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      The cellular and molecular mechanisms of tissue repair and regeneration as revealed by studies in Xenopus

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          Abstract

          Survival of any living organism critically depends on its ability to repair and regenerate damaged tissues and/or organs during its lifetime following injury, disease, or aging. Various animal models from invertebrates to vertebrates have been used to investigate the molecular and cellular mechanisms of wound healing and tissue regeneration. It is hoped that such studies will form the framework for identifying novel clinical treatments that will improve the healing and regenerative capacity of humans. Amongst these models, Xenopus stands out as a particularly versatile and powerful system. This review summarizes recent findings using this model, which have provided fundamental knowledge of the mechanisms responsible for efficient and perfect tissue repair and regeneration.

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          The genome of the Western clawed frog Xenopus tropicalis.

          Uffe Hellsten, Richard M. Harland, Michael Gilchrist … (2010)
          The western clawed frog Xenopus tropicalis is an important model for vertebrate development that combines experimental advantages of the African clawed frog Xenopus laevis with more tractable genetics. Here we present a draft genome sequence assembly of X. tropicalis. This genome encodes more than 20,000 protein-coding genes, including orthologs of at least 1700 human disease genes. Over 1 million expressed sequence tags validated the annotation. More than one-third of the genome consists of transposable elements, with unusually prevalent DNA transposons. Like that of other tetrapods, the genome of X. tropicalis contains gene deserts enriched for conserved noncoding elements. The genome exhibits substantial shared synteny with human and chicken over major parts of large chromosomes, broken by lineage-specific chromosome fusions and fissions, mainly in the mammalian lineage.
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            Cells keep a memory of their tissue origin during axolotl limb regeneration.

            Martin Kragl, Dunja Knapp, Eugen Nacu … (2009)
            During limb regeneration adult tissue is converted into a zone of undifferentiated progenitors called the blastema that reforms the diverse tissues of the limb. Previous experiments have led to wide acceptance that limb tissues dedifferentiate to form pluripotent cells. Here we have reexamined this question using an integrated GFP transgene to track the major limb tissues during limb regeneration in the salamander Ambystoma mexicanum (the axolotl). Surprisingly, we find that each tissue produces progenitor cells with restricted potential. Therefore, the blastema is a heterogeneous collection of restricted progenitor cells. On the basis of these findings, we further demonstrate that positional identity is a cell-type-specific property of blastema cells, in which cartilage-derived blastema cells harbour positional identity but Schwann-derived cells do not. Our results show that the complex phenomenon of limb regeneration can be achieved without complete dedifferentiation to a pluripotent state, a conclusion with important implications for regenerative medicine.
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              Amputation-induced reactive oxygen species (ROS) are required for successful Xenopus tadpole tail regeneration

              Nick Love, Yaoyao Chen, Shoko Ishibashi … (2013)
              Understanding the molecular mechanisms that promote successful tissue regeneration is critical for continued advancements in regenerative medicine. Vertebrate amphibian tadpoles of the species Xenopus laevis and Xenopus tropicalis have remarkable abilities to regenerate their tails following amputation 1, 2 , via the coordinated activity of numerous growth factor signaling pathways, including the Wnt, Fgf, BMP, notch, and TGFβ pathways 3-6 . Little is known, however, about the events that act upstream of these signalling pathways following injury. Here, we show that Xenopus tadpole tail amputation induces a sustained production of reactive oxygen species (ROS) during tail regeneration. Lowering ROS levels, via pharmacological or genetic approaches, reduces cell proliferation and impairs tail regeneration. Genetic rescue experiments restored both ROS production and the initiation of the regenerative response. Sustained increased ROS levels are required for Wnt/β-catenin signaling and the activation of one of its major downstream targets, fgf20 7 , which, in turn, is essential for proper tail regeneration. These findings demonstrate that injury-induced ROS production is an important regulator of tissue regeneration.
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                Author and article information

                Contributors
                Enrique Amaya:
                ORCID: http://orcid.org/0000-0002-1805-8548
                enrique.amaya@manchester.ac.uk
                Journal
                Journal ID (nlm-ta): Regeneration (Oxf)
                Journal ID (iso-abbrev): Regeneration (Oxf)
                Journal ID (doi): 10.1002/(ISSN)2052-4412
                Journal ID (publisher-id): REG2
                Title: Regeneration
                Publisher: John Wiley and Sons Inc. (Hoboken )
                ISSN (Electronic): 2052-4412
                Publication date (Electronic): 28 October 2016
                Publication date Collection: August 2016
                Volume: 3
                Issue: 4 ( doiID: 10.1002/reg2.2016.3.issue-4 )
                Pages: 198-208
                Affiliations
                [ 1 ] Division of Cell Matrix Biology and Regenerative Medicine School of Biological Sciences Faculty of Biology Medicine and HealthUniversity of Manchester Manchester M13 9PTUK
                Author notes
                [*] [* ] Correspondence

                Enrique Amaya, Division of Cell Matrix Biology and Regenerative Medicine, School of Biological Sciences, Faculty of Biology, Medicine and Health, University of Manchester, Manchester M13 9PT, UK. Email: enrique.amaya@ 123456manchester.ac.uk

                Author information
                http://orcid.org/0000-0002-1805-8548
                Article
                Publisher ID: REG269
                DOI: 10.1002/reg2.69
                PMC ID: 5084359
                PubMed ID: 27800170
                SO-VID: 58e21ccf-764d-46d1-9c6c-dfed7d3833fb
                Copyright © © 2016 The Authors. Regeneration published by John Wiley & Sons Ltd.
                License:

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 22 August 2016
                Date revision received : 09 September 2016
                Date accepted : 12 September 2016
                Page count
                Figures: 4, Tables: 0, Pages: 11, Words: 8147
                Funding
                Funded by: Healing Foundation
                Funded by: Medical Research Council
                Funded by: Wellcome Trust
                Award ID: 097820/Z/11/Z)
                Categories
                Subject: Review
                Subject: Review
                Custom metadata
                source-schema-version-number 2.0
                component-id reg269
                cover-date August 2016
                details-of-publishers-convertor Converter:WILEY_ML3GV2_TO_NLMPMC version:4.9.6 mode:remove_FC converted:28.10.2016

                Keywords: limb regeneration,scar‐free wound healing,tail regeneration,tissue regeneration
                Data availability:
                Keywords: limb regeneration, scar‐free wound healing, tail regeneration, tissue regeneration

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