Benzodiazepines protect hippocampal neurons from degeneration after transient cerebral ischemia: An ultrastructural study

Neuroscience

Volumn 98, Issue 3, 2000, Pages 471-484

  Schwartz Bloom, R D ^a   Miller, K A ^a   Evenson, D A ^a   Crain, B J ^b   Nadler, J V ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Apoptosis; Diazepam; DNA fragmentation; GABA(A) receptor; Neuroprotection; TUNEL

Indexed keywords

BENZODIAZEPINE DERIVATIVE; CELL DNA; DIAZEPAM; DNA FRAGMENT; IMIDAZENIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN PROTECTION; CAROTID ARTERY OBSTRUCTION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; GERBIL; HIPPOCAMPUS; HISTOPATHOLOGY; MALE; NERVE CELL NECROSIS; NERVE DEGENERATION; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; TRANSIENT ISCHEMIC ATTACK;

ANIMALS; APOPTOSIS; BENZODIAZEPINES; DIAZEPAM; DNA FRAGMENTATION; GABA MODULATORS; GERBILLINAE; IMIDAZOLES; IN SITU NICK-END LABELING; ISCHEMIC ATTACK, TRANSIENT; MALE; MICROSCOPY, ELECTRON; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; PYRAMIDAL CELLS; RECEPTORS, GABA-A;

EID: 0034046652     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00144-5     Document Type: Article

References (40)

1. Chan P.H., Kawase M., Murakami K., Chen S.F., Li Y., Calagui B., Reola L., Carlson E., Epstein C.J. Overexpression of SOD1 in transgenic rats protects vulnerable neurons against ischemic damage after global cerebral ischemia and reperfusion. J. Neurosci. 18:1998;8292-8299.
2. Chen J., Nagayama T., Jin K., Stelter R.A., Zhu R.L., Grahm S.H., Simon R.P. Induction of caspase-3-like protease may mediate delayed neuronal death in the hippocampus after transient cerebral ischemia. J. Neurosci. 18:1998;4914-4928.
3. Colbourne F., Sutherland G.R., Auer R.N. Electron microscopic evidence against apoptosis as the mechanism of neuronal death in global ischemia. J. Neurosci. 19:1999;4200-4210.
4. Crain B.J., Westerkam W.D., Harrison A.H., Nadler J.V. Selective neuronal death after transient forebrainischemia in the Mongolian gerbil: a silver impregnation study. Neuroscience. 27:1988;387-402.
5. Crain B.J., Evenson D.A., Polsky K., Nadler J.V. Electron microscopic study of the gerbil dentate gyrus after transient forebrain ischemia. Acta neuropath. 79:1990;409-417.
6. Deshpande J., Bergstedt K., Linden T., Kalimo H., Wieloch T. Ultrastructural changes in the hippocampal CA1 region following transient cerebral ischemia: evidence against programmed cell death. Expl Brain Res. 88:1992;91-105.
7. Dowden J., Reid C., Dooley P., Corbett D. Diazepam-induced neuroprotection: dissociating the effects of hypothermia following global ischemia. Brain Res. 829:1999;1-6.
8. Galeffi F., Sinnar S. and Schwartz-Bloom R. D. (2000) Diazepam promotes ATP recovery and prevents cytochrome c release in hippocampal slices after in vitro ischemia, J. Neurochem. (in press).
9. Gavrieli Y., Sherman Y., Ben-Sasson S. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119:1992;493-501.
10. Gwag B.J., Lobner D., Koh J.Y., Wie M.B., Choi D.W. Blockade of glutamate receptors unmasks neuronal apoptosis after oxygen-glucose deprivation in vitro. Neuroscience. 68:1995;615-619.
11. Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Heptology. 21:1995;1465-1468.
12. Honkaniemi J., Massa S.M., Breckinridge M., Sharp F.R. Global ischemia induces apoptosis-associated genes in hipppocampus. Molec. Brain Res. 42:1996;79-88.
13. A receptor α1-subunit-immunoreactive interneurons in the gerbil CA1 hippocampus. Hippocampus. 7:1997;511-523.
14. Kaplan T.M., Lasner T.M., Nadler J.V., Crain B.J. Lesions of excitatory pathways reduce hippocampal cell death after transient forebrain ischemia in the gerbil. Acta neuropath. 78:1989;283-290.
15. Kirino T. Delayed neuronal death in the gerbil hippocampus following ischemia. Brain Res. 239:1982;57-69.
16. Kirino T., Sano K. Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta neuropath. 62:1984;201-208.
17. Krajewski S., Mai J.K., Krajewski M., Sirkorska M., Mossakowski M.J., Reed J.C. Upregulation of bax protein levels in neurons following cerebral ischemia. J. Neurosci. 15:1995;6364-6376.
18. Lorente de Nó R. Studies on the sturcutre of the cerebral cortex. II. Continuation of the study of the ammonic system. J. Psychol. Neurol. Lpz. 46:1934;113-177.
19. MacManus J.P., Linnik M.D. Gene expression induced by cerebral ischemia: an apoptotic perspective. J. cerebr. Blood Flow Metab. 17:1997;815-832.
20. Martin L.J., Al-Abdulla N.A., Brambrink A.G., Kirsch J.R., Sieber F.E., Portera-Cailliau C. Neurodegeneration in excitotoxicity, global cerebral ischemia, and target deprivation: a perspective on the contributions of apoptosis and necrosis. Brain Res. Bull. 46:1998;281-309.
21. 2 analog, TEI-7165, on ischemic neuronal damage in gerbils. Brain Res. 769:1997;321-328.
22. Miller K.A., Sair H., Norfolk S., Coy A., Schwartz-Bloom R.D. Benzodiazepines prevent neuronal death by apoptosis and necrosis in the gerbil hippocampus following transient cerebral ischemia. Soc. Neurosci. Abstr. 24:1998;979.
23. Ni B., Wu X., Su Y., Stephenson D., Smalstig E.B., Clemens J., Paul S.M. Transient global ischemia induces a prolonged expression of the caspase-3 mRNA in rat hippocampal CA1 pyramidal neurons. J. cerebr. Blood Flow Metab. 18:1998;248-256.
24. Nitatori T., Sato N., Wauri S., Karasawa Y., Araki H., Shibanai K., Kominami E., Uchiyama Y. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 15:1995;1001-1011.
25. Okazaki M.M., Neill K.H., Crain B.J., Nadler J.V. Loss and recovery of synaptic response in hippocampal area CA1 partially protected from ischemic damage. Soc. Neurosci. Abstr. 19:1993;1668.
26. Pang Z., Geddes J.W. Mechanisms of cell death induced by the mitochondrial toxin 3-nitroproprionic acid: acute excitotoxic necrosis and delayed apoptosis. J. Neurosci. 17:1997;3064-3073.
27. Peng H., Wen T-C., Tanaka J., Maeda N., Matsuda S., Desaki J., Sudo S., Zhang B., Sakanaka M. Epidermal growth factor protects neuronal cells in vivo and in vitro against transient forebrain ischemia- and free radical-induced injuries. J. cerebr. Blood Flow Metab. 18:1998;349-360.
28. Petito C.K., Feldmann E., Pulsinelli W.A., Plum F.A. Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology. 37:1987;1286-1291.
29. Petito C.K., Torres-Munoz J., Roberts B., Olarte J-P., Nowak T.S. Jr., Pulsinelli W.A. DNA fragmentation follows delayed neuronal death in CA1 neurons exposed to transient global ischemia in the rat. J. cerebr. Blood Flow Metab. 17:1997;967-976.
30. Pulsinelli W.A., Brierley J.B., Plum F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 11:1982;491-498.
31. Schwartz-Bloom R., McDonough K., Chase P., Chadwick L., Inglefield J., Levin E. Long-term neuroprotection by benzodiazepine full versus partial agonists after transient cerebral ischemia in the gerbil. J. cerebr. Blood Flow Metab. 18:1998;548-568.
32. Schwartz R., Huff R., Yu X., Carter M., Bishop M. Postischemic diazepam is neuroprotective in the gerbil hippocampus. Brain Res. 647:1994;153-160.
33. Schwartz R., Yu X., Katzman M., Hayden-Hixson D., Perry J. Diazepam, given post-ischemia, protects selectively vulnerable neurons in the rat hippocampus and striatum. J. Neurosci. 15:1995;529-539.
34. Sloviter R.S., Dean E., Neubort S. Electron microscopic analysis of adrenalectomy-induced hippocmapal granuel cell degeneration in the rat: apoptosis in the adult central nervous system. J. comp. Neurol. 330:1993;337-351.
35. Sternau L., Lust W., Ricci A., Ratcheson R. Role for γ-aminobutyric acid in selective vulnerability in gerbils. Stroke. 20:1989;281-287.
36. Sugawara T., Fujimura M., Morita-Fujimura Y., Kawase M., Chan P.H. Mitochondrial release of Cytochrome c corresponds to the selective vulnerability of hippocampal CA1 neurons in rats after transient global cerebral ischemia. J. Neurosci. 19:1999;1-6.
37. Urban L., Neill K.H., Crain B.J., Nadler J.V., Somjen G.G. Postischemic synaptic physiology in area CA1 of the gerbil hippocampus studied in vitro. J. Neurosci. 9:1989;3966-3975.
38. Warner M.A., Neill K.H., Nadler J.V., Crain B.J. Regionally selective effects of NMDA receptor antagonists against ischemic brain damage in the gerbil. J. cerebr. Blood Flow Metab. 11:1991;600-610.
39. Wijsman J.H., Jonker R.R., Keijzer R., Van de Velda C.J.H., Cornelisse C.J., Van Dierendonck J.H. A new method to detect apoptosis in paraffin sections: in situ end-labeling of fragmented DNA. J. Histochem. Cytochem. 41:1993;7-12.
40. Yamamoto K., Hayakawa T., Mogami H., Akai F., Yanagihara T. Ultrastructural investigation of the CA1 region of the hippocampus after transient cerebral ischemia in gerbils. Acta neuropath. 80:1990;487-492.