Unique responses of differentiating neuronal growth cones to inhibitory cues presented by oligodendrocytes

Annemarie Shibata, M. V. Wright, S. David, L. McKerracher, P. E. Braun, S. B. Kater

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

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.

Original languageEnglish
Pages (from-to)191-202
Number of pages12
JournalJournal of Cell Biology
Volume142
Issue number1
DOIs
StatePublished - Jul 13 1998
Externally publishedYes

Fingerprint

Growth Cones
Oligodendroglia
Cues
Dendrites
Myelin-Associated Glycoprotein
Neurons
Axons
Central Nervous System

All Science Journal Classification (ASJC) codes

  • Cell Biology

Cite this

Unique responses of differentiating neuronal growth cones to inhibitory cues presented by oligodendrocytes. / Shibata, Annemarie; Wright, M. V.; David, S.; McKerracher, L.; Braun, P. E.; Kater, S. B.

In: Journal of Cell Biology, Vol. 142, No. 1, 13.07.1998, p. 191-202.

Research output: Contribution to journalArticle

Shibata, Annemarie ; Wright, M. V. ; David, S. ; McKerracher, L. ; Braun, P. E. ; Kater, S. B. / Unique responses of differentiating neuronal growth cones to inhibitory cues presented by oligodendrocytes. In: Journal of Cell Biology. 1998 ; Vol. 142, No. 1. pp. 191-202.
@article{5e2fbc6618384e24978d15d0d8c15c7a,
title = "Unique responses of differentiating neuronal growth cones to inhibitory cues presented by oligodendrocytes",
abstract = "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.",
author = "Annemarie Shibata and Wright, {M. V.} and S. David and L. McKerracher and Braun, {P. E.} and Kater, {S. B.}",
year = "1998",
month = "7",
day = "13",
doi = "10.1083/jcb.142.1.191",
language = "English",
volume = "142",
pages = "191--202",
journal = "Journal of Cell Biology",
issn = "0021-9525",
publisher = "Rockefeller University Press",
number = "1",

}

TY - JOUR

T1 - Unique responses of differentiating neuronal growth cones to inhibitory cues presented by oligodendrocytes

AU - Shibata, Annemarie

AU - Wright, M. V.

AU - David, S.

AU - McKerracher, L.

AU - Braun, P. E.

AU - Kater, S. B.

PY - 1998/7/13

Y1 - 1998/7/13

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=0032514207&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0032514207&partnerID=8YFLogxK

U2 - 10.1083/jcb.142.1.191

DO - 10.1083/jcb.142.1.191

M3 - Article

VL - 142

SP - 191

EP - 202

JO - Journal of Cell Biology

JF - Journal of Cell Biology

SN - 0021-9525

IS - 1

ER -