Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II

Yuki Hirota, Alice Meunier, Shihhui Huang, Togo Shimozawa, Osamu Yamada, Yasuyuki S. Kida, Masashi Inoue, Tsubasa Ito, Hiroko Kato, Masanori Sakaguchi, Takehiko Sunabori, Masa Aki Nakaya, Shigenori Nonaka, Toshihiko Ogura, Hideo Higuchi, Hideyuki Okano, Nathalie Spassky, Kazunobu Sawamoto

Research output: Contribution to journalArticle

64 Citations (Scopus)

Abstract

Motile cilia generate constant fluid flow over epithelial tissue, and thereby influence diverse physiological processes. Such functions of ciliated cells depend on the planar polarity of the cilia and on their basal bodies being oriented in the downstream direction of fluid flow. Recently, another type of basal body planar polarity, characterized by the anterior localization of the basal bodies in individual cells, was reported in the multiciliated ependymal cells that line the surface of brain ventricles. However, little is known about the cellular and molecular mechanisms by which this polarity is established. Here, we report in mice that basal bodies move in the apical cell membrane during differentiation to accumulate in the anterior region of ependymal cells. The planar cell polarity signaling pathway influences basal body orientation, but not their anterior migration, in the neonatal brain. Moreover, we show by pharmacological and genetic studies that non-muscle myosin II is a key regulator of this distribution of basal bodies. This study demonstrates that the orientation and distribution of basal bodies occur by distinct mechanisms.

Original languageEnglish
Pages (from-to)3037-3046
Number of pages10
JournalDevelopment
Volume137
Issue number18
DOIs
Publication statusPublished - 2010 Sep 15
Externally publishedYes

Fingerprint

Myosin Type II
Basal Bodies
Cilia
Physiological Phenomena
Cell Polarity
Brain
Epithelium
Cell Membrane
Pharmacology
Cell Line

Keywords

  • Cilia
  • Dvl2
  • Ependymal cell
  • Mouse
  • Non-muscle myosin II
  • Planar cell polarity

ASJC Scopus subject areas

  • Developmental Biology
  • Molecular Biology

Cite this

Hirota, Y., Meunier, A., Huang, S., Shimozawa, T., Yamada, O., Kida, Y. S., ... Sawamoto, K. (2010). Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II. Development, 137(18), 3037-3046. https://doi.org/10.1242/dev.050120

Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II. / Hirota, Yuki; Meunier, Alice; Huang, Shihhui; Shimozawa, Togo; Yamada, Osamu; Kida, Yasuyuki S.; Inoue, Masashi; Ito, Tsubasa; Kato, Hiroko; Sakaguchi, Masanori; Sunabori, Takehiko; Nakaya, Masa Aki; Nonaka, Shigenori; Ogura, Toshihiko; Higuchi, Hideo; Okano, Hideyuki; Spassky, Nathalie; Sawamoto, Kazunobu.

In: Development, Vol. 137, No. 18, 15.09.2010, p. 3037-3046.

Research output: Contribution to journalArticle

Hirota, Y, Meunier, A, Huang, S, Shimozawa, T, Yamada, O, Kida, YS, Inoue, M, Ito, T, Kato, H, Sakaguchi, M, Sunabori, T, Nakaya, MA, Nonaka, S, Ogura, T, Higuchi, H, Okano, H, Spassky, N & Sawamoto, K 2010, 'Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II', Development, vol. 137, no. 18, pp. 3037-3046. https://doi.org/10.1242/dev.050120
Hirota, Yuki ; Meunier, Alice ; Huang, Shihhui ; Shimozawa, Togo ; Yamada, Osamu ; Kida, Yasuyuki S. ; Inoue, Masashi ; Ito, Tsubasa ; Kato, Hiroko ; Sakaguchi, Masanori ; Sunabori, Takehiko ; Nakaya, Masa Aki ; Nonaka, Shigenori ; Ogura, Toshihiko ; Higuchi, Hideo ; Okano, Hideyuki ; Spassky, Nathalie ; Sawamoto, Kazunobu. / Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II. In: Development. 2010 ; Vol. 137, No. 18. pp. 3037-3046.
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