Centriole triplet microtubules are required for stable centriole formation and inheritance in human cells

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Cite as: eLife 2017;6:e29061 doi: 10.7554/eLife.29061

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Abstract

Centrioles are composed of long-lived microtubules arranged in nine triplets. However, the contribution of triplet microtubules to mammalian centriole formation and stability is unknown. Little is known of the mechanism of triplet microtubule formation, but experiments in unicellular eukaryotes indicate that delta-tubulin and epsilon-tubulin, two less-studied tubulin family members, are required. Here, we report that centrioles in delta-tubulin and epsilon-tubulin null mutant human cells lack triplet microtubules and fail to undergo centriole maturation. These aberrant centrioles are formed de novo each cell cycle, but are unstable and do not persist to the next cell cycle, leading to a futile cycle of centriole formation and disintegration. Disintegration can be suppressed by paclitaxel treatment. Delta-tubulin and epsilon-tubulin physically interact, indicating that these tubulins act together to maintain triplet microtubules and that these are necessary for inheritance of centrioles from one cell cycle to the next

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Jennifer T Wang

Department of Biology, Stanford University, Stanford, United States

Competing interests
The authors declare that no competing interests exist.

0000-0002-8506-5182
Dong Kong

Laboratory of Protein Dynamics and Signaling, Center for Cancer Research - Frederick, National Cancer Institute, National Institutes of Health, Frederick, United States

Competing interests
The authors declare that no competing interests exist.
Christian R Hoerner

Division of Oncology, Department of Medicine, Stanford School of Medicine, Stanford, United States

Competing interests
The authors declare that no competing interests exist.
Jadranka Loncarek

Laboratory of Protein Dynamics and Signaling, Center for Cancer Research - Frederick, National Cancer Institute, National Institutes of Health, Frederick, United States

Competing interests
The authors declare that no competing interests exist.
Tim Stearns

Department of Biology, Stanford University, Stanford, United States

For correspondence
stearns@stanford.edu

Competing interests
The authors declare that no competing interests exist.

0000-0002-0671-6582

Funding

National Institute of General Medical Sciences (5 F32 GM117678)

Jennifer T Wang

National Cancer Institute (Intramural Program)

Dong Kong
Jadranka Loncarek

National Institute of General Medical Sciences (R01GM052022)

Tim Stearns

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

Reviewing Editor

Anthony A Hyman, Max Planck Institute of Molecular Cell Biology and Genetics, Germany

Publication history

Received: June 2, 2017
Accepted: September 12, 2017
Accepted Manuscript published: September 14, 2017 (version 1)
Version of Record published: October 23, 2017 (version 2)

Copyright

This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.