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4. Local retinoic acid signaling directs emergence of the extraocular muscle functional unit

Author

Comai, G., Tesařová, Markéta, Dupé, Valerie, Rhinn, Muriel, Vallecillo-García, Pedro, Da Silva, Fabio, Feret, Betty, Exelby, Katherine, Dollé, Pascal, Carlsson, Leif, Pryce, Brian, Spitz, François, Stricker, Sigmar, Zikmund, Tomáš, Kaiser, Jozef, Briscoe, James, Schedl, Andreas, Ghyselinck, Norbert, Schweitzer, Ronen, Tajbakhsh, Shahragim, Cellules Souches et Développement / Stem Cells and Development, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Brno University of Technology [Brno] (BUT), Institut de Génétique et Développement de Rennes (IGDR), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Centre National de la Recherche Scientifique (CNRS)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ), Institut de Génétique et de Biologie Moléculaire et Cellulaire (IGBMC), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA), Freie Universität Berlin, Institut de Biologie Valrose (IBV), Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), The Francis Crick Institute, Umeå University, Shriners Hospital for Children [Portland], Génomique et Epigénomique du Développement des Animaux - Genomics and Epigenomics of Animal Development, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Université de Rennes (UR)-Centre National de la Recherche Scientifique (CNRS)-Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique ), Université de Strasbourg (UNISTRA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université Nice Sophia Antipolis (1965 - 2019) (UNS), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Côte d'Azur (UCA), The Francis Crick Institute [London], Génomique et Epigénomique du Développement des Vertébrés - Genomics and Epigenomics of Vertebrates Development, Institut Pasteur, French Muscular Dystrophy Association, ANR-10-LABX-73, Laboratoire d’Excellence Revive, Investissement d’Avenir, CNRS, ANR-10-LABX-0073,REVIVE,Stem Cells in Regenerative Biology and Medicine(2010), Comai, Glenda, Laboratoires d'excellence - Stem Cells in Regenerative Biology and Medicine - - REVIVE2010 - ANR-10-LABX-0073 - LABX - VALID, Structure Fédérative de Recherche en Biologie et Santé de Rennes ( Biosit : Biologie - Santé - Innovation Technologique )-Centre National de la Recherche Scientifique (CNRS)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES), COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015-2019) (COMUE UCA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Côte d'Azur (UCA)-Centre National de la Recherche Scientifique (CNRS), and Génomique et Epigénomique du Développement des Vertébrés - Genomics and Epigenomics of Vertebrate Development

Subjects
Cell- och molekylärbiologi, [SDV]Life Sciences [q-bio], Retinoic Acid, Immunostaining, Eye, Biochemistry, Tendons, Mice, Cell Signaling, Retinoic Acid Signaling Cascade, Medicine and Health Sciences, Morphogenesis, Metabolites, Biology (General), [SDV.BDD]Life Sciences [q-bio]/Development Biology, Staining, [SDV.BDD.EO] Life Sciences [q-bio]/Development Biology/Embryology and Organogenesis, Eye Muscles, Muscle Differentiation, eye, Signaling Cascades, [SDV.BDD.MOR] Life Sciences [q-bio]/Development Biology/Morphogenesis, [SDV] Life Sciences [q-bio], Chemistry, Connective Tissue, Mice, Inbred DBA, extraocular muscles, Physical Sciences, embryogenesis, Anatomy, Research Article, Signal Transduction, QH301-705.5, Ocular Anatomy, Muscle Tissue, Embryonic Development, Tretinoin, Research and Analysis Methods, Imaging, Three-Dimensional, Ocular System, [SDV.BDD] Life Sciences [q-bio]/Development Biology, Animals, Retinoid Signaling, development, EOM, Chemical Compounds, Biology and Life Sciences, [SDV.BDD.MOR]Life Sciences [q-bio]/Development Biology/Morphogenesis, Cell Biology, eye diseases, Mice, Inbred C57BL, Biological Tissue, Metabolism, [SDV.BDD.EO]Life Sciences [q-bio]/Development Biology/Embryology and Organogenesis, Specimen Preparation and Treatment, Oculomotor Muscles, sense organs, Acids, Cell and Molecular Biology, Developmental Biology
Abstract

Coordinated development of muscles, tendons, and their attachment sites ensures emergence of functional musculoskeletal units that are adapted to diverse anatomical demands among different species. How these different tissues are patterned and functionally assembled during embryogenesis is poorly understood. Here, we investigated the morphogenesis of extraocular muscles (EOMs), an evolutionary conserved cranial muscle group that is crucial for the coordinated movement of the eyeballs and for visual acuity. By means of lineage analysis, we redefined the cellular origins of periocular connective tissues interacting with the EOMs, which do not arise exclusively from neural crest mesenchyme as previously thought. Using 3D imaging approaches, we established an integrative blueprint for the EOM functional unit. By doing so, we identified a developmental time window in which individual EOMs emerge from a unique muscle anlage and establish insertions in the sclera, which sets these muscles apart from classical muscle-to-bone type of insertions. Further, we demonstrate that the eyeballs are a source of diffusible all-trans retinoic acid (ATRA) that allow their targeting by the EOMs in a temporal and dose-dependent manner. Using genetically modified mice and inhibitor treatments, we find that endogenous local variations in the concentration of retinoids contribute to the establishment of tendon condensations and attachment sites that precede the initiation of muscle patterning. Collectively, our results highlight how global and site-specific programs are deployed for the assembly of muscle functional units with precise definition of muscle shapes and topographical wiring of their tendon attachments., The extraocular muscles (EOMs) are an evolutionarily conserved group of muscles that are precisely engineered for fine displacement of the eyeball, and thus crucial for visual acuity. This study presents the first integrative blueprint for morphogenesis of the EOM functional unit, providing genetic evidence for the existence of a retinoic acid signaling module that coordinates the emergence of individual EOMs, their tendons and insertion sites.

Published
2020

6. Local retinoic acid directs emergence of the extraocular muscle functional unit

Author

Comai, Glenda, primary, Tesarova, Marketa, additional, Dupé, Valerie, additional, Rhinn, Muriel, additional, Vallecillo Garcia, Pedro, additional, da Silva, Fabio, additional, Feret, Betty, additional, Exelby, Katherine, additional, Dollé, Pascal, additional, Carlsson, Leif, additional, Pryce, Brian, additional, Spitz, Francois, additional, Stricker, Sigmar, additional, Zikmund, Tomas, additional, Kaiser, Jozef, additional, Briscoe, James, additional, Schedl, Andreas, additional, Ghyselinck, Norbert B., additional, Schweitzer, Ronen, additional, and Tajbakhsh, Shahragim, additional

Published
2020
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