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Development of the zebrafish myoseptum with emphasis on the myotendinous junction

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Abstract

Zebrafish myosepta connect two adjacent muscle cells and transmit muscular forces to axial structures during swimming via the myotendinous junction (MTJ). The MTJ establishes transmembrane linkages system consisting of extracellular matrix molecules (ECM) surrounding the basement membrane, cytoskeletal elements anchored to sarcolema, and all intermediate proteins that link ECM to actin filaments. Using a series of zebrafish specimens aged between 24 h post-fertilization and 2 years old, the present paper describes at the transmission electron microscope level the development of extracellular and intracellular elements of the MTJ. The transverse myoseptum development starts during the segmentation period by deposition of sparse and loosely organized collagen fibrils. During the hatching period, a link between actin filaments and sarcolemma is established. The basal lamina underlining sarcolemma is well differentiated. Later, collagen fibrils display an orthogonal orientation and fibroblast-like cells invade the myoseptal stroma. A dense network of collagen fibrils is progressively formed that both anchor myoseptal fibroblasts and sarcolemmal basement membrane. The differentiation of a functional MTJ is achieved when sarcolemma interacts with both cytoskeletal filaments and extracellular components. This solid structural link between contractile apparatus and ECM leads to sarcolemma deformations resulting in the formation of regular invaginations, and allows force transmission during muscle contraction. This paper presents the first ultrastructural atlas of the zebrafish MTJ development, which represents an useful tool to analyse the mechanisms of the myotendinous system formation and their disruption in muscle disorders.

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Acknowledgment

We thank L. Bernard (PRECI, IFR 128 Biosciences Gerland, Lyon) for fish maintenance and helpful advice.

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Authors and Affiliations

  1. Institut de Génomique Fonctionnelle de Lyon, ENS de Lyon, UMR CNRS 5242, Université Lyon 1, 46 Allée d’Italie, 69364, Lyon cedex 07, France

    Benjamin Charvet, Marilyne Malbouyres, Aurélie Pagnon-Minot & Florence Ruggiero

  2. IFR128 Lyon Biosciences Dysfonctionnement de l′Homéostasie Tissulaire et Ingénierie Thérapeutique, Université Lyon 1, CNRS, FRE 3310, Lyon, France

    Dominique Le Guellec

  3. IBCP, 7 passage du Vercors, Lyon, 69367 Lyon cedex 07, France

    Dominique Le Guellec

Authors
  1. Benjamin Charvet
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  2. Marilyne Malbouyres
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  3. Aurélie Pagnon-Minot
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  4. Florence Ruggiero
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  5. Dominique Le Guellec
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Corresponding author

Correspondence to Dominique Le Guellec.

Additional information

Florence Ruggiero and Dominique Le Guellec contributed equally to this work.

The work was supported by ANR (Muscolten) and AFM to F.R. B.C. was supported by FRM and by the University of Lyon.

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Charvet, B., Malbouyres, M., Pagnon-Minot, A. et al. Development of the zebrafish myoseptum with emphasis on the myotendinous junction. Cell Tissue Res 346, 439–449 (2011). https://doi.org/10.1007/s00441-011-1266-7

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  • DOI: https://doi.org/10.1007/s00441-011-1266-7

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