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Attenuated sensing of SHH by Ptch1 underlies evolution of bovine limbs

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  • Javier Lopez-Rios

    (Developmental Genetics, University of Basel, CH-4058 Basel, Switzerland)

  • Amandine Duchesne

    (Developmental Genetics, University of Basel, CH-4058 Basel, Switzerland
    Institut National de la Recherche Agronomique, Génétique Animale et Biologie Intégrative, F-78350 Jouy-en-Josas, France)

  • Dario Speziale

    (Developmental Genetics, University of Basel, CH-4058 Basel, Switzerland)

  • Guillaume Andrey

    (School of Life Sciences, Federal Institute of Technology Lausanne, CH-1015 Lausanne, Switzerland)

  • Kevin A. Peterson

    (Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, Keck School of Medicine, University of Southern California)

  • Philipp Germann

    (Federal Institute of Technology Zurich and Swiss Institute of Bioinformatics, CH-4058 Basel, Switzerland)

  • Erkan Ünal

    (Developmental Genetics, University of Basel, CH-4058 Basel, Switzerland
    Federal Institute of Technology Zurich and Swiss Institute of Bioinformatics, CH-4058 Basel, Switzerland)

  • Jing Liu

    (Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, Keck School of Medicine, University of Southern California)

  • Sandrine Floriot

    (Institut National de la Recherche Agronomique, Génétique Animale et Biologie Intégrative, F-78350 Jouy-en-Josas, France)

  • Sarah Barbey

    (Institut National de la Recherche Agronomique, Domaine Expérimental du Pin au Haras, F-61310 Exmes, France)

  • Yves Gallard

    (Institut National de la Recherche Agronomique, Domaine Expérimental du Pin au Haras, F-61310 Exmes, France)

  • Magdalena Müller-Gerbl

    (Institute of Anatomy, University of Basel, CH-4056 Basel, Switzerland)

  • Andrew D. Courtney

    (Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia)

  • Christophe Klopp

    (Institut National de la Recherche Agronomique, Biométrie et Intelligence Artificielle, F-31326 Castanet-Tolosan, France)

  • Sabrina Rodriguez

    (Institut National de la Recherche Agronomique, Génétique Animale et Biologie Intégrative, F-78350 Jouy-en-Josas, France
    Present address: Institut National de la Recherche Agronomique, Laboratoire d’Ingénierie des Systèmes Biologiques et des Procédés, F-31077 Toulouse, France.)

  • Robert Ivanek

    (Developmental Genetics, University of Basel, CH-4058 Basel, Switzerland
    Swiss Institute of Bioinformatics, CH-4058 Basel, Switzerland)

  • Christian Beisel

    (Federal Institute of Technology Zurich and Swiss Institute of Bioinformatics, CH-4058 Basel, Switzerland)

  • Carol Wicking

    (Institute for Molecular Bioscience, The University of Queensland, St Lucia, Queensland 4072, Australia)

  • Dagmar Iber

    (Federal Institute of Technology Zurich and Swiss Institute of Bioinformatics, CH-4058 Basel, Switzerland)

  • Benoit Robert

    (Institut Pasteur, Génétique Moléculaire de la Morphogenèse and Centre National de la Recherche Scientifique URA-2578, F-75015 Paris, France)

  • Andrew P. McMahon

    (Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, Keck School of Medicine, University of Southern California)

  • Denis Duboule

    (School of Life Sciences, Federal Institute of Technology Lausanne, CH-1015 Lausanne, Switzerland
    University of Geneva, CH-1211 Geneva, Switzerland)

  • Rolf Zeller

    (Developmental Genetics, University of Basel, CH-4058 Basel, Switzerland)

Abstract

The large spectrum of limb morphologies reflects the wide evolutionary diversification of the basic pentadactyl pattern in tetrapods. In even-toed ungulates (artiodactyls, including cattle), limbs are adapted for running as a consequence of progressive reduction of their distal skeleton to symmetrical and elongated middle digits with hoofed phalanges. Here we analyse bovine embryos to establish that polarized gene expression is progressively lost during limb development in comparison to the mouse. Notably, the transcriptional upregulation of the Ptch1 gene, which encodes a Sonic hedgehog (SHH) receptor, is disrupted specifically in the bovine limb bud mesenchyme. This is due to evolutionary alteration of a Ptch1 cis-regulatory module, which no longer responds to graded SHH signalling during bovine handplate development. Our study provides a molecular explanation for the loss of digit asymmetry in bovine limb buds and suggests that modifications affecting the Ptch1 cis-regulatory landscape have contributed to evolutionary diversification of artiodactyl limbs.

Suggested Citation

  • Javier Lopez-Rios & Amandine Duchesne & Dario Speziale & Guillaume Andrey & Kevin A. Peterson & Philipp Germann & Erkan Ünal & Jing Liu & Sandrine Floriot & Sarah Barbey & Yves Gallard & Magdalena Mül, 2014. "Attenuated sensing of SHH by Ptch1 underlies evolution of bovine limbs," Nature, Nature, vol. 511(7507), pages 46-51, July.
    • Handle: RePEc:nat:nature:v:511:y:2014:i:7507:d:10.1038_nature13289
    DOI: 10.1038/nature13289
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    Cited by:

    1. Rachel K. Lex & Weiqiang Zhou & Zhicheng Ji & Kristin N. Falkenstein & Kaleigh E. Schuler & Kathryn E. Windsor & Joseph D. Kim & Hongkai Ji & Steven A. Vokes, 2022. "GLI transcriptional repression is inert prior to Hedgehog pathway activation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.

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