Regeneration of neural crest derivatives in the Xenopustadpole tail

Lin, Gufa; Chen, Ying; Slack, Jonathan

doi:10.1186/1471-213x-7-56

Cited by 55 publications

(58 citation statements)

References 58 publications

(61 reference statements)

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“…The completeness of PNS regeneration seems to be a unique feature of the axolotl system. Similar tail amputation experiments carried out in Xenopus tadpoles revealed the lack of defined DRG regeneration (14), perhaps because of deficient expression of various embryonic signaling factors in the frog compared with the axolotl (21).…”

Section: Discussionmentioning

confidence: 59%

“…It was shown recently that, during development, melanocytes, another neural crest derivative, arise from precursors residing in peripheral nerve fibers (13). Furthermore, in Xenopus, studies of neural crest-ablated tadpoles showed that the melanophores regenerate from preexisting unpigmented melanophore precursors in the skin adjacent to the amputation site (14). This mechanism is similar to that described for the zebrafish fin regeneration, in which melanoblasts in the skin generate the new melanophores in the regenerated fin (15).…”

Section: Spinal Cord Transplantations Suggest That Newly Formed Drg Canmentioning

confidence: 61%

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Reconstitution of the central and peripheral nervous system during salamander tail regeneration

Mchedlishvili

Mazurov

Grassme

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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We show that after tail amputation in Ambystoma mexicanum (Axolotl) the correct number and spacing of dorsal root ganglia are regenerated. By transplantation of spinal cord tissue and nonclonal neurospheres, we show that the central spinal cord represents a source of peripheral nervous system cells. Interestingly, melanophores migrate from preexisting precursors in the skin. Finally, we demonstrate that implantation of a clonally derived spinal cord neurosphere can result in reconstitution of all examined cell types in the regenerating central spinal cord, suggesting derivation of a cell with spinal cord stem cell properties.neural stem cell | segmentation | Hox R egeneration of the central body axis occurs after tail amputation in salamander amphibians. During this process the spinal cord regrows, and the correct number of segmented vertebrae and myotomes are formed (1). Additionally, neural crest derivatives, such as melanophores, and the peripheral nervous system (PNS), including dorsal root ganglia (DRG) and Schwann cells, are regenerated (2-4).An important challenge is to define and study the stem cells that are responsible for regenerating the CNS and PNS. Previously, we used electroporation of GFP expression plasmids into the spinal cord to identify and track the radial glial cells that contribute to regenerating the spinal cord in the salamander Ambystoma mexicanum (axolotl) (5, 6). Live cell tracking showed that single cells could give rise to clones populating multiple molecular domains of the regenerating spinal cord (6). These results indicated that multipotent progenitors exist during spinal cord regeneration. Because of the transient expression of the plasmids, the long-term fate of the stem cells could not be tracked, so the origin of the PNS was not addressed.The source of neural crest derivatives in the regenerated tail has been an open question since 1885 (7). During early development the neural crest arises in the dorsal region of the neural tube, from which cells emigrate to the surroundings to form neurons and glia of PNS, smooth muscles, head skeletal elements, enteric neurons, and melanophores (8). It is not yet known conclusively, however, whether during regeneration newly regenerated neural crest structures derive from a population of neural crest-like cells that migrate out of the regenerating spinal cord or arise directly from cells in the periphery. Immunohistochemical studies using markers such as HNK1 suggested that there may be a population of cells in the lateral walls of the spinal cord with neural crest properties (4). Furthermore, morphological studies suggested that cells may migrate via the forming ventral roots to populate the spinal ganglia outside the spinal cord. Such findings could be consistent with recent findings in mouse that boundary cap cells can act as a neural crest source (9). To track the origin of neural crest structures during newt tail regeneration, Benraiss et al. (3) attempted to label spinal cord cells via biolistic transfection of a human alkaline phosph...

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Section: Discussionmentioning

confidence: 59%

Section: Spinal Cord Transplantations Suggest That Newly Formed Drg Canmentioning

confidence: 61%

Reconstitution of the central and peripheral nervous system during salamander tail regeneration

Mchedlishvili

Mazurov

Grassme

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…Spinal ganglia (dorsal root ganglia), normally present as organized collections of neural crest derived sensory neurons on each somite, are almost entirely missing, and the normal segmented pattern of the spinal nerves is not reestablished in the regenerate (Filoni and Bosco, 1981). Other neural crest cell derivatives such as melanophores (pigment cells) are regenerated normally, albeit through a different mechanism (Lin et al, 2007). During development, the neural crest cells arise from a region between the neural plate and flanking epidermis, and they migrate away after the neural plate folds up into a tube to form the spinal cord.…”

Section: Box 1: Does the Tail Regenerate Via A Blastema Or Regeneratimentioning

confidence: 99%

“…During development, the neural crest cells arise from a region between the neural plate and flanking epidermis, and they migrate away after the neural plate folds up into a tube to form the spinal cord. This interaction between epidermal cells and neural plate cells does not occur during regeneration, and the replacement melanophores do not originate from regenerated neural crest but from existing precursors located in the blastema and presumably recruited from fin tissue near the stump (Lin et al, 2007).…”

Section: Box 1: Does the Tail Regenerate Via A Blastema Or Regeneratimentioning

confidence: 99%

Beyond early development: Xenopus as an emerging model for the study of regenerative mechanisms

Beck

Belmonte

Christen

2009

Developmental Dynamics

150

139

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While Xenopus is a well-known model system for early vertebrate development, in recent years, it has also emerged as a leading model for regeneration research. As an anuran amphibian, Xenopus laevis can regenerate the larval tail and limb by means of the formation of a proliferating blastema, the lens of the eye by transdifferentiation of nearby tissues, and also exhibits a partial regeneration of the postmetamorphic froglet forelimb. With the availability of inducible transgenic techniques for Xenopus, recent experiments are beginning to address the functional role of genes in the process of regeneration. The use of soluble inhibitors has also been very successful in this model. Using the more traditional advantages of Xenopus, others are providing important lineage data on the origin of the cells that make up the tissues of the regenerate. Finally, transcriptome analyses of regenerating tissues seek to identify the genes and cellular processes that enable successful regeneration.

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“…In short, the selection of these neuronal and glial markers meet the following criteria: 1) they are useful tools to analyze the axonal regrowth process in regeneration models of both the central and peripheral nervous systems; 2) they are highly conserved molecules among vertebrates; and 3) the available antibodies also stain specifically in different vertebrates, particularly in nonmammalian species: chicken (Bergmann et al, 2000;Fischer, 2005;Soukkarieh et al, 2007), lizards (Rodger et al, 2006;Santos et al, 2008), salamanders, frogs (Yang et al, 2002;Lin et al, 2007), and fish (Good, 1995). Thus, a comparison among the available regeneration models of the nervous system is easily made.…”

mentioning

confidence: 99%

Expression of neuronal markers, synaptic proteins, and glutamine synthetase in the control and regenerating lizard visual system

Romero-Aleman

Monzon-Mayor

Santos

et al. 2010

J of Comparative Neurology

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Spontaneous regrowth of retinal ganglion cell (RGC) axons occurs after optic nerve (ON) transection in the lizard Gallotia galloti. To gain more insight into this event we performed an immunohistochemical study on selected neuron and glial markers, which proved useful for analyzing the axonal regrowth process in different regeneration models. In the control lizards, RGCs were beta-III tubulin- (Tuj1) and HuCD-positive. The vesicular glutamate transporter-1 (VGLUT1) preferentially stained RGCs and glial somata rather than synaptic layers. In contrast, SV2 and vesicular GABA/glycine transporter (VGAT) labeling was restricted to both plexiform layers. Strikingly, the strong expression of glutamine synthetase (GS) in both Müller glia processes and macroglial somata revealed a high glutamate metabolism along the visual system. Upregulation of Tuj1 and HuCD in the surviving RGCs was observed at all the timepoints studied (1, 3, 6, 9, and 12 months postlesion). The significant rise of Tuj1 in the optic nerve head and optic tract (OTr) by 1 and 6 months postlesion, respectively, suggests an increase of the beta-III tubulin transport and incorporation into newly formed axons. Persistent Tuj1(+) and SV2(+) puncta and swellings were abnormally observed in putative degenerating/dystrophic fibers. Unexpectedly, neuron-like cells of obscure significance were identified in the control and regenerating ON-OTr. We conclude that: 1) the persistent upregulation of Tuj1 and HuCD favors the long-lasting axonal regrowth process; 2) the latter succeeded despite the ectopia and dystrophy of some regrowing fibers; and 3) maintenance of the glutamate-glutamine cycle contributes to the homeostasis and plasticity of the system.

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Regeneration of neural crest derivatives in the Xenopustadpole tail

Cited by 55 publications

References 58 publications

Reconstitution of the central and peripheral nervous system during salamander tail regeneration

Reconstitution of the central and peripheral nervous system during salamander tail regeneration

Beyond early development: Xenopus as an emerging model for the study of regenerative mechanisms

Expression of neuronal markers, synaptic proteins, and glutamine synthetase in the control and regenerating lizard visual system

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