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Perineurial glia are essential for motor axon regrowth following nerve injury.

ABSTRACT: Development and maintenance of the peripheral nervous system (PNS) are essential for an organism to survive and reproduce, and damage to the PNS by disease or injury is often debilitating. Remarkably, the nerves of the PNS are capable of regenerating after trauma. However, full functional recovery after nerve injuries remains poor. Peripheral nerve regeneration has been studied extensively, with particular emphasis on elucidating the roles of Schwann cells and macrophages during degeneration and subsequent regeneration. In contrast, the roles of other essential nerve components, including perineurial glia, are poorly understood. Here, we use laser nerve transection and in vivo, time-lapse imaging in zebrafish to investigate the role and requirement of perineurial glia after nerve injury. We show that perineurial glia respond rapidly and dynamically to nerve transections by extending processes into injury sites and phagocytizing debris. Perineurial glia also bridge injury gaps before Schwann cells and axons, and we demonstrate that these bridges are essential for axon regrowth. Additionally, we show that perineurial glia and macrophages spatially coordinate early debris clearance and that perineurial glia require Schwann cells for their attraction to injury sites. This work highlights the complex nature of cell-cell interactions after injury and introduces perineurial glia as integral players in the regenerative process.

SUBMITTER: Lewis GM

PROVIDER: S-EPMC4166161 | biostudies-literature | 2014 Sep

REPOSITORIES: biostudies-literature

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Perineurial glia are essential for motor axon regrowth following nerve injury.

Lewis Gwendolyn M GM Kucenas Sarah S

The Journal of neuroscience : the official journal of the Society for Neuroscience 20140901 38

Development and maintenance of the peripheral nervous system (PNS) are essential for an organism to survive and reproduce, and damage to the PNS by disease or injury is often debilitating. Remarkably, the nerves of the PNS are capable of regenerating after trauma. However, full functional recovery after nerve injuries remains poor. Peripheral nerve regeneration has been studied extensively, with particular emphasis on elucidating the roles of Schwann cells and macrophages during degeneration and ...[more]

PMID: 25232113

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Project description:Peripheral nerve transection and neuroma-in-continuity injuries are associated with permanent functional deficits, often despite successful end-organ reinnervation. Axonal misdirection with non-specific reinnervation, frustrated regeneration and axonal attrition are believed to be among the anatomical substrates that underlie the poor functional recovery associated with these devastating injuries. Yet, functional deficits associated with axonal misdirection in experimental neuroma-in-continuity injuries have not yet been studied. We hypothesized that experimental neuroma-in-continuity injuries would result in motor axon misdirection and attrition with proportional persistent functional deficits. The femoral nerve misdirection model was exploited to assess major motor pathway misdirection and axonal attrition over a spectrum of experimental nerve injuries, with neuroma-in-continuity injuries simulated by the combination of compression and traction forces in 42 male rats. Sciatic nerve injuries were employed in an additional 42 rats, to evaluate the contribution of axonal misdirection to locomotor deficits by a ladder rung task up to 12 weeks. Retrograde motor neuron labeling techniques were utilized to determine the degree of axonal misdirection and attrition. Characteristic histological neuroma-in-continuity features were demonstrated in the neuroma-in-continuity groups and poor functional recovery was seen despite successful nerve regeneration and muscle reinnervation. Good positive and negative correlations were observed respectively between axonal misdirection (p<.0001, r(2)=.67), motor neuron counts (attrition) (p<.0001, r(2)=.69) and final functional deficits. We demonstrate prominent motor axon misdirection and attrition in neuroma-in-continuity and transection injuries of mixed motor nerves that contribute to the long-term functional deficits. Although widely accepted in theory, to our knowledge, this is the first experimental evidence to convincingly demonstrate these correlations with data inclusive of the neuroma-in-continuity spectrum. This work emphasizes the need to focus on strategies that promote both robust and accurate nerve regeneration to optimize functional recovery. It also demonstrates that clinically relevant neuroma-in-continuity injuries can now also be subjected to experimental investigation.

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Perineurial glia are essential for motor axon regrowth following nerve injury.

Publications

Perineurial glia are essential for motor axon regrowth following nerve injury.

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