Narrative Review
Published 2020-12-01
Keywords
- white matter,
- ischemic injury,
- ischemia,
- brain,
- central nervous system
- neuropathology ...More
How to Cite
1.
Alix J. The pathophysiology of ischemic injury to developing white matter. McGill J Med [Internet]. 2020 Dec. 1 [cited 2025 Oct. 6];9(2). Available from: https://mjm.mcgill.ca/article/view/616

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References
- Back, S.A., B.H. Han, N.L. Luo, et al. Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 2002; 22(2): 455-63.
- Duffy, T.E., Kohle, S.J., and Vannucci, R.C. Carbohydrate and energy metabolism in perinatal rat brain: relation to survival in anoxia. J Neurochem 1940; 24(2): 271-276.
- Kabat, H. The greater resistance of very young animals to arrest of the brain circulation. Am. J. Physiol 1940; 130: 588-599.
- Volpe, J.J. Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 2001; 50(5): 553-62.
- Lynch, J.K., D.G. Hirtz, G. DeVeber, and K.B. Nelson. Report of the National Institute of Neurological Disorders and Stroke workshop on perinatal and childhood stroke. Pediatrics 2002; 109(1): 116-23.
- Lynch, J.K. and K.B. Nelson. Epidemiology of perinatal stroke. Curr Opin Pediatr 2001; 13(6): 499-505.
- Virchow, R. Zur pathologischen Anatomie des Gehirns I. Congenitale Encephalitis und Myelitis. (In German). Virchows Arch Pathol Anat 1867; 38: 129-142.
- Banker, B.Q. and J.C. Larroche. Periventricular leukomalacia of infancy. A form of neonatal anoxic encephalopathy. Arch Neurol 1962; 7: 386-410.
- Volpe, J.J., Neurology of the Newborn. 2001: WB Saunders Company.
- Leviton, A., N. Paneth, M.L. Reuss, et al. Maternal infection, fetal inflammatory response, and brain damage in very low birth weight infants. Developmental Epidemiology Network Investigators. Pediatr Res 1999; 46(5): 566-75.
- Wu, Y.W. and J.M. Colford, Jr. Chorioamnionitis as a risk factor for cerebral palsy: A meta-analysis. JAMA 2000; 284(11): 1417-24.
- Follett, P.L., P.A. Rosenberg, J.J. Volpe, and F.E. Jensen. NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 2000; 20(24): 9235-41.
- Rees, S., M. Stringer, Y. Just, S.B. Hooper, and R. Harding. The vulnerability of the fetal sheep brain to hypoxemia at mid-gestation. Brain Res Dev Brain Res 1997; 103(2): 103-18.
- Vannucci, R.C., J.R. Connor, D.T. Mauger, et al. Rat model of perinatal hypoxic-ischemic brain damage. J Neurosci Res 1999; 55(2): 158-63.
- Yue, X., H. Mehmet, J. Penrice, et al. Apoptosis and necrosis in the newborn piglet brain following transient cerebral hypoxia-ischaemia. Neuropathol Appl Neurobiol 1997; 23(1): 16-25.
- Back, S.A. and S.A. Rivkees. Emerging concepts in periventricular white matter injury. Semin Perinatol 2004; 28(6): 405-14.
- Astrup, J., P.M. Sorensen, and H.R. Sorensen. Oxygen and glucose consumption related to Na+-K+ transport in canine brain. Stroke 1981; 12(6): 726-30.
- Rorke, L.B. Anatomical features of the developing brain implicated in pathogenesis of hypoxic-ischemic injury. Brain Pathol 1992; 2(3): 211-21.
- Altman, D.I., W.J. Powers, J.M. Perlman, P. Herscovitch, S.L.Volpe, and J.J. Volpe. Cerebral blood flow requirement for brain viability in newborn infants is lower than in adults. Ann Neurol 1988; 24(2): 218-26.
- Greisen, G. and K. Borch. White matter injury in the preterm neonate: the role of perfusion. Dev Neurosci 2001; 23(3): 209-12.
- Borch, K. and G. Greisen. Blood flow distribution in the normal human preterm brain. Pediatr Res 1998; 43(1): 28-33.
- Powers, W.J., R.L. Grubb, Jr., D. Darriet, and M.E. Raichle. Cerebral blood flow and cerebral metabolic rate of oxygen requirements for cerebral function and viability in humans. J Cereb Blood Flow Metab 1985; 5(4): 600-8.
- Tsuji, M., J.P. Saul, A. du Plessis, et al. Cerebral intravascular oxygenation correlates with mean arterial pressure in critically ill premature infants. Pediatrics 2000; 106(4): 625-32.
- Iida, K., S. Takashima, and K. Ueda. Immunohistochemical study of myelination and oligodendrocyte in infants with periventricular leukomalacia. Pediatr Neurol 1995; 13(4): 296-304.
- Paneth, N., R. Rudelli, W. Monte, et al. White matter necrosis in very low birth weight infants: neuropathologic and ultrasonographic findings in infants surviving six days or longer. J Pediatr 1990; 116(6): 975-84.
- Back, S.A., N.L. Luo, N.S. Borenstein, J.M. Levine, J.J. Volpe, and H.C. Kinney. Late oligodendrocyte progenitors coincide with the developmental window of vulnerability for human perinatal white matter injury. J Neurosci 2001; 21(4): 1302-12.
- Back, S.A., X. Gan, Y. Li, P.A. Rosenberg, and J.J. Volpe. Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci 1998; 18(16): 6241-53.
- Deng, W., P.A. Rosenberg, J.J. Volpe, and F.E. Jensen. Calcium-permeable AMPA/kainate receptors mediate toxicity and preconditioning by oxygen-glucose deprivation in oligodendrocyte precursors. Proc Natl Acad Sci USA 2003; 100(11): 6801-6.
- Fern, R. and T. Moller. Rapid ischemic cell death in immature oligodendrocytes: a fatal glutamate release feedback loop. J Neurosci 2000; 20(1): 34-42.
- Hagberg, H. Hypoxic-ischemic damage in the neonatal brain: excitatory amino acids. Dev Pharmacol Ther 1992; 18(3-4): 139-44.
- Silverstein, F.S., B. Naik, and J. Simpson. Hypoxia-ischemia stimulates hippocampal glutamate efflux in perinatal rat brain: an in vivo microdialysis study. Pediatr Res 1991; 30(6): 587-90.
- Karadottir, R., P. Cavelier, L.H. Bergersen, and D. Attwell. NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 2005; 438(7071): 1162-6.
- Salter, M.G. and R. Fern. NMDA receptors are expressed in developing oligodendrocyte processes and mediate injury. Nature 2005; 438(7071): 1167-71.
- Micu, I., Q. Jiang, E. Coderre, et al. NMDA receptors mediate calcium accumulation in myelin during chemical ischaemia. Nature 2005; 439(7079): 988-92.
- Wilke, S., R. Thomas, N. Allcock, and R. Fern. Mechanism of acute ischemic injury of oligodendroglia in early myelinating white matter: the importance of astrocyte injury and glutamate release. J Neuropathol Exp Neurol 2004; 63(8): 872-81.
- Rosenberg, P.A., W. Dai, X.D. Gan, et al. Mature myelin basic protein-expressing oligodendrocytes are insensitive to kainate toxicity. J Neurosci Res 2003; 71(2): 237-45.
- Burnashev, N., H. Monyer, P.H. Seeburg, and B. Sakmann. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 1992; 8(1): 189-98.
- Durand, G.M. and R.S. Zukin. Developmental regulation of mRNAs encoding rat brain kainate/AMPA receptors: a northern analysis study. J Neurochem 1993; 61(6): 2239-46.
- Monyer, H., N. Burnashev, D.J. Laurie, B. Sakmann, and P.H. Seeburg. Developmental and regional expression in the rat brain and functional properties of four NMDA receptors. Neuron 1994; 12(3): 529-40.
- Pellegrini-Giampietro, D.E., M.V. Bennett, and R.S. Zukin. Are Ca(2+)-permeable kainate/AMPA receptors more abundant in immature brain? Neurosci Lett 1992; 144(1-2): 65-9.
- Akins, P.T. and R.P. Atkinson. Glutamate AMPA receptor antagonist treatment for ischaemic stroke. Curr Med Res Opin 2002; 18 Suppl 2: s9-13.
- Ikonomidou, C. and L. Turski. Why did NMDA receptor antagonists fail clinical trials for stroke and traumatic brain injury? Lancet Neurol 2002; 1(6): 383-6.
- Low, S.J. and C.L. Roland. Review of NMDA antagonist-induced neurotoxicity and implications for clinical development. Int J Clin Pharmacol Ther 2004; 42(1): 1-14.
- Dingley, J., J. Tooley, H. Porter, and M. Thoresen. Xenon Provides Short-Term Neuroprotection in Neonatal Rats When Administered After Hypoxia-Ischemia. Stroke, 2005.
- Lipton, S.A. NMDA receptors, glial cells, and clinical medicine. Neuron 2006; 50(1): 9-11.
- Li, S. and P.K. Stys. Na(+)-K(+)-ATPase inhibition and depolarization induce glutamate release via reverse Na(+)-dependent transport in spinal cord white matter. Neuroscience 2001; 107(4): 675-83.
- Thomas, R., M.G. Salter, S. Wilke, et al. Acute ischemic injury of astrocytes is mediated by Na-K-Cl cotransport and not Ca2+ influx at a key point in white matter development. J Neuropathol Exp Neurol 2004; 63(8): 856-71.
- Oka, A., M.J. Belliveau, P.A. Rosenberg, and J.J. Volpe. Vulnerability of oligodendroglia to glutamate: pharmacology, mechanisms, and prevention. J Neurosci 1993; 13(4): 1441-53.
- Fellman, V. and K.O. Raivio. Reperfusion injury as the mechanism of brain damage after perinatal asphyxia. Pediatr Res 1997; 41(5): 599-606.
- Yonezawa, M., S.A. Back, X. Gan, P.A. Rosenberg, and J.J. Volpe. Cystine deprivation induces oligodendroglial death: rescue by free radical scavengers and by a diffusible glial factor. J Neurochem 1996; 67(2): 566-73.
- Lees, K.R., J.A. Zivin, T. Ashwood, et al. NXY-059 for acute ischemic stroke. N Engl J Med 2006; 354(6): 588-600.
- Fern, R. Intracellular calcium and cell death during ischemia in neonatal rat white matter astrocytes in situ. J Neurosci 1998; 18(18): 7232-43.
- Goldberg, M.P. and D.W. Choi. Combined oxygen and glucose deprivation in cortical cell culture: calcium-dependent and calcium-independent mechanisms of neuronal injury. J Neurosci 1993; 13(8): 3510-24.
- Duffy, S. and B.A. MacVicar. In vitro ischemia promotes calcium influx and intracellular calcium release in hippocampal astrocytes. J Neurosci 1996; 16(1): 71-81.
- Bondarenko, A., N. Svichar, and M. Chesler. Role of Na+-H+ and Na+-Ca2+ exchange in hypoxia-related acute astrocyte death. Glia 2005; 49(1): 143-52.
- Holgado, A. and L. Beauge. The Na(+)-Ca2+ exchange system in rat glial cells in culture: activation by external monovalent cations. Glia 1995; 14(2): 77-86.
- MacVicar, B.A. Voltage-dependent calcium channels in glial cells. Science 1984; 226(4680): 1345-7.
- Martin, L.J., A.M. Brambrink, C. Lehmann, et al. Hypoxia- ischemia causes abnormalities in glutamate transporters and death of astroglia and neurons in newborn striatum. Ann Neurol 1997; 42(3): 335-48.
- Deguchi, K., K. Oguchi, and S. Takashima. Characteristic neuropathology of leukomalacia in extremely low birth weight infants. Pediatr Neurol 1997; 16(4): 296-300.
- Farkas, E., A. Institoris, F. Domoki, A. Mihaly, P.G. Luiten, and F. Bari. Diazoxide and dimethyl sulphoxide prevent cerebral hypoperfusion-related learning dysfunction and brain damage after carotid artery occlusion. Brain Res 2004; 1008(2): 252-60.
- Haynes, R.L., R.D. Folkerth, R.J. Keefe, et al. Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol 2003; 62(5): 441-50.
- Sizonenko, S.V., J.Z. Kiss, T. Inder, P.D. Gluckman, and C.E. Williams. Distinctive neuropathologic alterations in the deep layers of the parietal cortex after moderate ischemic-hypoxic injury in the P3 immature rat brain. Pediatr Res 2005; 57(6): 865-72.
- Ridet, J.L., S.K. Malhotra, A. Privat, and F.H. Gage. Reactive astrocytes: cellular and molecular cues to biological function. Trends Neurosci 1997; 20(12): 570-7.
- Bruno, V., G. Battaglia, G. Casabona, A. Copani, F. Caciagli, and F. Nicoletti. Neuroprotection by glial metabotropic glutamate receptors is mediated by transforming growth factor-beta. J Neurosci 1998; 18(23): 9594-600.
- Dhandapani, K.M., M. Hadman, L. De Sevilla, M.F. Wade, V.B. Mahesh, and D.W. Brann. Astrocyte protection of neurons: role of transforming growth factor-beta signaling via a c-Jun-AP-1 protective pathway. J Biol Chem 2003; 278(44): 43329-39.
- D'Souza, S.D., K.A. Alinauskas, and J.P. Antel. Ciliary neurotrophic factor selectively protects human oligodendrocytes from tumor necrosis factor-mediated injury. J Neurosci Res 1996; 43(3): 289-98.
- Iwata-Ichikawa, E., Y. Kondo, I. Miyazaki, M. Asanuma, and N. Ogawa. Glial cells protect neurons against oxidative stress via transcriptional up-regulation of the glutathione synthesis. J Neurochem 1999; 72(6): 2334-44.
- Lucius, R. and J. Sievers. Postnatal retinal ganglion cells in vitro: protection against reactive oxygen species (ROS)-induced axonal degeneration by cocultured astrocytes. Brain Res 1996; 743(1-2): 56-62.
- Trendelenburg, G. and U. Dirnagl. Neuroprotective role of astrocytes in cerebral ischemia: focus on ischemic preconditioning. Glia 2005; 50(4): 307-20.
- Matute, C., M. Domercq, and M.V. Sanchez-Gomez. Glutamate- mediated glial injury: mechanisms and clinical importance. Glia 2006; 53(2): 212-24.
- Ransom, B.R. and R.K. Orkand. Glial-neuronal interactions in non-synaptic areas of the brain: studies in the optic nerve. Trends Neurosci 1996; 19(8): 352-8.
- Arai, Y., K. Deguchi, M. Mizuguchi, and S. Takashima. Expression of beta-amyloid precursor protein in axons of periventricular leukomalacia brains. Pediatr Neurol 1995; 13(2): 161-3.
- Meng, S.Z., Y. Arai, K. Deguchi, and S. Takashima. Early detection of axonal and neuronal lesions in prenatal-onset periventricular leukomalacia. Brain Dev 1997; 19(7): 480-4.
- Ohyu, J., G. Marumo, H. Ozawa, et al. Early axonal and glial pathology in fetal sheep brains with leukomalacia induced by repeated umbilical cord occlusion. Brain Dev 1999; 21(4): 248-52.
- Fern, R., P. Davis, S.G. Waxman, and B.R. Ransom. Axon conduction and survival in CNS white matter during energy deprivation: a developmental study. J Neurophysiol 1998; 79(1):
- -105.
- Stys, P.K., B.R. Ransom, S.G. Waxman, and P.K. Davis. Role of extracellular calcium in anoxic injury of mammalian central white matter. Proc Natl Acad Sci USA 1990; 87(11): 4212-6.
- Stys, P.K., S.G. Waxman, and B.R. Ransom. Ionic mechanisms of anoxic injury in mammalian CNS white matter: role of Na+ channels and Na(+)-Ca2+ exchanger. J Neurosci 1992; 12(2): 430-9.
- Fern, R., B.R. Ransom, and S.G. Waxman. Voltage-gated calcium channels in CNS white matter: role in anoxic injury. J Neurophysiol 1995; 74(1): 369-77.
- Leppanen, L. and P.K. Stys. Ion transport and membrane potential in CNS myelinated axons. II. Effects of metabolic inhibition. J Neurophysiol 1997; 78(4): 2095-107.
- Brown, A.M., R.E. Westenbroek, W.A. Catterall, and B.R. Ransom. Axonal L-type Ca2+ channels and anoxic injury in rat CNS white matter. J Neurophysiol 2001; 85(2): 900-11.
- Tekkok, S.B. and M.P. Goldberg. Ampa/kainate receptor activation mediates hypoxic oligodendrocyte death and axonal injury in cerebral white matter. J Neurosci 2001; 21(12): 4237-48.
- Tekkok SB, B.E.a.R.B. Older adult animals and the mechanisms of ischemic white matter injury. Program No. 100.12. 2005 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2005.
- B.R. Ransom, S.B.T. Perceptor pharmacology of excitotoxic injury in mouse optic nerve. in Program No. 100.13. 2005 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2005. 2005.
- Ransom, B.R. and A.M. Brown. Intracellular Ca2+ release and ischemic axon injury: the Trojan horse is back. Neuron 2003; 40(1): 2-4.
- Ouardouz, M., M.A. Nikolaeva, E. Coderre, et al. Depolarization-induced Ca2+ release in ischemic spinal cord white matter involves L-type Ca2+ channel activation of
- ryanodine receptors. Neuron 2003; 40(1): 53-63.