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The Journal of Neuroscience, May 9, 2007, 27(19):5012-5022; doi:10.1523/JNEUROSCI.4725-06.2007

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Development/Plasticity/Repair
Distinct cis-Regulatory Elements from the Dlx1/Dlx2 Locus Mark Different Progenitor Cell Populations in the Ganglionic Eminences and Different Subtypes of Adult Cortical Interneurons

Noël Ghanem,¹ Man Yu,¹ Jason Long,² Gary Hatch,¹ John L. R. Rubenstein,² and Marc Ekker¹

¹Centre for Advanced Research in Environmental Genomics, Department of Biology, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5, and ²Nina Ireland Laboratory of Developmental Neurobiology, Centre for Neurobiology and Psychiatry Genetics, Department of Psychiatry, University of California, San Francisco, San Francisco, California 94143

Correspondence should be addressed to Marc Ekker, Department of Biology, University of Ottawa, 30 Marie Curie, Ottawa, Ontario, Canada K1N 6N5. Email: mekker{at}uottawa.ca

Distinct subtypes of cortical GABAergic interneurons provide inhibitory signals that are indispensable for neural network function. The Dlx homeobox genes have a central role in regulating their development and function. We have characterized the activity of three cis-regulatory sequences involved in forebrain expression of vertebrate Dlx genes: upstream regulatory element 2 (URE2), I12b, and I56i. The three regulatory elements display regional and temporal differences in their activities within the lateral ganglionic eminence (LGE), medial ganglionic eminence (MGE), and caudal ganglionic eminence (CGE) and label distinct populations of tangentially migrating neurons at embryonic day 12.5 (E12.5) and E13.5. We provide evidence that the dorsomedial and ventral MGE are distinct sources of tangentially migrating neurons during midgestation. In the adult cortex, URE2 and I12b/I56i are differentially expressed in parvalbumin-, calretinin-, neuropeptide Y-, and neuronal nitric oxide synthase-positive interneurons; I12b and I56i were specifically active in somatostatin-, vasoactive intestinal peptide-, and calbindin-positive interneurons. These data suggest that interneuron subtypes use distinct combinations of Dlx1/Dlx2 enhancers from the time they are specified through adulthood.

Key words: ganglionic eminence; regionalization; migration; progenitors; enhancers; cerebral cortex; GABAergic neurons; homeobox; mice

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Received Oct. 30, 2006; revised March 7, 2007; accepted April 2, 2007.

Correspondence should be addressed to Marc Ekker, Department of Biology, University of Ottawa, 30 Marie Curie, Ottawa, Ontario, Canada K1N 6N5. Email: mekker{at}uottawa.ca

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