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Developmental switch from morphological replication to compensatory growth for salamander lung regeneration
Salamanders possess a pair of lungs for active air breathing, but the lung respiration is fully operational only during the late stage of development, particularly after metamorphosis. Larval salamanders mainly exchange air through the gills and skin, thus sparing the developing lungs. Salamanders c...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
John Wiley and Sons Inc.
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9977668/ https://www.ncbi.nlm.nih.gov/pubmed/36464792 http://dx.doi.org/10.1111/cpr.13369 |
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author | Yin, Binxu Zhang, Kun Du, Xinge Cai, Hao Ye, Tingting Wang, Heng |
author_facet | Yin, Binxu Zhang, Kun Du, Xinge Cai, Hao Ye, Tingting Wang, Heng |
author_sort | Yin, Binxu |
collection | PubMed |
description | Salamanders possess a pair of lungs for active air breathing, but the lung respiration is fully operational only during the late stage of development, particularly after metamorphosis. Larval salamanders mainly exchange air through the gills and skin, thus sparing the developing lungs. Salamanders can repair their lungs after injury, but a comparative analysis of regenerative responses between the lungs of young and adult animals is lacking. In this study, lung resections were performed in both larval and adult newts (Pleurodeles waltl). The cellular dynamics, tissue morphology and organ function during lung regeneration were examined and the Yap mutants were produced with CRISPR tools. We found that salamander switches the regenerative strategies from morphological replication through the blastema formation to compensatory growth via resident epithelial cells proliferation upon pulmonary resection injury as it transitions beyond metamorphosis. The larval animals achieve lung regeneration by forming a transient blastema‐like structure and regrowing full‐sized developing lungs, albeit unventilated. The adults repair injured lungs via massive proliferating epithelial cells and by expanding the existing alveolar epithelium without neo‐alveolarization. Yap signalling promotes epithelial cell proliferation and prevents epithelial‐to‐mesenchymal transition to restore functional respiration. The salamanders have evolved distinct regenerative strategies for lung repair during different phases of life. Our results demonstrate a novel strategy for functional lung recovery by inducing epithelial cell proliferation to strengthen the remaining alveoli without rebuilding new alveoli. |
format | Online Article Text |
id | pubmed-9977668 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | John Wiley and Sons Inc. |
record_format | MEDLINE/PubMed |
spelling | pubmed-99776682023-03-03 Developmental switch from morphological replication to compensatory growth for salamander lung regeneration Yin, Binxu Zhang, Kun Du, Xinge Cai, Hao Ye, Tingting Wang, Heng Cell Prolif Original Articles Salamanders possess a pair of lungs for active air breathing, but the lung respiration is fully operational only during the late stage of development, particularly after metamorphosis. Larval salamanders mainly exchange air through the gills and skin, thus sparing the developing lungs. Salamanders can repair their lungs after injury, but a comparative analysis of regenerative responses between the lungs of young and adult animals is lacking. In this study, lung resections were performed in both larval and adult newts (Pleurodeles waltl). The cellular dynamics, tissue morphology and organ function during lung regeneration were examined and the Yap mutants were produced with CRISPR tools. We found that salamander switches the regenerative strategies from morphological replication through the blastema formation to compensatory growth via resident epithelial cells proliferation upon pulmonary resection injury as it transitions beyond metamorphosis. The larval animals achieve lung regeneration by forming a transient blastema‐like structure and regrowing full‐sized developing lungs, albeit unventilated. The adults repair injured lungs via massive proliferating epithelial cells and by expanding the existing alveolar epithelium without neo‐alveolarization. Yap signalling promotes epithelial cell proliferation and prevents epithelial‐to‐mesenchymal transition to restore functional respiration. The salamanders have evolved distinct regenerative strategies for lung repair during different phases of life. Our results demonstrate a novel strategy for functional lung recovery by inducing epithelial cell proliferation to strengthen the remaining alveoli without rebuilding new alveoli. John Wiley and Sons Inc. 2022-12-04 /pmc/articles/PMC9977668/ /pubmed/36464792 http://dx.doi.org/10.1111/cpr.13369 Text en © 2022 The Authors. Cell Proliferation published by Beijing Institute for Stem Cell and Regenerative Medicine and John Wiley & Sons Ltd. https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
spellingShingle | Original Articles Yin, Binxu Zhang, Kun Du, Xinge Cai, Hao Ye, Tingting Wang, Heng Developmental switch from morphological replication to compensatory growth for salamander lung regeneration |
title | Developmental switch from morphological replication to compensatory growth for salamander lung regeneration |
title_full | Developmental switch from morphological replication to compensatory growth for salamander lung regeneration |
title_fullStr | Developmental switch from morphological replication to compensatory growth for salamander lung regeneration |
title_full_unstemmed | Developmental switch from morphological replication to compensatory growth for salamander lung regeneration |
title_short | Developmental switch from morphological replication to compensatory growth for salamander lung regeneration |
title_sort | developmental switch from morphological replication to compensatory growth for salamander lung regeneration |
topic | Original Articles |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9977668/ https://www.ncbi.nlm.nih.gov/pubmed/36464792 http://dx.doi.org/10.1111/cpr.13369 |
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