Sensory axon-derived neuregulin-1 is required for axoglial signaling and normal sensory function but not for long-term axon maintenance

J Neurosci. 2009 Jun 17;29(24):7667-78. doi: 10.1523/JNEUROSCI.6053-08.2009.

Abstract

Neuregulin-1 has a key role in mediating signaling between axons and Schwann cells during development. A limitation to studying its role in adulthood is the embryonic lethality of global Nrg1 gene deletion. We used the Cre-loxP system to generate transgenic mice in which neuregulin-1 is conditionally ablated in the majority of small-diameter and a proportion of large-diameter sensory neurons that have axons conducting in the C- and Adelta-fiber range, respectively. Sensory neuron-specific neuregulin-1 ablation resulted in abnormally large Remak bundles with axons clustered in "polyaxonal" pockets. The total number of axons in the sural nerve was unchanged, but a greater proportion was unmyelinated. In addition, we observed large-diameter axons that were in a 1:1 relationship with Schwann cells, surrounded by a basal lamina but not myelinated. There was no evidence of DRG or Schwann cell death; the markers of different DRG cell populations and cutaneous innervation were unchanged. These anatomical changes were reflected in a slowing of conduction velocity at the lower end of the A-fiber conduction velocity range and a new population of more rapidly conducting C-fibers that are likely to represent large-diameter axons that have failed to myelinate. Conditional neuregulin-1 ablation resulted in a reduced sensitivity to noxious mechanical stimuli. These findings emphasize the importance of neuregulin-1 in mediating the signaling between axons and both myelinating and nonmyelinating Schwann cells required for normal sensory function. Sensory neuronal survival and axonal maintenance, however, are not dependent on axon-derived neuregulin-1 signaling in adulthood.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analysis of Variance
  • Animals
  • Animals, Newborn
  • Axons / metabolism*
  • Axons / ultrastructure
  • Calcitonin Gene-Related Peptide / metabolism
  • Cells, Cultured
  • Electric Stimulation
  • Embryo, Mammalian
  • Ganglia, Spinal / cytology
  • Gene Expression Regulation / genetics
  • In Situ Nick-End Labeling / methods
  • Indoles
  • Lectins / metabolism
  • Mice
  • Mice, Knockout
  • Microscopy, Electron, Transmission / methods
  • NAV1.8 Voltage-Gated Sodium Channel
  • Nerve Fibers / physiology
  • Nerve Tissue Proteins / deficiency
  • Nerve Tissue Proteins / metabolism*
  • Neural Conduction / drug effects
  • Neural Conduction / genetics
  • Neuregulin-1
  • Neurofilament Proteins / metabolism
  • Neuroglia / physiology
  • Pain Measurement / methods
  • Pain Threshold / physiology*
  • Physical Stimulation / methods
  • Reaction Time / genetics
  • Schwann Cells / metabolism
  • Schwann Cells / physiology
  • Sensation / genetics
  • Sensation / physiology*
  • Sensory Receptor Cells / cytology*
  • Signal Transduction / genetics
  • Signal Transduction / physiology*
  • Skin / innervation
  • Sodium Channels / genetics
  • Sural Nerve / pathology
  • Sural Nerve / ultrastructure

Substances

  • Indoles
  • Lectins
  • NAV1.8 Voltage-Gated Sodium Channel
  • Nerve Tissue Proteins
  • Neuregulin-1
  • Neurofilament Proteins
  • Nrg1 protein, mouse
  • Scn10a protein, mouse
  • Sodium Channels
  • neurofilament protein H
  • DAPI
  • Calcitonin Gene-Related Peptide