» Articles » PMID: 31314751

Primary Cilium Loss in Mammalian Cells Occurs Predominantly by Whole-cilium Shedding

Overview
Journal PLoS Biol
Specialty Biology
Date 2019 Jul 18
PMID 31314751
Citations 43
Authors
Affiliations
Soon will be listed here.
Abstract

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.

Citing Articles

Permanent cilia loss during cerebellar granule cell neurogenesis involves withdrawal of cilia maintenance and centriole capping.

Constable S, Ott C, Lemire A, White K, Xun Y, Lim A Proc Natl Acad Sci U S A. 2024; 121(52):e2408083121.

PMID: 39705308 PMC: 11670249. DOI: 10.1073/pnas.2408083121.


Mechanisms of axoneme and centriole elimination in Naegleria gruberi.

Woglar A, Busso C, Garcia-Rodriguez G, Douma F, Croisier M, Knott G EMBO Rep. 2024; 26(2):385-406.

PMID: 39623167 PMC: 11772885. DOI: 10.1038/s44319-024-00329-w.


The intraflagellar transport cycle.

Lacey S, Pigino G Nat Rev Mol Cell Biol. 2024; 26(3):175-192.

PMID: 39537792 DOI: 10.1038/s41580-024-00797-x.


Permanent deconstruction of intracellular primary cilia in differentiating granule cell neurons.

Ott C, Constable S, Nguyen T, White K, Lee W, Lippincott-Schwartz J J Cell Biol. 2024; 223(10).

PMID: 39137043 PMC: 11320830. DOI: 10.1083/jcb.202404038.


Extracellular vesicles.

Wang J, Barr M, Wehman A Genetics. 2024; 227(4).

PMID: 38884207 PMC: 11304975. DOI: 10.1093/genetics/iyae088.


References
1.
Piao T, Luo M, Wang L, Guo Y, Li D, Li P . A microtubule depolymerizing kinesin functions during both flagellar disassembly and flagellar assembly in Chlamydomonas. Proc Natl Acad Sci U S A. 2009; 106(12):4713-8. PMC: 2660737. DOI: 10.1073/pnas.0808671106. View

2.
Ishikawa H, Thompson J, Yates 3rd J, Marshall W . Proteomic analysis of mammalian primary cilia. Curr Biol. 2012; 22(5):414-9. PMC: 3298568. DOI: 10.1016/j.cub.2012.01.031. View

3.
Lee K, Johmura Y, Yu L, Park J, Gao Y, Bang J . Identification of a novel Wnt5a-CK1ɛ-Dvl2-Plk1-mediated primary cilia disassembly pathway. EMBO J. 2012; 31(14):3104-17. PMC: 3400010. DOI: 10.1038/emboj.2012.144. View

4.
Sanders M, Salisbury J . Centrin plays an essential role in microtubule severing during flagellar excision in Chlamydomonas reinhardtii. J Cell Biol. 1994; 124(5):795-805. PMC: 2119956. DOI: 10.1083/jcb.124.5.795. View

5.
Satir B, Sale W, Satir P . Membrane renewal after dibucaine deciliation of Tetrahymena. Freeze-fracture technique, cilia, membrane structure. Exp Cell Res. 1976; 97:83-91. DOI: 10.1016/0014-4827(76)90657-1. View