The evolutionary conserved proteins CEP90, FOPNL, and OFD1 recruit centriolar distal appendage proteins to initiate their assembly

Pierrick Le Borgne (1) , Logan Greibill (1) , Marine Hélène Laporte (2) , Michel Lemullois (1) , Khaled Bouhouche (1) , Mebarek Temagoult (1) , Olivier Rosnet (3) , Maeva Le Guennec (2) , Laurent Lignières (4) , Guillaume Chevreux (4) , France Koll (1) , Virginie Hamel (2) , Paul Guichard (2) , Anne-Marie Tassin (1)

1 I2BC - Institut de Biologie Intégrative de la Cellule
2 UNIGE - Université de Genève = University of Geneva
3 CRCM - Centre de Recherche en Cancérologie de Marseille
4 IJM (UMR_7592) - Institut Jacques Monod

In metazoa, cilia assembly is a cellular process that starts with centriole to basal body maturation, migration to the cell surface, and docking to the plasma membrane. Basal body docking involves the interaction of both the distal end of the basal body and the transition fibers/distal appendages, with the plasma membrane. Mutations in numerous genes involved in basal body docking and transition zone assembly are associated with the most severe ciliopathies, highlighting the importance of these events in cilium biogenesis. In this context, the ciliate Paramecium has been widely used as a model system to study basal body and cilia assembly. However, despite the evolutionary conservation of cilia assembly events across phyla, whether the same molecular players are functionally conserved, is not fully known. Here, we demonstrated that CEP90, FOPNL, and OFD1 are evolutionary conserved proteins crucial for ciliogenesis. Using ultrastructure expansion microscopy, we unveiled that these proteins localize at the distal end of both centrioles/basal bodies in Paramecium and mammalian cells. Moreover, we found that these proteins are recruited early during centriole duplication on the external surface of the procentriole. Functional analysis performed both in Paramecium and mammalian cells demonstrate the requirement of these proteins for distal appendage assembly and basal body docking. Finally, we show that mammalian centrioles require another component, Moonraker (MNR), to recruit OFD1, FOPNL, and CEP90, which will then recruit the distal appendage proteins CEP83, CEP89, and CEP164. Altogether, we propose that this OFD1, FOPNL, and CEP90 functional module is required to determine in mammalian cells the future position of distal appendage proteins.

Domaines: Sciences du Vivant [q-bio]

Pierrick Le Borgne, Logan Greibill, Marine Hélène Laporte, Michel Lemullois, Khaled Bouhouche, et al.. The evolutionary conserved proteins CEP90, FOPNL, and OFD1 recruit centriolar distal appendage proteins to initiate their assembly. PLoS Biology, 2022, 20 (9), pp.e3001782. ⟨10.1371/journal.pbio.3001782⟩. ⟨hal-03843647⟩