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The Journal of Neuroscience, April 19, 2006, 26(16):4359-4369; doi:10.1523/JNEUROSCI.1898-05.2006

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Neurobiology of Disease
Neural Stem/Progenitor Cells Participate in the Regenerative Response to Perinatal Hypoxia/Ischemia

Ryan J. Felling,¹ Matthew J. Snyder,¹ Michael J. Romanko,¹ Raymond P. Rothstein,² Amber N. Ziegler,¹ Zhengang Yang,² Maria I. Givogri,³ Ernesto R. Bongarzone,³ and Steven W. Levison^1,2

¹Department of Neural and Behavioral Sciences, Pennsylvania State University College of Medicine, Hershey, Pennsylvania 17033, ²Department of Neurology and Neuroscience, University of Medicine and Dentistry of New Jersey–New Jersey Medical School, Newark, New Jersey 07103, and ³San Raffaele Telethon Institute for Gene Therapy, 20132 Milan, Italy

Correspondence should be address to Dr. Steven W. Levison, Laboratory for Regenerative Neurobiology, Department of Neurology and Neuroscience, University of Medicine and Dentistry of New Jersey–New Jersey Medical School, 185 South Orange Avenue, H-506, Newark, NJ 07101. Email: steve.levison{at}umdnj.edu

Perinatal hypoxia/ischemia (H/I) is the leading cause of neurologic injury resulting from birth complications. Recent advances in critical care have dramatically improved the survival rate of infants suffering this insult, but 50% of survivors will develop neurologic sequelae such as cerebral palsy, epilepsy or cognitive deficits. Here we demonstrate that tripotential neural stem/progenitor cells (NSPs) participate in the regenerative response to perinatal H/I as their numbers increase 100% by 3 d and that they alter their intrinsic properties to divide using expansive symmetrical cell divisions. We further show that production of new striatal neurons follows the expansion of NSPs. Increased proliferation within the NSP niche occurs at 2 d after perinatal H/I, and the proliferating cells express nestin. Of those stem-cell related genes that change, the membrane receptors Notch1, gp-130, and the epidermal growth factor receptor, as well as the downstream transcription factor Hes5, which stimulate NSP proliferation and regulate stem cellness are induced before NSP expansion. The mechanisms for the reactive expansion of the NSPs reported here reveal potential therapeutic targets that could be exploited to amplify this response, thus enabling endogenous precursors to restore a normal pattern of brain development after perinatal H/I.

Key words: regeneration; cerebral palsy; Notch; self-renewal; neurogenesis; subventricular zone

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Received Jan. 21, 2005; revised March 5, 2006; accepted March 8, 2006.

Correspondence should be address to Dr. Steven W. Levison, Laboratory for Regenerative Neurobiology, Department of Neurology and Neuroscience, University of Medicine and Dentistry of New Jersey–New Jersey Medical School, 185 South Orange Avenue, H-506, Newark, NJ 07101. Email: steve.levison{at}umdnj.edu

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