A Cell/Cilia Cycle Biosensor for Single-Cell Kinetics Reveals Persistence of Cilia after G1/S Transition Is a General Property in Cells and Mice

Ford, Matthew J. and Yeyati, Patricia L. and Mali, Girish R. and Keighren, Margaret A. and Waddell, Scott H. and Mjoseng, Heidi K. and Douglas, Adam T. and Hall, Emma A. and Sakaue-Sawano, Asako and Miyawaki, Atsushi and Meehan, Richard R. and Boulter, Luke and Jackson, Ian J. and Mill, Pleasantine and Mort, Richard L. (2018) A Cell/Cilia Cycle Biosensor for Single-Cell Kinetics Reveals Persistence of Cilia after G1/S Transition Is a General Property in Cells and Mice. Developmental Cell, 47 (4). 509-523.e5. ISSN 1534-5807

Abstract

The cilia and cell cycles are inextricably linked. Centrioles in the basal body of cilia nucleate the ciliary axoneme and sequester pericentriolar matrix (PCM) at the centrosome to organize the mitotic spindle. Cilia themselves respond to growth signals, prompting cilia resorption and cell cycle re-entry. We describe a fluorescent cilia and cell cycle biosensor allowing live imaging of cell cycle progression and cilia assembly and disassembly kinetics in cells and inducible mice. We define assembly and disassembly in relation to cell cycle stage with single-cell resolution and explore the intercellular heterogeneity in cilia kinetics. In all cells and tissues analyzed, we observed cilia that persist through the G1/S transition and into S/G2/M-phase. We conclude that persistence of cilia after the G1/S transition is a general property. This resource will shed light at an individual cell level on the interplay between the cilia and cell cycles in development, regeneration, and disease. The cilia and cell cycles are fundamental processes coupled through shared machinery. Ford et al. develop and characterize a multicistronic biosensor that can simultaneously label the cell and cilia cycles in mice, enabling live imaging studies of their kinetics.