TY - JOUR
T1 - Planar cell polarity induces local microtubule bundling for coordinated ciliary beating
AU - Nakayama, Shogo
AU - Yano, Tomoki
AU - Namba, Toshinori
AU - Konishi, Satoshi
AU - Takagishi, Maki
AU - Herawati, Elisa
AU - Nishida, Tomoki
AU - Imoto, Yasuo
AU - Ishihara, Shuji
AU - Takahashi, Masahide
AU - Furuta, Ken’Ya
AU - Oiwa, Kazuhiro
AU - Tamura, Atsushi
AU - Tsukita, Sachiko
N1 - Publisher Copyright:
© 2021 Nakayama et al.
PY - 2021/7/5
Y1 - 2021/7/5
N2 - 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 sideby-side association with one side of the apical junctional complex, to which Daple was localized. In vitro binding and singlemolecule 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.
AB - 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 sideby-side association with one side of the apical junctional complex, to which Daple was localized. In vitro binding and singlemolecule 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.
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U2 - 10.1083/jcb.202010034
DO - 10.1083/jcb.202010034
M3 - Article
C2 - 33929515
AN - SCOPUS:85106069019
SN - 0021-9525
VL - 220
JO - Journal of Cell Biology
JF - Journal of Cell Biology
IS - 7
M1 - e202010034
ER -