Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells

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 cel...

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Main Authors: Nicolaas C Baudoin, Joshua M Nicholson, Kimberly Soto, Olga Martin, Jing Chen, Daniela Cimini
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2020-04-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/54565
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author Nicolaas C Baudoin
Joshua M Nicholson
Kimberly Soto
Olga Martin
Jing Chen
Daniela Cimini
author_facet Nicolaas C Baudoin
Joshua M Nicholson
Kimberly Soto
Olga Martin
Jing Chen
Daniela Cimini
author_sort Nicolaas C Baudoin
collection DOAJ
description 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.
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spelling doaj.art-d10c3842d6ed4a50bbcb757557243f132022-12-22T02:05:13ZengeLife Sciences Publications LtdeLife2050-084X2020-04-01910.7554/eLife.54565Asymmetric clustering of centrosomes defines the early evolution of tetraploid cellsNicolaas C Baudoin0https://orcid.org/0000-0003-3316-5293Joshua M Nicholson1Kimberly Soto2Olga Martin3Jing Chen4https://orcid.org/0000-0001-6321-0505Daniela Cimini5https://orcid.org/0000-0002-4082-4894Department of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United StatesDepartment of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United StatesDepartment of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United StatesDepartment of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United StatesDepartment of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United StatesDepartment of Biological Sciences and Fralin Life Sciences Institute, Virginia Tech, Blacksburg, United StatesTetraploidy 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.https://elifesciences.org/articles/54565tetraploidycentrosomescell division
spellingShingle Nicolaas C Baudoin
Joshua M Nicholson
Kimberly Soto
Olga Martin
Jing Chen
Daniela Cimini
Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells
eLife
tetraploidy
centrosomes
cell division
title Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells
title_full Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells
title_fullStr Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells
title_full_unstemmed Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells
title_short Asymmetric clustering of centrosomes defines the early evolution of tetraploid cells
title_sort asymmetric clustering of centrosomes defines the early evolution of tetraploid cells
topic tetraploidy
centrosomes
cell division
url https://elifesciences.org/articles/54565
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