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Articles, Development/Plasticity/Repair

Reassembly of Excitable Domains after CNS Axon Regeneration

Miguel A. Marin, Silmara de Lima, Hui-Ya Gilbert, Roman J. Giger, Larry Benowitz and Matthew N. Rasband
Journal of Neuroscience 31 August 2016, 36 (35) 9148-9160; DOI: https://doi.org/10.1523/JNEUROSCI.1747-16.2016
Miguel A. Marin
1Department of Neuroscience, Baylor College of Medicine, Houston, Texas 77030,
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Silmara de Lima
2Boston Children's Hospital and
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Hui-Ya Gilbert
2Boston Children's Hospital and
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Roman J. Giger
4Department of Cell and Developmental Biology, University of Michigan School of Medicine, Ann Arbor, Michigan 48109
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Larry Benowitz
2Boston Children's Hospital and
3Harvard Medical School, Boston, Massachusetts 02115, and
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Matthew N. Rasband
1Department of Neuroscience, Baylor College of Medicine, Houston, Texas 77030,
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Abstract

Action potential initiation and propagation in myelinated axons require ion channel clustering at axon initial segments (AIS) and nodes of Ranvier. Disruption of these domains after injury impairs nervous system function. Traditionally, injured CNS axons are considered refractory to regeneration, but some recent approaches challenge this view by showing robust long-distance regeneration. However, whether these approaches allow remyelination and promote the reestablishment of AIS and nodes of Ranvier is unknown. Using mouse optic nerve crush as a model for CNS traumatic injury, we performed a detailed analysis of AIS and node disruption after nerve crush. We found significant disruption of AIS and loss of nodes within days of the crush, and complete loss of nodes 1 week after injury. Genetic deletion of the tumor suppressor phosphatase and tensin homolog (Pten) in retinal ganglion cells (RGCs), coupled with stimulation of RGCs by inflammation and cAMP, dramatically enhanced regeneration. With this treatment, we found significant reestablishment of RGC AIS, remyelination, and even reassembly of nodes in regions proximal, within, and distal to the crush site. Remyelination began near the retina, progressed distally, and was confirmed by electron microscopy. Although axons grew rapidly, remyelination and nodal ion channel clustering was much slower. Finally, genetic deletion of ankyrinG from RGCs to block AIS reassembly did not affect axon regeneration, indicating that preservation of neuronal polarity is not required for axon regeneration. Together, our results demonstrate, for the first time, that regenerating CNS axons can be remyelinated and reassemble new AIS and nodes of Ranvier.

SIGNIFICANCE STATEMENT We show, for the first time, that regenerated CNS axons have the capacity to both remyelinate and reassemble the axon initial segments and nodes of Ranvier necessary for rapid and efficient action potential propagation.

  • axon
  • ion channel
  • myelin
  • regeneration
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The Journal of Neuroscience: 36 (35)
Journal of Neuroscience
Vol. 36, Issue 35
31 Aug 2016
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Reassembly of Excitable Domains after CNS Axon Regeneration
Miguel A. Marin, Silmara de Lima, Hui-Ya Gilbert, Roman J. Giger, Larry Benowitz, Matthew N. Rasband
Journal of Neuroscience 31 August 2016, 36 (35) 9148-9160; DOI: 10.1523/JNEUROSCI.1747-16.2016

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Reassembly of Excitable Domains after CNS Axon Regeneration
Miguel A. Marin, Silmara de Lima, Hui-Ya Gilbert, Roman J. Giger, Larry Benowitz, Matthew N. Rasband
Journal of Neuroscience 31 August 2016, 36 (35) 9148-9160; DOI: 10.1523/JNEUROSCI.1747-16.2016
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Keywords

  • axon
  • ion channel
  • myelin
  • regeneration

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