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The Journal of Neuroscience, May 20, 2009, 29(20):6677-6690; doi:10.1523/JNEUROSCI.4361-08.2009

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Cellular/Molecular
Lewis^x and 2,3-Sialyl Glycans and Their Receptors TAG-1, Contactin, and L1 Mediate CD24-Dependent Neurite Outgrowth

Annika Lieberoth,^1 * Frauke Splittstoesser,^1 * Nainesh Katagihallimath,¹ Igor Jakovcevski,¹ Gabriele Loers,¹ Barbara Ranscht,² Domna Karagogeos,³ Melitta Schachner,^1,4,5 and Ralf Kleene¹

¹Zentrum für Molekulare Neurobiologie, Universitätsklinikum Hamburg-Eppendorf, 20246 Hamburg, Germany, ²Burnham Institute for Medical Research, La Jolla, California 92037, ³Department of Basic Science, Medical School and Institute of Molecular Biology and Biotechnology, University of Crete, 71110 Heraklion, Greece, ⁴Keck Center for Collaborative Neuroscience, Rutgers University, Piscataway, New Jersey 08854, and ⁵Center for Neuroscience, Shantou University Medical College, Shantou 515041, China

Correspondence should be addressed to Melitta Schachner, Zentrum für Molekulare Neurobiologie, Universitätsklinikum Hamburg-Eppendorf, Martinistrasse 52, D-20246 Hamburg, Germany. Email: melitta.schachner{at}zmnh.uni-hamburg.de

Although carbohydrates have been implicated in cell interactions in the nervous system, the molecular bases of their functions have remained largely obscure. Here, we show that promotion or inhibition of neurite outgrowth of cerebellar or dorsal root ganglion neurons, respectively, induced by the mucin-type adhesion molecule CD24 depends on 2,3-linked sialic acid and Lewis^x present on glia-specific CD24 glycoforms. 2,3-Sialyl residues of CD24 bind to a structural motif in the first fibronectin type III domain of the adhesion molecule L1. Following the observation that the adhesion molecules TAG-1 and Contactin show sequence homologies with fucose-specific lectins, we obtained evidence that TAG-1 and Contactin mediate Lewis^x-dependent CD24-induced effects on neurite outgrowth. Thus, L1, TAG-1, and Contactin function as lectin-like neuronal receptors. Their cis interactions with neighboring adhesion molecules, e.g., Caspr1 and Caspr2, and with their triggered signal transduction pathways elicit cell type-specific promotion or inhibition of neurite outgrowth induced by glial CD24 in a glycan-dependent trans interaction.

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Received Sept. 12, 2008; revised Feb. 24, 2009; accepted March 3, 2009.

Correspondence should be addressed to Melitta Schachner, Zentrum für Molekulare Neurobiologie, Universitätsklinikum Hamburg-Eppendorf, Martinistrasse 52, D-20246 Hamburg, Germany. Email: melitta.schachner{at}zmnh.uni-hamburg.de

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