Recruitment of postmitotic neurons into the regenerating spinal cord of urodeles

Zhang, Fang; Ferretti, Patrizia; Clarke, Jon

doi:10.1002/dvdy.10230

Cited by 36 publications

(32 citation statements)

References 34 publications

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“…Ultimately, the regenerated skeletal system (a cartilaginous cone) encloses the ependymal tube. A similar pattern of ependymal tube regeneration is observed in urodeles [19,48]. However unlike lizards, regeneration of ependymal tube in urodeles is followed by the complete restoration of the spinal cord.…”

Section: Discussionsupporting

confidence: 57%

A novel amniote model of epimorphic regeneration: the leopard gecko, Eublepharis macularius

2011

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BackgroundEpimorphic regeneration results in the restoration of lost tissues and structures from an aggregation of proliferating cells known as a blastema. Among amniotes the most striking example of epimorphic regeneration comes from tail regenerating lizards. Although tail regeneration is often studied in the context of ecological costs and benefits, details of the sequence of tissue-level events are lacking. Here we investigate the anatomical and histological events that characterize tail regeneration in the leopard gecko, Eublepharis macularius.ResultsTail structure and tissue composition were examined at multiple days following tail loss, revealing a conserved pattern of regeneration. Removal of the tail results in a consistent series of morphological and histological events. Tail loss is followed by a latent period of wound healing with no visible signs of regenerative outgrowth. During this latent period basal cells of the epidermis proliferate and gradually cover the wound. An additional aggregation of proliferating cells accumulates adjacent to the distal tip of the severed spinal cord marking the first appearance of the blastema. Continued growth of the blastema is matched by the initiation of angiogenesis, followed by the re-development of peripheral axons and the ependymal tube of the spinal cord. Skeletal tissue differentiation, corresponding with the expression of Sox9, and muscle re-development are delayed until tail outgrowth is well underway.ConclusionsWe demonstrate that tail regeneration in lizards involves a highly conserved sequence of events permitting the establishment of a staging table. We show that tail loss is followed by a latent period of scar-free healing of the wound site, and that regeneration is blastema-mediated. We conclude that the major events of epimorphic regeneration are highly conserved across vertebrates and that a comparative approach is an invaluable biomedical tool for ongoing regenerative research.

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Section: Discussionsupporting

confidence: 57%

A novel amniote model of epimorphic regeneration: the leopard gecko, Eublepharis macularius

2011

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“…The role of the FGFRs in the proliferation of neural progenitors in BS and spinal cord is currently unknown. Our findings of high levels of FGFR2 expression in BS and lower levels in the posterior segment of spinal cord support previous suggestions stating that FGF2-induced proliferation of neural progenitor cells in BS is mediated primarily by FGFR2 while proliferation in spinal cord mainly depends on FGFR1 (Zhang et al, 2003). An alternative is that FGF2 simultaneously activates FGFR1 and 2, perhaps at different points in the regeneration process.…”

Section: Ajnsupporting

confidence: 92%

“…In each case, the regenerated tail contains a complete spinal cord with sensory ganglia, motor neurons and interneurons, spinal projection neurons and spinal tracts (Nordlander and Singer, 1978;Zhang et al, 2003).…”

Section: Ajnmentioning

confidence: 99%

SPATIAL DISTRIBUTION OF FIBROBLAST GROWTH FACTOR RECEPTOR 2 IN NORMAL AND LESIONED CENTRAL NERVOUS SYSTEM OF <I>PLEURODELES WALTLII</I>

Moftah

Landry

Nagy

et al. 2012

American Journal of Neuroscience

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Fibroblast Growth Factors (FGFs) have been implicated in numerous cellular processes including proliferation, migration, differentiation and neuronal survival. One of these growth factors, Fibroblast Growth Factor 2 (FGF2), is apparently implicated in the ability of the adult salamander (Pleurodeles waltlii) to recover locomotion following complete transection of the spinal cord. In a previous study, we reported up regulation of FGF2 during regeneration of damaged axons and recovery of hind limb locomotion. In this study reported here, we investigated the spatial distribution of FGFR2-one of the receptors that mediate the effects of FGF2-using a variety of techniques, namely, western blot, immunohistochemistry and in situ hybridization. We find that in intact animals FGFR2 is mainly expressed in the most posterior part of body Spinal Cord (SC3) specifically in neurons. However, lesioning the spinal cord produces increased expression in Brainstem (BS) neurons and decreased expression in posterior parts of the spinal cord not only in neurons but also in the neuroglial ependymal cells lining the central canal. This suggests that FGF2 simultaneously activates FGFR1 and 2, perhaps at different points in the regeneration process and thus FGFR2 might play at least an indirect role in the spontaneous regeneration observed in this species and might be relevant to the treatment of spinal cord lesions in humans. Verification of this possibility will require studies of additional time points.

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“…During epimorphic tail regeneration in salamanders, ERGs, labeled by dye or electroporation of a GFP expression plasmid, generated neurons in the spinal cord, but also gave rise to tissues outside the CNS (Benraiss et al, 1999;Echeverri and Tanaka, 2002;Zhang et al, 2003). Moreover, neurospheres derived from single spinal cord cells contribute to regeneration of a variety of cell types upon transplantation into a regenerating tail, suggesting the presence of multi-potent stem cells in the salamander spinal cord that contribute to the regenerate (McHedlishvili et al, 2012).…”

Section: Types and Extent Of Neuronal Regeneration In The Cns Of Anammentioning

confidence: 97%

Neuronal Regeneration from Ependymo-Radial Glial Cells: Cook, Little Pot, Cook!

Becker

2015

Developmental Cell

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Adult fish and salamanders regenerate specific neurons as well as entire CNS areas after injury. Recent studies shed light on how these anamniotes activate progenitor cells, generate the required cell types, and functionally integrate these into a complex environment. Some developmental signals and mechanisms are recapitulated during neuronal regeneration, whereas others are unique to the regeneration process. The use of genetic techniques, such as cell ablation and lineage-tracing, in combination with cell-type-specific expression profiling reveal factors that initiate, fine-tune, and terminate the regenerative response in anamniotes, with a view to translating findings to non-regenerating species.

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Recruitment of postmitotic neurons into the regenerating spinal cord of urodeles

Cited by 36 publications

References 34 publications

A novel amniote model of epimorphic regeneration: the leopard gecko, Eublepharis macularius

A novel amniote model of epimorphic regeneration: the leopard gecko, Eublepharis macularius

SPATIAL DISTRIBUTION OF FIBROBLAST GROWTH FACTOR RECEPTOR 2 IN NORMAL AND LESIONED CENTRAL NERVOUS SYSTEM OF <I>PLEURODELES WALTLII</I>

Neuronal Regeneration from Ependymo-Radial Glial Cells: Cook, Little Pot, Cook!

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