1. Cell Biology
  2. Developmental Biology

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

  1. Peter Walentek  Is a corresponding author
  2. Ian K Quigley
  3. Dingyuan I Sun
  4. Umeet K Sajjan
  5. Christopher Kintner
  6. Richard M Harland  Is a corresponding author
  1. University of California, Berkeley, United States
  2. Salk Institute for Biological Studies, United States
https://doi.org/10.7554/eLife.17557
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  1. Peter Walentek
  2. Ian K Quigley
  3. Dingyuan I Sun
  4. Umeet K Sajjan
  5. Christopher Kintner
  6. Richard M Harland
(2016)
Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis
eLife 5:e17557.
https://doi.org/10.7554/eLife.17557
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Abstract

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.

Data availability

The following data sets were generated
    1. Quigley IK
    2. Kintner C
    (2015) RNAseq profiling of multiciliated cells
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE76342).
    http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE76342
The following previously published data sets were used
    1. Ma L
    2. Quigley IK
    3. Kintner C
    (2014) Multicilin drives centriole biogenesis via E2f proteins
    Publicly available at the NCBI Gene Expression Omnibus (accession no: GSE59309).
    http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE59309

Article and author information

Author details

  1. Peter Walentek

    Division of Genetics, Genomics and Development, University of California, Berkeley, Berkeley, United States
    For correspondence
    walentek@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2332-6068

  2. Ian K Quigley

    Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0075-8324

  3. Dingyuan I Sun

    Division of Genetics, Genomics and Development, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  4. Umeet K Sajjan

    Division of Genetics, Genomics and Development, University of California, Berkeley, Berkeley, United States
    Competing interests
    The authors declare that no competing interests exist.

  5. Christopher Kintner

    Molecular Neurobiology Laboratory, Salk Institute for Biological Studies, La Jolla, United States
    Competing interests
    The authors declare that no competing interests exist.

  6. Richard M Harland

    Division of Genetics, Genomics and Development, University of California, Berkeley, Berkeley, United States
    For correspondence
    harland@berkeley.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8247-4880

Funding

Deutsche Forschungsgemeinschaft (Wa 3365/1-1)

  • Peter Walentek

National Heart, Lung, and Blood Institute (K99HL127275)

  • Peter Walentek

National Institute of General Medical Sciences (GM42341)

  • Richard M Harland

National Institute of General Medical Sciences (GM076507)

  • Christopher Kintner

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Janet Rossant, University of Toronto, Canada

Ethics

Animal experimentation: This work was done with approval of University of California, Berkeley's Animal Care and Use Committee. University of California, Berkeley's assurance number is A3084-01, and is on file at the National Institutes of Health Office of Laboratory Animal Welfare.

Version history

  1. Received: May 5, 2016
  2. Accepted: September 12, 2016
  3. Accepted Manuscript published: September 13, 2016 (version 1)
  4. Version of Record published: September 30, 2016 (version 2)

Copyright

© 2016, Walentek et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Peter Walentek
  2. Ian K Quigley
  3. Dingyuan I Sun
  4. Umeet K Sajjan
  5. Christopher Kintner
  6. Richard M Harland
(2016)
Ciliary transcription factors and miRNAs precisely regulate Cp110 levels required for ciliary adhesions and ciliogenesis
eLife 5:e17557.
https://doi.org/10.7554/eLife.17557

Share this article

https://doi.org/10.7554/eLife.17557

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