TEADs, Yap, Taz, Vgll4s transcription factors control the establishment of Left-Right asymmetry in Zebrafish

  1. Jonathan Fillatre
  2. Jean-Daniel Fauny
  3. Jasmine Alexandra Fels
  4. Cheng Li
  5. Mary Goll
  6. Christine Thisse
  7. Bernard Thisse  Is a corresponding author
  1. University of Virginia, United States
  2. CNRS/INSERM/Université de Strasbourg, France
  3. University of Georgia, United States

Abstract

In many vertebrates, establishment of Left-Right (LR) asymmetry results from the activity of a ciliated organ functioning as the LR Organizer (LRO). While regulation of the formation of this structure by major signaling pathways has been described, the transcriptional control of LRO formation is poorly understood. Using the zebrafish model, we show that the transcription factors and cofactors mediating or regulating the transcriptional outcome of the Hippo signaling pathway play a pivotal role in controlling the expression of genes essential to the formation of the LRO including ligands and receptors of signaling pathways involved in this process and most genes required for motile ciliogenesis. Moreover, the transcription cofactor, Vgll4l regulates epigenetic programming in LRO progenitors by controlling the expression of writers and readers of DNA methylation marks. Altogether, our study uncovers a novel and essential role for the transcriptional effectors and regulators of the Hippo pathway in establishing LR asymmetry.

Data availability

RNA sequencing data that support the findings of this study have been deposited in the Gene Expression Omnibus (GEO) under accession code GSE119623 and are also provided in Supplementary File 1.All data generated or analysed during this study are included in the manuscript and supporting files.Source data for Figure 1, 2, 3, 9 and Figure Supplement 1 are provided in source data 1.

The following data sets were generated

Article and author information

Author details

  1. Jonathan Fillatre

    Department of Cell Biology, University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Jean-Daniel Fauny

    Institut de Génétique et de Biologie Moléculaire et Cellulaire, CNRS/INSERM/Université de Strasbourg, Strasbourg, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Jasmine Alexandra Fels

    Department of Cell Biology, University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Cheng Li

    Department of Genetics, University of Georgia, Athens, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Mary Goll

    Department of Genetics, University of Georgia, Athens, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5003-6958
  6. Christine Thisse

    Department of Cell Biology, University of Virginia, Charlottesville, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Bernard Thisse

    Department of Cell Biology, University of Virginia, Charlottesville, United States
    For correspondence
    bernardthisse@virginia.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8365-1081

Funding

Centre National de la Recherche Scientifique

  • Christine Thisse

National Institutes of Health (R01GM110092)

  • Mary Goll

Institut National de la Santé et de la Recherche Médicale

  • Christine Thisse

University of Virginia

  • Christine Thisse

National Science Foundation (1455901)

  • Bernard Thisse

Centre National de la Recherche Scientifique

  • Bernard Thisse

Institut National de la Santé et de la Recherche Médicale

  • Bernard Thisse

University of Virginia

  • Bernard Thisse

National Institutes of Health (R01GM132131)

  • Christine Thisse

National Institutes of Health (R01GM132131)

  • Jonathan Fillatre

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendationsin the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All ofthe animals were handled according to approved institutional animal care and use committee(IACUC) protocols (#3661) of the University of Virginia. All surgery was performed under tricain anesthesia and every effort was made to minimize suffering.

Reviewing Editor

  1. Julien Vermot, Institut de Génétique et de Biologie Moléculaire et Cellulaire, France

Version history

  1. Received: January 16, 2019
  2. Accepted: September 11, 2019
  3. Accepted Manuscript published: September 12, 2019 (version 1)
  4. Version of Record published: September 24, 2019 (version 2)

Copyright

© 2019, Fillatre et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Jonathan Fillatre
  2. Jean-Daniel Fauny
  3. Jasmine Alexandra Fels
  4. Cheng Li
  5. Mary Goll
  6. Christine Thisse
  7. Bernard Thisse
(2019)
TEADs, Yap, Taz, Vgll4s transcription factors control the establishment of Left-Right asymmetry in Zebrafish
eLife 8:e45241.
https://doi.org/10.7554/eLife.45241

Share this article

https://doi.org/10.7554/eLife.45241

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