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Skeletal muscle MACF1 maintains myonuclei and mitochondria localization through microtubules to control muscle functionalities

Alireza Ghasemizadeh, Emilie Christin, Alexandre Guiraud, Nathalie Couturier, View ORCID ProfileValérie Risson, Emmanuelle Girard, Christophe Jagla, Cedric Soler, Lilia Laddada, Colline Sanchez, Francisco Jaque, Audrey Garcia, Marine Lanfranchi, Vincent Jacquemond, Julien Gondin, Julien Courchet, Laurent Schaeffer, View ORCID ProfileVincent Gache
doi: https://doi.org/10.1101/636464
Alireza Ghasemizadeh
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Emilie Christin
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Alexandre Guiraud
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Nathalie Couturier
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Valérie Risson
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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  • ORCID record for Valérie Risson
Emmanuelle Girard
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Christophe Jagla
GReD Laboratory, Clermont-Auvergne University, INSERM U1103, CNRS, UMR6293, 63000 Clermont-Ferrand, France
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Cedric Soler
GReD Laboratory, Clermont-Auvergne University, INSERM U1103, CNRS, UMR6293, 63000 Clermont-Ferrand, France
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Lilia Laddada
GReD Laboratory, Clermont-Auvergne University, INSERM U1103, CNRS, UMR6293, 63000 Clermont-Ferrand, France
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Colline Sanchez
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Francisco Jaque
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Audrey Garcia
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Marine Lanfranchi
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Vincent Jacquemond
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Julien Gondin
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Julien Courchet
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Laurent Schaeffer
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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Vincent Gache
Institut NeuroMyoGène, CNRS UMR5310, INSERM U1217, Faculté de Médecine, Rockefeller, Université Claude Bernard Lyon I, 8 Avenue Rockefeller, 69373, Lyon Cedex 08, France
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  • ORCID record for Vincent Gache
  • For correspondence: vincent.gache@inserm.fr
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Abstract

Skeletal muscle is made from multinuclear myofiber, where myonuclei are positioned at the periphery or clustered below neuromuscular junctions (NMJs). While mispositioned myonuclei are the hallmark of numerous muscular diseases, the molecular machinery maintaining myonuclei positioning in mature muscle is still unknown. Here, we identified microtubule-associated protein MACF1 as an evolutionary conserved regulator of myonuclei positioning, in vitro and in vivo, controlling the “microtubule code” and stabilizing the microtubule dynamics during myofibers maturation, preferentially at NMJs. Specifically, MACF1 governs myonuclei motion, mitochondria positioning and structure and acetylcholine receptors (AChRs) clustering. Macf1-KO in young and adult mice decreases muscle excitability and causes evolutionary myonuclei positioning alterations in adult mice, paralleled with high mitochondria content and improved resistance to fatigue. We present MACF1 as a primary actor of the maintenance of synaptic myonuclei and AChRs clustering, peripheral myonuclei positioning and mitochondria organization through the control of microtubule network dynamics in muscle fibers.

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Posted May 15, 2019.
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Skeletal muscle MACF1 maintains myonuclei and mitochondria localization through microtubules to control muscle functionalities
Alireza Ghasemizadeh, Emilie Christin, Alexandre Guiraud, Nathalie Couturier, Valérie Risson, Emmanuelle Girard, Christophe Jagla, Cedric Soler, Lilia Laddada, Colline Sanchez, Francisco Jaque, Audrey Garcia, Marine Lanfranchi, Vincent Jacquemond, Julien Gondin, Julien Courchet, Laurent Schaeffer, Vincent Gache
bioRxiv 636464; doi: https://doi.org/10.1101/636464
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Skeletal muscle MACF1 maintains myonuclei and mitochondria localization through microtubules to control muscle functionalities
Alireza Ghasemizadeh, Emilie Christin, Alexandre Guiraud, Nathalie Couturier, Valérie Risson, Emmanuelle Girard, Christophe Jagla, Cedric Soler, Lilia Laddada, Colline Sanchez, Francisco Jaque, Audrey Garcia, Marine Lanfranchi, Vincent Jacquemond, Julien Gondin, Julien Courchet, Laurent Schaeffer, Vincent Gache
bioRxiv 636464; doi: https://doi.org/10.1101/636464

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