGANS; CALPAIN; CELL DEATH; HAPLORHINI; HUMANS; NEURONS;

EID: 3342900223     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceca.2004.03.001     Document Type: Article

References (92)

1. Lipton S.A. Nicotera P. Calcium, free radicals and excitotoxins in neuronal apoptosis Cell Calcium 23 1998 165-171
2. Mattson M.P. Apoptosis in neurodegenerative disorders Nat. Rev. Mol. Cell Biol. 1 2000 120-129
3. Sattler R. Tymianski M. Molecular mechanisms of calcium-dependent excitotoxicity J. Mol. Med. 78 2000 3-13
4. 2+ release from the endoplasmic reticulum Neuron 31 2001 957-971
5. De Duve C. Wattiaux R. Functions of lysosomes Annu. Rev. Physiol. 28 1966 435-492
6. Metzstein M.M. Stanfield G.M. Horvitz H.R. Genetics of programmed cell death in C. elegans: past, present and future Trends Genet. 14 1998 410-416
7. Meier P. Finch A. Evan G. Apoptosis in development Nature 407 2000 796-801
8. Ameisen J.C. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years Cell Death Differ. 9 2002 367-393
9. Kerr J.F. Wyllie A.H. Currie A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics Br. J. Cancer 26 1972 239-257
10. Wyllie A.H. Kerr J.F. Currie A.R. Cell death: the significance of apoptosis Int. Rev. Cytol. 68 1980 251-306
11. Majno G. Joris I. Apoptosis, oncosis, and necrosis. An overview of cell death Am. J. Pathol. 146 1995 3-15
12. Martin L.J. Al-Abdulla N.A. Brambrink A.M. Kirsch J.R. Sieber F.E. Portera-Cailliau C. Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis Brain Res. Bull. 46 1998 281-309
13. Martin L.J. Neuronal cell death in nervous system development, disease, and injury (review) Int. J. Mol. Med. 7 2001 455-478
14. Los M. Wesselborg S. Schulze-Osthoff K. The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice Immunity 10 1999 629-639
15. Leist M. Jaattela M. Four deaths and a funeral: from caspases to alternative mechanisms Nat. Rev. Mol. Cell Biol. 2 2001 589-598
16. Turmaine M. Raza A. Mahal A. Mangiarini L. Bates G.P. Davies S.W. Nonapoptotic neurodegeneration in a transgenic mouse model of Huntington's disease Proc. Natl. Acad. Sci. U.S.A. 97 2000 8093-8097
17. Sperandio S. de Belle I. Bredesen D.E. An alternative, nonapoptotic form of programmed cell death Proc. Natl. Acad. Sci. U.S.A. 97 2000 14376-14381
18. Tsukada T. Watanabe M. Yamashima T. Implications of CAD and DNase II in ischemic neuronal necrosis specific for the primate hippocampus J. Neurochem. 79 2001 1196-1206
19. T. Yamashima, A.B. Tonchev, T. Tsukada, T.C. Saido, S. Imajoh-Ohmi, T. Momoi, E. Kominami, Sustained calpain activation associated with lysosomal rupture executes necrosis of the postischemic CA1 neurons in primates, Hippocampus 13 (2003) 791-800.
20. Fujikawa D.G. Confusion between neuronal apoptosis and activation of programmed cell death mechanisms in acute necrotic insults Trends Neurosci. 23 2000 410-411
21. Roy M. Sapolsky R. Neuronal apoptosis in acute necrotic insults: why is this subject such a mess? Trends Neurosci. 22 1999 419-422
22. Boveris A. Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen Biochem. J. 134 1973 707-716
23. Kontos H.A. George E. Brown memorial lecture. Oxygen radicals in cerebral vascular injury Circ. Res. 57 1985 508-516
24. Coyle J.T. Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders Science 262 1993 689-695
25. Chan P.H. Role of oxidants in ischemic brain damage Stroke 27 1996 1124-1129
26. Nicotera P. Lipton S.A. Excitotoxins in neuronal apoptosis and necrosis J. Cereb. Blood Flow Metab. 19 1999 583-591
27. Lankiewicz S. Marc Luetjens C. Truc Bui N. Krohn A.J. Poppe M. Cole G.M. Saido T.C. Prehn J.H. Activation of calpain I converts excitotoxic neuron death into a caspase-independent cell death J. Biol. Chem. 275 2000 17064-17071
28. Yamashima T. Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates Prog. Neurobiol. 62 2000 273-295
29. 2 and calpain responses prior to delayed neuronal death in monkeys Eur. J. Neurosci. 8 1996 1932-1944
30. Zhao L. Yamashima T. Wang X.D. Tonchev A.B. Yamashita J. Kakiuchi T. Nishiyama S. Kuhara S. Takahashi K. Tsukada H. PET imaging of ischemic neuronal death of living monkeys Hippocampus 12 2002 109-118
31. Yoshida M. Yamashima T. Zhao L. Tsuchiya K. Kohda Y. Tonchev A.B. Matsuda M. Kominami E. Primate neurons show different vulnerability to transient ischemia and response to cathepsin inhibition Acta Neuropathol. (Berl.) 104 2002 267-272
32. Syntichaki P. Xu K. Driscoll M. Specific aspartyl and calpain proteases are required for neurodegeneration in C. elegans Nature 419 2002 939-944
33. Yamashima T. Kohda Y. Tsuchiya K. Ueno T. Yamashita J. Yoshioka T. Kominami E. Inhibition of ischaemic hippocampal neuronal death in primates with catepsin B inhibitor CA-074: a novel strategy for neuroprotection based on 'calpain-cathepsin hypothesis' Eur. J. Neurosci. 10 1998 1723-1733
34. Charriaut-Marlangue C. Ben-Ari Y. A cautionary note on the use of the TUNEL stain to determine apoptosis Neuroreport 7 1995 61-64
35. Mangili F. Cigala C. Santambrogio G. Staining apoptosis in paraffin sections. Advantages and limits Anal. Quant. Cytol. Histol. 21 1999 273-276
36. Stadelmann C. Lassmann H. Detection of apoptosis in tissue sections Cell Tissue Res. 301 2000 19-31
37. Cohen G.M. Caspases: the executioners of apoptosis Biochem. J. 326 Pt. 1 1997 1-16
38. Earnshaw W.C. Martins L.M. Kaufmann S.H. Mammalian caspases: structure, activation, substrates, and functions during apoptosis Annu. Rev. Biochem. 68 1999 383-424
39. Hengartner M.O. The biochemistry of apoptosis Nature 407 2000 770-776
40. Strasser A. O'Connor L. Dixit V.M. Apoptosis signaling Annu. Rev. Biochem. 69 2000 217-245
41. Kaufmann S.H. Hengartner M.O. Programmed cell death: alive and well in the new millennium Trends Cell Biol. 11 2001 526-534
42. Nicholson D.W. Thornberry N.A. Caspases: killer proteases Trends Biochem. Sci. 22 1997 299-306
43. Kuida K. Zheng T.S. Na S. Kuan C. Yang D. Karasuyama H. Rakic P. Flavell R.A. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice Nature 384 1996 368-372
44. Chen J. Nagayama T. Jin K. Stetler R.A. Zhu R.L. Graham S.H. Simon R.P. Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia J. Neurosci. 18 1998 4914-4928
45. Liu X. Zou H. Slaughter C. Wang X. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis Cell 89 1997 175-184
46. Enari M. Sakahira H. Yokoyama H. Okawa K. Iwamatsu A. Nagata S. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD Nature 391 1998 43-50
47. Sakahira H. Enari M. Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis Nature 391 1998 96-99
48. Mukae N. Enari M. Sakahira H. Fukuda Y. Inazawa J. Toh H. Nagata S. Molecular cloning and characterization of human caspase-activated DNase Proc. Natl. Acad. Sci. U.S.A. 95 1998 9123-9128
49. Cao G. Pei W. Lan J. Stetler R.A. Luo Y. Nagayama T. Graham S.H. Yin X.M. Simon R.P. Chen J. Caspase-activated DNase/DNA fragmentation factor 40 mediates apoptotic DNA fragmentation in transient cerebral ischemia and in neuronal cultures J. Neurosci. 21 2001 4678-4690
50. Saido T.C. Sorimachi H. Suzuki K. Calpain: new perspectives in molecular diversity and physiological-pathological involvement FASEB J. 8 1994 814-822
51. Suzuki K. Sorimachi H. Yoshizawa T. Kinbara K. Ishiura S. Calpain: novel family members, activation, and physiologic function Biol. Chem. Hoppe Seyler 376 1995 523-529
52. Melloni E. Michetti M. Salamino F. Minafra R. Pontremoli S. Modulation of the calpain autoproteolysis by calpastatin and phospholipids Biochem. Biophys. Res. Commun. 229 1996 193-197
53. 2+ influx upregulate calpain and induce apoptosis in PC12 cells Brain Res. 852 2000 326-334
54. Schoonbroodt S. Ferreira V. Best-Belpomme M. Boelaert J.R. Legrand-Poels S. Korner M. Piette J. Crucial role of the amino-terminal tyrosine residue 42 and the carboxyl-terminal PEST domain of I kappa B alpha in NF-kappa B activation by an oxidative stress J. Immunol. 164 2000 4292-4300
55. Ray S.K. Wilford G.G. Crosby C.V. Hogan E.L. Banik N.L. Diverse stimuli induce calpain overexpression and apoptosis in C6 glioma cells Brain Res. 829 1999 18-27
56. Andersson M. Sjostrand J. Petersen A. Karlsson J.O. Calcium-dependent proteolysis in rabbit lens epithelium after oxidative stress Ophthalmic Res. 30 1998 157-167
57. Kinbara K. Ishiura S. Tomioka S. Sorimachi H. Jeong S.Y. Amano S. Kawasaki H. Kolmerer B. Kimura S. Labeit S. Suzuki K. Purification of native p94, a muscle-specific calpain, and characterization of its autolysis Biochem. J. 335 Pt 3 1998 589-596
58. Lee M.S. Kwon Y.T. Li M. Peng J. Friedlander R.M. Tsai L.H. Neurotoxicity induces cleavage of p35 to p25 by calpain Nature 405 2000 360-364
59. Mouatt-Prigent A. Karlsson J.O. Agid Y. Hirsch E.C. Increased m-calpain expression in the mesencephalon of patients with Parkinson's disease but not in other neurodegenerative disorders involving the mesencephalon: a role in nerve cell death? Neuroscience 73 1996 979-987
60. K. Takahashi, Intracellular calcium-dependent proteolysis, in: R.L. Mellgren, T. Murachi (Eds.), Calpain Substrate Specificity, CRC Press, Boca Raton, 1990, pp. 55-74 (Chapter 4).
61. Fahn S. Cohen G. The oxidant stress hypothesis in Parkinson's disease: evidence supporting it Ann. Neurol. 32 1992 804-812
62. Behl C. Moosmann B. Oxidative nerve cell death in Alzheimer's disease and stroke: antioxidants as neuroprotective compounds Biol. Chem. 383 2002 521-536
63. Putney J.W. Jr. Excitement about calcium signaling in inexcitable cells Science 262 1993 676-678
64. Ghosh A. Greenberg M.E. Calcium signaling in neurons: molecular mechanisms and cellular consequences Science 268 1995 239-247
65. Brunk U.T. Dalen H. Roberg K. Hellquist H.B. Photo-oxidative disruption of lysosomal membranes causes apoptosis of cultured human fibroblasts Free. Radic. Biol. Med. 23 1997 616-626
66. Brachfeld N. Bioenergetics of the normal and anoxic myocardium Adv. Cardiopulm. Dis. 4 1969 66-90
67. Ichihara K. Haneda T. Onodera S. Abiko Y. Inhibition of ischemia-induced subcellular redistribution of lysosomal enzymes in the perfused rat heart by the calcium entry blocker, diltiazem J. Pharmacol. Exp. Ther. 242 1987 1109-1113
68. Molchanova L.V. Nickulina S.E. Ivanova T.N. Ivanov A.I. Polyskova E.D. Role of cAMP in regulation of activity of acid hydrolases of rat heart and liver during ischemia and after recirculation Resuscitation 22 1991 261-274
69. White B.C. Daya A. De Gracia D.J. O'Neil B.J. Skjaerlund J.M. Trumble S. Krause G.S. Rafols J.A. Florescent histochemical localization of lipid peroxidation during brain reperfusion following cardiac arrest Acta Neuropathol. (Berl.) 86 1993 1-9
70. Adamec E. Mohan P.S. Cataldo A.M. Vonsattel J.P. Nixon R.A. Up-regulation of the lysosomal system in experimental models of neuronal injury: implications for Alzheimer's disease Neuroscience 100 2000 663-675
71. Murata M. Miyashita S. Yokoo C. Tamai M. Hanada K. Hatayama K. Towatari T. Nikawa T. Katunuma N. Novel epoxysuccinyl peptides. Selective inhibitors of cathepsin B, in vitro FEBS Lett. 280 1991 307-310
72. Towatari T. Nikawa T. Murata M. Yokoo C. Tamai M. Hanada K. Katunuma N. Novel epoxysuccinyl peptides. A selective inhibitor of cathepsin B, in vivo FEBS Lett. 280 1991 311-315
73. Hashida S. Towatari T. Kominami E. Katunuma N. Inhibitions by E-64 derivatives of rat liver cathepsin B and cathepsin L in vitro and in vivo J. Biochem. (Tokyo) 88 1980 1805-1811
74. Hashida S. Kominami E. Katunuma N. Inhibitions of cathepsin B and cathepsin L by E-64 in vivo. II. Incorporation of [3H]E-64 into rat liver lysosomes in vivo J. Biochem. (Tokyo) 91 1982 1373-1380
75. Katunuma N. Kominami E. Structure, properties, mechanisms, and assays of cysteine protease inhibitors: cystatins and E-64 derivatives Methods Enzymol. 251 1995 382-397
76. Gray J. Haran M.M. Schneider K. Vesce S. Ray A.M. Owen D. White I.R. Cutler P. Davis J.B. Evidence that inhibition of cathepsin-B contributes to the neuroprotective properties of caspase inhibitor Tyr-Val-Ala-Asp-chloromethyl ketone J. Biol. Chem. 276 2001 32750-32755
77. de Duve C. Lysosomes revisited Eur. J. Biochem. 137 1983 391-397
78. Kitao Y. Ozawa K. Miyazaki M. Tamatani M. Kobayashi T. Yanagi H. Okabe M. Ikawa M. Yamashima T. Stern D.M. Hori O. Ogawa S. Expression of the endoplasmic reticulum molecular chaperone (ORP150) rescues hippocampal neurons from glutamate toxicity J. Clin. Invest. 108 2001 1439-1450
79. Roberts L.R. Kurosawa H. Bronk S.F. Fesmier P.J. Agellon L.B. Leung W.Y. Mao F. Gores G.J. Cathepsin B contributes to bile salt-induced apoptosis of rat hepatocytes Gastroenterology 113 1997 1714-1726
80. Guicciardi M.E. Miyoshi H. Bronk S.F. Gores G.L. Cathepsin B knockout mice are resistant to tumor necrosis factor-α-mediated hepatocyte apoptosis and liver injury: implications for therapeutic applications Am. J. Pathol. 159 2001 2045-2054
81. Foghsgaard L. Wissing D. Mauch D. Lademann U. Bastholm L. Boes M. Elling F. Leist M. Jaattela M. Cathepsin B acts as a dominant execution protease in tumor cell apoptosis induced by tumor necrosis factor J. Cell Biol. 153 2001 999-1010
82. Davis J.N. Antonawich F.J. Role of apoptotic proteins in ischemic hippocampal damage Ann. N.Y. Acad. Sci. 835 1997 309-320
83. MacManus J.P. Buchan A.M. Apoptosis after experimental stroke: fact or fashion? J. Neurotrauma. 10 2000 899-914
84. Schwab B.L. Guerini D. Didszun C. Bano D. Ferrando-May E. Fava E. Tam J. Xu D. Xanthoudakis S. Nicholson D.W. Carafoli E. Nicotera P. Cleavage of plasma membrane calcium pumps by caspases: a link between apoptosis and necrosis Cell Death Differ. 9 2002 818-831
85. Porn-Ares M.I. Samali A. Orrenius S. Cleavage of the calpain inhibitor, calpastatin, during apoptosis Cell Death Differ. 5 1998 1028-1033
86. Ferri K.F. Kroemer G. Organelle-specific initiation of cell death pathways Nat. Cell Biol. 3 2001 E255-E263
87. Iwamoto N. Thangnipon W. Crawford C. Emson P.C. Localization of calpain immunoreactivity in senile plaques and in neurones undergoing neurofibrillary degeneration in Alzheimer's disease Brain Res. 561 1991 177-180
88. Shimohama S. Suenaga T. Araki W. Yamaoaka Y. Shimizu K. Kimura J. Presence of calpain II immunoreactivity in senile plaques in Alzheimer's disease Brain Res. 558 1991 105-108
89. Saito K.I. Elce J.S. Hamos J.E. Nixon R.A. Widespread activation of calcium-activated neutral proteinase calpain in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration Proc. Natl. Acad. Sci. U.S.A. 90 1993 2628-2632
90. Nixon R.A. Saito K.I. Grynspan F. Griffin W.R. Katayama S. Honda T. Mohan P.S. Shea T.B. Beermann M. Calcium-activated neutral proteinase calpain system in aging and Alzheimer disease Ann. NY Acad. Sci. 747 1994 77-91
91. Taniguchi S. Fujita Y. Hayashi S. Kakita A. Takahashi H. Murayama S. Saido T.C. Hisanaga S. Iwatsubo T. Hasegawa M. Calpain-mediated degradation of p35 to p25 in postmortem human and rat brains FEBS Lett. 489 2001 46-50
92. Adamec E. Mohan P. Vonsattel J.P. Nixon R.A. Calpain activation in neurodegenerative diseases: confocal immunofluorescence study with antibodies specifically recognizing the active form of calpain 2 Acta Neuropathol. (Berl.) 104 2002 92-104