Distinguishing excitotoxic from apoptotic neurodegeneration in the developing rat brain

Journal of Comparative Neurology

Volumn 408, Issue 4, 1999, Pages 461-476

  Ishimaru, M J ^a   Ikonomidou, C ^b   Tenkova, T I ^c   Der, T C ^c   Dikranian, K ^c   Sesma, M A ^c   Olney, J W ^c  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

^b HUMBOLDT UNIVERSITY   (Germany)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Glutamate; Head trauma; Ischemia; Necrosis; Physiologic cell death

Indexed keywords

ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN DEVELOPMENT; BRAIN ISCHEMIA; CELL DEATH; DNA DAMAGE; HEAD INJURY; NERVE CELL NECROSIS; NERVOUS SYSTEM DEVELOPMENT; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; APOPTOSIS; BRAIN; BRAIN INJURIES; ELECTROPHORESIS, AGAR GEL; GLIAL FIBRILLARY ACIDIC PROTEIN; GLUTAMIC ACID; IN SITU NICK-END LABELING; MICROGLIA; MICROSCOPY, ELECTRON; NERVE DEGENERATION; RATS; RATS, SPRAGUE-DAWLEY; SILVER STAINING;

EID: 0033553786     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19990614)408:4<461::AID-CNE2>3.0.CO;2-9     Document Type: Article

References (44)

1. Beilharz EJ, Williams CE, Dragunow M, Sirimanne ES, Gluckman PD. 1995. Mechanisms of delayed cell death following hypoxic-ischemic injury in the immature rat: evidence for apoptosis during selective neuronal loss. Mol Brain Res 29:1-14.
2. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. 1995. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 92:7162-7166.
3. Charriaut-Marlangue C, Ben-Ari Y. 1995. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport 7:61-64.
4. Clarke PGH. 1990. Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol 181:195-213.
5. 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.
6. Collins RJ, Harmon BB, Gobé GC, Kerr JFR. 1992. Internucleosomal DNA cleavage should not be the sole criterion for identifying apoptosis. Int J Radiat Biol 61:451-453.
7. Corso TD, Sesma MA, Tenkova TI, Der TC, Wozniak DF, Farber NB, Olney JW. 1997. Multifocal brain damage induced by phencyclidine is augmented by pilocarpine. Brain Res 752:1-14.
8. DeOlmos JS, Ingram WR. 1971. An improved cupric-silver method for impregnation of axonal and terminal degeneration. Brain Res 33:523-529.
9. Dikranian K, Ishimaru MJ, Tenkova T, Ikonomidou C, Olney JW. 1998. Histological characterization of apoptotic neurodegeneration induced in the developing rat CNS by NMDA antagonists. Soc Neurosci Abstr 24:1299.
10. Ferrer I, Martin F, Serrano T, Reiriz J, Pérez-Navarro E, Alberch J, Macaya A, Planas AM. 1995. Both apoptosis and necrosis occur following intrastriatal administration of excitotoxins. Acta Neuropathol 90:504-510.
11. Filipkowski RK, Hetman M, Kaminska B, Kaczmarek L. 1994. DNA fragmentation in rat brain after intraperitoneal administration of kainate. Neuroreport 5:1538-1540.
12. Gavrieli Y, Sherman Y, Ben-Sasson SA. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J Cell Biol 119:493-501.
13. Grasl-Kraupp B, Ruttkay-Nedecky B, Koudelka H, Bukowska K, Bursch W, Schulte-Hermann R. 1995. In situ detection of fragmented DNA(TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology 21:1465-1468.
14. Gwag BJ, Koh JY, Demaro JA, Ying HS, Jacquin M, Choi DW. 1997. Slowly triggered excitotoxicity occurs by necrosis in cortical cultures. Neuroscience 77:393-401.
15. Ikonomidou C, Price MT, Mosinger JL, Frierdich G, Labruyere J, Shahid Salles K, Olney JW. 1989a. Hypobaric-ischemic conditions produce glutamate-like cytopathology in infant rat brain. J Neurosci 9:1693-1700.
16. Ikonomidou C, Mosinger JL, Shahid Salles K, Labruyere J, Olney JW. 1989b. Sensitivity of the developing rat brain to hypobaric/ischemic damage parallels sensitivity to N-Methyl-Aspartate neurotoxicity. J Neurosci 9:2809-2818.
17. Ikonomidou C, Qin Y, Labruyere J, Kirby C, Olney JW. 1996a. Prevention of trauma-induced neurodegeneration in infant rat brain. Pediatr Res 39:1020-1027.
18. Ikonomidou C, Ishimaru M, Bittigau P, Der TC, Qin YQ, Olney JW. 1996b. Delayed degeneration of distant neurons following neocortical brain concussion in infant rats. Soc Neurosci Abstr 22:20.
19. Ikonomidou C, Qin YQ, Labruyere J, Olney JW. 1996c. Motor neuron degeneration induced by excitotoxin agonists has features in common with that seen in the SOD-1 transgenic mouse model of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 55:211-224.
20. Ikonomido C, Bosch F, Bittigau P, Miksa M, Turski L, Olney JW. 1998. NMDA antagonists induce massive apoptotic neurodegeneration in the developing rat CNS. Soc Neurosci Abstr 24:274.
21. Ikonomidou C, Bosch F, Miksa M, Vockler J, Bittigau P, Dikranian K, Tenkova T, Turski L, Olney JW. 1999. Blockade of glutamate receptors triggers apoptotic neurodegeneration in the developing brain. Science 283:70-74.
22. Kerr JFR, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wideranging implications in tissue kinetics. Br J Cancer 26:239-257.
23. Kure S, Tominaga T, Yoshimoto T, Tada K, Narisawa K. 1991. Glutamate triggers internucleosomal DNA cleavage in neuronal cells. Biochem Biophys Res Commun 179:39-45.
24. Li L, Houenou JL, Wu W, Lei M, Prevette DM, Oppenheim RW. 1998. Characterization of spinal motoneuron degeneration following different types of peripheral nerve injury in neonatal and adult mice. J Comp Neurol 396:158-168.
25. Linnik MD, Zobrist RH, Hatfield MD. 1993. Evidence supporting a role for programmed cell death in focal cerebral ischemia in rats. Stroke 24:2002-2009.
26. MacManus JP, Buchan AM, Hill IE, Rasquinha I, Preston E. 1993. Global ischemia can cause DNA fragmentation indicative of apoptosis in rat brain. Neurosci Lett 164:89-92.
27. MacManus JP, Hill IE, Huang ZG, Rasquinha I, Don X, Buchan AM. 1994. DNA damage consistent with apoptosis in transient focal ischaemic neocortex. Neuroreport 5:493-496.
28. Olney JW. 1971. Glutamate-induced neuronal necrosis in the infant mouse hypothalamus: an electron microscopic study. J Neuropathol Exp Neurol 30:75-90.
29. Olney JW. 1974. Toxic effects of glutamate and related amino acids on the developing central nervous system. In: Nyhan WN, editor. Heritable disorders of amino acid metabolism. New York: John Wiley. p 501-512.
30. Olney JW, Ishimaru MJ. 1999. Excitotoxic cell death. In: Koliatsos VE, Ratan R, editors. Cell death in diseases of the nervous system. New Jersey: Humana Press Pubs, p 197-220.
31. Olney JW, Ho OL, Rhee V. 1971. Cytotoxic effects of acidic and sulphur-containing amino acids on the infant mouse central nervous system. Exp Brain Res 14:61-76.
32. Olney JW, Sharpe LG, Feigin RD. 1972. Glutamate-induced brain damage in infant primates. J Neuropathol Exp Neurol 31:464-488.
33. Olney JW, Rhee V, Ho OL. 1974. Kainic acid: a powerful neurotoxic analogue of glutamate. Brain Res 77:507-512.
34. Olney JW, Ikonomidou C, Mosinger JL, Frierdich G. 1989. MK-801 prevents hypobaric-ischemic neuronal degeneration in infant rat brain. J Neurosci 9:1701-1704.
35. Portera-Cailliau C, Price DL, Martin LJ. 1997. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol 378:70-87.
36. Pravdenkova SV, Basnakian AG, James SJ, Andersen BJ. 1996. DNA fragmentation and nuclear endonucleaae activity in rat brain after severe closed head injury. Brain Res 729:151-155.
37. Rink A, Fung KM, Trojanowski JQ, Lee VMY, Neugebauer E, McIntosh TK. 1995. Evidence of apoptotic cell death after experimental traumatic brain injury in the rat. Am J Pathol 147:1575-1583.
38. Sei Y, Von Lubitz DKJE, Basile AS, Borner MM, Lin RCS, Skolnick P, Fossom LH. 1994. Internucleosomal DNA fragmentation in gerbil hippocampus following forebrain ischemia. Neurosci Lett 171:179-82.
39. Sherwood NM, Timiras PS. 1970. A stereotaxic atlas of the developing rat brain. Berkeley, CA: University of California Press.
40. Sloviter RS, Dean E, Neubort S. 1993. An electron microscopic analysis of adrenalectomy-induced hippocampal granule cell degeneration in the rat; apoptosis in the adult central nervous system. J Comp Neurol 330:337-351.
41. Streit WJ. 1990. An improved staining method for rat microglial cells using the lectin from Griffonia simplicifolia (GSA I-B4) J Histochem Cytochem 38:1683-1686.
42. Tominaga T, Kure S, Narisawa K, Yoshimoto T. 1993. Endonuclease activation following focal ischemic injury in the rat brain. Brain Res 608:21-26.
43. West MJ. 1993. New stereological methods for counting neurons. Neurobiol Aging 14:275-285.
44. Wyllie AH, Kerr JFR, Currie AR. 1980. Cell death: the significance of apoptosis. Int Rev Cytol 68:251-306.