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A liquid-like organelle at the root of motile ciliopathy

Motile ciliopathies are characterized by specific defects in cilia beating that result in chronic airway disease, subfertility, ectopic pregnancy, and hydrocephalus. While many patients harbor mutations in the dynein motors that drive cilia beating, the disease also results from mutations in so-call...

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Autores principales: Huizar, Ryan L, Lee, Chanjae, Boulgakov, Alexander A, Horani, Amjad, Tu, Fan, Marcotte, Edward M, Brody, Steven L, Wallingford, John B
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6349401/
https://www.ncbi.nlm.nih.gov/pubmed/30561330
http://dx.doi.org/10.7554/eLife.38497
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author Huizar, Ryan L
Lee, Chanjae
Boulgakov, Alexander A
Horani, Amjad
Tu, Fan
Marcotte, Edward M
Brody, Steven L
Wallingford, John B
author_facet Huizar, Ryan L
Lee, Chanjae
Boulgakov, Alexander A
Horani, Amjad
Tu, Fan
Marcotte, Edward M
Brody, Steven L
Wallingford, John B
author_sort Huizar, Ryan L
collection PubMed
description Motile ciliopathies are characterized by specific defects in cilia beating that result in chronic airway disease, subfertility, ectopic pregnancy, and hydrocephalus. While many patients harbor mutations in the dynein motors that drive cilia beating, the disease also results from mutations in so-called dynein axonemal assembly factors (DNAAFs) that act in the cytoplasm. The mechanisms of DNAAF action remain poorly defined. Here, we show that DNAAFs concentrate together with axonemal dyneins and chaperones into organelles that form specifically in multiciliated cells, which we term DynAPs, for dynein axonemal particles. These organelles display hallmarks of biomolecular condensates, and remarkably, DynAPs are enriched for the stress granule protein G3bp1, but not for other stress granule proteins or P-body proteins. Finally, we show that both the formation and the liquid-like behaviors of DynAPs are disrupted in a model of motile ciliopathy. These findings provide a unifying cell biological framework for a poorly understood class of human disease genes and add motile ciliopathy to the growing roster of human diseases associated with disrupted biological phase separation.
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spelling pubmed-63494012019-01-30 A liquid-like organelle at the root of motile ciliopathy Huizar, Ryan L Lee, Chanjae Boulgakov, Alexander A Horani, Amjad Tu, Fan Marcotte, Edward M Brody, Steven L Wallingford, John B eLife Cell Biology Motile ciliopathies are characterized by specific defects in cilia beating that result in chronic airway disease, subfertility, ectopic pregnancy, and hydrocephalus. While many patients harbor mutations in the dynein motors that drive cilia beating, the disease also results from mutations in so-called dynein axonemal assembly factors (DNAAFs) that act in the cytoplasm. The mechanisms of DNAAF action remain poorly defined. Here, we show that DNAAFs concentrate together with axonemal dyneins and chaperones into organelles that form specifically in multiciliated cells, which we term DynAPs, for dynein axonemal particles. These organelles display hallmarks of biomolecular condensates, and remarkably, DynAPs are enriched for the stress granule protein G3bp1, but not for other stress granule proteins or P-body proteins. Finally, we show that both the formation and the liquid-like behaviors of DynAPs are disrupted in a model of motile ciliopathy. These findings provide a unifying cell biological framework for a poorly understood class of human disease genes and add motile ciliopathy to the growing roster of human diseases associated with disrupted biological phase separation. eLife Sciences Publications, Ltd 2018-12-18 /pmc/articles/PMC6349401/ /pubmed/30561330 http://dx.doi.org/10.7554/eLife.38497 Text en © 2018, Huizar et al http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Cell Biology
Huizar, Ryan L
Lee, Chanjae
Boulgakov, Alexander A
Horani, Amjad
Tu, Fan
Marcotte, Edward M
Brody, Steven L
Wallingford, John B
A liquid-like organelle at the root of motile ciliopathy
title A liquid-like organelle at the root of motile ciliopathy
title_full A liquid-like organelle at the root of motile ciliopathy
title_fullStr A liquid-like organelle at the root of motile ciliopathy
title_full_unstemmed A liquid-like organelle at the root of motile ciliopathy
title_short A liquid-like organelle at the root of motile ciliopathy
title_sort liquid-like organelle at the root of motile ciliopathy
topic Cell Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6349401/
https://www.ncbi.nlm.nih.gov/pubmed/30561330
http://dx.doi.org/10.7554/eLife.38497
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