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Nr6a1 controls Hox expression dynamics and is a master regulator of vertebrate trunk development

Author

Listed:
  • Yi-Cheng Chang

    (Monash University
    Monash University)

  • Jan Manent

    (Monash University
    Monash University)

  • Jan Schroeder

    (Monash University
    Monash University
    Monash Biomedicine Discovery Institute)

  • Siew Fen Lisa Wong

    (Monash University
    Monash University)

  • Gabriel M. Hauswirth

    (Monash University
    Monash University)

  • Natalia A. Shylo

    (Stowers Institute for Medical Research)

  • Emma L. Moore

    (Stowers Institute for Medical Research)

  • Annita Achilleos

    (Stowers Institute for Medical Research
    University of Nicosia)

  • Victoria Garside

    (Monash University
    Monash University)

  • Jose M. Polo

    (Monash University
    Monash University
    Monash Biomedicine Discovery Institute)

  • Paul Trainor

    (Stowers Institute for Medical Research
    University of Kansas Medical Center)

  • Edwina McGlinn

    (Monash University
    Monash University)

Abstract

The vertebrate main-body axis is laid down during embryonic stages in an anterior-to-posterior (head-to-tail) direction, driven and supplied by posteriorly located progenitors. Whilst posterior expansion and segmentation appears broadly uniform along the axis, there is developmental and evolutionary support for at least two discrete modules controlling processes within different axial regions: a trunk and a tail module. Here, we identify Nuclear receptor subfamily 6 group A member 1 (Nr6a1) as a master regulator of trunk development in the mouse. Specifically, Nr6a1 was found to control vertebral number and segmentation of the trunk region, autonomously from other axial regions. Moreover, Nr6a1 was essential for the timely progression of Hox signatures, and neural versus mesodermal cell fate choice, within axial progenitors. Collectively, Nr6a1 has an axially-restricted role in all major cellular and tissue-level events required for vertebral column formation, supporting the view that changes in Nr6a1 levels may underlie evolutionary changes in axial formulae.

Suggested Citation

  • Yi-Cheng Chang & Jan Manent & Jan Schroeder & Siew Fen Lisa Wong & Gabriel M. Hauswirth & Natalia A. Shylo & Emma L. Moore & Annita Achilleos & Victoria Garside & Jose M. Polo & Paul Trainor & Edwina , 2022. "Nr6a1 controls Hox expression dynamics and is a master regulator of vertebrate trunk development," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35303-4
    DOI: 10.1038/s41467-022-35303-4
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    References listed on IDEAS

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    1. Smyth Gordon K, 2004. "Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 3(1), pages 1-28, February.
    2. Deborah L. Chapman & Virginia E. Papaioannou, 1998. "Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6," Nature, Nature, vol. 391(6668), pages 695-697, February.
    3. Tatsuya Takemoto & Masanori Uchikawa & Megumi Yoshida & Donald M. Bell & Robin Lovell-Badge & Virginia E. Papaioannou & Hisato Kondoh, 2011. "Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells," Nature, Nature, vol. 470(7334), pages 394-398, February.
    4. Gabriel M. Hauswirth & Victoria C. Garside & Lisa S. F. Wong & Heidi Bildsoe & Jan Manent & Yi-Cheng Chang & Christian M. Nefzger & Jaber Firas & Joseph Chen & Fernando J. Rossello & Jose M. Polo & Ed, 2022. "Breaking constraint of mammalian axial formulae," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Yacine Kherdjemil & Robert L. Lalonde & Rushikesh Sheth & Annie Dumouchel & Gemma de Martino & Kyriel M. Pineault & Deneen M. Wellik & H. Scott Stadler & Marie-Andrée Akimenko & Marie Kmita, 2016. "Evolution of Hoxa11 regulation in vertebrates is linked to the pentadactyl state," Nature, Nature, vol. 539(7627), pages 89-92, November.
    6. Nian Zhang & Thomas Gridley, 1998. "Defects in somite formation in lunatic fringe-deficient mice," Nature, Nature, vol. 394(6691), pages 374-377, July.
    7. Blanca Pijuan-Sala & Jonathan A. Griffiths & Carolina Guibentif & Tom W. Hiscock & Wajid Jawaid & Fernando J. Calero-Nieto & Carla Mulas & Ximena Ibarra-Soria & Richard C. V. Tyser & Debbie Lee Lian H, 2019. "A single-cell molecular map of mouse gastrulation and early organogenesis," Nature, Nature, vol. 566(7745), pages 490-495, February.
    8. Céline Gomez & Ertuğrul M. Özbudak & Joshua Wunderlich & Diana Baumann & Julian Lewis & Olivier Pourquié, 2008. "Control of segment number in vertebrate embryos," Nature, Nature, vol. 454(7202), pages 335-339, July.
    9. Yvonne A. Evrard & Yi Lun & Alexander Aulehla & Lin Gan & Randy L. Johnson, 1998. "lunatic fringe is an essential mediator of somite segmentation and patterning," Nature, Nature, vol. 394(6691), pages 377-381, July.
    Full references (including those not matched with items on IDEAS)

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