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The Journal of Neuroscience, March 14, 2007, 27(11):3037-3045; doi:10.1523/JNEUROSCI.0172-07.2007

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Development/Plasticity/Repair
Robo1 and Robo2 Control the Development of the Lateral Olfactory Tract

Coralie Fouquet,^1,2 Thomas Di Meglio,^1,2 Le Ma,⁴ Takahiko Kawasaki,³ Hua Long,⁴ Tatsumi Hirata,³ Marc Tessier-Lavigne,³ Alain Chédotal,^1,2 and Kim T. Nguyen-Ba-Charvet^1,2

¹Centre National de la Recherche Scientifique and ²Université Pierre et Marie Curie-Paris 6, Unité Mixte de Recherche 7102, Paris, 75005 France, ³Division of Brain Function, National Institute of Genetics, Graduate University for advanced Studies (Sokendai), Yata 1111, Mishima 411-8540, Japan, and ⁴Howard Hughes Medical Institute, Department of Biological sciences, Stanford University, Stanford, California 94305

Correspondence should be addressed to Alain Chédotal, Centre National de la Recherche Scientifique Unité Mixte de Recherche 7102, Université Pierre et Marie Curie, Equipe Développement Neuronal, Case 12, 9 quai Saint-Bernard, 75005 Paris, France. Email: alain.chedotal{at}snv.jussieu.fr

The development of olfactory bulb projections that form the lateral olfactory tract (LOT) is still poorly understood. It is known that the septum secretes Slit1 and Slit2 which repel olfactory axons in vitro and that in Slit1^–/–;Slit2^–/– mutant mice, the LOT is profoundly disrupted. However, the involvement of Slit receptors, the roundabout (Robo) proteins, in guiding LOT axons has not been demonstrated. We show here that both Robo1 and Robo2 receptors are expressed on early developing LOT axons, but that only Robo2 is present at later developmental stages. Olfactory bulb axons from Robo1^–/–;Robo2^–/– double-mutant mice are not repelled by Slit in vitro. The LOT develops normally in Robo1^–/– mice, but is completely disorganized in Robo2^–/– and Robo1^–/–;Robo2^–/– double-mutant embryos, with many LOT axons spreading along the ventral surface of the telencephalon. Finally, the position of lot1-expressing cells, which have been proposed to be the LOT guidepost cells, appears unaffected in Slit1^–/–;Slit2^–/– mice and in Robo1^–/–;Robo2^–/– mice. Together, our results indicate that Robo1 and Robo2 directly mediate the repulsive activity of Slit receptors on LOT axons, and are required for normal guidance of these axons in vivo.

Key words: chemorepulsion; olfactory bulb; Slit; roundabout; axon guidance; midline

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Received Nov. 6, 2006; revised Feb. 13, 2007; accepted Feb. 14, 2007.

Correspondence should be addressed to Alain Chédotal, Centre National de la Recherche Scientifique Unité Mixte de Recherche 7102, Université Pierre et Marie Curie, Equipe Développement Neuronal, Case 12, 9 quai Saint-Bernard, 75005 Paris, France. Email: alain.chedotal{at}snv.jussieu.fr

This article has been cited by other articles:

				W. T. Farmer, A. L. Altick, H. F. Nural, J. P. Dugan, T. Kidd, F. Charron, and G. S. Mastick Pioneer longitudinal axons navigate using floor plate and Slit/Robo signals Development, November 15, 2008; 135(22): 3643 - 3653. [Abstract] [Full Text] [PDF]

				T. Di Meglio, K. T. Nguyen-Ba-Charvet, M. Tessier-Lavigne, C. Sotelo, and A. Chedotal Molecular Mechanisms Controlling Midline Crossing by Precerebellar Neurons J. Neurosci., June 18, 2008; 28(25): 6285 - 6294. [Abstract] [Full Text] [PDF]

				K. T. Nguyen-Ba-Charvet, T. Di Meglio, C. Fouquet, and A. Chedotal Robos and Slits Control the Pathfinding and Targeting of Mouse Olfactory Sensory Axons J. Neurosci., April 16, 2008; 28(16): 4244 - 4249. [Abstract] [Full Text] [PDF]

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