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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...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2019
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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. |
format | Online Article Text |
id | pubmed-6699714 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2019 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
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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