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Multi-species atlas resolves an axolotl limb development and regeneration paradox

Author

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  • Jixing Zhong

    (Swiss Federal Institute of Technology Lausanne, EPFL)

  • Rita Aires

    (University Hospital Carl Gustav Carus, Technische Universität Dresden)

  • Georgios Tsissios

    (Swiss Federal Institute of Technology Lausanne, EPFL)

  • Evangelia Skoufa

    (Swiss Federal Institute of Technology Lausanne, EPFL)

  • Kerstin Brandt

    (University Hospital Carl Gustav Carus, Technische Universität Dresden)

  • Tatiana Sandoval-Guzmán

    (University Hospital Carl Gustav Carus, Technische Universität Dresden
    University Hospital Carl Gustav Carus, Technische Universität Dresden)

  • Can Aztekin

    (Swiss Federal Institute of Technology Lausanne, EPFL)

Abstract

Humans and other tetrapods are considered to require apical-ectodermal-ridge (AER) cells for limb development, and AER-like cells are suggested to be re-formed to initiate limb regeneration. Paradoxically, the presence of AER in the axolotl, a primary model organism for regeneration, remains controversial. Here, by leveraging a single-cell transcriptomics-based multi-species atlas, composed of axolotl, human, mouse, chicken, and frog cells, we first establish that axolotls contain cells with AER characteristics. Further analyses and spatial transcriptomics reveal that axolotl limbs do not fully re-form AER cells during regeneration. Moreover, the axolotl mesoderm displays part of the AER machinery, revealing a program for limb (re)growth. These results clarify the debate about the axolotl AER and the extent to which the limb developmental program is recapitulated during regeneration.

Suggested Citation

  • Jixing Zhong & Rita Aires & Georgios Tsissios & Evangelia Skoufa & Kerstin Brandt & Tatiana Sandoval-Guzmán & Can Aztekin, 2023. "Multi-species atlas resolves an axolotl limb development and regeneration paradox," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41944-w
    DOI: 10.1038/s41467-023-41944-w
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    References listed on IDEAS

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    1. Jonathan A. Griffiths & Arianne C. Richard & Karsten Bach & Aaron T. L. Lun & John C. Marioni, 2018. "Detection and removal of barcode swapping in single-cell RNA-seq data," Nature Communications, Nature, vol. 9(1), pages 1-6, December.
    2. Martin Kragl & Dunja Knapp & Eugen Nacu & Shahryar Khattak & Malcolm Maden & Hans Henning Epperlein & Elly M. Tanaka, 2009. "Cells keep a memory of their tissue origin during axolotl limb regeneration," Nature, Nature, vol. 460(7251), pages 60-65, July.
    3. Nicholas D. Leigh & Garrett S. Dunlap & Kimberly Johnson & Rachelle Mariano & Rachel Oshiro & Alan Y. Wong & Donald M. Bryant & Bess M. Miller & Alex Ratner & Andy Chen & William W. Ye & Brian J. Haas, 2018. "Transcriptomic landscape of the blastema niche in regenerating adult axolotl limbs at single-cell resolution," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    4. Eugeniu Nacu & Elena Gromberg & Catarina R. Oliveira & David Drechsel & Elly M. Tanaka, 2016. "FGF8 and SHH substitute for anterior–posterior tissue interactions to induce limb regeneration," Nature, Nature, vol. 533(7603), pages 407-410, May.
    5. Yingyao Zhou & Bin Zhou & Lars Pache & Max Chang & Alireza Hadj Khodabakhshi & Olga Tanaseichuk & Christopher Benner & Sumit K. Chanda, 2019. "Metascape provides a biologist-oriented resource for the analysis of systems-level datasets," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    6. Suoqin Jin & Christian F. Guerrero-Juarez & Lihua Zhang & Ivan Chang & Raul Ramos & Chen-Hsiang Kuan & Peggy Myung & Maksim V. Plikus & Qing Nie, 2021. "Inference and analysis of cell-cell communication using CellChat," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
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