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An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra

Author

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  • Matthias C. Vogg

    (University of Geneva)

  • Leonardo Beccari

    (University of Geneva)

  • Laura Iglesias Ollé

    (University of Geneva)

  • Christine Rampon

    (CNRS UMR 7241/INSERM U1050/Collège de France
    Université Paris Diderot, Sorbonne Paris Cité, Biology Department
    PSL Research University)

  • Sophie Vriz

    (CNRS UMR 7241/INSERM U1050/Collège de France
    Université Paris Diderot, Sorbonne Paris Cité, Biology Department
    PSL Research University)

  • Chrystelle Perruchoud

    (University of Geneva)

  • Yvan Wenger

    (University of Geneva)

  • Brigitte Galliot

    (University of Geneva)

Abstract

Polyps of the cnidarian Hydra maintain their adult anatomy through two developmental organizers, the head organizer located apically and the foot organizer basally. The head organizer is made of two antagonistic cross-reacting components, an activator, driving apical differentiation and an inhibitor, preventing ectopic head formation. Here we characterize the head inhibitor by comparing planarian genes down-regulated when β-catenin is silenced to Hydra genes displaying a graded apical-to-basal expression and an up-regulation during head regeneration. We identify Sp5 as a transcription factor that fulfills the head inhibitor properties: leading to a robust multiheaded phenotype when knocked-down in Hydra, acting as a transcriptional repressor of Wnt3 and positively regulated by Wnt/β-catenin signaling. Hydra and zebrafish Sp5 repress Wnt3 promoter activity while Hydra Sp5 also activates its own expression, likely via β-catenin/TCF interaction. This work identifies Sp5 as a potent feedback loop inhibitor of Wnt/β-catenin signaling, a function conserved across eumetazoan evolution.

Suggested Citation

  • Matthias C. Vogg & Leonardo Beccari & Laura Iglesias Ollé & Christine Rampon & Sophie Vriz & Chrystelle Perruchoud & Yvan Wenger & Brigitte Galliot, 2019. "An evolutionarily-conserved Wnt3/β-catenin/Sp5 feedback loop restricts head organizer activity in Hydra," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-018-08242-2
    DOI: 10.1038/s41467-018-08242-2
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    Cited by:

    1. Eudald Pascual-Carreras & Marta Marín-Barba & Sergio Castillo-Lara & Pablo Coronel-Córdoba & Marta Silvia Magri & Grant N. Wheeler & Jose Luis Gómez-Skarmeta & Josep F. Abril & Emili Saló & Teresa Ade, 2023. "Wnt/β-catenin signalling is required for pole-specific chromatin remodeling during planarian regeneration," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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