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The Journal of Neuroscience, September 13, 2006, 26(37):9404-9412; doi:10.1523/JNEUROSCI.2575-06.2006

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Development/Plasticity/Repair
Stromal-Derived Factor-1 (CXCL12) Regulates Laminar Position of Cajal-Retzius Cells in Normal and Dysplastic Brains

Mercedes F. Paredes,^1,2 Guangnan Li,^1,3 Omri Berger,³ Scott C. Baraban,^1,2 and Samuel J. Pleasure^1,3

¹Neuroscience Program and Departments of ²Neurosurgery and ³Neurology, University of California, San Francisco, California 94143

Correspondence should be addressed to Samuel J. Pleasure at the above address. Email: sam.pleasure{at}ucsf.edu

Normal brain development requires a series of highly complex and interrelated steps. This process presents many opportunities for errors to occur, which could result in developmental defects in the brain, clinically referred to as malformations of cortical development. The marginal zone and Cajal-Retzius cells are key players in cortical development and are established early, yet there is little understanding of the factors resulting in the disruption of the marginal zone in many types of cortical malformation syndromes. We showed previously that treatment with methylazoxymethanol in rats causes marginal zone dysplasia with displacement of Cajal-Retzius cells to deeper cortical layers. Here we establish that loss of activity of the chemokine stromal-derived factor-1 (SDF1) (CXCL12), which is expressed by the leptomeninges, is necessary and sufficient to cause marginal zone disorganization in this widely used teratogenic animal model. We also found that mice with mutations in the main receptor for SDF1 (CXCR4) have Cajal-Retzius cells displaced to deeper cortical layers. Furthermore, by inhibiting SDF1 signaling in utero by intraventricular injection of a receptor antagonist, we establish that SDF1 signaling is required for the maintenance of Cajal-Retzius cell position in the marginal zone during normal cortical development. Our data imply that cortical layering is not a static process, but rather requires input from locally produced molecular cues for maintenance, and that complex syndromes of cortical malformation as a result of environmental insults may still be amenable to explanation by interruption of specific molecular signaling pathways.

Key words: lamination; cortex; cortical dysplasia; migration; marginal zone; teratogen

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Received June 19, 2006; revised Aug. 2, 2006; accepted Aug. 2, 2006.

Correspondence should be addressed to Samuel J. Pleasure at the above address. Email: sam.pleasure{at}ucsf.edu

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