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A Yap-dependent mechanoregulatory program sustains cell migration for embryo axis assembly

Author

Listed:
  • Ana Sousa-Ortega

    (Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA))

  • Javier Vázquez-Marín

    (Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA))

  • Estefanía Sanabria-Reinoso

    (Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA))

  • Jorge Corbacho

    (Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA))

  • Rocío Polvillo

    (Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA))

  • Alejandro Campoy-López

    (Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA))

  • Lorena Buono

    (Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA))

  • Felix Loosli

    (Institute of Biological and Chemical Systems, Biological Information Processing (IBCS-BIP), Karlsruhe Institute of Technology)

  • María Almuedo-Castillo

    (Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA))

  • Juan R. Martínez-Morales

    (Centro Andaluz de Biología del Desarrollo (CSIC/UPO/JA))

Abstract

The assembly of the embryo’s primary axis is a fundamental landmark for the establishment of the vertebrate body plan. Although the morphogenetic movements directing cell convergence towards the midline have been described extensively, little is known on how gastrulating cells interpret mechanical cues. Yap proteins are well-known transcriptional mechanotransducers, yet their role in gastrulation remains elusive. Here we show that the double knockout of yap and its paralog yap1b in medaka results in an axis assembly failure, due to reduced displacement and migratory persistence in mutant cells. Accordingly, we identified genes involved in cytoskeletal organization and cell-ECM adhesion as potentially direct Yap targets. Dynamic analysis of live sensors and downstream targets reveal that Yap is acting in migratory cells, promoting cortical actin and focal adhesions recruitment. Our results indicate that Yap coordinates a mechanoregulatory program to sustain intracellular tension and maintain the directed cell migration for embryo axis development.

Suggested Citation

  • Ana Sousa-Ortega & Javier Vázquez-Marín & Estefanía Sanabria-Reinoso & Jorge Corbacho & Rocío Polvillo & Alejandro Campoy-López & Lorena Buono & Felix Loosli & María Almuedo-Castillo & Juan R. Martíne, 2023. "A Yap-dependent mechanoregulatory program sustains cell migration for embryo axis assembly," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38482-w
    DOI: 10.1038/s41467-023-38482-w
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    1. Démosthène Mitrossilis & Jens-Christian Röper & Damien Le Roy & Benjamin Driquez & Aude Michel & Christine Ménager & Gorky Shaw & Simon Le Denmat & Laurent Ranno & Frédéric Dumas-Bouchiat & Nora M. De, 2017. "Mechanotransductive cascade of Myo-II-dependent mesoderm and endoderm invaginations in embryo gastrulation," Nature Communications, Nature, vol. 8(1), pages 1-15, April.
    2. Thibaut Brunet & Adrien Bouclet & Padra Ahmadi & Démosthène Mitrossilis & Benjamin Driquez & Anne-Christine Brunet & Laurent Henry & Fanny Serman & Gaëlle Béalle & Christine Ménager & Frédéric Dumas-B, 2013. "Evolutionary conservation of early mesoderm specification by mechanotransduction in Bilateria," Nature Communications, Nature, vol. 4(1), pages 1-15, December.
    3. Carl-Philipp Heisenberg & Masazumi Tada & Gerd-Jörg Rauch & Leonor Saúde & Miguel L. Concha & Robert Geisler & Derek L. Stemple & James C. Smith & Stephen W. Wilson, 2000. "Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation," Nature, Nature, vol. 405(6782), pages 76-81, May.
    4. Giorgia Nardone & Jorge Oliver-De La Cruz & Jan Vrbsky & Cecilia Martini & Jan Pribyl & Petr Skládal & Martin Pešl & Guido Caluori & Stefania Pagliari & Fabiana Martino & Zuzana Maceckova & Marian Haj, 2017. "YAP regulates cell mechanics by controlling focal adhesion assembly," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
    5. John B. Wallingford & Brian A. Rowning & Kevin M. Vogeli & Ute Rothbächer & Scott E. Fraser & Richard M. Harland, 2000. "Dishevelled controls cell polarity during Xenopus gastrulation," Nature, Nature, vol. 405(6782), pages 81-85, May.
    6. José M. Santos-Pereira & Lourdes Gallardo-Fuentes & Ana Neto & Rafael D. Acemel & Juan J. Tena, 2019. "Pioneer and repressive functions of p63 during zebrafish embryonic ectoderm specification," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    7. Leonardo Beccari & Naomi Moris & Mehmet Girgin & David A. Turner & Peter Baillie-Johnson & Anne-Catherine Cossy & Matthias P. Lutolf & Denis Duboule & Alfonso Martinez Arias, 2018. "Multi-axial self-organization properties of mouse embryonic stem cells into gastruloids," Nature, Nature, vol. 562(7726), pages 272-276, October.
    8. Sean Porazinski & Huijia Wang & Yoichi Asaoka & Martin Behrndt & Tatsuo Miyamoto & Hitoshi Morita & Shoji Hata & Takashi Sasaki & S. F. Gabriel Krens & Yumi Osada & Satoshi Asaka & Akihiro Momoi & Sar, 2015. "YAP is essential for tissue tension to ensure vertebrate 3D body shape," Nature, Nature, vol. 521(7551), pages 217-221, May.
    9. Soline Chanet & Callie J. Miller & Eeshit Dhaval Vaishnav & Bard Ermentrout & Lance A. Davidson & Adam C. Martin, 2017. "Actomyosin meshwork mechanosensing enables tissue shape to orient cell force," Nature Communications, Nature, vol. 8(1), pages 1-13, August.
    10. Naomi Moris & Kerim Anlas & Susanne C. van den Brink & Anna Alemany & Julia Schröder & Sabitri Ghimire & Tina Balayo & Alexander van Oudenaarden & Alfonso Martinez Arias, 2020. "An in vitro model of early anteroposterior organization during human development," Nature, Nature, vol. 582(7812), pages 410-415, June.
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