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The Journal of Neuroscience, October 8, 2003, 23(27):9229-9239

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Development/Plasticity/Repair
The Transmembrane Semaphorin Sema4D/CD100, an Inhibitor of Axonal Growth, Is Expressed on Oligodendrocytes and Upregulated after CNS Lesion

Caroline Moreau-Fauvarque,^1,4 Atsushi Kumanogoh,³ Emeline Camand,^1,4 Céline Jaillard,² Gilles Barbin,² Isabelle Boquet,⁴ Christopher Love,⁵ E. Yvonne Jones,⁵ Hitoshi Kikutani,³ Catherine Lubetzki,² Isabelle Dusart,^1,4 and Alain Chédotal^1,4

¹Institut National de la Santé et de la Recherche Médicale (INSERM) U106 and ²Biologie des Interactions Neurones/Glie INSERM U495, Institut Fédératif des Neurosciences, Hôpital de la Salpêtrière, 75013 Paris, France, ³Department of Molecular Immunology, Research Institute for Microbial Diseases, Osaka University, Osaka 565-0871, Japan, ⁴Centre National de la Recherche Scientifique Unité Mixte de Recherche 7102, Université Paris 6, 75005 Paris, France, and ⁵Division of Structural Biology, Wellcome Trust Centre for Human Genetics, University of Oxford, Oxford OX3 7BN, United Kingdom

Semaphorins are a family of secreted and membrane-bound proteins, known to regulate axonal pathfinding. Sema4D, also called CD100, was first isolated in the immune system where it is involved in B and T cell activation. We found that in the mouse, Sema4D is expressed in cells throughout the CNS white matter, with a peak during the myelination period. Double-labeling experiments with different markers of oligodendrocyte lineage such as olig1, olig2, platelet-derived growth factor receptor , and proteolipid protein showed that Sema4D was expressed selectively by oligodendrocytes and myelin. The presence of Sema4D in myelin was confirmed using Western blot. Sema4D expression in myelinating oligodendrocytes was further observed using neuron-oligodendrocyte cocultures. Moreover, using stripe assay, we found that Sema4D is strongly inhibitory for postnatal sensory and cerebellar granule cell axons. This prompted us to examine whether Sema4D expression is modified after CNS injury. At 8 d after spinal cord lesions, Sema4D expression was strongly upregulated in oligodendrocytes at the periphery of the lesion. Sema4D-positive cells were not colabeled with the astrocyte marker GFAP, with the microglial and macrophagic marker isolectin B4, or with NG2, a marker of oligodendrocyte precursors. This upregulation was transient because from 1 month after the lesion, Sema4D expression was back to its normal level. These results indicate that Sema4D is a novel inhibitory factor for axonal regeneration expressed in myelin.

Key words: semaphorin; oligodendrocyte; myelin; axon; spinal cord; regeneration

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Received July 28, 2003; revised August 21, 2003; accepted August 22, 2003.

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