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Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging

Author

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  • Adelaida R. Palla

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine)

  • Keren I. Hilgendorf

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine
    University of Utah School of Medicine)

  • Ann V. Yang

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine)

  • Jaclyn P. Kerr

    (GlaxoSmithKline Research and Development, Muscle Metabolism Discovery Performance Unit)

  • Aaron C. Hinken

    (GlaxoSmithKline Research and Development, Muscle Metabolism Discovery Performance Unit)

  • Janos Demeter

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine)

  • Peggy Kraft

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine)

  • Nancie A. Mooney

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine)

  • Nora Yucel

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine)

  • David M. Burns

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine)

  • Yu Xin Wang

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine)

  • Peter K. Jackson

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine
    Stanford University School of Medicine)

  • Helen M. Blau

    (Institute for Stem Cell Biology and Regenerative Medicine, Stanford School of Medicine)

Abstract

During aging, the regenerative capacity of muscle stem cells (MuSCs) decreases, diminishing the ability of muscle to repair following injury. We found that the ability of MuSCs to regenerate is regulated by the primary cilium, a cellular protrusion that serves as a sensitive sensory organelle. Abolishing MuSC cilia inhibited MuSC proliferation in vitro and severely impaired injury-induced muscle regeneration in vivo. In aged muscle, a cell intrinsic defect in MuSC ciliation was associated with the decrease in regenerative capacity. Exogenous activation of Hedgehog signaling, known to be localized in the primary cilium, promoted MuSC expansion, both in vitro and in vivo. Delivery of the small molecule Smoothened agonist (SAG1.3) to muscles of aged mice restored regenerative capacity leading to increased strength post-injury. These findings provide fresh insights into the signaling dysfunction in aged MuSCs and identify the ciliary Hedgehog signaling pathway as a potential therapeutic target to counter the loss of muscle regenerative capacity which accompanies aging.

Suggested Citation

  • Adelaida R. Palla & Keren I. Hilgendorf & Ann V. Yang & Jaclyn P. Kerr & Aaron C. Hinken & Janos Demeter & Peggy Kraft & Nancie A. Mooney & Nora Yucel & David M. Burns & Yu Xin Wang & Peter K. Jackson, 2022. "Primary cilia on muscle stem cells are critical to maintain regenerative capacity and are lost during aging," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29150-6
    DOI: 10.1038/s41467-022-29150-6
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    References listed on IDEAS

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    1. Alessandra Sacco & Regis Doyonnas & Peggy Kraft & Stefan Vitorovic & Helen M. Blau, 2008. "Self-renewal and expansion of single transplanted muscle stem cells," Nature, Nature, vol. 456(7221), pages 502-506, November.
    2. Markus Delling & Paul G. DeCaen & Julia F. Doerner & Sebastien Febvay & David E. Clapham, 2013. "Primary cilia are specialized calcium signalling organelles," Nature, Nature, vol. 504(7479), pages 311-314, December.
    3. Joe V. Chakkalakal & Kieran M. Jones & M. Albert Basson & Andrew S. Brack, 2012. "The aged niche disrupts muscle stem cell quiescence," Nature, Nature, vol. 490(7420), pages 355-360, October.
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    Cited by:

    1. Alessandra M. Norris & Ambili Bai Appu & Connor D. Johnson & Lylybell Y. Zhou & David W. McKellar & Marie-Ange Renault & David Hammers & Benjamin D. Cosgrove & Daniel Kopinke, 2023. "Hedgehog signaling via its ligand DHH acts as cell fate determinant during skeletal muscle regeneration," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Jiayin Peng & Lili Han & Biao Liu & Jiawen Song & Yuang Wang & Kunpeng Wang & Qian Guo & XinYan Liu & Yu Li & Jujin Zhang & Wenqing Wu & Sheng Li & Xin Fu & Cheng-le Zhuang & Weikang Zhang & Shengbao , 2023. "Gli1 marks a sentinel muscle stem cell population for muscle regeneration," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

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