Caspase-3 apoptotic signaling following injury to the central nervous system

Clinical Chemistry and Laboratory Medicine

Volumn 39, Issue 4, 2001, Pages 299-307

  Springer, Joe E ^a   Nottingham, Stephanie A ^a   McEwen, Melanie L ^a   Azbill, Robert D ^a   Jin, Ying ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

Author keywords

Apoptosis; Brain trauma; Caspases; Spinal cord trauma

Indexed keywords

CALPAIN; CASPASE 3; DNA FRAGMENT; GLUTAMIC ACID; PROTEIN P53; REACTIVE OXYGEN METABOLITE; TACROLIMUS;

APOPTOSIS; ARTICLE; BRAIN INJURY; BRAIN ISCHEMIA; CELL DEATH; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; MITOCHONDRION; NERVOUS SYSTEM INJURY; NONHUMAN; OXIDATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN TARGETING; RAT; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SPINAL CORD INJURY;

ANIMALS; APOPTOSIS; BRAIN INJURIES; CASPASE 3; CASPASES; CENTRAL NERVOUS SYSTEM; HUMANS; NEURONS; PHENOTYPE; SIGNAL TRANSDUCTION;

EID: 0035036508     PISSN: 14346621     EISSN: None     Source Type: Journal    
DOI: 10.1515/CCLM.2001.046     Document Type: Article

References (136)

1. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972; 26(4):239-57.
2. Wyllie AH, Kerr JF, Currie AR. Cell death: the significance of apoptosis. Int Rev Cytol 1980; 68:251-306.
3. Searle J, Kerr JF, Bishop CJ. Necrosis and apoptosis: distinct modes of cell death with fundamentally different significance. Pathol Annu 1982;17 Pt 2:229-59.
4. Yuan J, Horvitz HR. The Caenorhabditis elegans cell death gene ced-4 encodes a novel protein and is expressed during the period of extensive programmed cell death. Development 1992; 116(2):309-20.
5. Hengartner MO, Horvitz HR. Programmed cell death in Caenorhabditis elegans. Curr Opin Genet Dev 1994; 4(4):581-6.
6. Hengartner MO, Ellis RE, Horvitz HR. Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature 1992; 356(6369):494-9.
7. Yuan JY, Horvitz HR. The Caenorhabditis elegans genes ced-3 and ced-4 act cell autonomously to cause programmed cell death. Dev Biol 1990; 138(1):33-41.
8. Chinnaiyan AM, O'Rourke K, Lane BR, Dixit VM. Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science 1997; 275(5303):1122-6.
9. Xue D, Shaham S, Horvitz HR. 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 1996; 10(9):1073-83.
10. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 1993; 75(4):641-52.
11. Schwartz LM, Osborne BA. Ced-3/ICE: evolutionary conserved regulation of cell death. Bioessays 1994; 16(6):387-9.
12. Schlegel J, Peters I, Orrenius S, Miller DK, Thornberry NA, Yamin TT, et al. CPP32/apopain is a key interleukin 1 beta converting enzyme-like protease involved in Fas-mediated apoptosis. J Biol Chem 1996; 271(4):1841-4.
13. Tewari M, Quan LT, O'Rourke K, Desnoyers S, Zeng Z, Beidler DR, et al. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 1995; 81(5):801-9.
14. Thornberry NA. The caspase family of cysteine proteases. Br Med Bull 1997; 53(3):478-90.
15. Cohen GM. Caspases: the executioners of apoptosis. Biochem J 1997; 326(Pt 1):1-16.
16. Liu X, Kim CN, Pohl J, Wang X. Purification and characterization of an interleukin-1beta-converting enzyme family protease that activates cysteine protease P32 (CPP32). J Biol Chem 1996; 271(23):13371-6.
17. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, et al. Human ICE/CED-3 protease nomenclature. Cell 1996; 87(2):171.
18. Nicholson DW, Ali A, Thornberry NA, Vaillancourt JP, Ding CK, Gallant M, et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995; 376(6535):37-43.
19. Dixit VM. Role of ICE-proteases in apoptosis. Adv Exp Med Biol 1996; 406:113-7.
20. Hu Y, Ding L, Spencer DM, Nunez G. WD-40 repeat region regulates Apaf-1 self-association and procaspase-9 activation. J Biol Chem 1998; 273(50):33489-94.
21. HuY, Benedict MA, Ding L, Nunez G. Role of cytochrome c and dATP/ATP hydrolysis in Apaf-1-mediated caspase-9 activation and apoptosis. Embo J 1999; 18(13):3586-95.
22. Adrain C, Slee EA, Harte MT, Martin SJ. Regulation of apoptotic protease activating factor-1 oligomerization and apoptosis by the WD-40 repeat region. J Biol Chem 1999; 274(30):20855-60.
23. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, et al. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997; 91(4):479-89.
24. Qin H, Srinivasula SM, Wu G, Fernandes-Alnemri T, Alnemri ES, Shi Y. Structural basis of procaspase-9 recruitment by the apoptotic protease-activating factor 1. Nature 1999; 399(6736):549-57.
25. Saleh A, Srinivasula SM, Acharya S, Fishel R, Alnemri ES. Cytochrome c and dATP-mediated oligomerization of Apaf-1 is a prerequisite for procaspase-9 activation. J Biol Chem 1999; 274(25):17941-5.
26. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependert activation of caspase-3. Cell 1997; 90(3):405-13.
27. Zou H, Li Y, Liu X, Wang X. An APAF-1.cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J Biol Chem 1999; 274(17):11549-56.
28. Korsmeyer SJ. BCL-2 gene family and the regulation of programmed cell death. Cancer Res 1999; 59(7 Suppl): 1693s-1700s.
29. Oltvai ZN, Milliman CL, Korsmeyer SJ. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74(4):609-19.
30. Korsmeyer SJ, Shutter JR, Veis DJ, Merry DE, Oltvai ZN. Bcl-2/Bax: a rheostat that regulates an anti-oxidant pathway and cell death. Semin Cancer Biol 1993; 4(6):327-32.
31. Zha J, Harada H, Osipov K, Jockel J, Waksman G, Korsmeyer SJ. BH3 domain of BAD is required for heterodimerization with BCL-XL and pro-apoptotic activity. J Biol Chem 1997; 272(39):24101-4.
32. Chao DT, Linette GP, Boise LH, White LS, Thompson CB, Korsmeyer SJ. Bcl-XL and Bcl-2 repress a common pathway of cell death. J Exp Med 1995; 182(3):821-8.
33. Sedlak TW, Oltvai ZN, Yang E, Wang K, Boise LH, Thompson CB, et al. Multiple Bcl-2 family members demonstrate selective dimerizations with Bax. Proc Natl Acad Sci USA 1995; 92(17):7834-8.
34. Yang E, Zha J, Jockel J, Boise LH, Thompson CB, Korsmeyer SJ. Bad, a heterodimeric partner for Bel-XL and Bcl-2, displaces Bax and promotes cell death. Cell 1995; 80(2):285-91.
35. Talanian RV, Quinlan C, Trautz S, Hackett MC, Mankovich JA, Banach D, et al. Substrate specificities of caspase family proteases. J Biol Chem 1997; 272(15):9677-82.
36. Villa P, Kaufmann SH, Earnshaw WC. Caspases and caspase inhibitors. Trends Biochem Sci 1997; 22(10):388-93.
37. Wolf BB, Green DR. Suicidal tendencies: apoptotic cell death by caspase family proteinases. J Biol Chem 1999; 274(29):20049-52.
38. Stennicke HR, Salvesen GS. Biochemical characteristics of caspases-3, -6, -7, and -8. J Biol Chem 1997; 272(41): 25719-23.
39. Salvesen GS, Dixit VM. Caspases: intracellular signaling by proteolysis. Cell 1997; 91(4):443-6.
40. Muzio M, Stockwell BR, Stennicke HR, Salvesen GS, Dixit VM. An induced proximity model for caspase-8 activation. J Biol Chem 1998; 273(5):2926-30.
41. Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, Ni J, et al. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 1996; 85(6):817-27.
42. Chinnaiyan AM, Tepper CG, Seldin MF, O'Rourke K, Kischkel FC, Hellbardt S, et al. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J Biol Chem 1996; 271(9):4961-5.
43. Chinnaiyan AM, O'Rourke K, Tewari M, Dixit VM. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 1995; 81(4):505-12.
44. Grimm S, Stanger BZ, Leder P. RIP and FADD: two "death domain"-containing proteins can induce apoptosis by convergent, but dissociable, pathways. Proc Natl Acad Sci USA 1996; 93(20):10923-7.
45. Hsu H, Shu HB, Pan MG, Goeddel DV. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 1996; 84(2): 299-308.
46. Hsu H, Xiong J, Goeddel DV. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 1995; 81(4):495-504.
47. Boldin MP, Goncharov TM, Goltsev YV, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1-and TNF receptor-induced cell death. Cell 1996;85(6):803-15.
48. Liu X, Kim CN, Yang J, Jemmerson R, Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996; 86(1):147-57.
49. Bossy-Wetzel E, Newmeyer DD, Green DR. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. Embo J 1998; 17(1):37-49.
50. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, et al. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 1997; 275(5303): 1129-32.
51. Pan G, Humke EW, Dixit VM. Activation of caspases triggered by cytochrome c in vitro. FEBS Lett 1998; 426(1):151-4.
52. Skulachev VP. Cytochrome c in the apoptotic and antioxidant cascades. FEBS Lett 1998; 423(3):275-80.
53. Slee EA, Harte MT, Kluck RM, Wolf BB, Casiano CA, Newmeyer DD, et al. Ordering the cytochrome c-initiated caspase cascade: hierarchical activation of caspases-2, -3, -6, -7, -8, and -10 in a caspase-9-dependent manner. J Cell Biol 1999; 144(2):281-92.
54. Kluck RM, Bossy-Wetzel E, Green DR, Newmeyer DD. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 1997; 275(5303): 1132-6.
55. Kluck RM, Martin SJ, Hoffman BM, Zhou JS, Green DR, Newmeyer DD. Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. Embo J 1997; 16(15):4639-49.
56. Luo X, Budihardjo I, Zou H, Slaughter C, Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 1998; 94(4):481-90.
57. Li H, Zhu H, Xu CJ, Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 1998; 94(4):491-501.
58. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, et al. Bid-induced conformational change of Bax Is responsible for mitochondrial cytochrome c release during apoptosis. J Cell Biol 1999; 144(5):891-901.
59. von Ahsen O, Waterhouse N, Kuwana T, Newmeyer D, Green D. The harmless release of cytochrome c. Cell Death and Differentiation 2000; 7:1192-9.
60. Budd S, Tenneti L, Lishnak T, Lipton S. Mitochondrial and extramitochondrial apoptotic signaling pathways in cerebrocortical neurons. Proc Natl Acad Sci USA 2000; 97(11):6161-6.
61. Duckett CS, Li F, Wang Y, Tomaselli KJ, Thompson CB, Armstrong RC. Human IAP-like protein regulates programmed cell death downstream of Bcl-xL and cytochrome c. Mol Cell Biol 1998; 18(1):608-15.
62. Deveraux QL, Roy N, Stennicke HR, Van Arsdale T, Zhou Q, Srinivasula SM, et al. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. Embo J 1998; 17(8):2215-23.
63. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, et al. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 2000; 102(1):43-53.
64. Du C, Fang M, Li Y, Li L, Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000; 102(1):33-42.
65. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, et al. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 1996; 384(6607): 368-72.
66. Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P. Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 1998; 94(6):727-37.
67. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, et al. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 1998; 94(3):325-37.
68. Hakem R, Hakem A, Duncan GS, Henderson JT, Woo M, Soengas MS, et al. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 1998; 94(3):339-52.
69. Hara H, Friedlander RM, Gagliardini V, Ayata C, Fink K, Huang Z, et al. Inhibition of interleukin 1beta converting enzyme family proteases reduces ischemci and excitotoxic neuronal damage. Proc Natl Acad Sci USA 1997; 94(5):2007-12.
70. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, et al. Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 1995; 15(4):961-73.
71. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. 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 1995; 92(16):7162-6.
72. Nicotera P, Ankarcrona M, Bonfoco E, Orrenius S, Lipton SA. Neuronal necrosis and apoptosis: two distinct events induced by exposure to glutamate or oxidative stress. Adv Neurol 1997; 72:95-101.
73. Du Y, Bales KR, Dodel RC, Hamilton-Byrd E, Horn JW, Czilli DL, et al. Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultured cerebellar granule neurons. Proc Natl Acad Sci USA 1997; 94(21):11657-62.
74. Namura S, Zhu J, Fink K, Endres M, Srinivasan A, Tomaselli KJ, et al. Activation and cleavage of caspase-3 in apoptosis induced by experimental cerebral ischemia. J Neurosci 1998; 18(10):3659-68.
75. Endres M, Namura S, Shimizu-Sasamata M, Waeber C, Zhang L, Gomez-Isla T, et al. Attenuation of delayed neuronal death after mild focal ischemia in mice by inhibition of the caspase family. J Cereb Blood Flow Metab 1998; 18(3):238-47.
76. Endres M, Wang ZQ, Namura S, Waeber C, Moskowitz MA. Ischemic brain injury is mediated by the activation of poly(ADP-ribose)polymerase. J Cereb Blood Flow Metab 1997; 17(11):1143-51.
77. Ma J, Endres M, Moskowitz MA. Synergistic effects of caspase inhibitors and MK-801 in brain injury after transient focal cerebral ischaemia in mice. Br J Pharmacol 1998; 124(4):756-62.
78. Chen J, Nagayama T, Jin K, Stetler RA, Zhu RL, Graham SH, et al. Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J Neurosci 1998; 18(13):4914-28.
79. Ni B, Wu X, Su Y, Stephenson D, Smalstig EB, Clemens J, et al. Transient global forebrain ischemia induces a prolonged expression of the caspase-3 mRNA in rat hippocampal CA1 pyramidal neurons. J Cereb Blood Flow Metab 1998; 18(3):248-56.
80. Han BH, Holtzman DM. BDNF protects the neonatal brain from hypoxic-ischemic injury in vivo via the ERK pathway. J Neurosci 2000; 20(15):5775-81.
81. Han BH, D'Costa A, Back SA, Parsadanian M, Patel S, Shah AR, et al. BDNF blocks caspase-3 activation in neonatal hypoxia-ischemia. Neurobiol Dis 2000; 7(1):38-53.
82. Velier JJ, Ellison JA, Kikly KK, Spera PA, Barone FC, Feuerstein GZ. 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 1999; 19(14):5932-41.
83. Cheng Y, Deshmukh M, D'Costa A, Demaro JA, Gidday JM, Shah A, et al. Caspase inhibitor affords neuroprotection with delayed administration in a rat model of neonatal hypoxicischemic brain injury. J Clin Invest 1998; 101(9):1992-9.
84. Krajewski S, Krajewska M, Ellerby LM, Welsh K, Xie Z, Deveraux QL, et al. Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc Natl Acad Sci USA 1999; 96(10):5752-7.
85. Pulera MR, Adams LM, Liu H, Santos DG, Nishimura RN, Yang F, et al. Apoptosis in a neonatal rat model of cerebral hypoxia-ischemia [see comments]. Stroke 1998; 29(12):2622-30.
86. Gillardon F, Bottiger B, Schmitz B, Zimmermann M, Hossmann KA. Activation of CPP-32 protease in hippocampal neurons following ischemia and epilepsy. Brain Res Mol Brain Res 1997; 50(1-2):16-22.
87. Rink A, Fung KM, Trojanowski JQ, Lee VM, Neugebauer E, McIntosh TK. Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am J Pathol 1995; 147(6):1575-83.
88. Clark RS, Chen J, Watkins SC, Kochanek PM, Chen M, Stetler RA, et al. Apoptosis-suppressor gene bcl-2 expression after traumatic brain injury in rats. J Neurosci 1997; 17(23):9172-82.
89. Newcomb JK, Zhao X, Pike BR, Hayes RL. Temporal profile of apoptotic-like changes in neurons and astrocytes following controlled cortical impact injury in the rat. Exp Neurol 1999;158(1):76-88.
90. Yakovlev AG, Knoblach SM, Fan L, Fox GB, Goodnight R, Faden AI. Activation of CPP32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. J Neurosci 1997; 17(19):7415-24.
91. Zhang C, Raghupathi R, Saatman K, LaPlaca M, McIntosh T. Regional and temporal alterations in DNA fragmentation factor (DFF)-like proteins following experimental brain trauma in the rat. J Neurochemistry 1999; 73:1650-9.
92. Pike BR, Zhao X, Newcomb JK, Posmantur RM, Wang KK, Hayes RL. Regional calpain and caspase-3 proteolysis of alpha-spectrin after traumatic brain injury. Neuroreport 1998; 9(11):2437-42.
93. Posmantur RM, Zhao X, Kampfl A, Clifton GL, Hayes RL. Immunoblot analyses of the relative contributions of cysteine and aspartic proteases to neurofilament breakdown products following experimental brain injury in rats. Neurochem Res 1998; 23(10):1265-76.
94. Pike BR, Zhao X, Newcomb JK, Wang KK, Posmantur RM, Hayes RL. Temporal relationships between de novo protein synthesis, calpain and caspase 3-like protease activation, and DNA fragmentation during apoptosis in septohippocampal cultures. J Neurosci Res 1998; 52(5):505-20.
95. Clark RS, Kochanek PM, Chen M, Watkins SC, Marion DW, Chen J, et al. Increases in Bcl-2 and cleavage of caspase-1 and caspase-3 in human brain after head injury. Faseb J 1999; 13(8):813-21.
96. Emery E, Aldana P, Bunge MB, Puckett W, Srinivasan A, Keane RW, et al. Apoptosis after traumatic human spinal cord injury. J Neurosurg 1998; 89(6):911-20.
97. Lou J, Lenke LG, Ludwig FJ, O'Brien MF. Apoptosis as a mechanism of neuronal cell death following acute experimental spinal cord injury. Spinal Cord 1998; 36(10): 683-90.
98. Hayashi T, Sakurai M, Abe K, Sadahiro M, Tabayashi K, Iltoyama Y. Apoptosis of motor neurons with induction of caspases in the spinal cord after ischemia. Stroke 1998; 29(5):1007-12.
99. Shuman SL, Bresnahan JC, Beattie MS. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J Neurosci Res 1997; 50(5):798-808.
100. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, et al. Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 1997; 17(14):5395-406.
101. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 1997; 3(1):73-6.
102. Katoh K, Ikata T, Katoh S, Hamada Y, Nakauchi K, Sano T, et al. Induction and its spread of apoptosis in rat spinal cord after mechanical trauma. Neurosci Lett 1996; 216(1):9-12.
103. Li GL, Brodin G, Farooque M, Funa K, Holtz A, Wang WL, et al. Apoptosis and expression of Bcl-2 after compression trauma to rat spinal cord. J Neuropathol Exp Neurol 1996; 55(3):280-9.
104. Blight AR. Delayed demyelination and macrophage invasion: a candidate for secondary cell damage in spinal cord injury. Cent Nerv Syst Trauma 1985; 2(4):299-315.
105. Blight AR. Cellular morphology of chronic spinal cord injury in the cat: analysis of myelinated axons by line-sampling. Neuroscience 1983; 10(2):521-43.
106. Blight AR. Effect of 4-aminopyridine on axonal conduction-block in chronic spinal cord injury. Brain Res Bull 1989; 22(1):47-52.
107. Springer J, Azbill R, Knapp P. Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat Med 1999; 5(8):943-6.
108. Zipfel G, Babcock D, Lee J-M, Choi D. Neuronal apoptosis after CNS injury: the roles of glutamate and calcium. J. Neurotrauma 2000; 17(10):857-69.
109. Wang HG, Pathan N, Ethell IM, Krajewski S, Yamaguchi Y, Shibasaki F,. Ca2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 1999; 284(5412): 339-43.
110. Nunez G, del Peso L. Linking extracellular survival signals and the apoptotic machinery. Curr Opin Neurobiol 1998; 8(5):613-8.
111. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y, et al. Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 1997; 91(2): 231-41.
112. Brunei A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999; 96(6):857-68.
113. Kennedy SG, Kandel ES, Cross TK, Hay N. Akt/Protein kinase B inhibits cell death by preventing the release of cytochrome c from mitochondria. Mol Cell Biol 1999; 19(8):5800-10.
114. Scheid MP, Schubert KM, Duronio V. Regulation of bad phosphorylation and association with Bcl-x(L) by the MAPK/Erk kinase. J Biol Chem 1999; 274(43):31108-13.
115. Springer J, Azbill R, Nottingham S, Kennedy S. Calcineurin-mediated BAD dephosphorylation activates the caspase-3 apoptotic cascade in traumatic spinal cord injury. J. Neurosci. 2000; 20(19):7246-51.
116. Deshmukh M, Johnson EM, Jr. Evidence of a novel event during neuronal death: development of competence-to-die in response to cytoplasmic cytochrome c. Neuron 1998; 21(4):695-705.
117. Deshmukh M, Kuida K, Johnson EM, Jr. Caspase inhibition extends the commitment to neuronal death beyond cytochrome c release to the point of mitochondrial depolarization. J Cell Biol 2000; 150(1):131-43.
118. Mu X, Azbill RD, Springer JE. Riluzole improves measures of oxidative stress in traumatic spinal cord injury. Brain Research 2000; 870:66-72.
119. Azbill RD, Mu X, Bruce-Keller AJ, Mattson MP, Springer JE. Impaired mitochondrial function, oxidative stress and altered antioxidant enzyme activities following traumatic spinal cord injury. Brain Res 1997; 765(2):283-90.
120. Oliver CN, Starke-Reed PE, Stadtman ER, Liu GJ, Carney JM, Floyd RA. Oxidative damage to brain proteins, loss of glutamine synthetase activity, and production of free radicals during ischemia/reperfusion-induced injury to gerbil brain. Proc Natl Acad Sci USA 1990; 87(13):5144-7.
121. Halliwell B. Reactive oxygen species and the central nervous system. J Neurochem 1992; 59(5):1609-23.
122. Choi BH. Oxygen, antioxidants and brain dysfunction. Yonsei Med J 1993; 34(1):1-10.
123. Anderson D, Hall E. Pathophysiology of spinal cord trauma. Ann Emer Med 1993; 22(6):987-92.
124. Hall ED, Braughler JM. Free radicals in CNS injury. Res Publ Assoc Res Nerv Ment Dis 1993; 71:81-105.
125. Xiang H, Kinoshita Y, Knudson CM, Korsmeyer SJ, Schwartzkroin PA, Morrison RS. Bax involvement in p53-mediated neuronal cell death. J Neurosci 1998; 18(4): 1363-73.
126. Wood KA, Youle RJ, Bonfoco E. The role of free radicals and p53 in neuron apoptosis in vivo. J Neurosci 1995; 15(8):5851-7.
127. Raghupathi R, Graham Dl, McIntosh TK. Apoptosis after traumatic brain injury. J Neurotrauma 2000; 17(10):927-38.
128. Kaya SS, Mahmood A, Li Y, Yavuz E, Goksel M, Chopp M. Apoptosis and expression of p53 response proteins and cyclin D1 after cortical impact in rat brain. Brain Res 1999; 818(1):23-33.
129. Napieralski JA, Raghupathi R, McIntosh TK. The tumor-suppressor gene, p53, is induced in injured brain regions following experimental traumatic brain injury. Brain Res Mol Brain Res 1999;71(1):78-86.
130. Sakhi S, Bruce A, Sun N, Tocco G, Baudry M, Schreiber SS. p53 induction is associated with neuronal damage in the central nervous system. Proc Natl Acad Sci USA 1994; 91(16):7525-9.
131. Bredesen DE. Apoptosis: overview and signal transduction pathways. J Neurotrauma 2000; 17(10):801-10.
132. Eldadah BA, Faden AI. Caspase pathways, neuronal apoptosis, and CNS injury. J Neurotrauma 2000; 17(10): 811-29.
133. Graham SH, Chen J, Clark RS. Bcl-2 family gene products in cerebral ischemia and traumatic brain injury. J Neurotrauma 2000; 17(10):831-41.
134. Fiskum G. Mitochondrial participation in ischemic and traumatic neural cell death. J Neurotrauma 2000; 17(10): 843-55.
135. Lewen A, Matz P, Chan PH. Free radical pathways in CNS injury. J Neurotrauma 2000; 17(10):871-90.
136. Beattie MS, Farooqui AA, Bresnahan JC. Review of current evidence for apoptosis after spinal cord injury. J Neurotrauma 2000; 17(10):915-25.