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The Journal of Neuroscience, January 5, 2005, 25(1):247-251; doi:10.1523/JNEUROSCI.2899-04.2005
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Pax6, Tbr2, and Tbr1 Are Expressed Sequentially by Radial Glia, Intermediate Progenitor Cells, and Postmitotic Neurons in Developing Neocortex
Chris Englund,1 Andy Fink,1 Charmaine Lau,1 Diane Pham,1 Ray A. M. Daza,1 Alessandro Bulfone,2 Tom Kowalczyk,1 andRobert F. Hevner1 1Department of Pathology, University of Washington, Seattle, Washington 98195-7470, and 2Stem Cell Research Institute, Istituto Scientifico San Raffaele, 20132 Milan, Italy
The developing neocortex contains two types of progenitor cells for glutamatergic, pyramidal-projection neurons. The first type, radial glia, produce neurons and glia, divide at the ventricular surface, and express Pax6, a homeodomain transcription factor. The second type, intermediate progenitor cells, are derived from radial glia, produce only neurons, and divide away from the ventricular surface. Here we show that the transition from radial glia to intermediate progenitor cell is associated with upregulation of Tbr2, a T-domain transcription factor, and downregulation of Pax6. Accordingly, Tbr2 expression in progenitor compartments (the subventricular zone and ventricular zone) rises and falls with cortical plate neurogenesis. The subsequent transition from intermediate progenitor cell to postmitotic neuron is marked by downregulation of Tbr2 and upregulation of Tbr1, another T-domain transcription factor. These findings delineate the transcription factor sequence Pax6
Tbr2
Key words: cerebral cortex; eomesodermin; neurogenesis; projection neurons; subventricular zone; ventricular zone
Received July 16, 2004; revised November 18, 2004; accepted November 20, 2004.
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[Abstract] [Full Text] [PDF]
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