Journal Article

Centriole amplification by mother and daughter centrioles differs in multiciliated cells

Spassky, Nathalie, Faucourt, Marion, Meunier, Alice, Lemaître, Anne-Iris, Delgehyr, Nathalie, Al Jord, Adel

2014

Overview

Using advanced microscopy techniques, the process of centriole amplification in multiciliated cells is explored, and the daughter centriole identified as the primary nucleation site of more than 90% of the new centrioles, contesting existing de novo theories of centriolar amplification and highlighting a new centrosome asymmetry. Control of the centriole count in mammalian cells Cells that undergo division contain two centrioles, mother and the daughter, packaged into a centrosome. Mother and daughter centrioles are thought to have the same capacity to form new centrioles when cells divide. By contrast, multiciliated cells, which propel physiological fluids and are essential for health, contain as many as 200 centrioles, each one giving rise to a motile cilium, with new centrioles arising de novo independent of a centriole template. Studying multiciliated cells of the mouse brain, Alice Meunier and colleagues contest these long-held beliefs. Using state-of-the-art microscopy techniques, they document the process of centriole amplification in action, and find that the daughter centriole is the primary nucleation site for more than 90% of the new centrioles. The semi-conservative centrosome duplication in cycling cells gives rise to a centrosome composed of a mother and a newly formed daughter centriole 1 . Both centrioles are regarded as equivalent in their ability to form new centrioles and their symmetric duplication is crucial for cell division homeostasis 2 , 3 , 4 . Multiciliated cells do not use the archetypal duplication program and instead form more than a hundred centrioles that are required for the growth of motile cilia and the efficient propelling of physiological fluids 5 . The majority of these new centrioles are thought to appear de novo , that is, independently from the centrosome, around electron-dense structures called deuterosomes 6 , 7 , 8 . Their origin remains unknown. Using live imaging combined with correlative super-resolution light and electron microscopy, we show that all new centrioles derive from the pre-existing progenitor cell centrosome through multiple rounds of procentriole seeding. Moreover, we establish that only the daughter centrosomal centriole contributes to deuterosome formation, and thus to over ninety per cent of the final centriole population. This unexpected centriolar asymmetry grants new perspectives when studying cilia-related diseases 5 , 9 and pathological centriole amplification observed in cycling cells and associated with microcephaly and cancer 2 , 3 , 4 , 10 .

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 14 / 14/1 / 14/19 / 14/28 / 14/35 / 14/63 / 631/136/142 / 631/80/642 / Animals / Asymmetry / Biosynthesis / Cell division / Cell research / Cells / Cells, Cultured / Centrioles / Centrioles - physiology / Centrioles - ultrastructure / Centrosome - physiology / Centrosome - ultrastructure / Cilia - physiology / Cilia - ultrastructure / Cytoplasm / Humanities and Social Sciences / letter / Mice / Microscopy / Microscopy, Electron, Transmission / multidisciplinary / Proteins / Science