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The Journal of Neuroscience, March 21, 2007, 27(12):3230-3243; doi:10.1523/JNEUROSCI.5265-06.2007

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Development/Plasticity/Repair
Dlx-Dependent and -Independent Regulation of Olfactory Bulb Interneuron Differentiation

Jason E. Long,¹ Sonia Garel,^1,3 Manuel Alvarez-Dolado,^2,4 Kazuaki Yoshikawa,⁵ Noriko Osumi,⁶ Arturo Alvarez-Buylla,² and John L. R. Rubenstein¹

¹Nina Ireland Laboratory of Developmental Neurobiology and ²Department of Neurological Surgery and Developmental and Stem Cell Biology Program, University of California at San Francisco, San Francisco, California 94143, ³Institut National de la Santé et de la Recherche Médicale, Unité 784, École Normale Supérieure, 75230 Paris cedex 05, France, ⁴Laboratorio de Regeneración Celular, Centro Investigación Príncipe Felipe, 46013 Valencia, Spain, ⁵Laboratory of Regulation of Neuronal Development, Institute for Protein Research, Osaka University, Suita, Osaka 565-0871, Japan, and ⁶Division of Developmental Neuroscience, Center for Translational and Advanced Animal Research, Tohoku University Graduate School of Medicine, Sendai 980-8575, Japan

Correspondence should be addressed to John L. R. Rubenstein, University of California at San Francisco, 1550 4th Street, 2nd Floor South, Room GD 282, San Francisco, CA 94158-2324. Email: john.rubenstein{at}ucsf.edu

Olfactory bulb interneuron development is a complex multistep process that involves cell specification in the ventral telencephalon, tangential migration into the olfactory bulb, and local neuronal maturation. Although several transcription factors have been implicated in this process, how or when they act remains to be elucidated. Here we explore the mechanisms that result in olfactory bulb interneuron defects in Dlx1&2^–/– (distal-less homeobox 1 and 2) and Mash1^–/– (mammalian achaete-schute homolog 1) mutants. We provide evidence that Dlx1&2 and Mash1 regulate parallel molecular pathways that are required for the generation of these cells, thereby providing new insights into the mechanisms underlying olfactory bulb development. The analysis also defined distinct anatomical zones related to olfactory bulb development. Finally we show that Dlx1&2 are required for promoting tangential migration to the olfactory bulb, potentially via regulating the expression of ErbB4 (v-erb-a erythroblastic leukemia viral oncogene homolog 4), Robo2 (roundabout homolog 2), Slit1 (slit homolog 1), and PK2 (prokineticin 2), which have all been shown to play essential roles in this migration.

Key words: GABA; interneuron; migration; olfactory bulb; forebrain; development

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Received Dec. 5, 2006; revised Feb. 7, 2007; accepted Feb. 12, 2007.

Correspondence should be addressed to John L. R. Rubenstein, University of California at San Francisco, 1550 4th Street, 2nd Floor South, Room GD 282, San Francisco, CA 94158-2324. Email: john.rubenstein{at}ucsf.edu

This article has been cited by other articles:

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