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

Abstract

Polarized epithelial cells assemble a primary cilium by an unknown mechanism. After cytokinesis, the central part of the intercellular bridge, which is referred to as the midbody, is inherited as a remnant by one of the daughter cells. Here, Bernabé-Rubio et al. show that the midbody remnant meets the centrosome at the cell apex, enabling primary ciliogenesis.

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.