Implication of cysteine proteases calpain, cathepsin and caspase in ischemic neuronal death of primates

Progress in Neurobiology

Volumn 62, Issue 3, 2000, Pages 273-295

  Yamashima, Tetsumori ^a  

^a KANAZAWA UNIV SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

[1 [(1 FORMYL 2 PHENYLETHYL)CARBAMOYL] 2 METHYLPROPYL]CARBAMIC ACID BENZYL ESTER; ALOXISTATIN ACID; CALPAIN; CASPASE; CASPASE INHIBITOR; CATHEPSIN; CYSTEINE PROTEINASE; CYSTEINE PROTEINASE INHIBITOR; FREE RADICAL; LYSOSOME ENZYME;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; BRAIN ISCHEMIA; CELL DEATH; ENZYME ACTIVATION; HUMAN; LYSOSOME MEMBRANE; MONKEY; NERVE CELL; NEUROPROTECTION; NONHUMAN; PRIMATE; PRIORITY JOURNAL; REVIEW;

ANIMALS; BRAIN ISCHEMIA; CALPAIN; CASPASES; CATHEPSINS; CELL DEATH; HIPPOCAMPUS; NEURONS; PRIMATES; PYRAMIDAL CELLS;

EID: 0034739734     PISSN: 03010082     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-0082(00)00006-X     Document Type: Review

References (200)

1. Alnemri E.S. Mammalian cell death proteases: a family of highly conserved aspartate specific cysteine proteases. J. Cell Biochem. 64:1997;33-42.
2. Alnemri E.S., Livingston D.J., Nicholson D.W., Salvesen G., Thornberry N.A., Wong W.W., Yuan J. Human ICE/CED-3 protease nomenclature. Cell. 87:1996;171.
3. Althaus F.R., Richter C. ADP-ribosylation of proteins. Enzymology and biological significance. Mol. Biol. Biochem. Biophys. 37:1987;1-237.
4. Ambrosini G., Adida C., Altieri D. A novel anti-apoptosis gene, survivin, expressed in cancer and lymphoma. Nature Med. 3:1997;917-921.
5. Ankarcrona M., Dypbukt J.M., Bonfoco E., Zhivotovsky B., Orrenius S., Lipton S.A., Nicotera P. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron. 15:1995;961-973.
6. Arai H., Passonneau J.V., Lust W.D. Energy metabolism in delayed neuronal death of CA1 neurons of the hippocampus following transient ischemia in the gerbil. Metab. Brain Dis. 1:1986;263-278.
7. Auer R.N., Benveniste H. Hypoxia and related conditions. Graham D., Lantos P.L. Greenfield's Neuropathology. 1997;263-314 Arnold, London, Sydney, Auckland.
8. Auer R.N., Kalimo H., Olsson Y., Siesjö B.K. The temporal evolution of hypoglycemic brain damage. Part I: Light and electron microscopic findings in the rat cerebral cortex. Acta Neuropathol (Berl). 67:1985;13-24.
9. Auer R.N., Kalimo H., Olsson Y., Siesjö B.K. The temporal evolution of hypoglycemic brain damage. Part II: Light and electron microscopic findings in the rat cerebral cortex. Acta Neuropathol (Berl). 67:1985;25-36.
10. Bando Y., Kominami E., Katunuma N. Purification and tissue distribution of cathepsin L. J. Biochem. Tokyo. 100:1986;35-42.
11. Barinaga M. Stroke-damaged neurons may commit cellular suicide. Science. 281:1998;1302-1303.
12. Bartus R.T., Hayward N.J., Elliott P.J., Sawyer S.D., Baker K.L., Dean R.L., Akiyama A., Straub J.A., Harbeson S.L., Li Z., Powers J. Calpain inhibitor AK295 protects neurons from focal brain ischemia. Effects of postocclusion intra-arterial administration. Stroke. 25:1994;2265-2270.
13. Bartus R.T., Baker K.L., Heiser A.D., Sawyer S.D., Dean R.L., Elliott P.J., Straub J.A. Postischemic administration of AK275, a calpain inhibitor, provides substantial protection against focal ischemic brain damage. J. Cereb. Blood Flow. Metab. 14:1994;537-544.
14. Bednarski E., Ribak E.C., Lynch G. Suppression of cathepsins B and L causes a proliferation of lysosomes and the formation of meganeurites in hippocampus. J. Neurosci. 17:1997;4006-4021.
15. Bernstein H.G., Kirschke H., Wiederanders B., Kloss P., Rinne A., Dorn A. Cathepsin B immunoreactive neurons in rat brain. A combined light and electron microscopic study. J. Hirnforsch. 29:1988;17-19.
16. Bernstein H.G., Kirschke H., Wiederanders B., Schmidt D., Rinne A. Antigenic expression of cathepsin B in aged human brain. Brain Res. Bull. 24:1990;543-549.
17. Bonfoco E., Krainc D., Ankarcrona M., Nicotera P., Lipton S.A. Apoptosis and necrosis: two distinct events induced respectively by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc. Natl. Acad. Sci. USA. 92:1995;7162-7166.
18. Bossy-Wetzel E., Newmeyer D., Green D. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J. 17:1998;37-49.
19. Boveris A., Chance B. The mitochondrial generation of hydrogen peroxide. Biochem. J. 134:1973;707-716.
20. Bowen D.M., Smith C.B., Davison A.N. Molecular changes in senile dementia. Brain. 96:1973;849-856.
21. Brachfeld N. Maintenance of cell viability. Circ. Res. Suppl. IV. 39/40:1969;202-219.
22. Bredesen D.E. Neural apoptosis. Ann. Neurol. 38:1995;839-851.
23. Brizzee K.R., Cancilla P.A., Sherwood N., Timiras P.S. The amount and distribution of pigments in neurons and glia of the cerebral cortex. J. Gerontol. 24:1969;127-135.
24. 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.
25. Brunk U., Ericsson J.L.E. Electron microscopic studies on rat brain neurons. Localization of acid phosphatase and mode of formation of lipofuscin bodies. J. Ultrastr. Res. 38:1972;1-15.
26. Canu N., Dus L., Barbato C., Ciotti M.T., Brancolini C., Rinaldi A.M., Novak M., Cattaneo A., Bradbury A., Calissano P. Tau cleavage and dephosphorylation in cerebellar granule neurons undergoing apoptosis. J. Neurosci. 18:1998;7061-7074.
27. Casciola-Rosen L.A., Anhalt G.J., Rosen A. DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. J. Exp. Med. 182:1995;1625-1634.
28. Cataldo A.M., Hamilton D.J., Barnett J.L., Paskevich P.A., Nixon R.A. Properties of the endosomal-lysosomal system in the human central nervous system: disturbances mark most neurons in populations at risk to degenerate in Alzheimer's disease. J. Neurosci. 16:1996;186-199.
29. Cataldo A.M., Paskevich P.A., Kominami E., Nixon R.A. Lysosomal hydrolases of different classes are abnormally distributed in brains of patient with Alzheimer disease. Proc. Natl. Acad. Sci. USA. 88:1990;10998-11002.
30. Chan P.H. Oxygen radicals in focal cerebral ischemia. Brain Pathol. 4:1994;59-65.
31. Chan P.H. Role of oxidants in ischemic brain damage. Stroke. 27:1996;1124-1129.
32. Chan P.H., Kawase M., Murakami K., Chen S.F., Li Y., Calagui B., Reola L., Carlson E., Epstein C.J. Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J. Neurosci. 18:1998;8292-8299.
33. Chapman H.A., Riese R.J., Shi G.P. Emerging roles for cysteine proteases in human biology. Annu. Rev. Physiol. 59:1997;63-88.
34. Charriault-Marlangue C., Margail I., Represa A., Popovici T., Plotkine M., Ben-Ari Y. Apoptosis and necrosis after reversible focal ischemia: an in situ DNA fragmentation analysis. J. Cereb. Blood Flow Metab. 16:1996;186-194.
35. 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.
36. Chen J., Zhu R.L., Nakayama M., Kawaguchi K., Jin K., Stetler R.A., Simon R.P., Graham S.H. Expression of the apoptosis-effector gene, Bax is up-regulated in vulnerable hippocampal CA1 neurons following global ischemia. J. Neurochem. 67:1996;64-71.
37. Choi D.W. Ischemia-induced neuronal apoptosis. Curr. Opin. Neurobiol. 6:1996;667-672.
38. Choi Y.H., Lee S.J., Nguyen P., Jang J.S., Lee J., Wu M.I., Takano E., Maki M., Henkart P.A., Trepel J.B. Regulation of cyclin D1 by calpain protease. J. Biol. Chem. 272:1997;28479-28484.
39. Choi J.H., Yu B.P. Brain synaptosomal ageing-free radicals and membrane fluidity. Free Rad. Biol. Med. 18:1995;133-139.
40. Chopp M., Vande L.A., Chen H., Knight R., Helpern J.A., Welch K.M. Chronic cerebral intracellular alkalosis following forebrain ischemic insult in rats. Stroke. 21:1990;463-466.
41. Cohen G.M. Caspases: the executioners of apoptosis. Biochem. J. 326:1997;1-16.
42. Colbourne F., Sutherland G.R., Auer R.N. Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J. Neurosci. 19:1999;4200-4210.
43. Corbett D., Nurse S. The problem of assessing effective neuroprotection in experimental cerebral ischemia. Prog. Neurobiol. 54:1998;531-548.
44. Coyle J.T., Puttfarcken P. Oxidative stress, glutamate, and neurodegenerative disorders. Science. 262:1993;689-695.
45. Croall D.E., Demartino G.N. Calcium-activated neutral protease (calpain) system: structure, function, and regulation. Physiol. Rev. 81:1991;813-847.
46. de Duve C., Wattiaux R. Functions of lysosomes. Annu. Rev. Physiol. 28:1996;435-492.
47. Deshpande J., Bergstedt K., Lindén T., Kalimo H., Wieloch T. Ultrastructural changes in the hippocampal CA1 region following transient cerebral ischemia: evidence against programmed cell death. Exp. Brain Res. 88:1992;91-105.
48. Duckett C.S., Nava V.E., Gedrich R.W., Clem R.J., Van Dongen J.L., Gilfillan M.C., Shiels H., Hardwick J.M., Thompson C.B. A conserved family of cellular genes related to the becuovirus iap gene and encoding apoptosis inhibitors. EMBO J. 15:1996;2685-2689.
49. Eguchi Y., Shimizu S., Tsujimoto Y. Intracellular ATP levels determine cell death fate by apoptosis or necrosis. Cancer Res. 57:1997;1835-1840.
50. 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.
51. Endres M., Namura S., Shimizu-Sasamala M., Waeber C., Zhang L., Gomez-Isla T., Hyman B.T., Moskowitz M.A. Attenuation of delayed neuronal death after mild focal ischemia in mice by inhibition of the caspase family. J. Cereb. Blood Flow Meatb. 18:1998;238-247.
52. Fernandes-Alnemri T., Litwack G., Alnemri E.S. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 β-converting enzyme. J. Biol. Chem. 269:1994;30761-30764.
53. Fujimura M., Morita-Fujimura Y., Kawase M., Copin J.C., Calagui B., Epstein C.J., Chan P.H. Mananese superoxide dismutase mediates the early release of mitochondrial cytochrome C and subsequent DNA fragmentation after permanent focal cerebral ischemia in mice. J. Neurosci. 19:1999;3414-3422.
54. Ghayur T., Hugunin M., Talanian R.V., Ratnofsky S., Quinlan C., Emoto Y., Pandey P., Datta R., Huang Y., Kharbanda S., Allen H., Kamen R., Wong W., Kufe D. Proteolytic activation of protein kinase C δ by an ICE/CED 3-like protease induces characteristics of apoptosis. J. Exp. Med. 184:1996;2399-2404.
55. Gillardon F., Lenz C., Waschke K.F., Krajewski S., Reed J.C., Zimmermann M., Kuschinsky W. Altered expression of Bcl-2, Bcl-X, Bax, and c-Fos colocalizes with DNA fragmentation and ischemic cell damage following middle cerebral artery occlusion in rats. Mol. Brain Res. 40:1996;254-260.
56. Green G.D., Shaw E. Peptidyl diazomethyl ketones are specific inactivators of thiol proteinases. J. Biol. Chem. 256:1981;1923-1928.
57. Gregoriou M., Willis A.C., Pearson M.A., Crawford C. The calpain cleavage sites in the epidermal growth factor receptor kinase domain. Eur. J. Biochem. 223:1994;455-464.
58. Gwag B.J., Lobner D., Koh J.Y., Wie M.B., Choi D.W. Blockade of glutamate receptors unmasks neuronal apoptosis after oxygen-glucose deprivation in vitro. Neurosci. 68:1995;615-619.
59. Hampton M.B., Orrenius S. Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis. FEBS Lett. 414:1997;552-556.
60. Han Z., Malik N., Carter T., Reeves W.H., Wyche J.H., Hendrickson E.A. DNA-dependent protein kinase is a target for a CPP32-like apoptotic protease. J. Biol. Chem. 271:1996;25035-25040.
61. Handa K., Tamai M., Yamagishi M., Ohmura S., Sawada J., Tanaka I. Isolation and characterization of E-64, a new thiol protease inhibitor. Agric. Biol. Chem. 42:1978;523-528.
62. Hara A., Iwai T., Niwa M., Uematsu T., Yoshimi N., Tanaka T., Mori H. Immunohistochemical detection of Bax and Bcl-2 proteins in gerbil hippocampus following transient forebrain ischemia. Brain Res. 711:1996;249-253.
63. Hay B.A., Wassarman D.A., Rubin G.M. Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell. 83:1995;1253-1262.
64. Hengartner M.O., Horvitz H.R. Programmed cell death in Caenorhabditis elegans. Curr. Opin. Genet. Dev. 4:1994;581-586.
65. Hinds J.W., McNelly N.A. Ageing in the rat olfactory bulb: quantitative changes in mitral cell organelles and somato-dendritic synapses. J. Comp. Neurol. 184:1979;811-819.
66. Hirsch T., Susin S.A., Marzo I., Marchetti P., Zamzami N., Kroemer G. Mitochondrial permeability transition in apoptosis and necrosis. Cell Biol. Toxicol. 14:1998;141-145.
67. Hong S.C., Goto Y., Lanzino G., Soleau S., Kassell N.F., Lee K.S. Neuroprotection with a calpain inhibitor in a model of focal cerebral ischemia. Stroke. 25:1994;663-669.
68. Honkaniemi J., Massa S.M., Breckinridge M., Sharp F.R. Global ischemia induces apoptosis-associated genes in hippocampus. Brain Res. 42:1996;79-88.
69. Horn M., Schlote W. Delayed neuronal death and delayed neuronal recovery in the human brain following global ischemia. Acta Neuropathol. (Berl). 85:1992;79-87.
70. 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. Pharm. Exp. Therap. 242:1987;1109-1113.
71. Ishisaka R., Utsumi T., Yabuki M., Kanno T., Furuo T., Inoue M., Utsumi K. Activation of caase-3-like protease by digitonin-treated Iysosomes. FEBS Lett. 435:1998;233-236.
72. Iwai T., Hara A., Niwa M., Nozaki M., Uematsu T., Sakai N., Yamada H. Temporal profile of nuclear DNA fragmentation in situ in gerbil hippocampus following transient forebrain ischemia. Brain Res. 671:1995;305-308.
73. Johnson E.M. Jr., Deckwerth T.L. Molecular mechanisms of developmental neuronal death. Annu. Rev. Neurosci. 16:1993;31-46.
74. Johnson E.M. Jr., Deckwerth T.L., Deshmukh M. Neuronal death in developmental models: possible implications in neuropathology. Brain Pathol. 6:1996;397-409.
75. Kalra J., Lautner D., Massey K.L., Prasad K. Oxygen free radicals induced release of lysosomal enzymes in vitro. Mol. Cell Biochem. 84:1988;233-238.
76. Katunuma N., Kominami E. Structure, properties, mechanisms, and assays of cyteine protease inhibitors: cystatins and E-64 derivatives. Methods Enzymol. 251:1995;382-397.
77. Kawahara A., Ohsawa Y., Matsumura H., Uchiyama Y., Nagata S. Caspase-independent cell killing by Fas-associated protein with death domain. J. Cell Biol. 143:1998;1353-1360.
78. Keller J.N., Kindy M.S., Holtsberg F.W., St Clair D.K., Yen H.C., Germeyer A., Steiner S.M., Bruce-Keller A.J., Hutchins J.B., Mattson M.P. Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J. Neurosci. 18:1998;687-697.
79. Keppler D., Sameni M., Moin K., Mikkelsen T., Diglio C.A., Sloane B.F. Tumor progression and angiogenesis: cathepsin B & Co. Biochem. Cell Biol. 74:1996;799-810.
80. L as an inhibitor of cytosolic cytochrome c accumulation in DNA damage-induced apoptosis. Proc. Natl. Acad. Sci. USA. 94:1997;6939-6942.
81. Kihara S., Shiraishi T., Nakagawa S., Toda K., Tabuchi K. Visualization of DNA double strand breaks in the gerbil hippocampal CA1 following transient ischemia. Neurosci. Lett. 175:1994;133-136.
82. Kimura Y., Koga H., Araki N., Mugita N., Fujita N., Takeshima H., Nishi T., Yamashima T., Saido T.C., Yamasaki T., Moritake K., Saya H., Nakao M. The involvement of calpain-dependent proteolysis of the tumor suppressor NF2 (merlin) in schwannomas and meningiomas. Nat. Med. 4:1998;915-922.
83. Kinouchi H., Epstein C.J., Mizui T., Carlson E., Chen S.F., Chan P.H. Attenuation of focal cerebral ischemic injury in transgenic mice overexpressing CuZn superoxide dismutase. Proc. Natl. Acad. Sci. USA. 88:1991;11158-11162.
84. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 239:1982;57-69.
85. Kirino T., Sano K. Fine structural nature of delayed neuronal death following ischemia in the gerbil hippocampus. Acta Neuropathol (Berl). 62:1984;209-218.
86. Kluck R.M., Bossy-Wetzel E., Green D.R., Newmeyer D.D. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science. 275:1997;1132-1136.
87. Kohda Y., Yamashima T., Sakuda K., Yamashita J., Ueno T., Kominami E., Yoshioka T. Dynamic changes of cathepsin B and L expression in the monkey hippocampus after transient ischemia. Biochem. Biophys. Res. Commun. 228:1996;616-622.
88. Kominami E., Tsukahara T., Bando Y., Katunuma N. Distribution of cathepsins B and H in rat tissues and peripheral blood cells. J. Biochem. Tokyo. 98:1985;87-93.
89. Kondo T., Reaume A.G., Huang T.T., Murakami K., Carlson E., Chen S., Scott R.W., Epstein C.J., Chan P.H. Edema formation exacerbates neurological and histological outcomes after focal cerebral ischemia in CuZn-superoxide dismutase gene knockout mutant mice. Acta Neurochir. (Wien). 70:1997;62-64.
90. Kontos H.A. George E. Brown memorial lecture: oxygen radicals in cerebral vascular injury. Circ. Res. 57:1985;508-516.
91. Kouroku Y., Urase K., Fujita E., Isahara K., Ohsawa Y., Uchiyama Y., Momoi M.Y., Momoi T. Detection of activated caspase-3 by a cleavage site-directed antiserum during naturally occurring DRG neurons apoptosis. Biochem. Biophys. Res. Commu. 247:1998;780-784.
92. Krajewski S., Krajewska M., Ellerby L.M., Welsh K., Xie Z., Deveraux Q.L., Salvesen G.S., Bredesen D.E., Rosenthal R.E., Fiskum G., Reed J.C. Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc. Natl. Acad. Sci. USA. 96:1999;5752-5757.
93. Kubbutat M.H., Vousden K.H. Proteolytic cleavage of human p53 by calpain: a potential regulator of protein stability. Mol. Cell Biol. 17:1997;460-468.
94. 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.
95. Lee K.S., Frank S., Vanderklish P., Arai A., Lynch G. Inhibition of proteolysis protects hippocampal neurons from ischemia. Proc. Natl. Acad. Sci. USA. 88:1991;7233-7237.
96. Lee J.M., Zipfel G.J., Choi D.W. The changing landscape of ischaemic brain injury mechanisms. Nature. 399:(6738 Suppl):1999;A7-A14.
97. Leist M., Volbracht C., Kühnle S., Fava E., Ferrando-May E., Nicotera P. Caspase-mediated apoptosis in neuronal excitotoxicity triggered by nitric oxide. Mol. Med. 11:1997;750-764.
98. Lemaire C., Andreau K., Souvannavong V., Adam A. Inhibition of caspase activity induces a switch from apoptosis to necrosis. FEBS Lett. 425:1998;266-270.
99. Li H., Bunchan A.M. Delayed treatment with NBQX or SNX-111 following transient forebrain ischemia in rats. Can. J. Neurol. Sci. 22:1995;S47.
100. Li P., Nijhawan D., Budihardjo I., Srinivasula S., Ahmad M., Alnemri E., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1-Caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:1997;479-489.
101. Li Y., Sharov V.G., Jiang N., Zaloga C., Sabbah H.N., Chopp M. Ultrastructural and light microscopic evidence of apoptosis after middle cerebral artery occlusion in the rat. Am. J. Pathol. 146:1995;1045-1051.
102. Liston P., Roy N., Tamai K., Lefebvre C., Baird S., Cherton-Horvat G., Farahani R., McLean M., Ikeda J.E., MacKenzie A., Korneluk R.G. Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature. 379:1996;349-353.
103. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 86:1996;147-157.
104. Liu X., Zou H., Slaughter C., Wang X. DEF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell. 89:1997;175-184.
105. MacManus J.P., Buchan A.M., Hill I.E., Rasquinha I., Preston E. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci. Lett. 164:1993;89-92.
106. MacManus J.P., Hill I.E., Preston E., Rasquinha I., Walker T., Buchan A.M. Differences in DNA fragmentation following transient cerebral or decapitation ischemia in rats. J. Cereb. Blood Flow. Metab. 15:1995;728-737.
107. MacManus J.P., Linnik M.D. Gene expression induced by cerebral ischemia: an apoptotic perspective. J. Cereb. Blood Flow Metab. 17:1997;815-832.
108. MacManus J.P., Rasquinha I., Tuor U., Preston E. Detection of higher-order 50 and 10 kbp DNA fragments before apoptotic internucleosomal cleavage following transient cerebral ischemia. J. Cereb. Blood Flow Metab. 17:1997;376-387.
109. Markgraf C.G., Velayo N.L., Johnson M.P., McCarty D.R., Medhi S., Koehl J.R., Chmielewski P.A., Linnik M.D. Six-hour window of opportunity for calpain inhibition in focal cerebral ischemia in rats. Stroke. 29:1998;152-158.
110. 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.
111. Mashima T., Naito M., Noguchi K., Miller D.K., Nicholson D.W., Tsuruo T. Actin cleavage by CPP-32/apopain during the development of apoptosis. Oncogene. 14:1997;1007-1012.
112. Mehdi S. Cell-penetrating inhibitors of calpain. Trends. Biochem. Sci. 16:1991;150-153.
113. Melchior F., Gerace L. Mechanisms of nuclear protein import. Curr. Opin. Cell Biol. 7:1995;310-318.
114. Monmaur P., Thomson M.A., M'Harzi M. Temporal changes in hippocampal theta activity following twenty minutes of forebrain ischemia in the chronic rat. Brain Res. 378:1986;262-273.
115. Molchanova, L.V., Nickulina, S.E., Ivanova, T.N., Ivanov, A.I., Polyskova, E.D., 1991. Role of cAMP in regulation of activity of acid hydrolases of rat heart and liver during ischemia and after recirculation. Resuscitation 22, 261-274.
116. 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. USA. 95:1998;9123-9128.
117. Murachi T. Calcium-dependent proteinases and specific inhibitors: calpain and calpastatin. Biochem. Soc. Symp. 49:1984;149-167.
118. Murakami K., Kondo T., Kawase M., Li Y., Sato S., Chen S.F., Chan P.H. Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J. Neurosci. 18:1998;205-213.
119. 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.
120. Musil D., Zucic D., Turk D., Engh R.A., Mayr I., Huber R., Popovic T., Turk V., Towatari T., Katunuma N., Bode W. The refined 2.15 A X-ray crystal structure of human liver cathepsin B: the structural basis for its specificity. EMBO J. 10:1991;2321-2330.
121. Nagarajan S., Theodore D.R., Abraham J., Balasubramanian A.S. Free fatty acids, lipid peroxidation, and lysosomal enzymes in experimental focal cerebral ischemia in primates: loss of lysosomal latency by lipid peroxidation. Neurochem. Res. 13:1988;193-201.
122. Nakamura Y., Takeda M., Suzuki H., Morita H., Tada K., Hariguchi S., Nishimura T. Lysosome instability in aged rat brain. Neurosci. Lett. 97:1989;215-220.
123. Nakanishi H., Tsukuba T., Kondou T., Tanaka T., Yamamoto K. Transient forebrain ischemia induces increased expression and specific localization of cathepsins E and D in rat hippocampus and neostriatum. Exp. Neurol. 121:1993;215-223.
124. Nakanishi H., Tominaga K., Amano T., Hirotsu I., Inoue T., Yamamo to K. Age-related changes in activities and localizations of cathepsins D, E, B, and L in the rat brain tissues. Exp. Neurol. 126:1994;119-128.
125. Namura S., Zhu J., Fink K., Endres M., Srinivasan A., Tomaselli K.J., Yuan J., Moskowitz M.A. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J. Neurosci. 18:1998;3659-3668.
126. Narula J., Pandey P., Arbustini E., Haider N., Narula N., Kolodgie F.D., Dal Bello B., Semigran M.J., Bielsa-Masdeu A., Dec G.W., Israels S., Ballester M., Virmani R., Saxena S., Kharbanda S. Apoptosis in heart failure: release of cytochrome c from mitochondria and activation of caspase-3 in human cardiomyopathy. Proc. Natl. Acad. Sci. USA. 96:1999;8144-8149.
127. Neumar R.W., DeGracia D.J., White B.C., McDermott P.J., Evans D.R., Krause G.S. Eukaryotic initiation factor 4E degradation during brain ischemia. J. Neurochem. 65:1995;1391-1394.
128. Ni B., Wu X., Su Y., Stephenson D., Smalstig E.B., Clemens J., Paul S.M. Transient global forebrain ischemia induces a prolonged expression of the caspase-3 mRNA in rat hippocampal CA1 pyramidal neurons. J. Cereb. Blood Flow Metab. 18:1998;248-256.
129. Nicholson D.W. ICE/CED3-like proteases as therapeutic targets for the control of inappropriate apoptosis. Nature Biotechnol. 14:1996;297-301.
130. Nicholson D.W., Ali A., Thornberry N.A., Vaillancourt J.P., Ding C.K., Gallant M., Gareau Y., Griffin P.R., Labelle M., Lazebnik Y.A. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature. 376:1995;37-43.
131. Nicholson D.W., Thornberry N.A. Caspases: killer proteases. Trends Biochem. Sci. 22:1997;299-306.
132. Nicotera P., Leist M., Manzo L. Neuronal cell death: a demise with different shapes. Trends Pharmacol. Sci. 20:1999;46-51.
133. Nicotera P., Leist M., Single B., Volbracht C. Execution of apoptosis: converging or diverging pathways? Biol. Chem. 380:1999;1035-1040.
134. Nitatori T., Sato N., Waguri S., Karasawa Y., Araki H., Shibanai K., Kominami E., Uchiyama Y. Delayed neuronal death in the CA-1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 15:1995;1001-1011.
135. Nixon R.A., Cataldo A.M. The Iysosomal system in neuronal cell death: a review. Ann. NY Acad. Sci. 679:1993;87-109.
136. Okamoto M., Matsumoto M., Ohtsuki T., Taguchi A., Mikoshiba K., Yanagihara T., Kamada T. Internucleosomal DNA cleavage involved in ischemia-induced neuronal death. Biochem. Biophys. Res. Commun. 196:1993;1356-1362.
137. Öllinger K., Brunk U.T. Cellular injury induced by oxidative stress is mediated through lysosomal damage. Free Rad. Biol. Med. 19:1995;565-574.
138. Pante N., Aebi U. Toward the molecular dissection of protein import into nuclei. Curr. Opin. Cell Biol. 8:1996;397-406.
139. Petito C.K., Feldmann E., Pulsinelli W.A., Plum F. Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurol. 37:1987;1281-1286.
140. Piantadosi C.A., Zhang J. Mitochondrial generation of reactive oxygen species after brain ischemia in the rat. Stroke. 27:1996;327-332.
141. Pike B.R., Zhao X., Newcomb J.K., Posmantur R.M., Wang K.K., Hayes R.L. Regional calpain and caspase-3 proteolysis of α-spectrin after traumatic brain injury. NeuroReport. 9:1998;2437-2442.
142. Pike B.R., Zhao X., Newcomb J.K., Wang K.K., Posmantur R.M., Hayes R.L. Temporal relationships between de novo protein synthesis, calpain and caspase-3-like protease activation, and DNA fragmentation during apoptosis in septo-hippocampal cultures. J. Neurosci. Res. 52:1998;505-520.
143. Pliura D.H., Bonaventura B.J., Smith R.A., Coles P.J., Krantz A. Comparative behaviour of calpain and cathepsin B toward peptidyl acyloxymethyl ketones, sulphonium methyl ketones and other potential inhibitors of cysteine proteinases. Biochem. J. 288:1992;759-762.
144. Pope A., Nixon R.A. Proteases of human brain. Neurochem. Res. 9:1984;291-323.
145. Porn-Ares M.I., Samali A., Orrenius S. Cleavage of the calpain inhibitor, calpastatin, during apoptosis. Cell Death Differ. 5:1998;1028-1033.
146. Posmantur R.M., Zhao X., Kampfl A., Clifton G.L., Hayes R.L. Immunoblot analyses of the relative contributions of cysteine and aspartic proteases to neurofilament breakdown products following experimental brain injury in rats. Neurochem. Res. 23:1998;1265-1276.
147. Pulsinelli W.A., Brierley J.B., Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 11:1982;491-498.
148. Rinkenberger J.L., Korsmeyer S.J. Errors of homeostasis and deregulated apoptosis. Curr. Opin. Genet. Dev. 7:1997;589-596.
149. Roberg K., Öllinger K. Oxidative stress causes relocation of the lysosomal enzyme cathepsin D with ensuing apoptosis in neonatal rat cardiomyocytes. Am. J. Pathol. 152:1998;1151-1156.
150. Roberts-Lewis J.M., Savage M.J., Marcy V.R., Pinsker L.R., Siman R. Immunolocalization of calpain I-mediated spectrin degradation to vulnerable neurons in the ischemic gerbil brain. J. Neurosci. 14:1994;3934-3944.
151. Rothe M., Pan M.G., Henzel W.J., Ayres T.M., Goeddel D.V. The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell. 83:1995;1243-1252.
152. Roy N., Deveraux Q.L., Takahashi R., Salvesen G.S., Reed J.C. The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO J. 16:1997;6914-6925.
153. Roy N., Mahadevan M.S., McLean M., Shutler G., Yaraghi Z., Farahani R., Baird S., Besner-Johnston A., Lefebvre C., Kang X., Salih M., Aubry H., Tamai K., Guan X., Ioannou P., Crawford T.O., de Jong P.J., Surh L., Ikeda J.E., Korneluk R.G., Mackenzie A. The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell. 80:1995;167-178.
154. Saido T.C., Kawashima S., Tani E., Yokota M. Up- and down-regulation of calpain inhibitor polypeptide, calpastatin, in postischemic hippocampus. Neurosci. Lett. 227:1997;75-78.
155. Saido T.C., Nagao S., Shiramine M., Tsukaguchi M., Sorimachi H., Muraofushi H., Tsuchiya T., Ito H., Suzuki K. Autolytic transition of μ-calpain upon activation as resolved by antibodies distinguishing between the pre- and post-autolysis forms. J. Biochem. 111:1992;81-86.
156. Saido T.C., Yokota M., Nagao S., Yamaura I., Tani E., Tsuchiya T., Suzuki K., Kawashima S. Spatial resolution of fodrin proteolysis in postischemic brain. J. Biol. Chem. 25:1993;25239-25243.
157. Sakahira H., Enari M., Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature. 391:1998;96-99.
158. Satoh M.S., Lindahl T. Role of poly(ADP-ribose) formation in DNA repair. Nature. 356:1992;356-358.
159. Sawada M., Carlson J.C. Changes in superoxide radical and lipid peroxide formation in the brain, heart and liver during the lifetime of the rat. Mech. Ageing Dev. 41:1987;125-137.
160. Shimizu S., Eguchi Y., Kamiike W., Waguri S., Uchiyama Y., Matsuda H., Tsujimoto Y. Retardation of chemical hypoxia-inducd necrotic cell death by Bcl-2 and ICE inhibitors: possible involvement of common mediators in apoptotic and necrotic signal transductions. Oncogene. 12:1996;2045-2050.
161. Shimizu S., Eguchi Y., Kamiike W., Matsuda H., Tsujimoto Y. Bcl-2 expression prevents activation of the ICE protease cascade. Oncogene. 12:1996;2251-2257.
162. Shimizu S., Eguchi Y., Kamiike W., Waguri S., Uchiyama Y., Matsuda H., Tsujimoto Y. Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene. 13:1996;21-29.
163. Shimizu S., Eguchi Y., Kamiike W., Akao Y., Kosaka H., Hasegawa J., Matsuda H., Tsujimoto Y. Involvement of ICE family proteases in apoptosis induced by reoxygenation of hypoxic hepatocytes. Am. J. Physiol. 271:1996;G949-G954.
164. Song Q., Wei T., Lees-Miller S., Alnemri E., Watters D., Lavin M.F. Resistence of actin to cleavage during apoptosis. Proc. Natl. Acad. Sci. USA. 94:1997;157-162.
165. Sorimachi H., Ishiura S., Suzuki K. Structure and physiological function of calpains. Biochem. J. 328:1997;721-732.
166. Sorimachi Y., Harada K., Saido T.C., Ono T., Kawashima S., Yoshida K. Downregulation of calpastatin in rat heart after brief ischemia and reperfusion. J. Biochem. 122:1997;743-748.
167. Spizz G., Blackshear P.J. Identification and characterization of cathepsin B as the cellular MARCKS cleaving enzyme. J. Biol. Chem. 272:1997;23833-23842.
168. Tabuchi E., Endo S., Ono T., Nishijo H., Kuze S., Kogure K. Hippocampal neuronal damage after transient forebrain ischemia in monkey. Brain Res. Bull. 29:1992;685-690.
169. Tabuchi E., Ono T., Nishijo H., Endo S., Kuze S. Ischemic neuronal damage specific to monkey hippocampus: histological investigation. Brain Res. Bull. 37:1995;73-87.
170. Terry R.D., Gonatas N.K., Weiss M. Ultrastructural studies in Alzheimer's presenile dementia. Am. J. Pathol. 44:1964;269-297.
171. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science. 267:1995;1456-1462.
172. 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.
173. Tsuchiya K., Kohda Y., Yoshida M., Zhao L., Ueno T., Yamashita J., Yoshioka T., Kominam E., Yamashima T. Postictal blockade of ischemic hippocampal neuronal death in primates using selective cathepsin inhibitors. Exp. Neurol. 155:1999;187-194.
174. Uren A.G., Pakusch M., Hawkins C.J., Puls K.L., Vaux D.L. Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors. Proc. Natl. Acad. Sci. USA. 93:1996;4974-4978.
175. Vancompernolle K., Van Herreweghe F., Pynaert G., Van de Craen M., De Vos K., Totty N., Sterling A., Fiers W., Vandenabeele P., Grooten J. Atractyloside-induced release of cathepsin B, a protease with caspase-processing activity. FEBS Lett. 438:1998;150-158.
176. Van de Craen M., Vandenabeele P., Declercq W., Van den Brande I., Van Loo
177. Velier J.J., Ellison J.A., Kikly K.K., Spera P.A., Barone F.C., Feuerstein G.Z. Caspase-8 and caspase-3 are expressed by different populations of cortical neurons undergoing delayed cell death after focal stroke in the rat. J. Neurosci. 19:1999;5932-5941.
178. Villa P.G., Henzel W.J., Sensenbrenner M., Henderson C.E., Pettmann B. Calpain inhibitors, but not caspase inhibitors, prevent actin proteolysis and DNA fragmentation during apoptosis. J. Cell Sci. 111:1998;713-722.
179. Wang K.K. Developing selective inhibitors of calpain. Trends Pharmacol. Sci. 11:1990;139-142.
180. Wang K.K., Nath R., Posner A., Raser K.J., Buroker-Kilgore M., Hajimohammadreza I., Probert A.W. Jr., Marcoux F.W., Ye Q., Takano E., Hatanaka M., Maki M., Caner H., Collins J.L., Fergus A., Lee K.S., Lunney E.A., Hays S.J., Yuen P. An α-mercaptoacrylic acid derivative is a selective nonpeptide cell-permeable calpain inhibitor and is neuroprotective. Proc. Natl. Acad. Sci. USA. 93:1996;6687-6692.
181. Wang K.K., Posmantur R., Nadimpalli R., Nath R., Mohan P., Nixon R.A., Talanian R.V., Keegan M., Herzog L., Allen H. Caspase-mediated fragmentation of calpain inhibitor protein calpastatin during apoptosis. Arch. Biochem. Biophys. 356:1998;187-196.
182. Wang X., Zelenski N.G., Yang J., Sakai J., Brown M.S., Goldstein J.L. Cleavage of sterol regulatory element binding proteins (SREBPs) by CPP32 during apoptosis. EMBO J. 15:1996;1012-1020.
183. Waterhouse N.J., Finucane D.M., Green D.M., Green D.R., Elce J.S., Kumar S., Alnemri E.S., Litwack G., Khanna K., Lavin M.F., Watters D.J. Calpain activation is upstream of caspases in radiation-induced apoptosis. Cell Death Differ. 12:1998;1051-1061.
184. Watt F., Molloy P.L. Specific cleavage of transcription factors by the thiol protease, m-calpain. Nucleic Acid Res. 21:1993;5092-5100.
185. 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.
186. Wyllie A.H., Kerr J.F., Currie A.R. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:1980;251-306.
187. Xu D., Bureau Y., McIntyre D.C., Nicholson D.W., Liston P., Zhu Y., Fong W.G., Crocker S.J., Korneluk R.G., Robertson G.S. Attenuation of ischemia-induced cellular and behavioral deficits by X chromosome-linked inhibitor of apoptosis protein overexpression in the rat hippocampus. J. Neurosci. 19:1999;5026-5033.
188. Xu D.G., Crocker S.J., Doucet J.P., St-Jean M., Tamai K., Hakim A.M., Ikeda J.E., Liston P., Thompson C.S., Korneluk R.G., MacKenzie A., Robertson G.S. Elevation of neuronal expression of NAIP reduces ischemic damage in the rat hippocampus. Nat. Med. 3:1997;997-1004.
189. Xue D., Shaham S., Horvitz H.R. The Caenorhabditis elegans cell-death protein CED-3 is a cysteine protease with substrate specificities similar to those of the human CPP32 protease. Genes Dev. 10:1996;1073-1083.
190. Yakovlev A.G., Knoblach S.M., Fan L., Fox G.B., Goodnight R., Faden A.I. Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. J. Neurosci. 17:1997;7415-7424.
191. Yamamoto K., Hayakawa T., Mogami H., Akai F., Yanagihara T. Ultrastructural investigation of the CA1 region of the hippocampus after transient cerebral ischemia in gerbils. Acta Neuropathol. (Berl). 80:1990;487-492.
192. 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.
193. 2 and calpain responses prior to delayed neuronal death in monkeys. Eur. J. Neurosci. 8:1996;1932-1944.
194. 2+ mobilization induced by hypoxia-hypoglycemia in the monkey hippocampal slices. Biochem. Biophys. Res. Commun. 205:1994;1843-1849.
195. Yang J., Liu X., Bhalla K., Kim C.N., Ibrado A.M., Cai J., Peng I.I., Jones D.P., Wang X. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science. 275:1997;1129-1132.
196. Yasuhara N., Eguchi Y., Tachibana T., Imamoto N., Yoneda Y., Tsujimoto Y. Essential role of active nuclear transport in apoptosis. Genes Cells. 2:1997;55-64.
197. Yokota M., Saido T.C., Tani E., Kawashima S., Suzuki K. Three distinct phases of fodrin proteolysis induced in postischemic hippocampus. Involvement of calpain and unidentified protease. Involvement of calpain and unidentified protease. Stroke. 26:1995;1901-1907.
198. Yuan J., Shaham S., Ledoux S., Ellis H.M., Horvitz H.R. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 β-converting enzyme. Cell. 75:1993;641-652.
199. Zola-Morgan S., Squire L.R., Amaral D.G. Human amnesia and the medial temporal region: Enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J. Neurosci. 6:1986;2950-2967.
200. Zou H., Henzel W.J., Liu X., Lutschg A., Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 90:1997;405-413.