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The Journal of Neuroscience, January 15, 2002, 22(2):455-463
Selective Vulnerability of Late Oligodendrocyte Progenitors to Hypoxia-Ischemia
Stephen A. Back1, 2, Byung Hee Han3, *, Ning Ling Luo1, *, Charlene A. Chricton1, Steve Xanthoudakis3, John Tam3, Kara L. Arvin4, and David M. Holtzman4, 5, 6 Departments of 1 Pediatrics and 2 Neurology, Oregon Health Sciences University, Portland, Oregon 97201, 3 Department of Pharmacology, Biochemistry and Molecular Biology, Merck Frosst Centre for Therapeutic Research, Merck Research Laboratories, Kirkland, Quebec, Canada H9H 3L1, and Departments of 4 Neurology, 5 Molecular Biology and Pharmacology and 6 Center for the Study of Nervous System Injury, Washington University School of Medicine, Saint Louis, Missouri 63110
In the premature infant, hypoxic-ischemic damage to the cerebral white matter [periventricular leukomalacia (PVL)] is a common and leading cause of brain injury that often results in chronic neurologic disability from cerebral palsy. The cellular basis for the propensity of white matter injury to occur in the developing brain and the greater resistance of the adult white matter to similar injury remains unknown. By using a neonatal rat model of hypoxic-ischemic injury, we found that the mechanism of perinatal white matter injury involved maturation-dependent vulnerability in the oligodendroctye (OL) lineage. The timing of appearance of late OL progenitors was the major developmental factor that accounted for the susceptibility of the neonatal white matter to injury. Late OL progenitors were the major OL lineage stage killed by apoptosis, whereas early OL progenitors and more mature OLs were highly resistant. The density of pyknotic late OL progenitors was significantly increased in the ischemic hemisphere (67 ± 31 cells/mm2) versus the control hemisphere (2.2 ± 0.4 cells/mm2; mean ± SEM; p = 0.05), which resulted in the death of 72 ± 6% of this OL stage. Surviving late OL progenitors displayed a reactive response in which an increase in cell density was accompanied by accelerated maturation to a P27/kip1-positive oligodendrocyte. Because we showed recently that late OL progenitors populate human cerebral white matter during the high risk period for PVL (Back et al., 2001), maturation-dependent vulnerability of OL progenitors to hypoxia-ischemia may underlie the selective vulnerability to PVL of the white matter in the premature infant.
Key words: hypoxia-ischemia; development; cell lineage; progenitor; cerebral white matter; cerebral cortex; O4 antibody; O1 antibody; NG2; immunohistochemistry; microglia; periventricular leukomalacia; prematurity; Ki-67; MIB-5; P27; actin; spectrin; cytochrome c; caspase-3
* B.H.H. and N.L.L. contributed equally to this paper.
Copyright © 2002 Society for Neuroscience 0270-6474/02/222455-09$05.00/0
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