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...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2019-07-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3000381 |
| _version_ | 1819124392562524160 |
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| author | Mary Mirvis Kathleen A Siemers W James Nelson Tim P Stearns |
| author_facet | Mary Mirvis Kathleen A Siemers W James Nelson Tim P Stearns |
| author_sort | Mary Mirvis |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-22T07:23:31Z |
| format | Article |
| id | doaj.art-578b385eeb72471ca0cb473a78099c4d |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-22T07:23:31Z |
| publishDate | 2019-07-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-578b385eeb72471ca0cb473a78099c4d2022-12-21T18:34:13ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852019-07-01177e300038110.1371/journal.pbio.3000381Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding.Mary MirvisKathleen A SiemersW James NelsonTim P StearnsThe 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.https://doi.org/10.1371/journal.pbio.3000381 |
| spellingShingle | Mary Mirvis Kathleen A Siemers W James Nelson Tim P Stearns Primary cilium loss in mammalian cells occurs predominantly by whole-cilium shedding. PLoS Biology |
| 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 |
| url | https://doi.org/10.1371/journal.pbio.3000381 |
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