Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis

Upon cell cycle exit, centriole-to-basal body transition facilitates cilia formation. The centriolar protein Cp110 is a regulator of this process and cilia inhibitor, but its positive roles in ciliogenesis remain poorly understood. Using Xenopus we show that Cp110 inhibits cilia formation at high le...

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Main Authors: Peter Walentek, Ian K Quigley, Dingyuan I Sun, Umeet K Sajjan, Christopher Kintner, Richard M Harland
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2016-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/17557
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spelling doaj-4e27a14dced0441298cbcaeed6db559d2021-05-05T00:34:35ZengeLife Sciences Publications LtdeLife2050-084X2016-09-01510.7554/eLife.17557Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesisPeter Walentek0https://orcid.org/0000-0002-2332-6068Ian K Quigley1https://orcid.org/0000-0003-0075-8324Dingyuan I Sun2Umeet K Sajjan3Christopher Kintner4Richard M Harland5https://orcid.org/0000-0001-8247-4880Division of Genetics, Genomics and Development, Center for Integrative Genomics, Department of Molecular and Cell Biology, University of California, Berkeley, United StatesMolecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, United StatesDivision of Genetics, Genomics and Development, Center for Integrative Genomics, Department of Molecular and Cell Biology, University of California, Berkeley, United StatesDivision of Genetics, Genomics and Development, Center for Integrative Genomics, Department of Molecular and Cell Biology, University of California, Berkeley, United StatesMolecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, United StatesDivision of Genetics, Genomics and Development, Center for Integrative Genomics, Department of Molecular and Cell Biology, University of California, Berkeley, United StatesUpon cell cycle exit, centriole-to-basal body transition facilitates cilia formation. The centriolar protein Cp110 is a regulator of this process and cilia inhibitor, but its positive roles in ciliogenesis remain poorly understood. Using Xenopus we show that Cp110 inhibits cilia formation at high levels, while optimal levels promote ciliogenesis. Cp110 localizes to cilia-forming basal bodies and rootlets, and is required for ciliary adhesion complexes that facilitate Actin interactions. The opposing roles of Cp110 in ciliation are generated in part by coiled-coil domains that mediate preferential binding to centrioles over rootlets. Because of its dual role in ciliogenesis, Cp110 levels must be precisely controlled. In multiciliated cells, this is achieved by both transcriptional and post-transcriptional regulation through ciliary transcription factors and microRNAs, which activate and repress cp110 to produce optimal Cp110 levels during ciliogenesis. Our data provide novel insights into how Cp110 and its regulation contribute to development and cell function.https://elifesciences.org/articles/17557centriolemucociliary epitheliamiR-34miR-449Foxj1RFX2
collection DOAJ
language English
format Article
sources DOAJ
author Peter Walentek
Ian K Quigley
Dingyuan I Sun
Umeet K Sajjan
Christopher Kintner
Richard M Harland
spellingShingle Peter Walentek
Ian K Quigley
Dingyuan I Sun
Umeet K Sajjan
Christopher Kintner
Richard M Harland
Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis
eLife
centriole
mucociliary epithelia
miR-34
miR-449
Foxj1
RFX2
author_facet Peter Walentek
Ian K Quigley
Dingyuan I Sun
Umeet K Sajjan
Christopher Kintner
Richard M Harland
author_sort Peter Walentek
title Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis
title_short Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis
title_full Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis
title_fullStr Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis
title_full_unstemmed Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis
title_sort ciliary transcription factors and mirnas precisely regulate cp110 levels required for ciliary adhesions and ciliogenesis
publisher eLife Sciences Publications Ltd
series eLife
issn 2050-084X
publishDate 2016-09-01
description Upon cell cycle exit, centriole-to-basal body transition facilitates cilia formation. The centriolar protein Cp110 is a regulator of this process and cilia inhibitor, but its positive roles in ciliogenesis remain poorly understood. Using Xenopus we show that Cp110 inhibits cilia formation at high levels, while optimal levels promote ciliogenesis. Cp110 localizes to cilia-forming basal bodies and rootlets, and is required for ciliary adhesion complexes that facilitate Actin interactions. The opposing roles of Cp110 in ciliation are generated in part by coiled-coil domains that mediate preferential binding to centrioles over rootlets. Because of its dual role in ciliogenesis, Cp110 levels must be precisely controlled. In multiciliated cells, this is achieved by both transcriptional and post-transcriptional regulation through ciliary transcription factors and microRNAs, which activate and repress cp110 to produce optimal Cp110 levels during ciliogenesis. Our data provide novel insights into how Cp110 and its regulation contribute to development and cell function.
topic centriole
mucociliary epithelia
miR-34
miR-449
Foxj1
RFX2
url https://elifesciences.org/articles/17557
work_keys_str_mv AT peterwalentek ciliarytranscriptionfactorsandmirnaspreciselyregulatecp110levelsrequiredforciliaryadhesionsandciliogenesis
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AT dingyuanisun ciliarytranscriptionfactorsandmirnaspreciselyregulatecp110levelsrequiredforciliaryadhesionsandciliogenesis
AT umeetksajjan ciliarytranscriptionfactorsandmirnaspreciselyregulatecp110levelsrequiredforciliaryadhesionsandciliogenesis
AT christopherkintner ciliarytranscriptionfactorsandmirnaspreciselyregulatecp110levelsrequiredforciliaryadhesionsandciliogenesis
AT richardmharland ciliarytranscriptionfactorsandmirnaspreciselyregulatecp110levelsrequiredforciliaryadhesionsandciliogenesis
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