BCL-2 overexpression attenuates cortical cell loss after traumatic brain injury in transgenic mice

Journal of Cerebral Blood Flow and Metabolism

Volumn 18, Issue 11, 1998, Pages 1259-1269

  Raghupathi, Ramesh ^a   Fernandez, Seamus C ^a   Murai, Hisayuki ^a   Trusko, Stephen P ^b   Scott, Richard W ^b   Nishioka, Walter K ^c   McIntosh, Tracy K ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CEPHALON INC   (United States)

^c Vical   (United States)

Author keywords

BCL 2; Behavior; Cell death; Neuroprotection; Transgenic mice; Traumatic brain injury

Indexed keywords

PROTEIN BCL 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CELL; BRAIN CONTUSION; BRAIN INJURY; CELL LOSS; CONTROLLED STUDY; GENE OVEREXPRESSION; HIPPOCAMPUS; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTO ONCOGENE; REGULATOR GENE; TRANSGENIC MOUSE;

EID: 0031770663     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1097/00004647-199811000-00013     Document Type: Article

References (64)

1. Adams JH, Doyle D, Graham DI, Lawrence AE, McLellan DR, Gennarelli TA, Pastuszko M, Sakamoto T (1985) The contusion index: a reappraisal in human and experimental non-missile injury. Neuropathol Appl Neurobiol 11:299-308
2. Allsopp TE, Kiselev S, Wyatt S, Davies AM (1995) Role of Bcl-2 in the brain-derived neurotrophic factor survival response. Eur J Neurosci 7:1266-1272
3. 3 subfield of the hippocampus following cortical contusion utilizing the optical dissector method for cell counting. J Neurotrauma 14:385-398
4. Bredesen DE (1995) Neural apoptosis. Ann Neurol 38:839-851
5. Chan PH, Epstein CJ, Li Y, Huang TT, Carlson E, Kinouchi H, Yang G, Kamii H, Mikawa S, Kondo T, Copin J-C, Chen SF, Chan T, Gafni J, Gobbel G, Reola E (1995) Transgenic mice and knockout mutants in the study of oxidative stress in brain injury. J Neurotrauma 12:815-824
6. Chen J, Graham SH, Chan PH, Lan P, Zhou RL, Simon RP (1995) Bcl-2 is expressed in neurons that survive focal ischemia in the rat. Neuroreport 6:394-398
7. Clark RSB, Chen J, Watkins SC, Kochanek PM, Chen M, Stetler RA, Loeffert JE, Graham SH (1997) Apoptosis-suppressor gene Bcl-2 expression after traumatic brain injury in rats. J Neurosci 17:9172-9182
8. Colicos MA, Dash PK (1996) Apoptotic morphology of dentate gyrus granule cells following experimental cortical impact injury in rats: possible role in memory deficits. Brain Res 739:120-131
9. Colicos MA, Dixon CE, Dash PK (1996) Delayed, selective neuronal death following experimental cortical impact injury in rats: possible role in memory deficits. Brain Res 739:111-119
10. Conti AC, Raghupath R, Trojanowski J, McIntosh TK (1998) Experimental brain injury induces regionally distinct apoptosis during the acute and delayed post-traumatic period. J Neurosci 18:5663-5672
11. Davies AM (1995) The Bcl-2 family of proteins, and the regulation of the neuronal survival. Trends Neurosci 18:355-358
12. de BilBao F, Dubois-Dauphin M (1996) Time course of axotomy-induced apoptotic cell death in facial motoneurons of neonatal wild type and bcl-2 transgenic mice. Neuroscience 71:1111-1119
13. Dietrich WD, Alonso O, Halley M (1994) Early microvascular and neuronal consequences of traumatic brain injury: a light and electron microscopic study in rats. J Neurotrauma 11:289-301
14. Dixon CE, Clifton GL, Lighthall JW, Yaghmai AA, Hayes RL (1991) A controlled cortical impact model of traumatic brain injury in the rat. J Neurosci Meth 39:253-262
15. Farlie PG, Dringen R, Rees SM, Kannourakis G, Bernard O (1995) Bcl-2 transgene expression can protect neurons against developmental and induced cell death. Proc Natl Acad Sci USA 92:4397-4401
16. 45Ca autoradiographic study. Brain Res 624:94-102
17. Franklin KBJ, Paxinos G (1996) The Mouse Brain in Stereotaxic Coordinates, San Diego, Academic Press
18. Garcia I, Martinou I, Tsujimoto Y, Martinou J-C (1992) Prevention of programmed cell death of sympathetic neurons by the bcl-2 protooncogene. Science 258:302-304
19. Gennarelli TA (1997) The pathobiology of traumatic brain injury. Neuroscientist 3:73-81
20. Gillardon F, Lenz C, Waschke KF, Krajewski S, Reed JC, Zimmermann M, Kuschinsky W (1996) 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 40:254-260
21. Greenlund LJS, Korsmeyer SJ, Johnson EM Jr (1995) Role of Bcl-2 in the survival and function of developing and mature sympathetic neurons. Neuron 15:649-661
22. Grosche J, Hartig W, Reichenbach A (1995) Expression of glial fibrillary acidic protein (GFAP), glutamine synthetase (GS), and Bcl-2 protooncogene protein by Muller (glial) cells in retinal light damage of rats. Neurosci Lett 185:119-122
23. Grubbs FE, Beck G (1972) Extension of sample sizes and percentage points for significance tests for outlying observations. Technometrics 14:847-854
24. Hamm RJ, Dixon CE, Gbadebo DM, Singha AK, Jenkins LW, Lyeth BG, Hayes RL (1992) Cognitive deficits following traumatic brain injury produced by controlled cortical impact. J Neurotrauma 9: 11-20
25. Hamm RJ, Pike BR, O'Dell DM, Lyeth BG, Jenkins LW (1994) The Rotorod test: an evaluation of its effectiveness in assessing motor deficits following traumatic brain injury. J Neurotrauma 11:187-196
26. Hicks RR, Soares HD, Smith DH, McIntosh TK (1996) Temporal and spatial characterization of neuronal injury following lateral fluid-percussion brain injury in the rat. Acta Neuropathol 91:236-246
27. Hockenberry D, Nunez G, Miliman C, Schreiber RD, Korsmeyer SJ (1990) Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348:334-336
28. Hoesche C, Sauerwald A, Veh RW, Krippl B, Kilimann MW (1993) The 5′ flanking region of the rat synapsin I gene directs neuron-specific and developmentally regulated reporter gene expression in transgenic mice. J Biol Chem 268:26494-26502
29. Hogan B, Constantini F, Lacy E (1982) Manipulating the Mouse Embryo: A Laboratory Manual, Cold Spring Harbor, NY, Cold Spring Harbor Press
30. Howland DS, Hemmendinger LM, Caroll PD, Estes PS, Melloni RH, DeGennaro LJ (1991) Positive- and negative-acting promoter sequences regulate cell-type specific expression of the rat synapsin I gene. Mol Brain Res 11:345-353
31. Howland DS, Savage MJ, Huntress FA, Wallace RA, Schwartz DA, Loh T, Melloni RH, DeGennarro LJ, Greenberg BA, Siman R, Swanson ME, Scott RW (1995) Mutant and native human β-amyloid precursor proteins in transgenic mouse brain. Neurobiol Aging 16:685-699
32. Jacobson MD, Raff MC (1995) Programmed cell death and bcl-2 protection in very low oxygen. Nature 374:814-816
33. Jia WW, Wang Y, Qiang D, Tufaro F, Remington R, Cynader M (1996) A Bcl-2 expressing viral vector protects cortical neurons from excitotoxicity even when administered several hours after the toxic insult. Mol Brain Res 42:350-353
34. Kane DJ, Sarafian TA, Anton R, Hahn H, Gfalla EB, Valentine JS, Ord T, Bredesen DE (1993) Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262:1274-1277
35. Kane DJ, Ord T, Anton R, Bredesen DE (1995) Expression of bcl-2 inhibits necrotic neural cell death. J Neurosci Res 40:269-275
36. Klein M, Houx PJ, Jolles J (1996) Long-term persisting cognitive sequelae of traumatic brain injury and the effect of age. J Nerv Ment Dis 184:459-467
37. Kotapka MJ, Graham DI, Adams JH, Gennarelli TA (1992) Hippocampal pathology in fatal non-missile human head injury. Acta Neuropathol 83:530-534
38. Kurth SM, Bigler ED, Blatter DD (1994) Neuropsychological outcome and quantitive image analysis of acute haemorrhage in traumatic brain injury: preliminary findings. Brain Inj 8:489-500
39. Lawrence MS, Ho DY, Sun GH, Steinberg GK, Sapolsky RM (1996) Overexpression of bcl-2 with herpes simplex virus vectors protects CNS neurons against neurological insults in vitro and in vivo. J Neurosci 16:486-496
40. Lawrence MS, McLaughlin JR, Sun GH, Ho DY, McIntosh L, Kunis DM, Sapolsky RM, Steinberg GK (1997) Herpes simplex viral vectors expressing Bcl-2 are neuroprotective when delivered after a stroke. J Cereb Blood Flow Metab 17:740-744
41. Li GL, Brodin G, Farooque M, Funa K, Holtz A, Wang WL, Olsson Y (1996) Apoptosis and expression of bcl-2 after compression trauma to rat spinal cord. J Neuropath Exp Neurol 55:280-289
42. Linnik MD, Zahosp P, Geschwind MD, Federoff HJ (1995) Expression of bcl-2 from a defective herpes simplex virus-1 vector limits neuronal death in focal cerebral ischemia. Stroke 26:1670-1675
43. Lowenstein DH, Thomas MJ, Smith DH, McIntosh TK (1992) Selective vulnerability of dentate hilar neurons following TBI: a potential mechanistic link between head trauma and disorders of the hippocampus. J Neurosci 12:4846-4853
44. Lyeth BG, Jenkins LW, Hamm PJ, Dixon CE, Phillips LL, Clifton GL, Young HF, Hayes RL (1990) Prolonged memory impairment in the absence of hippocampal cell death following traumatic brain injury in the rat. Brain Res 526:249-258
45. Martinou J-C, Dubois-Dauphin M, Staple JK, Rodriguez I, Frankowski H, Missotten M, Albertini P, Talabot D, Catsicas S, Pietra C, Huarte J (1994) Overexpression of bcl-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13:1017-1030
46. McIntosh TK (1994) Neurochemical sequelae of TBI: therapeutic implications. Cerebrovasc Brain Metab Rev 6:109-162
47. McIntosh TK, Vink R, Noble L, Yamakami I, Fernyak S, Soares H, Faden AI (1989) Traumatic brain injury in the rat: characterization of a lateral fluid-percussion model. Neuroscience 28:233-244
48. Mikawa S, Kinouchi H, Kamii H, Gobbel G, Chen SF, Carlson E, Epstein CJ, Chan PH (1996) Attenuation of acute and chronic damage following traumatic brain injury in copper, zinc-superoxide dismutase transgenic mice. J Neurosurg 85:885-891
49. Murphy AN, Bredesen DE, Cortopassi G, Wang E, Fiskum G (1996) Bcl-2 potentiates the maximum calcium uptake capacity of neural cell mitochondria. Proc Natl Acad Sci USA 93:9893-9898
50. Povlishock JT, Erb DE, Astruc J (1992) Axonal response to TBI: reactive axonal change, deafferentation, and neuroplasticity. J Neurotrauma 9:S189-S200
51. Raghupathi R, McIntosh TK (1995) Temporal changes in Bcl-immunoreactivity following experimental brain injury: implication for programmed cell death. J Neurotrauma 12:966
52. Reed JC (1994) Bcl-2 and the regulation of programmed cell death. J Cell Biol 124:1-6
53. Rink AD, Fung KM, Trojanowski JQ, Lee VM-Y, Neugebauer E, McIntosh TK (1995) Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am J Pathol 147:1575-1583
54. Ross DT, Graham DI, Adams JH (1993) Selective loss of neurons from the thalamic reticular nucleus following severe human head injury. J Neurotrauma 10:151-165
55. Smith DH, Okiyama K, Thomas MJ, Claussen B, McIntosh TK (1991) Evaluation of memory dysfunction following experimental brain injury using the Morris water maze. J Neurotrauma 8:259-269
56. Smith DH, Soares HD, Pierce JES, Perlman KG, Saatman KE, Meaney DF, Dixon CE, McIntosh TK (1995) A model of parasagittal controlled cortical impact in the mouse: cognitive and histopathologic effects. J Neurotrauma 12:169-178
57. Soblosky JS, Matthews MA, Davidson JF, Tabor SL, Carey ME (1996) Traumatic brain injury of the forelimb and hindlimb sensorimotor areas in the rat: physiological, histological and behavioral correlates. Behav Brain Res 79:79-92
58. Strauss KI, Raghupathi R, Krajewski S, Reed JC, McIntosh TK (1996) Modulation of apoptosis genes in a rat model of traumatic brain injury (abstract). J Neurotrauma 13:620
59. Su JH, Satou T, Anderson AJ, Cotman CW (1996) Up-regulation of Bcl-2 is associated with neuronal DNA damage in Alzheimer's disease. Neuroreport 7:437-440
60. Sutton RL, Lescaudron L, Stein DG (1993) Unilateral cortical contusion injury in the rat: vascular disruption and temporal development of cortical necrosis. J Neurotrauma 10:135-149
61. Troost D, Aten J, Morsink F, deJong JMBV (1995) Apoptosis in amyotrophic lateral sclerosis is not restricted to motor neurons. Bcl-2 expression is increased in unaffected in post-central gyrus. Neuropathol Appl Neurobiol 21:498-504
62. Yakovlev A, 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
63. Young W (1992) Role of calcium in central nervous system injuries. J Neurotrauma 9:S9-S25
64. Zhong L-T, Sarafian T, Kane DJ, Charles AC, Mah SP, Edwards RH, Bredesen DE (1993) Bcl-2 inhibits death of central neural cells induced by multiple agents. Proc Natl Acad Sci USA 90:4533-4537