Abstract
Ciliary shedding occurs from unicellular organisms to metazoans. Although required during the cell cycle and during neurogenesis, the process remains poorly understood. In all cellular models, this phenomenon occurs distal to the transition zone (TZ), suggesting conserved molecular mechanisms. The TZ module proteins (Meckel Gruber syndrome [MKS]/Nephronophtysis [NPHP]/Centrosomal protein of 290 kDa [CEP290]/Retinitis pigmentosa GTPase regulator-Interacting Protein 1-Like Protein [RPGRIP1L]) are known to cooperate to establish TZ formation and function. To determine whether they control deciliation, we studied the function of 5 of them (Transmembrane protein 107 [TMEM107], Transmembrane protein 216 [TMEM216], CEP290, RPGRIP1L, and NPHP4) in Paramecium. All proteins are recruited to the TZ of growing cilia and localize with 9-fold symmetry at the level of the most distal part of the TZ. We demonstrate that depletion of the MKS2/TMEM216 and TMEM107 proteins induces constant deciliation of some cilia, while depletion of either NPHP4, CEP290, or RPGRIP1L prevents Ca2+/EtOH deciliation. Our results constitute the first evidence for a role of conserved TZ proteins in deciliation and open new directions for understanding motile cilia physiology.
Highlights
Cilia are conserved cell appendages endowed with motility and sensory functions acting as “cellular antennae.” The cilia that emanate from the surface of most cells in multicellular organisms are key organelles in numerous developmental and physiological processes [1]
We performed this study in Paramecium tetraurelia, a unicellular organism that bears at its surface about 4,000 motile cilia
As in other species [40,50,68], the studied Paramecium transition zone (TZ) proteins localize with a 9-fold symmetry in several concentric rings located between the tubulin scaffold and the ciliary membrane
Summary
Cilia are conserved cell appendages endowed with motility and sensory functions acting as “cellular antennae.” The cilia that emanate from the surface of most cells in multicellular organisms are key organelles in numerous developmental and physiological processes [1]. The cilia that emanate from the surface of most cells in multicellular organisms are key organelles in numerous developmental and physiological processes [1] Their architecture consists of 3 structural regions: basal body (BB) at their proximal part, the axoneme composed of 9 microtubule doublets covered by the ciliary membrane at the distal part and in between, and the transition zone (TZ). The TZ is characterized by (i) Yshaped linkers connecting the microtubule doublets of the axoneme to the ciliary membrane, the so-called Y-links, and (ii) the transition fibers. These two structures are thought to function together as a gate [2], ensuring a specific ciliary composition.
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