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Featured ArticleResearch Articles, Development/Plasticity/Repair

Axon Initial Segments Are Required for Efficient Motor Neuron Axon Regeneration and Functional Recovery of Synapses

Lindsay H. Teliska, Irene Dalla Costa, Ozlem Sert, Jeffery L. Twiss and Matthew N. Rasband
Journal of Neuroscience 26 October 2022, 42 (43) 8054-8065; DOI: https://doi.org/10.1523/JNEUROSCI.1261-22.2022
Lindsay H. Teliska
1Department of Neuroscience, Baylor College of Medicine, Houston, Texas 77030
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Irene Dalla Costa
2Department of Biological Sciences, University of South Carolina, Columbia, South Carolina 29208
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Ozlem Sert
1Department of Neuroscience, Baylor College of Medicine, Houston, Texas 77030
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Jeffery L. Twiss
2Department of Biological Sciences, University of South Carolina, Columbia, South Carolina 29208
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Matthew N. Rasband
1Department of Neuroscience, Baylor College of Medicine, Houston, Texas 77030
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Abstract

The axon initial segment (AIS) generates action potentials and maintains neuronal polarity by regulating the differential trafficking and distribution of proteins, transport vesicles, and organelles. Injury and disease can disrupt the AIS, and the subsequent loss of clustered ion channels and polarity mechanisms may alter neuronal excitability and function. However, the impact of AIS disruption on axon regeneration after injury is unknown. We generated male and female mice with AIS-deficient multipolar motor neurons by deleting AnkyrinG, the master scaffolding protein required for AIS assembly and maintenance. We found that after nerve crush, neuromuscular junction reinnervation was significantly delayed in AIS-deficient motor neurons compared with control mice. In contrast, loss of AnkyrinG from pseudo-unipolar sensory neurons did not impair axon regeneration into the intraepidermal nerve fiber layer. Even after AIS-deficient motor neurons reinnervated the neuromuscular junction, they failed to functionally recover because of reduced synaptic vesicle protein 2 at presynaptic terminals. In addition, mRNA trafficking was disrupted in AIS-deficient axons. Our results show that, after nerve injury, an intact AIS is essential for efficient regeneration and functional recovery of axons in multipolar motor neurons. Our results also suggest that loss of polarity in AIS-deficient motor neurons impairs the delivery of axonal proteins, mRNAs, and other cargoes necessary for regeneration. Thus, therapeutic strategies for axon regeneration must consider preservation or reassembly of the AIS.

SIGNIFICANCE STATEMENT Disruption of the axon initial segment is a common event after nervous system injury. For multipolar motor neurons, we show that axon initial segments are essential for axon regeneration and functional recovery after injury. Our results may help explain injuries where axon regeneration fails, and suggest strategies to promote more efficient axon regeneration.

  • axon initial segment
  • cytoskeleton
  • polarity
  • regeneration

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The Journal of Neuroscience: 42 (43)
Journal of Neuroscience
Vol. 42, Issue 43
26 Oct 2022
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Axon Initial Segments Are Required for Efficient Motor Neuron Axon Regeneration and Functional Recovery of Synapses
Lindsay H. Teliska, Irene Dalla Costa, Ozlem Sert, Jeffery L. Twiss, Matthew N. Rasband
Journal of Neuroscience 26 October 2022, 42 (43) 8054-8065; DOI: 10.1523/JNEUROSCI.1261-22.2022

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Axon Initial Segments Are Required for Efficient Motor Neuron Axon Regeneration and Functional Recovery of Synapses
Lindsay H. Teliska, Irene Dalla Costa, Ozlem Sert, Jeffery L. Twiss, Matthew N. Rasband
Journal of Neuroscience 26 October 2022, 42 (43) 8054-8065; DOI: 10.1523/JNEUROSCI.1261-22.2022
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Keywords

  • axon initial segment
  • cytoskeleton
  • polarity
  • regeneration

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