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Long-Distance Signals Are Required for Morphogenesis of the Regenerating Xenopus Tadpole Tail, as Shown by Femtosecond-Laser Ablation

BACKGROUND: With the goal of learning to induce regeneration in human beings as a treatment for tissue loss, research is being conducted into the molecular and physiological details of the regeneration process. The tail of Xenopus laevis tadpoles has recently emerged as an important model for these...

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Autores principales: Mondia, Jessica P., Levin, Michael, Omenetto, Fiorenzo G., Orendorff, Ryan D., Branch, Mary Rose, Adams, Dany Spencer
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3174989/
https://www.ncbi.nlm.nih.gov/pubmed/21949803
http://dx.doi.org/10.1371/journal.pone.0024953
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author Mondia, Jessica P.
Levin, Michael
Omenetto, Fiorenzo G.
Orendorff, Ryan D.
Branch, Mary Rose
Adams, Dany Spencer
author_facet Mondia, Jessica P.
Levin, Michael
Omenetto, Fiorenzo G.
Orendorff, Ryan D.
Branch, Mary Rose
Adams, Dany Spencer
author_sort Mondia, Jessica P.
collection PubMed
description BACKGROUND: With the goal of learning to induce regeneration in human beings as a treatment for tissue loss, research is being conducted into the molecular and physiological details of the regeneration process. The tail of Xenopus laevis tadpoles has recently emerged as an important model for these studies; we explored the role of the spinal cord during tadpole tail regeneration. METHODS AND RESULTS: Using ultrafast lasers to ablate cells, and Geometric Morphometrics to quantitatively analyze regenerate morphology, we explored the influence of different cell populations. For at least twenty-four hours after amputation (hpa), laser-induced damage to the dorsal midline affected the morphology of the regenerated tail; damage induced 48 hpa or later did not. Targeting different positions along the anterior-posterior (AP) axis caused different shape changes in the regenerate. Interestingly, damaging two positions affected regenerate morphology in a qualitatively different way than did damaging either position alone. Quantitative comparison of regenerate shapes provided strong evidence against a gradient and for the existence of position-specific morphogenetic information along the entire AP axis. CONCLUSIONS: We infer that there is a conduit of morphology-influencing information that requires a continuous dorsal midline, particularly an undamaged spinal cord. Contrary to expectation, this information is not in a gradient and it is not localized to the regeneration bud. We present a model of morphogenetic information flow from tissue undamaged by amputation and conclude that studies of information coming from far outside the amputation plane and regeneration bud will be critical for understanding regeneration and for translating fundamental understanding into biomedical approaches.
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spelling pubmed-31749892011-09-26 Long-Distance Signals Are Required for Morphogenesis of the Regenerating Xenopus Tadpole Tail, as Shown by Femtosecond-Laser Ablation Mondia, Jessica P. Levin, Michael Omenetto, Fiorenzo G. Orendorff, Ryan D. Branch, Mary Rose Adams, Dany Spencer PLoS One Research Article BACKGROUND: With the goal of learning to induce regeneration in human beings as a treatment for tissue loss, research is being conducted into the molecular and physiological details of the regeneration process. The tail of Xenopus laevis tadpoles has recently emerged as an important model for these studies; we explored the role of the spinal cord during tadpole tail regeneration. METHODS AND RESULTS: Using ultrafast lasers to ablate cells, and Geometric Morphometrics to quantitatively analyze regenerate morphology, we explored the influence of different cell populations. For at least twenty-four hours after amputation (hpa), laser-induced damage to the dorsal midline affected the morphology of the regenerated tail; damage induced 48 hpa or later did not. Targeting different positions along the anterior-posterior (AP) axis caused different shape changes in the regenerate. Interestingly, damaging two positions affected regenerate morphology in a qualitatively different way than did damaging either position alone. Quantitative comparison of regenerate shapes provided strong evidence against a gradient and for the existence of position-specific morphogenetic information along the entire AP axis. CONCLUSIONS: We infer that there is a conduit of morphology-influencing information that requires a continuous dorsal midline, particularly an undamaged spinal cord. Contrary to expectation, this information is not in a gradient and it is not localized to the regeneration bud. We present a model of morphogenetic information flow from tissue undamaged by amputation and conclude that studies of information coming from far outside the amputation plane and regeneration bud will be critical for understanding regeneration and for translating fundamental understanding into biomedical approaches. Public Library of Science 2011-09-16 /pmc/articles/PMC3174989/ /pubmed/21949803 http://dx.doi.org/10.1371/journal.pone.0024953 Text en Mondia et al. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Mondia, Jessica P.
Levin, Michael
Omenetto, Fiorenzo G.
Orendorff, Ryan D.
Branch, Mary Rose
Adams, Dany Spencer
Long-Distance Signals Are Required for Morphogenesis of the Regenerating Xenopus Tadpole Tail, as Shown by Femtosecond-Laser Ablation
title Long-Distance Signals Are Required for Morphogenesis of the Regenerating Xenopus Tadpole Tail, as Shown by Femtosecond-Laser Ablation
title_full Long-Distance Signals Are Required for Morphogenesis of the Regenerating Xenopus Tadpole Tail, as Shown by Femtosecond-Laser Ablation
title_fullStr Long-Distance Signals Are Required for Morphogenesis of the Regenerating Xenopus Tadpole Tail, as Shown by Femtosecond-Laser Ablation
title_full_unstemmed Long-Distance Signals Are Required for Morphogenesis of the Regenerating Xenopus Tadpole Tail, as Shown by Femtosecond-Laser Ablation
title_short Long-Distance Signals Are Required for Morphogenesis of the Regenerating Xenopus Tadpole Tail, as Shown by Femtosecond-Laser Ablation
title_sort long-distance signals are required for morphogenesis of the regenerating xenopus tadpole tail, as shown by femtosecond-laser ablation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3174989/
https://www.ncbi.nlm.nih.gov/pubmed/21949803
http://dx.doi.org/10.1371/journal.pone.0024953
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