Functional role and therapeutic implications of neuronal caspase-1 and -3 in a mouse model of traumatic spinal cord injury

Neuroscience

Volumn 99, Issue 2, 2000, Pages 333-342

  Li, M ^a   Ona, V O ^a   Chen, M ^a   Kaul, M ^a   Tenneti, L ^a   Zhang, X ^a   Stieg, P E ^a   Lipton, S A ^a   Friedlander, R M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Apoptosis; ICE; Interleukin 1 ; Neuroprotection; zVAD fmk

Indexed keywords

CASPASE 3; CASPASE INHIBITOR; DNA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; KETONE DERIVATIVE;

ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SPINAL CORD INJURY;

AMINO ACID CHLOROMETHYL KETONES; ANIMALS; APOPTOSIS; CASPASE 1; CASPASE 3; CASPASES; ENZYME ACTIVATION; IN SITU NICK-END LABELING; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; NEURONS; NEUROPROTECTIVE AGENTS; SPINAL CORD INJURIES;

EID: 0034638259     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00173-1     Document Type: Article

References (51)

1. Price C., Makintubee S., Herndon W., Istre G.R. Epidemiology of traumatic spinal cord injury and acute hospitalization and rehabilitation charges for spinal cord injuries in Oklahoma. 1988-1990. Am. J. Epidemiol. 139:1994;37-47.
2. Gerhart K.A. Spinal cord injury outcomes in a population-based sample. J. Trauma. 31:1991;1529-1535.
3. Amar A.P., Levy M.L. Pathogenesis and pharmacological strategies for mitigating secondary damage in acute spinal cord injury. Neurosurgery. 44:1999;1027-1039.
4. Crowe M.J., Bresnahan J.C., Shuman S.L., Masters J.N., Beattie M.S. Apoptosis and delayed degeneration after spinal cord injury in rats and monkeys. Nat. Med. 3:1997;73-76.
5. Lou J., Lenke L.G., Ludwig F.J., O'Brien M.F. Apoptosis as a mechanism of neuronal cell death following acute experimental spinal cord injury. Spinal Cord. 36:1998;683-690.
6. Braughler J.M., Hall E.D. Current application of "high-dose" steroid therapy for CNS injury. A pharmacological perspective. J. Neurosurg. 62:1985;806-810.
7. Yong C., Arnold P.M., Zoubine M.N., Citron B.A., Watanabe I., Berman N.E., Festoff B.W. Apoptosis in cellular compartments of rat spinal cord after severe contusion injury. J. Neurotrauma. 15:1998;459-472.
8. Liu X.Z., Xu X.M., Hu R., Du C., Zhang S.X., McDonald J.W., Dong H.X., Wu Y.J., Fan G.S., Jacquin M.F., Hsu C.Y., Choi D.W. Neuronal and glial apoptosis after traumatic spinal cord injury. J. Neurosci. 17:1997;5395-5406.
9. Emery E., Aldana P., Bunge M.B., Puckett W., Srinivasan A., Keane R.W., Bethea J., Levi A.D. Apoptosis after traumatic human spinal cord injury. J. Neurosurg. 89:1998;911-920.
10. Springer J.E., Azbill R.D., Knapp P.E. Activation of the caspase-3 apoptotic cascade in traumatic spinal cord injury. Nat. Med. 5:1999;943-946.
11. Miura M., Zhu H., Rotello R., Hartwieg E.A., Yuan J. Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell. 75:1993;653-660.
12. Friedlander R.M., Yuan J. ICE, neuronal apoptosis and neurodegeneration. Cell Death Differ. 5:1998;823-831.
13. Friedlander R.M., Brown R.H., Gagliardini V., Wang J., Yuan J. Inhibition of ICE slows ALS in mice. Nature. 388:1997;31.
14. Friedlander R.M., Gagliardini V., Hara H., Fink K.B., Li W., MacDonald G., Fishman M.C., Greenberg A.H., Moskowitz M.A., Yuan J. Expression of a dominant negative mutant of interleukin-1 beta converting enzyme in transgenic mice prevents neuronal cell death induced by trophic factor withdrawal and ischemic brain injury. J. exp. Med. 185:1997;933-940.
15. Hara H., Friedlander R.M., Gagliardini V., Ayata C., Fink K., Huang Z., Shimizu-Sasamata M., Yuan J., Moskowitz M.A. Inhibition of interleukin-1beta converting enzyme family proteases reduces ischemic and excitotoxic neuronal damage. Proc. natn. Acad. Sci. USA. 94:1997;2007-2012.
16. Ona V.O., Li M., Vonsattel J.P., Andrews L.J., Khan S.Q., Chung W.M., Frey A.S., Menon A.S., Li X.J., Stieg P.E., Yuan J., Penney J.B., Young A.B., Cha J.H., Friedlander R.M. Inhibition of caspase-1 slows disease progression in a mouse model of Huntington's disease. Nature. 399:1999;263-267.
17. Klevenyi P., Andreassen O., Ferrante R.J., Schleicher J.R. Jr., Friedlander R.M., Beal M.F. Transgenic mice expressing a dominant negative mutant interleukin-1beta converting enzyme show resistance to MPTP neurotoxicity. NeuroReport. 10:1999;635-638.
18. Hara H., Fink K., Endres M., Friedlander R.M., Gagliardini V., Yuan J., Moskowitz M.A. Attenuation of transient focal cerebral ischemic injury in transgenic mice expressing a mutant ICE inhibitory protein. J. cerebr. Blood Flow Metab. 17:1997;370-375.
19. Fink K.B., Andrews L.J., Butler W.E., Ona V.O., Li M., Bogdanov M., Endres M., Khan S.Q., Namura S., Stieg P.E., Beal M.F., Moskowitz M.A., Yuan J., Friedlander R.M. Reduction of post-traumatic brain injury and free radical production by inhibition of the caspase-1 cascade. Neuroscience. 94:1999;1213-1218.
20. 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.
21. 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.
22. Burne J.F., Staple J.K., Raff M.C. Glial cells are increased proportionally in transgenic optic nerves with increased numbers of axons. J. Neurosci. 16:1996;2064-2073.
23. Forss-Petter S., Danielson P.E., Catsicas S., Battenberg E., Price J., Nerenberg M., Sutcliffe J.G. Transgenic mice expressing beta-galactosidase in mature neurons under neuron-specific enolase promoter control. Neuron. 5:1990;187-197.
24. Kuhn P.L., Wrathall J.R. A mouse model of graded contusive spinal cord injury. J. Neurotrauma. 15:1998;125-140.
25. Sambrook J., Fritch E. F. and Maniatis T. (1989) Analysis and cloning of eukaryotic genomic DNA. In Molecular Clonning (eds Ford N., Nolan C. and Ferguson M.), pp. 9.16-9.19. Cold Spring Harbour Laboratory Press, New York.
26. Mattson M.P., Keller J.N., Begley J.G. Evidence for synaptic apoptosis. Expl Neurol. 153:1998;35-48.
27. 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.
28. Li P., Allen H., Banerjee S., Franklin S., Herzog L., Johnston C., McDowell J., Paskind M., Rodman L., Salfeld J. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell. 80:1995;401-411.
29. Kuida K., Lippke J.A., Ku G., Harding M.W., Livingston D.J., Su M.S., Flavell R.A. Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science. 267:1995;2000-2003.
30. Miura M., Friedlander R.M., Yuan J. Tumor necrosis factor-induced apoptosis is mediated by a CrmA-sensitive cell death pathway. Proc. natn. Acad. Sci. USA. 92:1995;8318-8322.
31. Thornberry N.A., Bull H.G., Calaycay J.R., Chapman K.T., Howard A.D., Kostura M.J., Miller D.K., Molineaux S.M., Weidner J.R., Aunins J. A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature. 356:1992;768-774.
32. Nicholson D.W. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ. 6:1999;1028-1042.
33. Garcia-Calvo M., Peterson E.P., Leiting B., Ruel R., Nicholson D.W., Thornberry N.A. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J. biol. Chem. 273:1998;32608-32613.
34. Mullen R.J., Buck C.R., Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development. 116:1992;201-211.
35. Mao P.L., Jiang Y., Wee B.Y., Porter A.G. Activation of caspase-1 in the nucleus requires nuclear translocation of pro-caspase-1 mediated by its prodomain. J. biol. Chem. 273:1998;23621-23624.
36. Shuman S.L., Bresnahan J.C., Beattie M.S. Apoptosis of microglia and oligodendrocytes after spinal cord contusion in rats. J. Neurosci. Res. 50:1997;798-808.
37. Lee T.T., Green B.A., Dietrich W.D., Yezierski R.P. Neuroprotective effects of basic fibroblast growth factor following spinal cord contusion injury in the rat. J. Neurotrauma. 16:1999;347-356.
38. McTigue D.M., Horner P.J., Stokes B.T., Gage F.H. Neurotrophin-3 and brain-derived neurotrophic factor induce oligodendrocyte proliferation and myelination of regenerating axons in the contused adult rat spinal cord. J. Neurosci. 18:1998;5354-5365.
39. Abe Y., Yamamoto T., Sugiyama Y., Watanabe T., Saito N., Kayama H., Kumagai T. Apoptotic cells associated with Wallerian degeneration after experimental spinal cord injury: a possible mechanism of oligodendroglial death. J. Neurotrauma. 16:1999;945-952.
40. Friedlander R.M., Gagliardini V., Rotello R.J., Yuan J. Functional role of interleukin 1 beta (IL-1 beta) in IL-1 beta-converting enzyme-mediated apoptosis. J. exp. Med. 184:1996;717-724.
41. 2+ and reactive oxygen species in staurosporine-induced neuronal apoptosis. J. Neurochem. 68:1997;1679-1685.
42. Troy C.M., Stefanis L., Prochiantz A., Greene L.A., Shelanski M.L. The contrasting roles of ICE family proteases and interleukin-1beta in apoptosis induced by trophic factor withdrawal and by copper/zinc superoxide dismutase down-regulation. Proc. natn. Acad. Sci. USA. 93:1996;5635-5640.
43. Diaz-Ruiz A., Rios C., Duarte I., Correa D., Guizar-Sahagun G., Grijalva I., Ibarra A. Cyclosporin-A inhibits lipid peroxidation after spinal cord injury in rats. Neurosci. Lett. 266:1999;61-64.
44. Endres M., Namura S., Shimizu-Sasamata 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. cerebr. Blood Flow Metab. 18:1998;238-247.
45. Dinarello C.A. Interleukin-1 beta, interleukin-18, and the interleukin-1 beta converting enzyme. Ann. N. Y. Acad. Sci. 856:1998;1-11.
46. Bracken M.B., Shepard M.J., Holford T.R., Leo-Summers L., Aldrich E.F., Fazl M., Fehlings M., Herr D.L., Hitchon P.W., Marshall L.F., Nockels R.P., Pascale V., Perot P.L. Jr., Piepmeier J., Sonntag V.K., Wagner F., Wilberger J.E., Winn H.R., Young W. Administration of methylprednisolone for 24 or 48 hours or tirilazad mesylate for 48 hours in the treatment of acute spinal cord injury. Results of the Third National Acute Spinal Cord Injury Randomized Controlled Trial. National Acute Spinal Cord Injury Study. J. Am. med. Ass. 277:1997;1597-1604.
47. Wamil A.W., Wamil B.D., Hellerqvist C.G. CM101-mediated recovery of walking ability in adult mice paralyzed by spinal cord injury. Proc. natn. Acad. Sci. USA. 95:1998;13188-13193.
48. Chen H.S., Lipton S.A. Mechanism of memantine block of NMDA-activated channels in rat retinal ganglion cells: uncompetitive antagonism. J. Physiol., Lond. 499:1997;27-46.
49. Chen H.S., Pellegrini J.W., Aggarwal S.K., Lei S.Z., Warach S., Jensen F.E., Lipton S.A. Open-channel block of N-methyl-D-aspartate (NMDA) responses by memantine: therapeutic advantage against NMDA receptor-mediated neurotoxicity. J. Neurosci. 12:1992;4427-4436.
50. Goldberg Y.P., Nicholson D.W., Rasper D.M., Kalchman M.A., Koide H.B., Graham R.K., Bromm M., Kazemi-Esfarjani P., Thornberry N.A., Vaillancourt J.P., Hayden M.R. Cleavage of huntingtin by apopain, a proapoptotic cysteine protease, is modulated by the polyglutamine tract. Nat. Genet. 13:1996;442-449.
51. Gervais F.G., Xu D., Robertson G.S., Vaillancourt J.P., Zhu Y., Huang J., LeBlanc A., Smith D., Rigby M., Shearman M.S., Clarke E.E., Zheng H., Van Der Ploeg L.H., Ruffolo S.C., Thornberry N.A., Xanthoudakis S., Zamboni R.J., Roy S., Nicholson D.W. Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation. Cell. 97:1999;395-406.