Centriolar SAS-7 acts upstream of SPD-2 to regulate centriole assembly and pericentriolar material formation

  1. Kenji Sugioka
  2. Danielle R Hamill
  3. Joshua B Lowry
  4. Marie E McNeely
  5. Molly Enrick
  6. Alyssa C Richter
  7. Lauren E Kiebler
  8. James R Priess
  9. Bruce Bowerman  Is a corresponding author
  1. University of Oregon, United States
  2. Ohio Wesleyan University, United States
  3. Fred Hutchinson Cancer Research Center, United States

Abstract

The centriole/basal body is a eukaryotic organelle that plays essential roles in cell division and signaling. Among five known core centriole proteins, SPD-2/Cep192 is the first recruited to the site of daughter centriole formation and regulates the centriolar localization of the other components in C. elegans and in humans. However, the molecular basis for SPD-2 centriolar localization remains unknown. Here we describe a new centriole component, the coiled-coil protein SAS-7, as a regulator of centriole duplication, assembly and elongation. We also show that SAS-7 binds SPD-2 and regulates SPD-2 centriolar recruitment, while SAS-7 centriolar localization is SPD-2-independent. Furthermore, pericentriolar material (PCM) formation is abnormal in sas-7 mutants, and the PCM-dependent induction of cell polarity that defines the anterior-posterior body axis frequently fails. We conclude that SAS-7 functions at the earliest step in centriole duplication yet identified and plays important roles in the orchestration of centriole and PCM assembly.

Article and author information

Author details

  1. Kenji Sugioka

    Institute of Molecular Biology, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5830-9639
  2. Danielle R Hamill

    Department of Zoology, Ohio Wesleyan University, Delaware, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Joshua B Lowry

    Institute of Molecular Biology, University of Oregon, Eugene, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Marie E McNeely

    Department of Zoology, Ohio Wesleyan University, Delaware, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Molly Enrick

    Department of Zoology, Ohio Wesleyan University, Delaware, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alyssa C Richter

    Department of Zoology, Ohio Wesleyan University, Delaware, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Lauren E Kiebler

    Department of Zoology, Ohio Wesleyan University, Delaware, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. James R Priess

    Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Bruce Bowerman

    Institute of Molecular Biology, University of Oregon, Eugene, United States
    For correspondence
    bbowerman@molbio.uoregon.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6479-8707

Funding

Human Frontier Science Program

  • Kenji Sugioka

Journal of Cell Science Traveling Fellowship

  • Kenji Sugioka

National Institute of General Medical Sciences

  • Kenji Sugioka
  • Danielle R Hamill
  • Joshua B Lowry
  • Marie E McNeely
  • Molly Enrick
  • Alyssa C Richter
  • Lauren E Kiebler
  • James R Priess
  • Bruce Bowerman

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

Reviewing Editor

  1. Karen Oegema, University of California, San Diego, United States

Version history

  1. Received: August 4, 2016
  2. Accepted: January 15, 2017
  3. Accepted Manuscript published: January 16, 2017 (version 1)
  4. Version of Record published: March 8, 2017 (version 2)

Copyright

© 2017, Sugioka 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. Kenji Sugioka
  2. Danielle R Hamill
  3. Joshua B Lowry
  4. Marie E McNeely
  5. Molly Enrick
  6. Alyssa C Richter
  7. Lauren E Kiebler
  8. James R Priess
  9. Bruce Bowerman
(2017)
Centriolar SAS-7 acts upstream of SPD-2 to regulate centriole assembly and pericentriolar material formation
eLife 6:e20353.
https://doi.org/10.7554/eLife.20353

Share this article

https://doi.org/10.7554/eLife.20353

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