De novo centriole formation in human cells is error-prone and does not require SAS-6 self-assembly

  1. Won-Jing Wang
  2. Devrim Acehan
  3. Chien-Han Kao
  4. Wann-Neng Jane
  5. Kunihiro Uryu
  6. Meng-Fu (Bryan) Tsou  Is a corresponding author
  1. National Yang-Ming University, Taiwan
  2. The Rockefeller University, United States
  3. Academia Sinica, Taiwan
  4. Memorial Sloan-Kettering Cancer Center, United States

Abstract

Vertebrate centrioles normally propagate through duplication, but in the absence of preexisting centrioles, de novo synthesis can occur. Consistently, centriole formation is thought to strictly rely on self-assembly, involving self-oligomerization of the centriolar protein SAS-6. Here, through reconstitution of de novo synthesis in human cells, we surprisingly found that normal looking centrioles capable of duplication and ciliation can arise in the absence of SAS-6 self-oligomerization. Moreover, whereas canonically duplicated centrioles always form correctly, de novo centrioles are prone to structural errors, even in the presence of SAS-6 self-oligomerization. These results indicate that centriole biogenesis does not strictly depend on SAS-6 self-assembly, and may require preexisting centrioles to ensure structural accuracy, fundamentally deviating from the current paradigm.

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Author details

  1. Won-Jing Wang

    Institute of Biochemistry and Molecular Biology, College of Life Sciences, National Yang-Ming University, Taipei, Taiwan
    Competing interests
    The authors declare that no competing interests exist.
  2. Devrim Acehan

    Electron Microscopy Resource Center, The Rockefeller University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Chien-Han Kao

    Institute of Biochemistry and Molecular Biology, College of Life Sciences, National Yang-Ming University, Taipei, Taiwan
    Competing interests
    The authors declare that no competing interests exist.
  4. Wann-Neng Jane

    Institute of Plant and Microbial Biology, Academia Sinica, Taipei, Taiwan
    Competing interests
    The authors declare that no competing interests exist.
  5. Kunihiro Uryu

    Electron Microscopy Resource Center, The Rockefeller University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Meng-Fu (Bryan) Tsou

    Cell Biology Program, Memorial Sloan-Kettering Cancer Center, New York, United States
    For correspondence
    tsoum@mskcc.org
    Competing interests
    The authors declare that no competing interests exist.

Reviewing Editor

  1. Tim Stearns, Stanford University, United States

Publication history

  1. Received: August 5, 2015
  2. Accepted: November 25, 2015
  3. Accepted Manuscript published: November 26, 2015 (version 1)
  4. Version of Record published: December 31, 2015 (version 2)

Copyright

© 2015, Wang 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. Won-Jing Wang
  2. Devrim Acehan
  3. Chien-Han Kao
  4. Wann-Neng Jane
  5. Kunihiro Uryu
  6. Meng-Fu (Bryan) Tsou
(2015)
De novo centriole formation in human cells is error-prone and does not require SAS-6 self-assembly
eLife 4:e10586.
https://doi.org/10.7554/eLife.10586

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