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© The Rockefeller University Press, 0021-9525/1998//191 $5.00
The Journal of Cell Biology, Volume 142, Number 1, , 1998 191-202


Articles

Unique Responses of Differentiating Neuronal Growth Cones to Inhibitory Cues Presented by Oligodendrocytes



A. Shibata*, M.V. Wright{ddagger}, S. David, L. McKerracher**, P.E. Braun||, and S.B. Kater§

* Department of Anatomy and Neurobiology, Colorado State University, Fort Collins, Colorado; {ddagger} Division of Science, Truman State University, Kirksville, Missouri; § Department of Neurobiology and Anatomy, University of Utah School of Medicine, Salt Lake City, Utah; || Department of Biochemistry, McGill University, Montréal, Canada; Centre for Research in Neuroscience, Montréal General Hospital Research Institute, Montréal, Canada; and ** Department dé Pathologie, Université de Montréal, Montréal, Canada

During central nervous system development, neurons differentiate distinct axonal and dendritic processes whose outgrowth is influenced by environmental cues. Given the known intrinsic differences between axons and dendrites and that little is known about the response of dendrites to inhibitory cues, we tested the hypothesis that outgrowth of differentiating axons and dendrites of hippocampal neurons is differentially influenced by inhibitory environmental cues. A sensitive growth cone behavior assay was used to assess responses of differentiating axonal and dendritic growth cones to oligodendrocytes and oligodendrocyte- derived, myelin-associated glycoprotein (MAG). We report that >90% of axonal growth cones collapsed after contact with oligodendrocytes. None of the encounters between differentiating, MAP-2 positive dendritic growth cones and oligodendrocytes resulted in growth cone collapse. The insensitivity of differentiating dendritic growth cones appears to be acquired since they develop from minor processes whose growth cones are inhibited (nearly 70% collapse) by contact with oligodendrocytes. Recombinant MAG(rMAG)-coated beads caused collapse of 72% of axonal growth cones but only 29% of differentiating dendritic growth cones. Unlike their response to contact with oligodendrocytes, few growth cones of minor processes were inhibited by rMAG-coated beads (20% collapsed). These results reveal the capability of differentiating growth cones of the same neuron to partition the complex molecular terrain they navigate by generating unique responses to particular inhibitory environmental cues.

Key Words: neuronal growth cones • inhibition • oligodendrocytes • myelin-associated glycoprotein • differentiation



Abbreviations used in this paper: CNS, central nervous system; DIV, days in vitro; Gal-C, galactocerebroside; GS, goat serum; MAP, microtubule-associated protein; MAG, myelin-associated glycoprotein; RT, room temperature.

This research was supported by a National Institute of Mental Health predoctoral fellowship (5 F31 MH10860-02, NS 24683) and the Neuroscience Network (Canada).

Address all correspondence to Annemarie Shibata, Ph.D., The Eppley Institute for Research in Cancer and Allied Diseases, 600 South 42nd Street, Box 986805, Omaha, NE 68198-6805. Tel.: (402) 559-8271. Fax: (402) 559-4651. E-mail: ashibata{at}unmc.edu



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