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The Journal of Neuroscience, October 31, 2007, 27(44):12012-12024; doi:10.1523/JNEUROSCI.3281-07.2007

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Development/Plasticity/Repairs
Paucity of Pericytes in Germinal Matrix Vasculature of Premature Infants

Alex Braun,¹ Hongmin Xu,² Furong Hu,² Praneeth Kocherlakota,³ Donald Siegel,³ Praveen Chander,¹ Zoltan Ungvari,⁴ Anna Csiszar,⁴ Maiken Nedergaard,⁵ and Praveen Ballabh^2,3

Departments of ¹Pathology, ²Pediatrics, ³Anatomy and Cell Biology, and ⁴Physiology, New York Medical College, Westchester Medical Center, Valhalla, New York 10595, and ⁵Neurosurgery and Center of Aging and Developmental Biology, University of Rochester, Rochester, New York 14642

Correspondence should be addressed to Dr. Praveen Ballabh, Regional Neonatal Center, Maria Fareri Children's Hospital at Westchester Medical Center, Valhalla, NY 10595. Email: pballabh{at}msn.com

Germinal matrix (GM) is a richly vascularized collection of neuronal–glial precursor cells in the developing brain, which is selectively vulnerable to hemorrhage in premature infants. It has rapid angiogenesis associated with high levels of vascular endothelial growth factor (VEGF). Because pericytes provide structural stability to blood vessels, we asked whether pericytes were fewer in the GM than in the subjacent white matter and neocortex and, if so, whether angiogenic inhibition could increase the pericyte density in the GM. We found pericyte coverage and density less in the GM vasculature than in the cortex or white matter in human fetuses, premature infants, and premature rabbit pups. Notably, although VEGF suppression significantly enhanced pericyte coverage in the GM, it remained less than in other brain regions. Therefore, to further elucidate the basis of fewer pericytes in the GM vasculature, we examined expression of ligand–receptor systems responsible for pericyte recruitment. Transforming growth factor-β1 (TGF-β1) protein expression was lower, whereas sphingosine-1-phosphate1 (S1P1) and N-cadherin levels were higher in the GM than in the cortex or white matter. Low TGF-β1 may be involved in promoting endothelial proliferation, whereas elevated S1P1 with N-cadherin may assist vascular maturation. Hence, a paucity of pericytes in the GM vasculature may contribute to its propensity to hemorrhage, and a lower expression of TGF-β1 could be a basis of reduced pericyte density in its vasculature.

Key words: GM; intraventricular hemorrhage; GM hemorrhage; pericytes; cortex; white matter; PDGF-B; PDGFR-β; TGF-β; ALK-1; ALK-5; N-cadherin; sphingosine 1 phosphate

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Received July 19, 2007; revised Sept. 9, 2007; accepted Sept. 14, 2007.

Correspondence should be addressed to Dr. Praveen Ballabh, Regional Neonatal Center, Maria Fareri Children's Hospital at Westchester Medical Center, Valhalla, NY 10595. Email: pballabh{at}msn.com

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