E-64-d prevents both calpain upregulation and apoptosis in the lesion and penumbra following spinal cord injury in rats

Brain Research

Volumn 867, Issue 1-2, 2000, Pages 80-89

  Ray, Swapan K ^a   Matzelle, Denise C ^a   Wilford, Gloria G ^a   Hogan, Edward L ^a   Banik, Naren L ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

68 kD Neurofilament protein; Apoptosis; Bax bcl 2; Calpain calpastatin; E 64 d; Spinal cord injury

Indexed keywords

ALOXISTATIN; CALPAIN; CALPASTATIN; DNA FRAGMENT; MESSENGER RNA; NEUROFILAMENT PROTEIN; PROTEIN BAX; PROTEIN BCL 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; FEMALE; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD INJURY;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CALCIUM-BINDING PROTEINS; CALPAIN; CYSTEINE PROTEINASE INHIBITORS; DNA FRAGMENTATION; DNA PRIMERS; FEMALE; GENE EXPRESSION; LEUCINE; NEUROFILAMENT PROTEINS; NUCLEOSOMES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SPINAL CORD INJURIES;

EID: 0034625693     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(00)02260-5     Document Type: Article

References (70)

1. Allen A.R. Surgery of experimental lesion of spinal cord equivalent to crush injury of fracture dislocation of spinal column: a preliminary report. J. Am. Med. Assoc. 57:1911;878-880.
2. Anderson D.K., Hall E.D. Pathophysiology of spinal cord trauma. Ann. Emerg. Med. 22:1993;987-992.
3. Balentine J.D. Pathology of experimental spinal cord trauma. Part I. The necrotic lesion as a function of vascular injury. Lab. Invest. 39:1978;236-253.
4. Balentine J.D., Hogan E.L., Banik N.L., Perot P.L. Calcium and the pathogenesis of spinal cord injury. Dacey R.G., Winn H.R., Rimel R.W., Jane J.A. Trauma of the Central Nervous System. 1985;285-295 Raven Press, New York.
5. Banik N., Hogan E., Hsu E. The multimolecular cascade of spinal cord injury. Neurochem. Pathol. 7:1987;57-77.
6. Banik N.L., Matzelle D.L., Gantt-Wilford G., Osborne A., Hogan E.L. Increased calpain content and progressive degradation of neurofilament protein in spinal cord injury. Brain Res. 752:1997;301-306.
7. Banik N.L., Ray S.K., Matzelle D.L., Wilford G.G., Hogan E.L. Loxastatin (E-64-d) inhibits calpain upregulation and provides neuroprotection from internucleosomal DNA fragmentation in rat SCI (Abstract). J. Neurochem. 74 Suppl. 2000;S11.
8. Bartus R., Baker K.L., Keiser A.D., Sawyer S.D., Dean R.L., Elliott P.J., Straub J.A. Postischemic administration of AK295, a calpain inhibitor, provides substantial protection against focal ischemic brain damage. J. Cereb. Blood Flow Metab. 14:1994;537-544.
9. 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 post occlusion intra-arterial administration. Stroke. 25:1994;2265-2270.
10. Brorson J.R., Marcucilli C.J., Miller R.J. Delayed antagonism of calpain reduces excitotoxicity in cultured neurons. Stroke. 26:1995;1259-1267.
11. Cohen G.M. Caspases: the executioners of apoptosis. Biochem. J. 326:1997;1-16.
12. 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.
13. DeLuca C.I., Davies P.L., Samis J.A., Elce J. Molecular cloning and bacterial expression of cDNA for rat calpain II 80-kD subunit. Biochim. Biophys. Acta. 1216:1993;81-93.
14. Ducker T.B., Kindt G.W., Kempe L.G. Pathological findings in acute experimental spinal cord trauma. J. Neurosurg. 35:1971;700-708.
15. Ellis R.E., Yuan J., Horvitz H.R. Mechanisms and functions of cell death. Annu. Rev. Cell. Biol. 7:1991;663-698.
16. 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.
17. Emori Y., Kawasaki H., Imajoh S., Imahori K., Suzuki K. Endogenous inhibitor for calcium-dependent cysteine protease contains four internal repeats that could be responsible for its multiple reactive sites. Proc. Natl. Acad. Sci. USA. 84:1987;3590-3594.
18. 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-1β-converting enzyme. J. Biol. Chem. 269:1994;30761-30764.
19. 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.
20. Greenwood J.A., Troncoso J.C., Costello A.C., Johnson G.V. Phosphorylation modulates calpain-mediated proteolysis and calmodulin binding of the 200-kDa and 160-kDa neurofilament proteins. J. Neurochem. 61:1993;191-199.
21. Gruner J.A. A monitored contusion model of spinal cord injury in the rat. J. Neurotrauma. 9:1992;123-128.
22. 2+-accumulation in experimental spinal cord trauma. Brain Res. 211:1981;476-479.
23. Han J., Sabbatini P., Perez D., Rao L., Modha D., White E. The E1b 19K protein blocks apoptosis by interacting with and inhibiting the p53-inducible and death-promoting Bax protein. Genes Dev. 10:1996;461-477.
24. Ishida S., Emori Y., Suzuki K. Rat calpastatin has diverged primary sequence from other mammalian calpastatins but retains functionally important sequences. Biochim. Biophys. Acta. 1088:1991;436-438.
25. Jacobsen M.D., Weil M., Raff M.C. Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death. J. Cell Biol. 133:1996;1041-1051.
26. James T., Matzelle D., Bartus R., Hogan E.L., Banik N.L. New inhibitors of calpain prevent degradation of cytoskeletal and myelin proteins in spinal cord in vitro. J. Neurosci. Res. 51:1998;218-222.
27. Johnson G.V., Greenwood J.A., Costello A.C., Troncoso J.C. The regulatory role of calmodulin in the proteolysis of individual neurofilament proteins by calpain. Neurochem. Res. 16:1991;869-873.
28. Jordan J., Galindo M.F., Miller R.J. Role of calpain- and interleukin-1β converting enzyme-like proteases in the β-amyloid-induced death of rat hippocampal neurons in culture. J. Neurochem. 68:1997;1612-1621.
29. Kampfl A., Posmantur R., Nixon R., Grynspan F., Zhao X., Lin S.J., Newcomb J.K., Clifton G.L., Hayes R.L. μCalpain activation and calpain-mediated cytoskeletal proteolysis following traumatic brain injury. J. Neurochem. 67:1996;1575-1583.
30. Korsmeyer S.J. Bcl-2 initiates a new category of oncogenes: Regulators of cell death. Blood. 80:1992;879-886.
31. Kroemer G. The proto-oncogene bcl-2 and its role in regulating apoptosis. Nat. Med. 3:1997;614-620.
32. Li G.L., Brodin G., Farooque M., Funa K., Holtz A., Wang W.L., Olsson Y. Apoptosis and expression of Bcl-2 after compression trauma to rat spinal cord. J. Neuropathol. Exp. Neurol. 55:1996;280-289.
33. 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.
34. 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.
35. Martin S.J., O'Brien G.A., Nishioka W.K., McGahon A.J., Mahboubi A., Saido T.C., Green D.R. Proteolysis of fodrin (non-erythroid spectrin) during apoptosis. J. Biol. Chem. 270:1995;6425-6428.
36. Merry D.E., Korsmeyer S.J. Bcl-2 gene family in the nervous system. Annu. Rev. Neurosci. 20:1997;245-267.
37. Miura M., Zhu H., Rotello R., Hartwieg E.A., Yuan J. Induction of apoptosis in fibroblasts by IL-1β-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell. 75:1993;653-660.
38. Mu X., He J., Anderson D.W., Trojanowski J.Q., Springer J.E. Altered expression of bcl-2 and bax mRNA in amyotrophic lateral sclerosis spinal cord motor neurons. Ann. Neurol. 40:1996;379-386.
39. Nath R., Raser K.J., McGinnis K., Nadimpalli R., Stafford D., Wang K.K. Effects of ICE-like protease and calpain inhibitors on neuronal apoptosis. Neuroreport. 8:1996;249-255.
40. 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., Munday N.A., Raju S.M., Smulson M.E., Yamin T., Yu V.L., Miller D.K. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature. 376:1995;37-43.
41. Oltvai Z.N., Milliman C.L., Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog. Bax, that accelerates programmed cell death. Cell. 74:1993;609-619.
42. Pant H.C. Dephosphorylation of neurofilament proteins enhances their susceptibility to degradation by calpain. Biochem. J. 256:1988;665-668.
43. Pontremoli S., Melloni E., Viotti P.L., Michetti M., Salamino F., Horecker B.L. Identification of two calpastatin forms in rat skeletal muscle and their susceptibility to digestion by homologous calpains. Arch. Biochem. Biophys. 288:1991;646-652.
44. Pontremoli S., Salamino F., Sparatore B., De Tullio R., Pontremoli R., Melloni E. Characterization of the calpastatin defect in erythrocytes from patients with essential hypertension. Biochem. Biophys. Res. Commun. 157:1988;867-874.
45. Raabe T.D., Nguyen T., Archer C., Bittner G.D. Mechanisms for the maintenance and eventual degradation of neurofilament proteins in the distal segments of severed goldfish mauthner axons. J. Neurosci. 16:1996;1605-1613.
46. Raff T., van der Giet M., Endemann D., Wiederholt T., Paul M. Design and testing of β-actin primers for RT-PCR that do not co-amplify processed pseudogenes. BioTechniques. 23:1997;456-460.
47. Ray S., Davis D., Shields D., Matzelle D., Wilford G., Hogan E.L., Banik N.L. Increased calpain expression, cell death, and neuroprotection in rat spinal cord injury. J. Neurochem. 70:1998;S63.
48. 2+ influx upregulate calpain and induce apoptosis in PC12 cells. Brain Res. 852:2000;326-334.
49. Ray S., Ponnathpur V., Huang Y., Tang C., Mahoney M., Ibrado A., Bullock G., Bhalla K. 1-β-D-Arabinofuranosylcytosine-, mitoxantrone-, paclitaxel-induced apoptosis in HL-60 cells: improved method for detection of inernucleosomal DNA fragmentation. Cancer Chemother. Pharmacol. 34:1994;365-371.
50. Ray S.K., Shields D.C., Saido T.C., Matzelle D.C., Wilford G.G., Hogan E.L., Banik N.L. Calpain activity and translational expression increased in spinal cord injury. Brain Res. 816:1999;375-380.
51. 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.
52. Ray S.K., Wilford G.G., Matzelle D.D., Hogan E.L., Banik N.L. Calpeptin and methylprednisolone inhibit apoptosis in rat spinal cord injury. Ann. N.Y. Acad. Sci. 890:1999;261-269.
53. Reed J.C. Bcl-2 and regulation of programmed cell death. J. Cell Biol. 124:1994;1-6.
54. Saatman K.E., Murai H., Bartus R.T., Smith D.H., Hayward N.J., Perri B.R., McIntosh T.K. Calpain inhibitor AK295 attenuates motor and cognitive deficits following experimental brain injury in the rat. Proc. Natl. Acad. Sci. USA. 93:1996;3428-3433.
55. 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. 268:1993;25239-25243.
56. Sakurai M., Hayashi T., Abe K., Sadahiro M., Tabayashi K. Delayed selective motor neuron death and Fas antigen induction after spinal cord ischemia in rabbits. Brain Res. 797:1998;23-28.
57. Sato T., Irie S., Krajewski S., Reed J.C. Cloning and sequencing of a cDNA encoding the rat Bcl-2 protein. Gene. 140:1994;291-292.
58. Shearer T.R., Throneburg D.B., Shih M. In vitro precipitation of rat lens crystallins by calpain I-A calpain requiring low amounts of calcium for activation. Opththalmic Res. 28:1996;109-114.
59. Springer J.E., Azbill R.D., Kennedy S.E., George J., Geddes J.W. Rapid calpain I activation and cytoskeletal protein degradation following traumatic spinal cord injury-attenuation with riluzole pretreatment. J. Neurochem. 69:1997;1592-1600.
60. 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.
61. Squier M.K.T., Cohen J.J. Calpain and cell death. Cell Death Differen. 3:1996;275-283.
62. Squier M.K.T., Miller A.C., Malkinson A.M., Cohen J.J. Calpain activation in apoptosis. J. Cell Physiol. 159:1994;229-237.
63. Stokes B.T., Fox P., Hollinden G. Extracellular calcium activity in the injured spinal cord. Exp. Neurol. 80:1983;561-572.
64. Suzuki K., Imajoh S., Emori Y., Kawasaki H., Minami Y., Ohno S. Calcium-activated neutral protease and its endogenous inhibitor. Activation at the cell membrane and biological function. FEBS Lett. 220:1987;271-277.
65. Tamai M., Matsumoto K., Omura S., Koyama I., Ozawa Y., Hanada K. In vitro and in vivo inhibition of cysteine proteinases by EST, a new analog of E-64. J. Pharmacobio-Dyn. 9:1986;672-677.
66. Tator C.H., Fehlings M.G. Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanism. J. Neurosurg. 75:1991;15-26.
67. White R.J. Pathology of spinal cord injury in experimental lesions. Clin. Orthop. 112:1975;16-26.
68. Williams G.T., Smith C.A., McCarthy N.J., Grimes E.A. Apoptosis. Final control point in cell biology. Trends Cell Biol. 2:1992;263-267.
69. Young W. Secondary injury mechanisms in acute spinal cord injury. J. Emerg. Med. 11:1993;13-22.
70. Zhivotovsky B., Burgess D.H., Vanags D.M., Orrenius S. Involvement of cellular proteolytic machinery in apoptosis. Biochem. Biophys. Res. Commun. 230:1997;481-488.