Neural crest‐like cells originate from the spinal cord during tail regeneration in adult amphibian urodeles

Benraiss, A.; Arsanto, J.‐P.; Coulon, J.; Thouveny, Y.

doi:10.1002/(sici)1097-0177(199705)209:1<15::aid-aja2>3.3.co;2-c

Cited by 9 publications

(12 citation statements)

References 31 publications

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“…The terminal vesicle has in fact long been characterized as a region where an epithelial to mesenchymal transition occurs, and where cells are proposed to delaminate from the ependymal tube to join the surrounding blastema tissue (Benraiss et al, 1997;Egar and Singer, 1972;O'Hara et al, 1992). Our eGFP + spinal cord transplantation and the eGFP + embryonic neural tube grafting experiments allowed us to confirm that cells escape the regenerating spinal cord from this region, as we observe trails of cells emanating from the posterior-dorsal wall of the terminal vesicle.…”

Section: Contribution Of Spinal Cord Cells To Tissues Outside Of the supporting

confidence: 52%

“…The epithelial to mesenchymal transition is reminiscent of embryonic neural crest. Benraiss et al, using biolistic transfection of an alkaline phosphatase expression vector into the newt spinal cord, found alkaline phosphatase-expressing cells emanating from the ependymal tube (Benraiss et al, 1997). At later timepoints alkaline phosphatase expression was observed in melanophores and Schwann cells.…”

Section: Contribution Of Spinal Cord Cells To Tissues Outside Of the mentioning

confidence: 99%

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A clonal analysis of neural progenitors during axolotl spinal cord regeneration reveals evidence for both spatially restricted and multipotent progenitors

et al. 2007

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Complete regeneration of the spinal cord occurs after tail regeneration in urodele amphibians such as the axolotl. Little is known about how neural progenitor cells are recruited from the mature tail, how they populate the regenerating spinal cord, and whether the neural progenitor cells are multipotent. To address these issues we used three types of cell fate mapping. By grafting green fluorescent protein-positive (GFP + ) spinal cord we show that a 500 m region adjacent to the amputation plane generates the neural progenitors for regeneration. We further tracked single nuclear-GFP-labeled cells as they proliferated during regeneration, observing their spatial distribution, and ultimately their expression of the progenitor markers PAX7 and PAX6. Most progenitors generate descendents that expand along the anterior/posterior (A/P) axis, but remain close to the dorsal/ventral (D/V) location of the parent. A minority of clones spanned multiple D/V domains, taking up differing molecular identities, indicating that cells can execute multipotency in vivo. In parallel experiments, bulk labeling of dorsally or ventrally restricted progenitor cells revealed that ventral cells at the distal end of the regenerating spinal cord switch to dorsal cell fates. Analysis of PAX7 and PAX6 expression along the regenerating spinal cord indicated that these markers are expressed in dorsal and lateral domains all along the spinal cord except at the distal terminus. These results suggest that neural progenitor identity is destabilized or altered in the terminal vesicle region, from which clear migration of cells into the surrounding blastema is also observed.

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Section: Contribution Of Spinal Cord Cells To Tissues Outside Of the supporting

confidence: 52%

Section: Contribution Of Spinal Cord Cells To Tissues Outside Of the mentioning

confidence: 99%

A clonal analysis of neural progenitors during axolotl spinal cord regeneration reveals evidence for both spatially restricted and multipotent progenitors

et al. 2007

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“…Ependymal cells undergo intense mitotic activity during spinal cord regeneration, as demonstrated by using bromodeoxyuridine as a marker for DNA synthesis (Nordlander and Singer, 1978;Singer et al, 1979). It has also been suggested that radial glial cells can generate all of the cell types in newt spinal cord (Benraiss et al, 1997). In line with the above evi- Fig.…”

Section: O L O Rmentioning

confidence: 59%

“…Some tailed amphibians, such as Axolotl, have the capacity to regenerate the spinal cord after injury (Holder and Clarke, 1988;Benraiss et al, 1997). If the same were true of Necturus, information about the function of specific neuron groups in the intact animals would provide a critical background for studying the specificity of circuit formation during and after regeneration.…”

Section: Discussionmentioning

confidence: 99%

Morphology of brachial segments in mudpuppy (Necturus maculosus) spinal cord studied with confocal and electron microscopy

Jovanovic

Burke

2004

J of Comparative Neurology

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The isolated brachial spinal cord of Necturus maculosus is useful for studies of neural networks underlying forelimb locomotion, but information about its cellular morphology is scarce. We addressed this issue by using confocal and electron microscopy. Remarkably, the central region of gray matter was aneural and consisted exclusively of a tenuous meshwork of glial fibers and large extracellular spaces. Somata of motoneurons (MNs) and interneurons (INs), labeled by retrograde transport of fluorescent tracers from ventral roots and axons in the ventrolateral funiculus, respectively, were confined within a gray neuropil layer abutting the white matter borders, whereas their dendrites projected widely throughout the white matter. About one-third of labeled INs were found contralaterally, with axons crossing ventral to a thick layer of ependyma surrounding the central canal. Lateral MN dendrites proliferated under the pial surface to form a dense, thin (1-2 m) plexus immediately beneath a thin layer of glial fibrillary acidic protein-positive glia limitans. The latter contained arrays of unusual tubular structures (diameter 200 -400 nm, length 3 m) that resembled mitochondria but lacked double membranes or cristae. Dorsal roots (DRs) produced dense presynaptic arbors within a wedge-shaped afferent termination zone medial to the dorsal root entry, within which dendrites of MNs and INs mingled with dense collections of synaptic boutons. Our data suggest that a major fraction of synaptic interactions takes place within the white matter. This study provides a detailed foundation for designing electrophysiological experiments to study the neural circuits involved in locomotor pattern generation.

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“…Interestingly, a recent work has supported the view that multipotent cells are still present in the SC of adult urodeles (Benraiss et al, 1996). Ependymoglial cells in the adult newt SC may be considered as pluripotent stem cells, which can be recruited for both CNS and PNS regeneration (Benraiss et al, 1996(Benraiss et al, , 1997. The continued expression of Fig.…”

Section: Graded Axial Expression Patterns Of Pwnt Genes In Adult Scmentioning

confidence: 89%

Possible roles for Wnt genes in growth and axial patterning during regeneration of the tail in urodele amphibians

1997

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Urodele amphibians are nearly the only adult vertebrates able to regenerate their missing or amputated tail. An interesting aspect of this biological model lies in the ability of regenerates to differentiate the spinal cord (SC), the vertebral cartilage, and muscles. The main questions addressed in this study concern the possible roles of Wnt genes in these regenerative processes. We have previously reported the expression pattern of a Pleurodeles Waltl wnt‐10a gene (Pwnt‐10a) in tail blastema (Caubit et al. [1997] Dev. Dyn. 208:139–148). We report here the cloning and tissue distribution of three additional Wnt genes (Pwnt‐5a, Pwnt‐5b, and Pwnt‐7a) in adult and regenerating tail tissues and in the central nervous system (CNS) of adult newt. In adult and regenerating tails, Pwnt‐5a and Pwnt‐5b transcripts exhibit a graded distribution along the antero‐posterior (A‐P) axis, the maximal accumulation of these transcripts being detected in the mesenchyme within the subectodermal apical region of the normal tail and blastema. In contrast to Pwnt‐5a and Pwnt‐5b, Pwnt‐7a is expressed in adult normal tail skin and in the epidermis of the regenerating tail. In the adult CNS, Pwnt‐5a, Pwnt‐5b, Pwnt‐7a, and Pwnt‐10a genes are expressed in sharp overlapping but not identical domains along the A‐P axis. The sustained expression of Wnt genes in the adult newt and the spatial distribution of transcripts in adult and regenerating tail tissues suggest roles of these genes in continuous growth capacities in the urodeles and may explain the ability for CNS and tail regeneration. Dev. Dyn. 1997;210:1–10. © 1997 Wiley‐Liss, Inc.

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Neural crest‐like cells originate from the spinal cord during tail regeneration in adult amphibian urodeles

Abstract: Using in vitro cell-marking experiments and transplantation in tail regener

Cited by 9 publications

References 31 publications

A clonal analysis of neural progenitors during axolotl spinal cord regeneration reveals evidence for both spatially restricted and multipotent progenitors

A clonal analysis of neural progenitors during axolotl spinal cord regeneration reveals evidence for both spatially restricted and multipotent progenitors

Morphology of brachial segments in mudpuppy (Necturus maculosus) spinal cord studied with confocal and electron microscopy

Possible roles for Wnt genes in growth and axial patterning during regeneration of the tail in urodele amphibians

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