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Microtubule-based transport is essential to distribute RNA and nascent protein in skeletal muscle

Author

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  • Lance T. Denes

    (Center for NeuroGenetics, Genetics Institute, University of Florida
    Biomedical Sciences Graduate Program, University of Florida)

  • Chase P. Kelley

    (Center for NeuroGenetics, Genetics Institute, University of Florida
    Genetics and Genomics Graduate Program, University of Florida)

  • Eric T. Wang

    (Center for NeuroGenetics, Genetics Institute, University of Florida
    Myology Institute, University of Florida)

Abstract

While the importance of RNA localization in highly differentiated cells is well appreciated, basic principles of RNA localization in skeletal muscle remain poorly characterized. Here, we develop a method to detect and quantify single molecule RNA localization patterns in skeletal myofibers, and uncover a critical role for directed transport of RNPs in muscle. We find that RNAs localize and are translated along sarcomere Z-disks, dispersing tens of microns from progenitor nuclei, regardless of encoded protein function. We find that directed transport along the lattice-like microtubule network of myofibers becomes essential to achieve this localization pattern as muscle development progresses; disruption of this network leads to extreme accumulation of RNPs and nascent protein around myonuclei. Our observations suggest that global active RNP transport may be required to distribute RNAs in highly differentiated cells and reveal fundamental mechanisms of gene regulation, with consequences for myopathies caused by perturbations to RNPs or microtubules.

Suggested Citation

  • Lance T. Denes & Chase P. Kelley & Eric T. Wang, 2021. "Microtubule-based transport is essential to distribute RNA and nascent protein in skeletal muscle," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26383-9
    DOI: 10.1038/s41467-021-26383-9
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    References listed on IDEAS

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    1. Ning Zhao & Kouta Kamijo & Philip D. Fox & Haruka Oda & Tatsuya Morisaki & Yuko Sato & Hiroshi Kimura & Timothy J. Stasevich, 2019. "A genetically encoded probe for imaging nascent and mature HA-tagged proteins in vivo," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    2. Thomas O. Vogler & Joshua R. Wheeler & Eric D. Nguyen & Michael P. Hughes & Kyla A. Britson & Evan Lester & Bhalchandra Rao & Nicole Dalla Betta & Oscar N. Whitney & Theodore E. Ewachiw & Edward Gomes, 2018. "TDP-43 and RNA form amyloid-like myo-granules in regenerating muscle," Nature, Nature, vol. 563(7732), pages 508-513, November.
    3. Emily A. Scarborough & Keita Uchida & Maria Vogel & Noa Erlitzki & Meghana Iyer & Sai Aung Phyo & Alexey Bogush & Izhak Kehat & Benjamin L. Prosser, 2021. "Microtubules orchestrate local translation to enable cardiac growth," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. Brian Glancy & Lisa M. Hartnell & Daniela Malide & Zu-Xi Yu & Christian A. Combs & Patricia S. Connelly & Sriram Subramaniam & Robert S. Balaban, 2015. "Mitochondrial reticulum for cellular energy distribution in muscle," Nature, Nature, vol. 523(7562), pages 617-620, July.
    5. Pabitra K. Sahoo & Seung Joon Lee & Poonam B. Jaiswal & Stefanie Alber & Amar N. Kar & Sharmina Miller-Randolph & Elizabeth E. Taylor & Terika Smith & Bhagat Singh & Tammy Szu-Yu Ho & Anatoly Urisman , 2018. "Axonal G3BP1 stress granule protein limits axonal mRNA translation and nerve regeneration," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    6. María Cristina Estañ & Elisa Fernández-Núñez & Maha S. Zaki & María Isabel Esteban & Sandra Donkervoort & Cynthia Hawkins & José A. Caparros-Martin & Dimah Saade & Ying Hu & Véronique Bolduc & Katheri, 2019. "Recessive mutations in muscle-specific isoforms of FXR1 cause congenital multi-minicore myopathy," Nature Communications, Nature, vol. 10(1), pages 1-19, December.
    7. Kenth-Arne Hansson & Einar Eftestøl & Jo C. Bruusgaard & Inga Juvkam & Alyssa W. Cramer & Anders Malthe-Sørenssen & Douglas P. Millay & Kristian Gundersen, 2020. "Myonuclear content regulates cell size with similar scaling properties in mice and humans," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    8. Karl E. Bauer & Inmaculada Segura & Imre Gaspar & Volker Scheuss & Christin Illig & Georg Ammer & Saskia Hutten & Eugénia Basyuk & Sandra M. Fernández-Moya & Janina Ehses & Edouard Bertrand & Michael , 2019. "Live cell imaging reveals 3′-UTR dependent mRNA sorting to synapses," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
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    1. Ryan P. Hildebrandt & Kathryn R. Moss & Aleksandra Janusz-Kaminska & Luke A. Knudson & Lance T. Denes & Tanvi Saxena & Devi Prasad Boggupalli & Zhuangyue Li & Kun Lin & Gary J. Bassell & Eric T. Wang, 2023. "Muscleblind-like proteins use modular domains to localize RNAs by riding kinesins and docking to membranes," Nature Communications, Nature, vol. 14(1), pages 1-19, December.

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