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The Journal of Neuroscience, February 11, 2004, 24(6):1497-1506; doi:10.1523/JNEUROSCI.4729-03.2004

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Development/Plasticity/Repair
Multiple Roles for Slits in the Control of Cell Migration in the Rostral Migratory Stream

Kim T. Nguyen-Ba-Charvet,¹ Nathalie Picard-Riera,³ Marc Tessier-Lavigne,² Anne Baron-Van Evercooren,³ Constantino Sotelo,¹ and Alain Chédotal¹

¹Institut National de la Santé et de la Recherche Médicale (INSERM) U106, Bâtiment de Pédiatrie, Hôpital de la Salpêtrière, 75013 Paris, France, ²Department of Biological Sciences, Howard Hughes Medical Institute, Stanford University, Stanford, California 94305-5020, and ³INSERM U546, Centre Hospitalier Universitaire Pitie-Salpêtrière, 75013, Paris, France

The subventricular zone (SVZ) contains undifferentiated cells, which proliferate and generate olfactory bulb (OB) interneurons. Throughout life, these cells leave the SVZ and migrate along the rostral migratory stream (RMS) to the OB where they differentiate. In vitro, the septum and the choroid plexus (CP) secrete repulsive factors that could orient the migration of OB precursors. Slit1 and Slit2, two known chemorepellents for developing axons, can mimic this effect. We show here that the Slit receptors Robo2 and Robo3/Rig-1 are expressed in the SVZ and the RMS and that Slit1 and Slit2 are still present in the adult septum. Using Slit1/2-deficient mice, we found that Slit1 and Slit2 are responsible for both the septum and the CP repulsive activity in vitro. In adult mice lacking Slit1, small chains of SVZ-derived cells migrate caudally into the corpus callosum, supporting a role for Slits in orienting the migration of SVZ cells. Surprisingly, in adult mice, Slit1 was also expressed by type A and type C cells in the SVZ and RMS, suggesting that Slit1 could act cell autonomously. This hypothesis was tested using cultures of SVZ explants or isolated neurospheres from Slit1-/- or Slit1+/- mice. In both types of cultures, the migration of SVZ cells was altered in the absence of Slit1. This suggests that the regulation of the migration of OB precursors by Slit proteins is complex and not limited to repulsion.

Key words: migration; Slit; septum; choroid plexus; Robo; SVZ

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Received Oct 20, 2003; revised December 15, 2003; accepted December 23, 2003.

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