Ectocytosis prevents accumulation of ciliary cargo in C. elegans sensory neurons

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Abstract

Cilia are sensory organelles protruding from cell surfaces. Release of Extracellular Vesicles (EVs) from cilia was previously observed in mammals, Chlamydomonas, and in male C. elegans. Using the EV marker TSP-6 (an ortholog of mammalian CD9) and other ciliary receptors, we show that EVs are formed from ciliated sensory neurons in C. elegans hermaphrodites. Release of EVs is observed from two ciliary locations: the cilia tip and/or Periciliary Membrane Compartment (PCMC). Outward budding of EVs from the cilia tip leads to their release into the environment. EVs budding from the PCMC are concomitantly phagocytosed by the associated glial cells. To maintain cilia composition, a tight regulation of cargo import and removal is achieved by the action of Intra-Flagellar Transport (IFT). Unbalanced IFT due to cargo overexpression or mutations in the IFT machinery leads to local accumulation of ciliary proteins. Disposal of excess ciliary proteins via EVs reduces their local accumulation and exports them to the environment and/or to the glia associated to these ciliated neurons. We suggest that EV budding from cilia subcompartments acts as a safeguard mechanism to remove deleterious excess of ciliary material.

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All data generated or analysed during this study are included in the manuscript and supporting files. The manuscript is a microscopy study all datapoints are represented in figures and figure supplement. Supplementary table contain all material used in this work.

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Adria Razzauti

UNI, Laboratoire de neurophysiologie, Université libre de Bruxelles (ULB), Brussels, Belgium

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-1899-8599
Patrick FM Laurent

UNI, Laboratoire de neurophysiologie, Université libre de Bruxelles (ULB), Brussels, Belgium

For correspondence
patrick.laurent@ulb.ac.be

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5360-5597

Funding

Fonds De La Recherche Scientifique - FNRS (22445636)

Patrick FM Laurent

Fonds De La Recherche Scientifique - FNRS (5125519F)

Adria Razzauti

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.