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

Author:

Bernabé-Rubio Miguel1,Andrés Germán2ORCID,Casares-Arias Javier1ORCID,Fernández-Barrera Jaime1,Rangel Laura1ORCID,Reglero-Real Natalia1,Gershlick David C.3ORCID,Fernández José J.4,Millán Jaime1,Correas Isabel1,Miguez David G.5,Alonso Miguel A.1

Affiliation:

1. Department of Cell Biology and Immunology, Centro de Biología Molecular Severo Ochoa, Consejo Superior de Investigaciones Científicas and Universidad Autónoma de Madrid, 28049 Madrid, Spain

2. Electron Microscopy Unit, Centro de Biología Molecular Severo Ochoa, Consejo Superior de Investigaciones Científicas and Universidad Autónoma de Madrid, 28049 Madrid, Spain

3. Cell Biology and Neurobiology Branch, Eunice Kennedy Shriver National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, MD 20892

4. Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas, 28049 Madrid, Spain

5. Department of Condensed Matter Physics, Instituto de Ciencias de Materiales Nicolás Cabrera and Instituto de Física de la Materia Condensada, Universidad Autónoma de Madrid, 28049 Madrid, Spain

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.

Funder

Ministerio de Economía y Competitividad

Publisher

Rockefeller University Press

Subject

Cell Biology

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