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  4. Planar cell polarity induces local microtubule bundling for coordinated ciliary beating

Planar cell polarity induces local microtubule bundling for coordinated ciliary beating

Journal J. Cell Biol. 220(7):e202010034 (2021)
Title Planar cell polarity induces local microtubule bundling for coordinated ciliary beating
Laboratory Laboratory of Barriology and Cell Biology〈SA Prof. TSUKITA Sachiko〉
Abstract

Multiciliated cells (MCCs) in tracheas generate mucociliary clearance through coordinated ciliary beating. Apical microtubules (MTs) play a crucial role in this process by organizing the planar cell polarity (PCP)-dependent orientation of ciliary basal bodies (BBs), for which the underlying molecular basis remains elusive. Herein, we found that the deficiency of Daple, a dishevelled-associating protein, in tracheal MCCs impaired the planar polarized apical MTs without affecting the core PCP proteins, causing significant defects in the BB orientation at the cell level but not the tissue level. Using live-cell imaging and ultra-high voltage electron microscope tomography, we found that the apical MTs accumulated and were stabilized by side-by-side association with one side of the apical junctional complex, to which Daple was localized. In vitro binding and single-molecule imaging revealed that Daple directly bound to, bundled, and stabilized MTs through its dimerization. These features convey a PCP-related molecular basis for the polarization of apical MTs, which coordinate ciliary beating in tracheal MCCs.

Authors

Shogo Nakayama (1, 2), Tomoki Yano (1, 3), Toshinori Namba (4), Satoshi Konishi (1, 5), Maki Takagishi (6), Elisa Herawati (7), Tomoki Nishida (8), Yasuo Imoto (8), Shuji Ishihara (4), Masahide Takahashi (9, 10), Ken'ya Furuta (11), Kazuhiro Oiwa (11), Atsushi Tamura (1, 12, 13), Sachiko Tsukita (1, 13)

  1. Laboratory of Barriology and Cell Biology, Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan.
  2. Integrative Physiology, Graduate School of Medicine, Osaka University, Osaka, Japan.
  3. Department of Cardiovascular Medicine, Graduate School of Medicine, Osaka University, Osaka, Japan.
  4. Department of Basic Science, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan.
  5. Department of Respiratory Medicine, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
  6. Department of Molecular Biosciences, University of Texas at Austin, Austin, TX.
  7. Faculty of Mathematics and Natural Sciences, Universitas Sebelas Maret, Surakarta, Indonesia.
  8. Japan Textile Products Quality and Technology Center, Hyogo, Japan.
  9. Department of Pathology, Graduate School of Medicine, Nagoya University, Nagoya, Japan.
  10. International Center for Cell and Gene Therapy, Fujita Health University, Toyoake, Japan.
  11. Advanced Information and Communications Technology Research Institute, National Institute of Information and Communications Technology, Hyogo, Japan.
  12. Department of Pharmacology, School of Medicine, Teikyo University, Tokyo, Japan.
  13. Advanced Comprehensive Research Organization, Teikyo University, Tokyo, Japan.
PubMed 33929515

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