Histopathologic clues to the pathways of neuronal death following ischemia/hypoxia

Journal of Neurotrauma

Volumn 14, Issue 5, 1997, Pages 313-326

  Rosenblum, William I ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Delayed neuronal death; Excitotoxicity; Ischemic cell change; Selective vulnerability

Indexed keywords

APOPTOSIS; CALCIUM TRANSPORT; CELL DEATH; CROSS LINKING; CYTOTOXICITY; DNA SEQUENCE; ELECTRON MICROSCOPY; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HYPOXIA; ISCHEMIA; NERVE CELL; REVIEW; STAINING;

EID: 0030907037     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.1997.14.313     Document Type: Review

References (53)

1. ADAMS, J.H., CORSELLIS, J.A.N., and DUCKEN, L.W. (1984). Greenfield's Neuropathology (4th ed.), Wiley. New York.
2. AKINO, P.T., LIU, P.K., and HSU, C.Y. (1996). Immediately early gene expression in response to cerebral ischemia: Friend or foe? Stroke 27, 1682-1687.
3. ANDINE, P., JACOBSON, I., and HAGBERG, H. (1988). Calcium uptake evoked by electrical stimuli is enhanced post operatively and precedes delayed neuronal death in CA1 of rat hippocampus: Involvement of N-methyl-D-aspartate receptors. J. Cereb. Blood Flow Metab. 8, 799-807.
4. ANKARCRONA, M., DYPBUKT, J.M., BONFOCO, E., ZHIVOTOVSKY, B., ORRENIUS, S., LIPTON, S.A., and NICOTERA, P. (1995). Glutamate induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15, 961-973.
5. ASTRUP, J., SIESJO, B.K., and SYMON, L. (1981). Thresholds in cerebral ischemia - The ischemie penumbra. Stroke 12, 723-725.
6. BAR, P.R. (1996). Apoptosis. The cell's silent exit. Life Sci. 59, 369-378.
7. BIELSCHOWSKY, M. (1965). In Cytology and Cellular Pathology of the Nervous System. W. Penfield (ed.). (facsimile of 1932 edition). Hafner Publ. Co. New York, pp. 171-172.
8. BRIERLEY, J.B., BROWN, A.W., and MELDRUM, B.S. (1971). The nature and time course of the neuronal alterations resulting from oligoemia and hypoglycoemia in the brain of Macaca Mulatta. Brain Res. 25, 483-499.
9. BROWN, A.W., and BRIERLEY, J.B. (1968). The nature, distribution and earliest stages of anoxic-ischaemic nerve cell damage in the rat brain as defined by the optical microscope. Br. J. Exp. Path XLIX:87-106.
10. CHUAQUI, R., and TAPIA, J. (1993). Histologic assessment of the age of recent brain infarcts in man. J. Neuropath. Exp. Neurol. 52, 481-489.
11. DELEO, J., TOTH, L., SCHUBERT, P., RUDOLPHI, K., and KREUTZBERG, G.W. (1987). Ischemia induced neuronal cell death, calcium accumulation and glial response in the hippocampus of the Mongolian gerbil and protection by propentofylline (HWA 285). J. Cereb. Blood Flow Metab. 7, 745-751.
12. DESHPANDE, J., BERGSTEDT, K., LINDEN, T., KALIMO, H., and WIELOCH, T. (1992). Ultrastructural changes in the hippocampal CA1 region following transient cerebral ischemia: evidence against programmed cell death. Exp. Brain Res. 88, 91-105.
13. DESHPANDE, J., SIESJO, B.K., and WIELOCH, T. (1987). Calcium accumulation and neuronal damage in the rat hippocampus following cerebral ischemia. J. Cereb. Blood Flow Metab. 7, 89-95.
14. DESSI, F., CHARRIANT-MARLANGNE, C., KHRESTCHATISKY, M., and BEN-ARI, Y. (1993). Glutamate induced neuronal death is not programmed cell death in cerebellar culture. J. Neurochem. 60, 1953-1954.
15. DIDIER, M., BURSZTUJN, S., ADAMEC, E., PASSANI, L., NIXON, R.A., COYLE, J., WEI, J.Y., and BERMAN, S.A. (1996). DNA strand breaks induced by sustained glutamate excitotoxicity in primary neuronal cultures. J. Neuroscience 16, 2238-2250.
16. DIEMER, N.H., JOHANSEN, F.F., and JORGENSEN, M.B. (1990). N-methyl-D-aspartate and non-N-methyl-D-aspartate antagonists in global cerebral ischemia. Stroke 21 (Suppl III) III-39-III-42.
17. DU, C., HU, R., CSERNANSKY, C.A., HSU, C.Y., and CHOI, D.W. (1996). Very delayed infarction after mild focal cerebral ischemia: A role for apoptosis? J. Cereb. Blood Flow Metab. 16, 195-201.
18. GARCIA, J.H., LASSEN, N.A., WEILLER, C., SPERLING, B., and NAKAGAWARA, J. (1996). Ischemic stroke and incomplete infarction. Stroke 227, 761-765.
19. GLOBUS, M. Y-T., BUSTO, R., MARTINEZ, E., VALUES, I., and DIETRICH, D.W. (1990). Ischemia induces release of glutamate in regions spared from histopathologic damage in the rat. Stroke 21 (Suppl III), III-43-III-46.
20. GOTO, K., ISHIGE, A., SEKIGUCHI, K., IIZUKA, S., SUGIMOTO, A., YUZURIHARA, M., ABURADA, M., KOSAYA, E., and KOGURE, K. (1990). Effects of cyclohexamide on delayed neuronal death in rat hippocampus. Brain Res. 534, 299-302.
21. GWAG, B.J., LOLNER, D., KOH, J.Y., WIE, M.B., and CHOI, D.W. (1995). Blockade of glutamate receptors unmasks neuronal apoptosis after oxygen-glucose deprivation in vitro. Neuroscience 68, 615-619.
22. HASS, W.K. (1981). Beyond cerebral blood flow, metabolism and ischemia thresholds: an examination of the role of calcium in the initiation of cerebral infarction. in Cerebral Vascular Disease, vol 3. J.S. Meyer, H. Lechner, M. Reivich, E. Ott, and A. Aramibar (eds.). Excerpta Med. Amsterdam, pp. 3-20.
23. ITO, U., SPATZ, M., WALKER, JR, J.T., and KLATZO, I. (1975). Experimental cerebral ischemia in Mongolian gerbils. Light microscopic observations. Acta Neuropath. 32, 209-223.
24. JORGENSEN, M.B., and DIEMER, H.N. (1982). Selective neuron loss after cerebral ischemia in the rat. Possible role of transmitter glutamate. Act Neurol. Scand. 66, 536-546.
25. JOSEPH, R., LI, W., and HAM, E. (1993). Neuronal death, cytoplasmic calcium and internucleosomal DNA fragmentation: Evidence for DNA fragments being released from cells. Brain Res. Mol. Brain Res. 17, 70-76.
26. KIRINO, T. (1982). Delayed neuronal death in the gerbil hippocampus following ischemia. Br. Res. 239, 57-69.
27. KIRINO, T., and SANO, K. (1984). Selective vulnerability in the gerbil hippocampus following transient ischemia. Acta Neuropath. 62, 201-208.
28. KIRINO, T., TAMURA, A., and SANO, K. (1984). Delayed neuronal death in the rat hippocampus following transient forebrain ischemia. Acta Neuropath. 64, 139-147.
29. KRISTIAN, T., and SIESJO, B.K. (1996). Calcium related damage in ischemia. Life Sci. 59, 357-367.
30. LI, Y., CHOPP, M., JIANG, N., YAO, F., and ZALOGA, C. (1995). Temporal profile of in situ DNA fragmentation after transient middle cerebral artery occlusion in the rat. J. Cereb. Blood Flow Metab. 15, 389-397.
31. LINNIK, M.D., ZOBRIST, R.H., and HATFIELD, M.D. (1993). Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24, 2002-2009.
32. MACMANNUS, J.P., HILL, I.E., PRESTON, E., RASQUINHA, I., WALKER, T., and BUCHAN, A.M. (1995). Differences in DNA fragmentation following transient cerebral ischemia or decapitation ischemia in rats. J. Cereb. Blood Flow Metab. 15, 728-737.
33. MARTIN, S.J., GREEN, G.R., and COTTER, T.G. (1994). Dicing with death. Dissecting components of the apoptosis machinery. TIBS 19, 26-30.
34. MATSUMOTO, K., GRAF, R., ROSNER, G., TAGUCHI, J., and HESS, W-D. (1993). Elevation of neuroactive substances in the cortex of cats during prolonged focal ischemia. J. Cereb. Blood Flow Metab. 13, 586-594.
35. MELDRUM, B., EVANS, M., GRIFFITHS, T., and SIMON, R. (1985). Ischaemic brain damage: the role of excitatory activity and of calcium entry. Br. J. Anaesth. 57, 44-46.
36. MESNER, P.W., EPTING, C.L., HEGARTY, J.L., and GREEN, S.H. (1995). A timetable of events during programmed cell death induced by trophic factor withdrawal from neuronal PC 12 cells. J. Neurosci. 15, 7357-7366.
37. MIGHELI, A., ATTANANOSIO, A., and SCHIFFER, D. (1995). Ultrastructural detection of DNA strand breaks in apoptotic neural cells by in situ end-labeling techniques. J. Pathol. 176, 27-35.
38. MONTALBETTI, L., ROZZA, A., RIZZO, V., FAVALLI, L., SCAVINI, C., LANZA, E., SAVOLDI, F., RACAGNI, G., and SCELSI, R. (1995). Amino acid recovery via microdialysis and photoinduced focal cerebral ischemia in brain cortex of rats. Neurosci. Lett. 192, 153-156.
39. MPOKE, S., and WOLFE, J. (1996). DNA digestion and chromatin condensation during nuclear death in tetrahymena. Exp. Cell Res. 225, 357-365.
40. NITATORI, T., SATO, N., WAGURI, S., KARASAWA, Y., ARAKI, H., SHIBANAI, K., KOMINAMI, E., and UCHIYAMA, Y. (1995). Delayed neuronal death in CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J. Neurosci. 15, 1001-1011.
41. NOVELLI, A., REILLY, J.A., LYSKO, P.O., and HENNEBERRY, R.C. (1988). Glutamate becomes toxic via the N-methyl-D-Aspartate receptor when intracellular energy levels are reduced. Brain Res. 451, 205-212.
42. OHTA, S., SHIGERU, F., MATSUBARA, I., KOHNO, K., KUMON, Y., and SASAKI, S. (1996). Calcium movement in ischemia tolerant hippocampal CA1 neurons after transient forebrain ischemia in gerbils. J. Cereb. Blood Flow Metab. 16, 915-922.
43. PARK, C.K., NEHLS, D.G., GRAHAM, D.I., TEASDALE, G.M., and MCCULLOCH, J. (1988). Focal cerebral ischaemia in the cat: Treatment with the glutamate antagonist MK801 after induction of ischaemia. J. Cereb. Blood Flow Metab. 8, 757-762.
44. PETITO, C.K., FELDMANN, E., PULSINELLI, W.A., and PLUM, F. (1987). Delayed hippocampal damage in humans following cardiorespiratory arrest. Neurology, 37, 1281-1286.
45. PETITO, C.K., and ROBERTS, B. (1995). Effect of post mortem interval on in situ and labeling of DNA oligonucleosomes. J. Neuropath. Exp. Neurol. 54, 761-765.
46. PULSINELLI, W.A., BRIERLEY, J.B., and PLUM, F. (1982). Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann. Neurol. 11, 491-498.
47. RINK, A., FUNG, K-M., TROJANOWSKI, J.Q., LEE, V., M-Y., NENGEBAUER, E., and MCINTOSH, T.K. (1995). Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am. J. Path. 147, 1575-1583.
48. ROTHMAN, S.M., and OLNEY, J.W. (1987). Excitotoxicity and the NMDA receptor. TINS 10, 299-302.
49. SIESJO, B.K. (1981). Cell damage in the brain: A speculative synthesis. J. Cereb. Blood Flow Metab. 1, 155-185.
50. SIMON, R.P., SWAN, J.H., GRIFFITH, T., and MELDRUM, B.S. (1984). Blockade of N-methyl-D-aspartate receptors may protect against ischemie damage in the brain. Science 226, 850-852.
51. STATES, B.A., HONKANIEMI, J., WEINSTEIN, P.R., and SHARP, F.R. (1996). DNA fragmentation and HSP 70 protein induction in hippocampus and cortex occurs in separate neurons following permanent middle cerebral artery occlusions. J. Cereb. Blood Flow Metab. 16, 1165-1175.
52. TAKAGI, K., GINSBERG, M.D., GLOBUS, M. Y-T., DIETRICH, W.D., MARTINEZ, E., KRAYDIEH, S., and BUSTO, R. (1993). Changes in amino acid neurotransmitters and cerebral blood flow in the ischemic penumbral region following middle cerebral artery occlusion in the rat: correlation with histopathology. J. Cereb. Blood Row Metab. 13, 575-585.
53. WYLLIE, A.H., KERR, J.F.R., and CURRIE, A.R. (1980). Cell Death: The significance of apoptosis, in International Review of Cytology, vol. 69. Bourne, G.H. and Danielli, J.F. (eds.). N.Y.: Academic Press, pp. 251-306.