Novel role for the midbody in primary ciliogenesis by polarized epithelial cells

J Cell Biol. 2016 Aug 1;214(3):259-73. doi: 10.1083/jcb.201601020. Epub 2016 Jul 25.

Abstract

The primary cilium is a membrane protrusion that is crucial for vertebrate tissue homeostasis and development. Here, we investigated the uncharacterized process of primary ciliogenesis in polarized epithelial cells. We show that after cytokinesis, the midbody is inherited by one of the daughter cells as a remnant that initially locates peripherally at the apical surface of one of the daughter cells. The remnant then moves along the apical surface and, once proximal to the centrosome at the center of the apical surface, enables cilium formation. The physical removal of the remnant greatly impairs ciliogenesis. We developed a probabilistic cell population-based model that reproduces the experimental data. In addition, our model explains, solely in terms of cell area constraints, the various observed transitions of the midbody, the beginning of ciliogenesis, and the accumulation of ciliated cells. Our findings reveal a biological mechanism that links the three microtubule-based organelles-the midbody, the centrosome, and the cilium-in the same cellular process.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Biomarkers / metabolism
  • Carrier Proteins / metabolism
  • Cell Polarity*
  • Cell Survival
  • Centrosome / metabolism*
  • Cilia / metabolism*
  • Cilia / ultrastructure
  • Dogs
  • Epithelial Cells / cytology*
  • Epithelial Cells / metabolism*
  • Epithelial Cells / ultrastructure
  • Imaging, Three-Dimensional
  • Madin Darby Canine Kidney Cells
  • Microscopy, Video
  • Microvilli / metabolism
  • Mitosis
  • Models, Biological
  • Single-Cell Analysis
  • rab GTP-Binding Proteins / metabolism

Substances

  • Biomarkers
  • Carrier Proteins
  • rab GTP-Binding Proteins