Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells

Abstract

Tetraploidy has long been of interest to both cell and cancer biologists, partly because of its documented role in tumorigenesis. A common model proposes that the extra centrosomes that are typically acquired during tetraploidization are responsible for driving tumorigenesis. However, tetraploid cells evolved in culture have been shown to lack extra centrosomes. This observation raises questions about how tetraploid cells evolve and more specifically about the mechanisms(s) underlying centrosome loss. Here, using a combination of fixed cell analysis, live cell imaging, and mathematical modeling, we show that populations of newly formed tetraploid cells rapidly evolve in vitro to retain a near-tetraploid chromosome number while losing the extra centrosomes gained at the time of tetraploidization. This appears to happen through a process of natural selection in which tetraploid cells that inherit a single centrosome during a bipolar division with asymmetric centrosome clustering are favored for long-term survival.

Data availability

All data generated during the study are provided in clearly labeled source data files in excel format.

Article and author information

Author details

  1. Nicolaas C Baudoin

    Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Joshua M Nicholson

    Department of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Kimberly Soto

    Department of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Olga Martin

    Department of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Jing Chen

    Department of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United States
    For correspondence
    chenjing@vt.edu
    Competing interests
    The authors declare that no competing interests exist.
  6. Daniela Cimini

    Department of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United States
    For correspondence
    cimini@vt.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4082-4894

Funding

Virginia Tech College of Science (Dean's Discovery Fund)

  • Daniela Cimini

Fralin Life Sciences Institute (Discretionary funds)

  • Daniela Cimini

ICTAS Center for Engineered Health (Seed funding)

  • Daniela Cimini

National Science Foundation (MCB-1517506)

  • Daniela Cimini

Virginia Tech Graduate School (BIOTRANS IGEP)

  • Nicolaas C Baudoin

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

Reviewing Editor

  1. Jon Pines, Institute of Cancer Research Research, United Kingdom

Version history

  1. Received: December 19, 2019
  2. Accepted: April 28, 2020
  3. Accepted Manuscript published: April 29, 2020 (version 1)
  4. Version of Record published: May 26, 2020 (version 2)
  5. Version of Record updated: June 5, 2020 (version 3)

Copyright

© 2020, Baudoin 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. Nicolaas C Baudoin
  2. Joshua M Nicholson
  3. Kimberly Soto
  4. Olga Martin
  5. Jing Chen
  6. Daniela Cimini
(2020)
Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells
eLife 9:e54565.
https://doi.org/10.7554/eLife.54565

Share this article

https://doi.org/10.7554/eLife.54565

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