Reperfusion injury as the mechanism of brain damage after perinatal asphyxia

Pediatric Research

Volumn 41, Issue 5, 1997, Pages 599-606

  Fellman, Vineta ^a   Raivio, Kari O ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; XANTHINE DEHYDROGENASE; XANTHINE OXIDASE;

ARTICLE; BLOOD OXYGENATION; BRAIN INJURY; BRAIN ISCHEMIA; CAPILLARY ENDOTHELIUM; CELL DEATH; ENZYME ACTIVITY; GENE ACTIVATION; HUMAN; HUMAN CELL; HYPOXIA; INFLAMMATORY CELL; PERINATAL ASPHYXIA; PRIORITY JOURNAL; REPERFUSION INJURY; TISSUE INJURY;

EID: 0030895568     PISSN: 00313998     EISSN: None     Source Type: Journal    
DOI: 10.1203/00006450-199705000-00001     Document Type: Article

References (138)

1. Parks DA, Granger DN 1986 Contributions of ischemia and reperfusion to mucosal lesion formation. Am J Physiol 250:G749-G753
2. McCord JM 1985 Oxygen-derived free radicals in postischemic tissue injury. N Engl J Med 312:159-163
3. Saugstad OD 1988 Hypoxanthine as an indicator of hypoxia: its role in health and disease through free radical production. Pediatr Res 23:143-150
4. Kinnula VL, Crapo JD, Raivio KO 1995 Generation and disposal of reactive oxygen metabolites in the lung. Lab Invest 73:3-19
5. Halliwell B, Gutteridge JMC 1992 Free Radicals in Biology and Medicine, 2nd Ed. Clarendon Press, Oxford, UK
6. Granger DN 1988 Role of xanthine oxidase and granulocytes in ischemia-reperfusion injury. Am J Physiol 255:H1269-H1275
7. Weiss SJ 1989 Tissue destruction by neutrophils. N Engl J Med 320:365-376
8. Kinnula VL, Mirza Z, Crapo JD, Whorton AR 1993 Modultion of hydrogen peroxide release from vascular endothelial cells by oxygen. Am J Respir Cell Mol Biol 9:603-609
9. Pourcyrous M, Leffler CW, Bada HS, Korones SB, Busija DW 1993 Brain superoxide anion generation in asphyxiated piglets and the effect of indomethacin at therapeutic dose. Pediatr Res 34:366-369
10. Cross AR, Jones OGT 1991 Enzymatic mechanisms of superoxide production. Biochim Biophys Acta 1057:291-298
11. Mohazzab-H KM, Kaminski PM, Wolin MS 1994 NADH oxidoreductase is a major source of superoxide anion in bovine coronary artery endothelium. Am J Physiol 266:H2568-H2572
12. Parks DA, Granger DN 1986 Xanthine oxidase: biochemistry, distribution and physiology. Acta Physiol Scand Suppl 548:87-99
13. Nishino T 1994 The conversion of xanthine dehydrogenase to xanthine oxidase and the role of the enzyme in reperfusion injury. J Biochem 116:1-6
14. Stirpe F, Della Corte E 1969 The regulation of rat liver xanthine oxidase. Conversion in vitro of the enzyme activity from dehydrogenase (type D) to oxidase (type O). J Biol Chem 244:3855-3863
15. Xia Y, Zweier JL 1995 Substrate control of free radical generation from xanthine oxidase in the postischemic heart. J Biol Chem 270:18797-18803
16. Hagberg H, Andersson P, Lacarewicz J, Jacobson I, Butcher S, Sandberg M 1987 Extracellular adenosine, inosine, hypoxanthine, and xanthine in relation to tissue nucleotides and purines in rat striatum during transient ischemia. J Neurochem 49:227-231
17. Ruth V, Fyhrquist F, Clemons G, Raivio KO 1988 Cord plasma vasopressin, erythropoietin, and hypoxanthine as indices of asphyxia at birth. Pediatr Res 24:490-494
18. Ames BN, Cathcart R, Schwiers E, Hochstein P 1981 Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: a hypothesis. Proc Natl Acad Sci USA 78:6858-6862
19. Godin DV, Ko KM 1991 Allopurinol and ischemia/reperfusion injury: New use for an old drug? Can J Cardiol 7:163-169
20. Paller MS, Hoidal JR, Ferris TF 1984 Oxygen free radicals in ischemic acute renal failure in the rat. J Clin Invest 74:1156-1164
21. Lemasters J, Thurman RG 1993 Hypoxia and reperfusion injury to liver. Prog Liver Dis 11:85-114
22. Adkins WK, Taylor AE 1990 Role of xanthine oxidase and neutrophils in ischemia-reperfusion injury in rabbit lung. J Appl Physiol 69:2012-2018
23. 2O2 contributes to reperfusion injury of ischemic skeletal muscle. Am J Physiol 258:H1415-H1419
24. Palmer C 1995 Hypoxic-ischemic encephalopathy. Therapeutic approaches against microvascular injury, and role of neutrophils, PAF, and free radicals. Clin Perinatol 22:481-517
25. Lasley RD, Ely SW, Berne RM, Mentzer Jr RM 1988 Allopurinol enhanced adenine nucleotide repletion after myocardial ischemia in the isolated rat heart. J Clin Invest 81:16-20
26. Moorhouse PC, Grootveld M, Halliwell B, Quinlan JG, Gutteridge JMC 1987 Allopurinol and oxipurinol are hydroxyl radical scavengers. FEBS Lett 249:23-28
27. Johnson JL, Rajagopalan KV, Cohen HV 1974 Molecular basis for the biological function of molybdenum. Effect of tungsten on xanthine oxidase and sulfite oxidase in the rat. J Biol Chem 249:859-866
28. Brown JM, Terada LS, Grosso MA, Whitmann GJ, Velasco SE, Patt A, Harken AH, Repine JE 1988 Xanthine oxidase produces hydrogen peroxide which contributes to reperfusion injury of ischemic, isolated, perfused rat hearts. J Clin Invest 81:1297-1301
29. Nielsen VG, Tan S, Baird MS, McCammon AT, Parks DA 1996 Gastric intramucosal pH and multiple organ injury: impact of ischemia-reperfusion and xanthine oxidase. Crit Care Med 24:1339-1344
30. Linas SL, Whittenburg D, Repine JE 1990 Role of xanthine oxidase in ischemia/ reperfusion injury. Am J Physiol 258:F711-F716
31. Thompson-Gorman SL, Zweier JL 1990 Evaluation of the role of xanthine oxidase in myocardial reperfusion injury. J Biol Chem 265:6656-6663
32. Zweier JL, Kuppusamy P, Lutty GA 1988 Measurement of endothelial cell free radical generation: evidence for a central mechanism of free radical injury in postischemic tissues. Proc Natl Acad Sci USA 85:4046-4050
33. Zweier JL, Broderick R, Kuppusamy P, Thompson-Gorman S, Lutty GA 1994 Determination of the mechanism of free radical generation in human aortic endothelial cells exposed to anoxia and reoxygenation. J Biol Chem 269:24156-24162
34. Krenitsky TA, Tuttle JV, Cattau Jr EL, Wang P 1974 A comparison of the distribution and electron acceptor specificities of xanthine oxidase and aldehyde oxidase. Comp Biochem Physiol 496:687-703
35. Wajner M, Harkness RA 1989 Distribution of xanthine dehydrogenase and oxidase activities in human and rabbit tissues. Biochim Biophys Acta 991:79-84
36. Sarnesto A, Linder N, Raivio KO 1996 Organ distribution and molecular forms of human xanthine dehydrogenase/xanthine oxidase protein. Lab Invest 74:48-56
37. Vettenranta K, Raivio KO 1990 Xanthine oxidase during human fetal development. Pediatr Res 27:286-288
38. Jarasch E-D, Grund C, Bruder G, Heid HW, Keenan TW, Franke WW 1981 Localization of xanthine oxidase in mammary-gland epithelium and capillary endothelium. Cell 25:67-82
39. Jarasch E-D, Bruder G, Heid HW 1986 Significance of xanthine oxidase in capillary endothelial cells. Acta Physiol Scand Suppl 548:39-46
40. Moriwaki Y, Yamamoto T, Suda M, Nasako Y, Takahashi S, Agbedana OE, Hada T, Higashino K 1993 Purification and immunohistochemical localization of human xanthine oxidase. Biochim Biophys Acta 1164:327-330
41. Betz AL 1985 Identification of hypoxanthine transport and xanthine oxidase activity in brain capillaries. J Neurochem 44:574-579
42. Terada LS, Willingham IR, Rosandich ME, Leff JA, Kindt GW, Repine JE 1991 Generation of superoxide anion by brain endothelial cell xanthine oxidase. J Cell Physiol 148:191-196
43. Hassoun PM, Yu FS, Shedd AL, Zulueta JJ, Thannickal VJ, Lanzillo JJ, Fanburg BL 1994 Regulation of endothelial cell xanthine dehydrogenase/xanthine oxidase gene expression by oxygen tension. Am J Physiol 266:L163-L171
44. Dupont GP, Huecksteadt TP, Marshall BC, Ryan US, Michael JR, Hoidal JR 1992 Regulation of xanthine dehydrogenase and xanthine oxidase activity and gene expression in cultured rat pulmonary endothelial cells. J Clin Invest 89:197-202
45. Partridge CA, Blumenstock FA, Malik AB 1992 Pulmonary microvascular endothelial cells constitutively release xanthine oxidase. Arch Biochem Biophys 294:184-187
46. Terada LS, Guidot DM, Leff JA, Willingham IR, Hanley ME, Piermattei D, Repine JE 1992 Hypoxia injures endothelial cells by increasing endogenous xanthine oxidase activity. Proc Natl Acad Sci USA 89:3362-3366
47. Hassoun PM, Yu FS, Zulueta JJ, White AC, Lanzillo JJ 1995 Effect of nitric oxide and cell redox status on the regulation of endothelial cell xanthine dehydrogenase. Am J Physiol 268:L809-L817
48. 2-dependent form (type O). Arch Biochem Biophys 172:365-379
49. Engerson TD, McKelvey TG, Rhyne DB, Boggio EB, Snyder SJ, Jones HP 1987 Conversion of xanthine dehydrogenase to oxidase in ischemic rat tissues. J Clin Invest 79:1564-1570
50. McKelvey TG, Höllwarth ME, Granger DN, Engerson TD, Landler U, Jones HP 1988 Mechanisms of conversion of xanthine dehydrogenase to xanthine oxidase in ischemic rat liver and kidney. Am J Physiol 254:G753-G760
51. Brass CA, Narciso J, Gollan JL 1991 Enhanced activity of the free radical producing enzyme xanthine oxidase in hypoxic rat liver. Regulation and pathophysiologic significance. J Clin Invest 87:424-431
52. Wiezorek JS, Brown DH, Kupperman DE, Brass CA 1994 Rapid conversion to high xanthine oxidase activity in viable Kupffer cells during hypoxia. J Clin Invest 94:2224-2230
53. Nishino T, Tamura I 1991 The mechanism of conversion of xanthine dehydrogenase to oxidase and the role of the enzyme in reperfusion injury. Adv Exp Med Biol 309A:327-337
54. Rothwell NJ, Hopkins SJ 1995 Cytokines and the nervous system. II. Actions and mechanisms of action. Trends Neurol Sci 18:130-136
55. Minami M, Kurashi Y, Yabuuchi K, Yamazaki A, Satoh M 1992 Induction of interleukin-1β mRNA in rat brain after transient forebrain ischemia. J Neurochem 58:390-392
56. Gehrmann J, Bonnekoh P, Miyazawa T, Oschlies U, Duz E, Hosmann KA, Kreutzberg GW 1992 The microglia reaction in the rat hippocampus following global ischemia: immunoelectron microscopy. Acta Neuropathol 84:588-595
57. Morioka T, Kalehua AN, Streit WJ 1992 Progressive expression of immunomolecules on microglial cells in rat dorsal hippocampus following transient forebrain ischemia. Acta Neuropathol 83:149-157
58. McRae A, Gilland E, Bona E, Hagberg H 1995 Microglia activation after neonatal hypoxia-ischemia. Dev Brain Res 84:245-252
59. Yamasaki Y, Matsuura N, Shozuhara H, Onodera H, Itoyama Y, Kogure K 1995 Interleukin-1 as a pathogenic mediator of ischemic brain damage in rats. Stroke 26:676-681
60. Relton JK, Rothwell NJ 1992 Interleukin-1 receptor antagonist inhibits ischaemic and excitotoxic neuronal damage in the rat. Brain Res Bull 29:243-246
61. Betz AL, Yang G-Y, Davidson BL 1995 Attenuation of stroke size in rats using an adenoviral vector to induce overexpression of interleukin-1 receptor antagonist in brain. J Cereb Blood Flow Metab 15:547-551
62. Bruce AJ, Boling W, Kindy MS, Peschon J, Kraemer PJ, Carpenter MK, Holtsberg FW, Mattson MP 1996 Altered neuronal and microglial responses to excitotoxic and ischemic brain injury in mice lacking TNF receptor. Nat Med 2:788-794
63. Okada Y, Copeland BR, Mori E, Tung MM, Thomas WS, del Zoppo GJ 1994 P-selectin and intercellular adhesion molecule-1 expression after focal brain ischemia and reperfusion. Stroke 25:202-211
64. Matsuo Y, Onodera H, Shiga Y, Nakamura M, Ninomiya M, Kihara T, Kogure K 1994 Correlation between myeloperoxidase-quantified neutrophil accumulation and ischemic brain injury in the rat. Effects of neutrophil depletion. Stroke 25:1469-1475
65. 2 integrins in vivo. Proc Natl Acad Sci USA 88:7538-7542
66. Hansen PR 1995 Role of neutrophils in myocardial ischemia and reperfusion. Circulation 91:1872-1885
67. Etzioni A 1996 Adhesion molecules - their role in health and disease. Pediatr Res 39:191-198
68. Romson JL, Hook BG, Kunkel SL, Abrams GD, Schork MA, Lucchesi BR 1983 Reduction of the extent of ischemic myocardial injury by neutrophil depletion in the dog. Circulation 67:1016-1023
69. Hernandez LA, Grisham MB, Twohig B, Arfors KE, Harlan JM, Granger DN 1987 Role of neutrophils in ischemia-reperfusion-induced microvascular injury. Am J Physiol 253:H699-H703
70. Vedder NB, Winn RK, Rice CL, Chi EY, Arfors KE, Harlan JM 1988 A monoclonal antibody to adherence-promoting leukocyte glycoprotein, CD18, reduces organ injury and improves survival from hemorrhagic shock and resuscitation in rabbits. J Clin Invest 81:939-944
71. Ma X-L, Tsao PS, Lefer AM 1991 Antibody to CD-18 exerts endothelial and cardiac protective effects in myocardial ischemia and reperfusion. J Clin Invest 88:1237-1243
72. Yoshida N, Granger DN, Anderson DC, Rothlein R, Lane C, Kvietys PR 1992 Anoxia/reoxygenation-induced neutrophil adherence to cultured endothelial cells. Am J Physiol 262:H1891-H1898
73. Hallenbeck JM, Dutka AJ, Tanishima T, Kochanek PM, Kumaroo KK, Thompson CB, Obrenovich TP, Contreras TJ 1986 Polymorphonuclear leukocyte accumulation in brain regions with low blood flow during the early postischemic period. Stroke 17:246-253
74. Grisham MB, Hernandez LA, Granger DN 1986 Xanthine oxidase and neutrophil infiltration in intestinal ischemia. Am J Physiol 251:G567-G574
75. Patel KD, Zimmerman GA, Prescott SM, McEver RP, McIntyre TM 1991 Oxygen radicals induce human endothelial cells to express GMP-140 and bind neutrophils. J Cell Biol 112:749-759
76. McEver RP 1991 Selectins: novel receptors that mediate leukocyte adhesion during inflammation. Thromb Haemost 65:223-228
77. Vannucci RC 1993 Experimental models of perinatal hypoxic-ischemic brain damage. Acta Pathol Microb Scand 101(suppl 40):89-95
78. Siesjö BK 1992 Pathophysiology and treatment of focal cerebral ischemia. Part I. Pathophysiology. J Neurosurg 77:169-184
79. Rosenberg AA, Murdaugh E, White CW 1989 The role of oxygen free radicals in postasphyxia cerebral hypoperfusion in newborn lambs. Pediatr Res 26:215-219
80. Karlsson BR, Grögaard B, Gerdin B, Steen PA 1994 The severity of postischemic hypoperfusion increases with duration of cerebral ischemia in rats. Acta Anaesthesiol Scand 38:248-253
81. Pluta R, Lossinsky AS, Wisniewski HM, Mossakowski MJ 1994 Early blood-brain barrier changes in the rat following transient complete cerebral ischemia induced by cardiac arrest. Brain Res 633:41-52
82. Petito CK, Pulsinelli WA, Jacobson G, Plum F 1982 Edema and vascular permeability in cerebral ischemia: Comparison between ischemic neuronal damage and infarction. J Neuropathol Exp Neurol 41:423-436
83. del Zoppo GJ, Schmid-Schönbein GW, Mori E, Copeland BR, Chang C-M 1991 Polymorphonuclear leukocytes occlude capillaries following middle cerebral artery occlusion and reperfusion in baboons. Stroke 22:1276-1283
84. Zhang R-L, Chopp M, Chen H, Garcia JH 1994 Temporal profile of ischemic tissue damage, neutrophil response, and vascular plugging following permanent and transient (2H) middle cerebral artery occlusion in the rat. J Neurol Sci 125:3-10
85. Thomas WS, Mori E, Copeland BR, Yu J-Q, Morrissey JH, del Zoppo GJ 1993 Tissue factor contributes to microvascular defects after focal cerebral ischemia. Stroke 24:847-854
86. Connolly ES Jr, Winfree CJ, Springer TA, Naka Y, Liao H, Yan SD, Stern DM, Solomon RA, Gutierrez-Ramos J-C, Pinsky DJ 1996 Cerebral protection in homozygous null ICAM-1 mice after middle cerebral artery occlusion. Role of neutrophil adhesion in the pathogenesis of stroke. J Clin Invest 97:209-216
87. Vannucci RC 1990 Experimental biology of cerebral hypoxia-ischemia: relation to perinatal brain damage. Pediatr Res 27:317-326
88. Pulsinelli WA, Brierley JB, Plum F 1982 Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491-498
89. Lorek A, Takei Y, Cady E, Wyatt J, Penrice J, Edwards A, Peebles D, Wylezinska M, Owen-Reece H, Kirkbridge V, Cooper C, Aldrige R, Roth S, Brown G, Delpy D, Reynolds EOR 1994 Delayed ("secondary") cerebral energy failure following acute hypoxia-ischemia in the newborn piglet: continuous 48-hour studies by phosphorus magnetic resonance spectroscopy. Pediatr Res 36:699-706
90. Zini I, Tomasi A, Grimaldi R, Vannini V, Agnati LF 1992 Detection of free radicals during brain ischemia and reperfusion by spin trapping and microdialysis. Neurosci Lett 138:279-282
91. Phillis JW, Sen S 1993 Oxypurinol attenuates hydroxyl radical production during ischemia/reperfusion injury of the rat cerebral cortex: an ESR study. Brain Res 628:309-312
92. Hasegawa K, Yoshioka H, Sawada T, Nishikawa H 1993 Direct measurement of free radicals in the neonatal mouse brain subjected to hypoxia: an electron spin resonance spectroscopic study. Brain Res 607:161-166
93. Yang G, Chan PH, Chen J, Carlson E, Chen SF, Weinstein P, Epstein CJ, Kamii H 1994 Human copper-zinc superoxide dismutase transgenic mice are highly resistant to reperfusion injury after focal cerebral ischemia. Stroke 25:165-170
94. Connors G, Hunse C, Gagnon R, Richardson B, Han V, Rosenberg H 1992 Perinatal assessment of cerebral blood flow velocity wave forms in the human fetus and neonate. Pediatr Res 31:649-652
95. Eken P, Toet MC, Groenendaal F, de Vries LS 1995 Predictive value of early neuroimaging, pulsed Doppler and neurophysiology in full term infants with hypoxic-ischemic encephalopathy. Arch Dis Child 73:F75-F80
96. Archer LNJ, Levene MI, Evans DH 1986 Cerebral artery Doppler ultrasonography for prediction of outcome after perinatal asphyxia. Lancet 2:1116-1118
97. Frewen TC, Kissoon N, Kronick J, Fox M, Lee R, Bradwin N, Chance G 1991 Cerebral blood flow, cross-brain oxygen extraction, and fontanelle pressure after hypoxic-ischemic injury in newborn infants. J Pediatr 118:265-271
98. Wyatt JS 1993 Near-infrared spectroscopy in asphyxial brain injury. Clin Perinatol 20:369-378
99. Van Bel F, Dorrepaal CA, Benders MJNL, Zeeuwe PEM, van de Bor M, Berger HM 1993 Changes in cerebral hemodynamics and oxygenation in the first 24 hours after birth asphyxia. Pediatrics 92:365-372
100. Pryds O, Greisen G, Lou H, Friis-Hansen B 1990 Vasoparalysis associated with brain damage in asphyxiated term infants. J Pediatr 117:119-125
101. Volpe JJ, Herscovitch P, Perlman JM, Kreusser KL, Raichle ME 1985 Positron emission tomography in the asphyxiated term newborn: parasagittal impairment of cerebral blood flow. Ann Neurol 17:287-296
102. Shankaran S, Kottamasu SR, Kuhns L 1993 Brain sonography, computed tomography, and single-photon emission computed tomography in term neonates with perinatal asphyxia. Clin Perinatol 20:379-394
103. Wyatt JS, Edwards AD, Azzopardi D, Reynolds EO 1989 Magnetic resonance and near infrared spectroscopy for investigation of perinatal hypoxic-ischaemic brain injury. Arch Dis Child 64:953-963
104. Azzopardi D, Wyatt JS, Cady EB, Delpy DT, Baudin J, Stewart AL, Hope PL, Hamilton PA, Reynolds EO 1989 Prognosis of newborn infants with hypoxic-ischemic brain injury assessed by phosphorus magnetic resonance spectroscopy. Pediatr Res 25:445-451
105. Volpe, JJ 1995 Neurology of the Newborn, 3rd ed. WB Saunders, Philadelphia, pp 260-369
106. Rademakers RP, van der Knaap MS, Verbeeten Jr B, Barth PG, Valk J 1995 Central cortico-subcortical involvement: a distinct pattern of brain damage caused by perinatal and postnatal asphyxia in term infants. J Comput Assist Tomogr 19:256-263
107. Barkovich AJ, Westmark K, Partridge C, Sola A, Ferriero DM 1995 Perinatal asphyxia: MR findings in the first 10 days. AJNR 16:427-438
108. Dugan LL, Choi DW 1994 Excitotoxicity, free radicals, and cell membrane changes. Ann Neurol 35:S17-S21
109. Lipton SA, Rosenberg PA 1994 Mechanisms of disease: excitatory amino acids as a final common pathway for neurological disorders. N Engl J Med 330:613-622
110. Choi DW 1995 Calcium: still center-stage in hypoxic-ischemic neuronal cell death. Trends Neurosci 18:58-60
111. Pellegrini-Giampietro DE, Cherici G, Alesiani M, Carla F, Moroni F 1988 Excitatory amino acid release from rat hippocampal slices as a consequence of free-radical formation. J Neurochem 51:1960-1963
112. Lafon-Cazal M, Pietri S, Culcasi M, Bockaert J 1993 NMDA-dependent superoxide production and neurotoxicity. Nature 364:535-537
113. Uyama O, Matsuyama T, Michishita H, Nakamura H, Sugita M 1992 Protective effects of human recombinant superoxide dismutase on transient ischemic injury of CA1 neurons in gerbils. Stroke 23:75-81
114. Rosenbaum DM, Kalberg J, Kessler JA 1994 Superoxide dismutase ameliorates neuronal death from hypoxia in culture. Stroke 25:857-863
115. Dawson VL, Dawson TM, London ED, Bredt DS, Snyder SH 1991 Nitric oxide mediates glutamate neurotoxicity in primary cortical cultures. Proc Natl Acad Sci USA 88:6368-6371
116. Lipton SA, Choi Y-B, Pan Z-H, Lei SZ, Chen H-SV, Sucher NJ, Loscalzo J, Singel DJ, Stamler JS 1993 A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso compounds. Nature 364:626-632
117. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA 1990 Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87:1620-1624
118. 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
119. Ankarcrona M, Dypbukt JM, Bonfoco E, Zhivotovsky B, Orrenius S, Lipton SA, Nicotera P 1995 Glutamate-induced neuronal death: a succession of necrosis or apoptosis depending on mitochondrial function. Neuron 15:961-973
120. Tominaga T, Kure S, Narisawa K, Yoshimoto T 1993 Endonuclease activation following focal ischemic injury in the rat brain. Brain Res 608:21-26
121. 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
122. 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
123. Linnik MD, Zahos 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
124. Li Y, Chopp M, Jiang N, Zhang ZG, Zaloga C 1995 Induction of DNA fragmentation after 10 to 120 minutes of focal cerebral ischemia in rats. Stroke 26:1252-1258
125. Mehmet H, Yue X, Squier MV, Lorek A, Cady E, Penrice J, Sarraf C, Wylezinska M, Kirkbridge V, Cooper C, Brown GC, Wyatt JS, Reynolds EOR, Edwards AD 1994 Increased apoptosis in the cingulate sulcus of newborn piglets following transient hypoxia-ischemia is related to the degree of high energy phosphate depletion during the insult. Neurosci Lett 181:121-125
126. Ratan RR, Murphy TH, Baraban JM 1994 Oxidative stress induces apoptosis in embryonic cortical neurons. J Neurochem 62:376-379
127. Rosenbaum DM, Michaelson M, Batter DK, Doshi P, Kessler JA 1994 Evidence for hypoxia-induced, programmed cell death of cultured neurons. Ann Neurol 36:864-870
128. Hockenbery DM, Oltvai ZN, Yin X-M, Milliman CL, Korsmeyer SJ 1993 Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241-251
129. Zhong L, Kane DJ, Bredesen DE 1993 BCL-2 blocks glutamate toxicity in neural cell lines. Mol Brain Res 19:353-355
130. Behl C, Hovey LI, Krajewski S, Schubert D, Reed J 1993 Bcl-2 prevents killing of neuronal cells by glutamate but not by amyloid beta protein. Biochem Biophys Res Commun 197:949-956
131. An G, Lin T-N, Liu J-S, Xue J-J, He Y-Y, Hsu CY 1993 Expression of c-fos and c-jun family genes after focal cerebral ischemia. Ann Neurol 33:457-464
132. Brand T, Sharma HS, Fleischmann KE, Duncker DJ, McFalls EO, Verdouw PD, Schaper W 1992 Proto-oncogene expression in porcine myocardium subjected to ischemia and reperfusion. Cire Res 71:1351-1360
133. Witzgall R, Brown D, Schwarz C, Bonventre JV 1994 Localization of proliferating cell nuclear antigen, vimentin, c-Fos, and clusterin in the postischemic kidney. Evidence for a heterogenous genetic response among nephron segments, and a large pool of mitotically active and dedifferentiating cells. J Clin Invest 93:2175-2188
134. Pombo CM, Bonventre JV, Avruch J, Woodgett JR, Kyriakis JM, Force T 1994 The stress-activated protein kinases are major c-jun amino-terminal kinases activated by ischemia and reperfusion. J Biol Chem 269:26546-26551
135. Morooka H, Bonventre JV, Pombo CM, Kyriakis JM, Force T 1995 Ischemia and reperfusion enhance ATF-2 and c-jun binding to cAMP response elements and to an AP-1 binding site from the c-jun promoter. J Biol Chem 270:30084-30092
136. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson Jr EM 1994 Altered gene expression in neurons during programmed cell death: identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 127:1717-1727
137. Lindvall O, Ernfors P, Bengzon J, Kokaia Z, Smith M-L, Siesjö BK, Persson H 1992 Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor, and neurotrophin 3 in the adult rat brain following cerebral ischemia and hypoglycemic coma. Proc Natl Acad Sci USA 89:648-652
138. Rangan U, Bulkley GB 1993 Prospects for treatment of free radical-mediated tissue injury. Br Med Bull 49:700-718