The guidance molecule Semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons

D. E. Wright, F. A. White, R. W. Gerfen, I. Silos‐Santiago, William Snider

Research output: Contribution to journalArticle

131 Citations (Scopus)

Abstract

The protein collapsin was purified from chick brain on the basis of its ability to inhibit sensory neuron growth cones, implicating this molecule in sensory axon guidance (Luo et al. [1993] Cell 75:217–227). To examine the relationship between collapsin and sensory axon growth, we examined the pattern of mRNA expression of collapsin's mammalian paralogue, Semaphorin III (Sema III), and compared it to dorsal root ganglion (DRG) axon pathways in the developing rat embryo. Centrally, DRG axons enter the spinal cord by embryonic (E) 11 and branch into the gray matter by E 15 in brachial and thoracic regions. Laminar specific targets are reached by E17. Between E13 and E17, Sema III mRNA is expressed at high levels in the entire ventral half of the spinal cord except the floor plate. This pattern suggests that Sema III may inhibit non‐proprioceptive sensory axons from penetrating the ventral spinal cord. Peripherally, sensory axons have entered the anterior sclerotome by E 11 at all rostrocaudal levels. At this age, Sema III mRNA is already expressed in the dermamyotome and ventral aspect of the posterior sclerotome, areas which axons pass between but do not penetrate en route to their peripheral targets. From E12 to E15, the axons lengthen and branch into smaller fascicles which extend toward peripheral targets. During this time, Sema III mRNA isexpressed by many mesodermal structures surrounding the axon fascicles, with highest levels observed in the dermamyotome, perinotochordal mesenchyme, pelvic girdle, and limb. As development proceeds, Sema III mRNA expression is quickly downregulated before disappear ing by birth. Taken together, our results demonstrate that the gene for Sema III is expressed in central and peripheral regions which are avoided by growing DRG axons. These findings are consistent with the idea tha Sema III inhibits growth and branching of axons into inappropri ate areas during development. © 1995 Wiley‐Liss, Inc.

Original languageEnglish (US)
Pages (from-to)321-333
Number of pages13
JournalJournal of Comparative Neurology
Volume361
Issue number2
DOIs
StatePublished - Oct 16 1995

Fingerprint

Semaphorins
Axons
Spinal Cord
Semaphorin-3A
Spinal Ganglia
Messenger RNA
Growth Cones
Mesoderm
Sensory Receptor Cells
Growth
Arm
Thorax
Down-Regulation
Embryonic Structures
Extremities
Parturition

Keywords

  • axon branching
  • axon guidance
  • dorsal root ganglia
  • growth cones
  • inhibitory molecule

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

The guidance molecule Semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons. / Wright, D. E.; White, F. A.; Gerfen, R. W.; Silos‐Santiago, I.; Snider, William.

In: Journal of Comparative Neurology, Vol. 361, No. 2, 16.10.1995, p. 321-333.

Research output: Contribution to journalArticle

Wright, D. E. ; White, F. A. ; Gerfen, R. W. ; Silos‐Santiago, I. ; Snider, William. / The guidance molecule Semaphorin III is expressed in regions of spinal cord and periphery avoided by growing sensory axons. In: Journal of Comparative Neurology. 1995 ; Vol. 361, No. 2. pp. 321-333.
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abstract = "The protein collapsin was purified from chick brain on the basis of its ability to inhibit sensory neuron growth cones, implicating this molecule in sensory axon guidance (Luo et al. [1993] Cell 75:217–227). To examine the relationship between collapsin and sensory axon growth, we examined the pattern of mRNA expression of collapsin's mammalian paralogue, Semaphorin III (Sema III), and compared it to dorsal root ganglion (DRG) axon pathways in the developing rat embryo. Centrally, DRG axons enter the spinal cord by embryonic (E) 11 and branch into the gray matter by E 15 in brachial and thoracic regions. Laminar specific targets are reached by E17. Between E13 and E17, Sema III mRNA is expressed at high levels in the entire ventral half of the spinal cord except the floor plate. This pattern suggests that Sema III may inhibit non‐proprioceptive sensory axons from penetrating the ventral spinal cord. Peripherally, sensory axons have entered the anterior sclerotome by E 11 at all rostrocaudal levels. At this age, Sema III mRNA is already expressed in the dermamyotome and ventral aspect of the posterior sclerotome, areas which axons pass between but do not penetrate en route to their peripheral targets. From E12 to E15, the axons lengthen and branch into smaller fascicles which extend toward peripheral targets. During this time, Sema III mRNA isexpressed by many mesodermal structures surrounding the axon fascicles, with highest levels observed in the dermamyotome, perinotochordal mesenchyme, pelvic girdle, and limb. As development proceeds, Sema III mRNA expression is quickly downregulated before disappear ing by birth. Taken together, our results demonstrate that the gene for Sema III is expressed in central and peripheral regions which are avoided by growing DRG axons. These findings are consistent with the idea tha Sema III inhibits growth and branching of axons into inappropri ate areas during development. {\circledC} 1995 Wiley‐Liss, Inc.",
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AB - The protein collapsin was purified from chick brain on the basis of its ability to inhibit sensory neuron growth cones, implicating this molecule in sensory axon guidance (Luo et al. [1993] Cell 75:217–227). To examine the relationship between collapsin and sensory axon growth, we examined the pattern of mRNA expression of collapsin's mammalian paralogue, Semaphorin III (Sema III), and compared it to dorsal root ganglion (DRG) axon pathways in the developing rat embryo. Centrally, DRG axons enter the spinal cord by embryonic (E) 11 and branch into the gray matter by E 15 in brachial and thoracic regions. Laminar specific targets are reached by E17. Between E13 and E17, Sema III mRNA is expressed at high levels in the entire ventral half of the spinal cord except the floor plate. This pattern suggests that Sema III may inhibit non‐proprioceptive sensory axons from penetrating the ventral spinal cord. Peripherally, sensory axons have entered the anterior sclerotome by E 11 at all rostrocaudal levels. At this age, Sema III mRNA is already expressed in the dermamyotome and ventral aspect of the posterior sclerotome, areas which axons pass between but do not penetrate en route to their peripheral targets. From E12 to E15, the axons lengthen and branch into smaller fascicles which extend toward peripheral targets. During this time, Sema III mRNA isexpressed by many mesodermal structures surrounding the axon fascicles, with highest levels observed in the dermamyotome, perinotochordal mesenchyme, pelvic girdle, and limb. As development proceeds, Sema III mRNA expression is quickly downregulated before disappear ing by birth. Taken together, our results demonstrate that the gene for Sema III is expressed in central and peripheral regions which are avoided by growing DRG axons. These findings are consistent with the idea tha Sema III inhibits growth and branching of axons into inappropri ate areas during development. © 1995 Wiley‐Liss, Inc.

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