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Microridge-like structures anchor motile cilia

Author

Listed:
  • Takayuki Yasunaga

    (University of Freiburg)

  • Johannes Wiegel

    (University of Freiburg)

  • Max D. Bergen

    (University of Freiburg)

  • Martin Helmstädter

    (University of Freiburg)

  • Daniel Epting

    (University of Freiburg)

  • Andrea Paolini

    (University of Freiburg
    University of Freiburg)

  • Özgün Çiçek

    (University of Freiburg
    BIOSS Centre for Biological Signalling Studies, University of Freiburg)

  • Gerald Radziwill

    (BIOSS Centre for Biological Signalling Studies, University of Freiburg
    CIBSS Centre for Integrative Biological Signalling Studies, University of Freiburg)

  • Christina Engel

    (University of Freiburg)

  • Thomas Brox

    (University of Freiburg
    BIOSS Centre for Biological Signalling Studies, University of Freiburg
    CIBSS Centre for Integrative Biological Signalling Studies, University of Freiburg)

  • Olaf Ronneberger

    (University of Freiburg
    BIOSS Centre for Biological Signalling Studies, University of Freiburg)

  • Peter Walentek

    (University of Freiburg
    CIBSS Centre for Integrative Biological Signalling Studies, University of Freiburg)

  • Maximilian H. Ulbrich

    (University of Freiburg
    BIOSS Centre for Biological Signalling Studies, University of Freiburg)

  • Gerd Walz

    (University of Freiburg
    BIOSS Centre for Biological Signalling Studies, University of Freiburg
    CIBSS Centre for Integrative Biological Signalling Studies, University of Freiburg)

Abstract

Several tissues contain cells with multiple motile cilia that generate a fluid or particle flow to support development and organ functions; defective motility causes human disease. Developmental cues orient motile cilia, but how cilia are locked into their final position to maintain a directional flow is not understood. Here we find that the actin cytoskeleton is highly dynamic during early development of multiciliated cells (MCCs). While apical actin bundles become increasingly more static, subapical actin filaments are nucleated from the distal tip of ciliary rootlets. Anchorage of these subapical actin filaments requires the presence of microridge-like structures formed during MCC development, and the activity of Nonmuscle Myosin II. Optogenetic manipulation of Ezrin, a core component of the microridge actin-anchoring complex, or inhibition of Myosin Light Chain Kinase interfere with rootlet anchorage and orientation. These observations identify microridge-like structures as an essential component of basal body rootlet anchoring in MCCs.

Suggested Citation

  • Takayuki Yasunaga & Johannes Wiegel & Max D. Bergen & Martin Helmstädter & Daniel Epting & Andrea Paolini & Özgün Çiçek & Gerald Radziwill & Christina Engel & Thomas Brox & Olaf Ronneberger & Peter Wa, 2022. "Microridge-like structures anchor motile cilia," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29741-3
    DOI: 10.1038/s41467-022-29741-3
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    References listed on IDEAS

    as
    1. Renuka Raman & Indraneel Damle & Rahul Rote & Shamik Banerjee & Chaitanya Dingare & Mahendra Sonawane, 2016. "aPKC regulates apical localization of Lgl to restrict elongation of microridges in developing zebrafish epidermis," Nature Communications, Nature, vol. 7(1), pages 1-16, September.
    2. Brian Mitchell & Richard Jacobs & Julie Li & Shu Chien & Chris Kintner, 2007. "A positive feedback mechanism governs the polarity and motion of motile cilia," Nature, Nature, vol. 447(7140), pages 97-101, May.
    3. Anselm Levskaya & Orion D. Weiner & Wendell A. Lim & Christopher A. Voigt, 2009. "Spatiotemporal control of cell signalling using a light-switchable protein interaction," Nature, Nature, vol. 461(7266), pages 997-1001, October.
    4. Alexia Mahuzier & Asm Shihavuddin & Clémence Fournier & Pauline Lansade & Marion Faucourt & Nikita Menezes & Alice Meunier & Meriem Garfa-Traoré & Marie-France Carlier & Raphael Voituriez & Auguste Ge, 2018. "Ependymal cilia beating induces an actin network to protect centrioles against shear stress," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    5. Hyunchul Ryu & Haeryung Lee & Jiyeon Lee & Hyuna Noh & Miram Shin & Vijay Kumar & Sejeong Hong & Jaebong Kim & Soochul Park, 2021. "The molecular dynamics of subdistal appendages in multi-ciliated cells," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
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