Selective caspase activation may contribute to neurological dysfunction after experimental spinal cord trauma

Journal of Neuroscience Research

Volumn 80, Issue 3, 2005, Pages 369-380

  Knoblach, S M ^a   Huang, X ^a   VanGelderen, J ^b   Calva Cerqueira, D ^b   Faden, A I ^a  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b GEORGETOWN UNIVERSITY   (United States)

Author keywords

Apoptosis; Caspase inhibitor; CNS injury

Indexed keywords

ANTIBODY; BENZYLOXYCARBONYLASPARTYLGLUTAMYLVALYLASPARTYL FLUOROMETHYL KETONE; BIOLOGICAL MARKER; CASPASE; CASPASE 2; CASPASE 3; CASPASE 3 INHIBITOR; CASPASE 6; CASPASE 8; CASPASE 9; CASPASE INHIBITOR; FLUORINE DERIVATIVE; INTERLEUKIN 1BETA CONVERTING ENZYME; KETONE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASTROCYTE; BRAIN CONTUSION; BRAIN DYSFUNCTION; CELL TYPE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME SUBUNIT; FLUOROMETRY; GRAY MATTER; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LOCOMOTION; MALE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; RAT; SPINAL CORD INJURY; TISSUE HOMOGENATE; WHITE MATTER;

ANIMALS; APOPTOSIS; BIOLOGICAL MARKERS; CASPASES; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; ENZYME INHIBITORS; IMMUNOHISTOCHEMISTRY; MALE; MOTOR ACTIVITY; MOVEMENT DISORDERS; NERVE DEGENERATION; NEURONS; OLIGODENDROGLIA; PROTEIN SUBUNITS; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD INJURIES; TIME FACTORS; TREATMENT OUTCOME;

EID: 20344392207     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20465     Document Type: Article

References (60)

1. Allen JW, Eldadah BA, Huang X, Knoblach SM, Faden AI. 2001. Multiple caspases are involved in beta-amyloid-induced neuronal apoptosis. J Neurosci Res 65:45-53.
2. Allsopp TE, McLuckie J, Kerr LE, Macleod M, Sharkey J, Kelly JS. 2000. Caspase 6 activity initiates caspase 3 activation in cerebellar granule cell apoptosis. Cell Death Differ 7:984-993.
3. Bakshi R, Newman AH, Faden AI. 1990. Dynorphin a-(1-17) induces alterations in free fatty acids, excitatory amino acids, and motor function through an opiate-receptor-mediated mechanism. J Neurosci 10:3793-3800.
4. Bao F, Liu D. 2003. Peroxynitrite generated in the rat spinal cord induces apoptotic cell death and activates caspase-3. Neuroscience 116:59-70.
5. Basso DM. 2004. Behavioral testing after spinal cord injury: congruities, complexities and controversies. J Neurotrauma 21:395-404.
6. Basso DM, Beattie MS, Bresnahan JC. 1995. A sensitive and reliable locomotor rating scale for open field testing in rats. J Neurotrauma 12:1-21.
7. Basso DM, Beattie MS, Bresnahan JC. 1996. Graded histological and locomotor outcomes after spinal cord contusion using the NYU weight-drop device versus transection. Exp Neurol 139:244-256.
8. Beattie MS, Farooqui AA, Bresnahan JC. 2000. Review of current evidence for apoptosis after spinal cord injury. J Neurotrauma 17:915-925.
9. Benchoua A, Guegan C, Couriaud C, Hosseini H, Sampaio N, Morin D, Onteniente B. 2001. Specific caspase pathways are activated in the two stages of cerebral infarction. J Neurosci 21:7127-7134.
10. Blight AR. 1993. Remyelination, revascularization, and recovery of function in experimental spinal cord injury. Adv Neurol 59:91-104.
11. Blight AR, Decrescito V. 1986. Morphometric analysis of experimental spinal cord injury in the cat: the relation of injury intensity to survival of myelinated axons. Neuroscience 19:321-341.
12. Blomgren K, Zhu C, Wang X, Karlsson JO, Leverin AL, Bahr BA, Mallard C, Hagberg H. 2001. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis"? J Biol Chem 276:10191-10198.
13. Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254.
14. Casha S, Yu WR, Fehlings MG. 2001. Oligodendroglial apoptosis occurs along degenerating axons and is associated with fas and p75 expression following spinal cord injury in the rat. Neuroscience 103:203-218.
15. Chan SL, Mattson MP. 1999. Caspase and calpain substrates: roles in synaptic plasticity and cell death. J Neurosci Res 58:167-190.
16. Citron BA, Arnold PM, Sebastian C, Qin F, Malladi S, Ameenuddin S, Landis ME, Festoff BW. 2000. Rapid upregulation of caspase-3 in rat spinal cord after injury: mRNA, protein, and cellular localization correlates with apoptotic cell death. Exp Neurol 166:213-226.
17. Clark RS, Kochanek PM, Watkins SC, Chen M, Dixon CE, Seidberg NA, Melick J, Loeffert JE, Nathaniel PD, Jin KL, Graham SH. 2000. Caspase-3 mediated neuronal death after traumatic brain injury in rats. J Neurochem 74:740-753.
18. Crowe MJ, Bresnahan JC, Shuman SL, Masters JN, Beattie MS. 1997. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat Med 3:73-76.
19. D'Souza SD, Bonetti B, Balasingam V, Cashman NR, Barker PA, Troutt AB, Raine CS, Antel JP. 1996. Multiple sclerosis: Fas signaling in oligodendrocyte cell death. J Exp Med 184:2361-2370.
20. Emery E, Aldana P, Bunge MB, Puckett W, Srinivasan A, Keane RW, Bethea J, Levi AD. 1998. Apoptosis after traumatic human spinal cord injury. J Neurosurg 89:911-920.
21. Faden AI, Molineaux CJ, Rosenberger JG, Jacobs TP, Cox BM. 1985. Endogenous opioid immunoreactivity in rat spinal cord following traumatic injury. Ann Neurol 17:386-390.
22. Harrison DC, Davis RP, Bond BC, Campbell CA, James MF, Parsons AA, Philpott KL. 2001. Caspase mRNA expression in a rat model of focal cerebral ischemia. Brain Res Mol Brain Res 89:133-146.
23. Hayashi T, Sakurai M, Abe K, Sadahiro M, Tabayashi K, Itoyama Y. 1998. Apoptosis of motor neurons with induction of caspases in the spinal cord after ischemia. Stroke 29:1007-1012, discussion 1013.
24. Keane RW, Kraydieh S, Lotocki G, Bethea JR, Krajewski S, Reed JC, Dietrich WD. 2001. Apoptotic and anti-apoptotic mechanisms following spinal cord injury. J Neuropathol Exp Neurol 60:422-429.
25. Kingham PJ, Pocock JM. 2001. Microglial secreted cathepsin B induces neuronal apoptosis. J Neurochem 76:1475-1484.
26. Knoblach SM, Nikolaeva M, Huang X, Fan L, Krajewski S, Reed JC, Faden AI. 2002. Multiple caspases are activated after traumatic brain injury: evidence for involvement in functional outcome. J Neurotrauma 19:1155-1170.
27. Knoblach SM, Alroy DA, Nikolaeva M, Cernak I, Stoica BA, Faden AI. 2004. Caspase 3 inhibitor z-DEVD-fmk attenuates calpain and necrotic cell death in vitro and after traumatic brain injury. J Cereb Blood Flow Metab 24:1119-1132.
28. Krajewski S, Krajewska M, Ellerby LM, Welsh K, Xie Z, Deveraux QL, Salvesen GS, Bredesen DE, Rosenthal RE, Fiskum G, Reed JC. 1999. Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc Natl Acad Sci U S A 96:5752-5757.
29. Li GL, Farooque M, Holtz A, Olsson Y. 1999. Apoptosis of oligodendrocytes occurs for long distances away from the primary injury after compression trauma to rat spinal cord. Acta Neuropathol 98:473-480.
30. Li M, Ona VO, Chen M, Kaul M, Tenneti L, Zhang X, Stieg PE, Lipton SA, Friedlander RM. 2000a. Functional role and therapeutic implications of neuronal caspase-1 and -3 in a mouse model of traumatic spinal cord injury. Neuroscience 99:333-342.
31. Li X, Oudega M, Dancausse HA, Levi AD. 2000b. The effect of methyl-prednisolone on caspase-3 activation after rat spinal cord transection. Restor Neurol Neurosci 17:203-209.
32. Liao J, Xu X, Wargovich MJ. 2000. Direct reprobing with anti-beta-actin antibody as an internal control for western blotting analysis. Biotechniques 28:216-218.
33. Liu XZ, Xu XM, Hu R, Du C, Zhang SX, McDonald JW, Dong HX, Wu YJ, Fan GS, Jacquin MF, Hsu CY, Choi DW. 1997. Neuronal and glial apoptosis after traumatic spinal cord injury. J Neurosci 17:5395-5406.
34. Lopez-Hernandez FJ, Ortiz MA, Bayon Y, Piedrafita FJ. 2003. Z-FA-fmk inhibits effector caspases but not initiator caspases 8 and 10, and demonstrates that novel anticancer retinoid-related molecules induce apoptosis via the intrinsic pathway. Mol Cancer Ther 2:255-263.
35. McLaughlin B. 2004. The kinder side of killer proteases: caspase activation contributes to neuroprotection and CNS remodeling. In press.
36. Nesic O, Xu GY, McAdoo D, High KW, Hulsebosch C, Perez-Pol R. 2001. II-1 receptor antagonist prevents apoptosis and caspase-3 activation after spinal cord injury. J Neurotrauma 18:947-956.
37. Niquet J, Baldwin RA, Allen SG, Fujikawa DG, Wasterlain CG. 2003. Hypoxic neuronal necrosis: protein synthesis-independent activation of a cell death program. Proc Natl Acad Sci U S A 100:2825-2830.
38. Nottingham SA, Springer JE. 2003. Temporal and spatial distribution of activated caspase-3 after subdural kainic acid infusions in rat spinal cord. J Comp Neurol 464:463-471.
39. Nottingham S, Knapp P, Springer J. 2002. Fk506 treatment inhibits caspase-3 activation and promotes oligodendroglial survival following traumatic spinal cord injury. Exp Neurol 177:242-251.
40. O'Dell D, Raghupathi R, Crino P, Eberwine J, McIntosh T. 2000. Traumatic brain injury alters the molecular fingerprint of tunel-positive cortical neurons in vivo: a single-cell analysis. J Neurosci 20:4821-4828.
41. Ozawa H, Keane RW, Marcillo AE, Diaz PH, Dietrich WD. 2002. Therapeutic strategies targeting caspase inhibition following spinal cord injury in rats. Exp Neurol 177:306-313.
42. Schwab BL, Guerini D, Didszun C, Bano D, Ferrando-May E, Fava E, Tam J, Xu D, Xanthoudakis S, Nicholson DW, Carafoli E, Nicotera P. 2002. Cleavage of plasma membrane calcium pumps by caspases: a link between apoptosis and necrosis. Cell Death Differ 9:818-831.
43. Shuman SL, Bresnahan JC, Beattie MS. 1997. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J Neurosci Res 50:798-808.
44. Siegal S, Castellan NJ. 1998. Nonparametric statistics for the behavioral sciences, 2nd ed. New York: McGraw-Hill.
45. Springer JE, Azbill RD, Knapp PE. 1999. Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat Med 5:943-946.
46. Sugawara T, Lewen A, Gasche Y, Yu F, Chan PH. 2002. Overexpression of sod1 protects vulnerable motor neurons after spinal cord injury by attenuating mitochondrial cytochrome c release. FASEB J 16:1997-1999.
47. Sullivan PG, Keller JN, Bussen WL, Scheff SW. 2002. Cytochrome c release and caspase activation after traumatic brain injury. Brain Res 949:88-96.
48. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M, Kroemer G. 1996. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J Exp Med 184:1331-1341.
49. Tarlov IM, Klinger H. 1954. Spinal cord compression studies. II. Time limits for recovery after acute compression in dogs. AMA Arch Neurol Psychiatry 71:271-290.
50. Thornberry NA, Lazebnik Y. 1998. Caspases: enemies within. Science 281:1312-1316.
51. Thornberry NA, Rano TA, Peterson EP, Rasper DM, Timkey T, Garcia-Calvo M, Houtzager VM, Nordstrom PA, Roy S, Vaillancourt JP, Chapman KT, Nicholson DW. 1997. A combinatorial approach defines specificities of members of the caspase family and granzyme b. Functional relationships established for key mediators of apoptosis. J Biol Chem 272:17907-17911.
52. Troy CM, Rabacchi SA, Friedman WJ, Frappier TF, Brown K, Shelanski ML. 2000. Caspase-2 mediates neuronal cell death induced by beta-amyloid. J Neurosci 20:1386-1392.
53. Troy CM, Rabacchi SA, Hohl JB, Angelastro JM, Greene LA, Shelanski ML. 2001. Death in the balance: alternative participation of the caspase-2 and -9 pathways in neuronal death induced by nerve growth factor deprivation. J Neurosci 21:5007-5016.
54. Vancompernolle K, Van Herreweghe F, Pynaert G, Van de Craen M, De Vos K, Totty N, Sterling A, Fiers W, Vandenabeele P, Grooten J. 1998. Atractyloside-induced release of cathepsin b, a protease with caspase-processing activity. FEBS Lett 438:150-158.
55. Velier JJ, Ellison JA, Kikly KK, Spera PA, Barone FC, Feuerstein GZ. 1999. 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 19:5932-5941.
56. Wang CX, Olschowka JA, Wrathall JR. 1997. Increase of interleukin-1beta mRNA and protein in the spinal cord following experimental traumatic injury in the rat. Brain Res 759:190-196.
57. Wolf BB, Goldstein JC, Stennicke HR, Beere H, Amarante-Mendes GP, Salvesen GS, Green DR. 1999. Calpain functions in a caspase-independent manner to promote apoptosis-like events during platelet activation. Blood 94:1683-1692.
58. Wu KL, Chan SH, Chao YM, Chan JY. 2003. Expression of pro-inflammatory cytokine and caspase genes promotes neuronal apoptosis in pontine reticular formation after spinal cord transection. Neurobiol Dis 14:19-31.
59. Yakovlev AG, Knoblach SM, Fan L, Fox GB, Goodnight R, Faden AI. 1997. Activation of cpp32-like caspases contributes to neuronal apoptosis and neurological dysfunction after traumatic brain injury. J Neurosci 17:7415-7424.
60. Yong C, Arnold PM, Zoubine MN, Citron BA, Watanabe I, Berman NE, Festoff BW. 1998. Apoptosis in cellular compartments of rat spinal cord after severe contusion injury. J Neurotrauma 15:459-472.