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Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding

The primary cilium is a central signaling hub in cell proliferation and differentiation and is built and disassembled every cell cycle in many animal cells. Disassembly is critically important, as misregulation or delay of cilia loss leads to cell cycle defects. The physical means by which cilia are...

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Autores principales: Mirvis, Mary, Siemers, Kathleen A., Nelson, W. James, Stearns, Tim P.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6699714/
https://www.ncbi.nlm.nih.gov/pubmed/31314751
http://dx.doi.org/10.1371/journal.pbio.3000381
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author Mirvis, Mary
Siemers, Kathleen A.
Nelson, W. James
Stearns, Tim P.
author_facet Mirvis, Mary
Siemers, Kathleen A.
Nelson, W. James
Stearns, Tim P.
author_sort Mirvis, Mary
collection PubMed
description The primary cilium is a central signaling hub in cell proliferation and differentiation and is built and disassembled every cell cycle in many animal cells. Disassembly is critically important, as misregulation or delay of cilia loss leads to cell cycle defects. The physical means by which cilia are lost are poorly understood but are thought to involve resorption of ciliary components into the cell body. To investigate cilium loss in mammalian cells, we used live-cell imaging to comprehensively characterize individual events. The predominant mode of cilium loss was rapid deciliation, in which the membrane and axoneme of the cilium was shed from the cell. Gradual resorption was also observed, as well as events in which a period of gradual resorption was followed by rapid deciliation. Deciliation resulted in intact shed cilia that could be recovered from culture medium and contained both membrane and axoneme proteins. We modulated levels of katanin and intracellular calcium, two putative regulators of deciliation, and found that excess katanin promotes cilia loss by deciliation, independently of calcium. Together, these results suggest that mammalian ciliary loss involves a tunable decision between deciliation and resorption.
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spelling pubmed-66997142019-09-04 Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding Mirvis, Mary Siemers, Kathleen A. Nelson, W. James Stearns, Tim P. PLoS Biol Short Reports The primary cilium is a central signaling hub in cell proliferation and differentiation and is built and disassembled every cell cycle in many animal cells. Disassembly is critically important, as misregulation or delay of cilia loss leads to cell cycle defects. The physical means by which cilia are lost are poorly understood but are thought to involve resorption of ciliary components into the cell body. To investigate cilium loss in mammalian cells, we used live-cell imaging to comprehensively characterize individual events. The predominant mode of cilium loss was rapid deciliation, in which the membrane and axoneme of the cilium was shed from the cell. Gradual resorption was also observed, as well as events in which a period of gradual resorption was followed by rapid deciliation. Deciliation resulted in intact shed cilia that could be recovered from culture medium and contained both membrane and axoneme proteins. We modulated levels of katanin and intracellular calcium, two putative regulators of deciliation, and found that excess katanin promotes cilia loss by deciliation, independently of calcium. Together, these results suggest that mammalian ciliary loss involves a tunable decision between deciliation and resorption. Public Library of Science 2019-07-17 /pmc/articles/PMC6699714/ /pubmed/31314751 http://dx.doi.org/10.1371/journal.pbio.3000381 Text en © 2019 Mirvis et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Short Reports
Mirvis, Mary
Siemers, Kathleen A.
Nelson, W. James
Stearns, Tim P.
Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding
title Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding
title_full Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding
title_fullStr Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding
title_full_unstemmed Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding
title_short Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding
title_sort primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding
topic Short Reports
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6699714/
https://www.ncbi.nlm.nih.gov/pubmed/31314751
http://dx.doi.org/10.1371/journal.pbio.3000381
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