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Tig1 regulates proximo-distal identity during salamander limb regeneration

Author

Listed:
  • Catarina R. Oliveira

    (Technische Universität Dresden, CRTD/Center for Regenerative Therapies Dresden)

  • Dunja Knapp

    (Technische Universität Dresden, CRTD/Center for Regenerative Therapies Dresden)

  • Ahmed Elewa

    (Department of Cell and Molecular Biology, Karolinska Institute)

  • Tobias Gerber

    (European Molecular Biology Laboratory (EMBL))

  • Sandra G. Gonzalez Malagon

    (University College London
    University of Ioannina Campus)

  • Phillip B. Gates

    (University College London)

  • Hannah E. Walters

    (Technische Universität Dresden, CRTD/Center for Regenerative Therapies Dresden)

  • Andreas Petzold

    (Technische Universität Dresden, CRTD/Center for Regenerative Therapies Dresden)

  • Hernan Arce

    (National Scientific and Technical Research Council (CONICET) and University of La Plata
    Instituto de Tecnología, Universidad Argentina de la Empresa (UADE))

  • Rodrigo C. Cordoba

    (National Scientific and Technical Research Council (CONICET) and University of La Plata)

  • Elaiyaraja Subramanian

    (Department of Cell and Molecular Biology, Karolinska Institute)

  • Osvaldo Chara

    (National Scientific and Technical Research Council (CONICET) and University of La Plata
    Instituto de Tecnología, Universidad Argentina de la Empresa (UADE)
    Technische Universität Dresden, Center for Information Services and High Performance Computing ZIH)

  • Elly M. Tanaka

    (Institute of Molecular Pathology, Vienna Biocenter)

  • András Simon

    (Department of Cell and Molecular Biology, Karolinska Institute)

  • Maximina H. Yun

    (Technische Universität Dresden, CRTD/Center for Regenerative Therapies Dresden
    Max Planck Institute for Molecular Cell Biology and Genetics)

Abstract

Salamander limb regeneration is an accurate process which gives rise exclusively to the missing structures, irrespective of the amputation level. This suggests that cells in the stump have an awareness of their spatial location, a property termed positional identity. Little is known about how positional identity is encoded, in salamanders or other biological systems. Through single-cell RNAseq analysis, we identified Tig1/Rarres1 as a potential determinant of proximal identity. Tig1 encodes a conserved cell surface molecule, is regulated by retinoic acid and exhibits a graded expression along the proximo-distal axis of the limb. Its overexpression leads to regeneration defects in the distal elements and elicits proximal displacement of blastema cells, while its neutralisation blocks proximo-distal cell surface interactions. Critically, Tig1 reprogrammes distal cells to a proximal identity, upregulating Prod1 and inhibiting Hoxa13 and distal transcriptional networks. Thus, Tig1 is a central cell surface determinant of proximal identity in the salamander limb.

Suggested Citation

  • Catarina R. Oliveira & Dunja Knapp & Ahmed Elewa & Tobias Gerber & Sandra G. Gonzalez Malagon & Phillip B. Gates & Hannah E. Walters & Andreas Petzold & Hernan Arce & Rodrigo C. Cordoba & Elaiyaraja S, 2022. "Tig1 regulates proximo-distal identity during salamander limb regeneration," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28755-1
    DOI: 10.1038/s41467-022-28755-1
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    References listed on IDEAS

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    1. Nadia Mercader & Esther Leonardo & Natalia Azpiazu & Antonio Serrano & Ginés Morata & Carlos Martínez-A & Miguel Torres, 1999. "Conserved regulation of proximodistal limb axis development by Meis1/Hth," Nature, Nature, vol. 402(6760), pages 425-429, November.
    2. Francesca V. Mariani & Christina P. Ahn & Gail R. Martin, 2008. "Genetic evidence that FGFs have an instructive role in limb proximal–distal patterning," Nature, Nature, vol. 453(7193), pages 401-405, May.
    3. John L Rinn & Chanda Bondre & Hayes B Gladstone & Patrick O Brown & Howard Y Chang, 2006. "Anatomic Demarcation by Positional Variation in Fibroblast Gene Expression Programs," PLOS Genetics, Public Library of Science, vol. 2(7), pages 1-13, July.
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