Cargando…

Regulated changes in material properties underlie centrosome disassembly during mitotic exit

Centrosomes must resist microtubule-mediated forces for mitotic chromosome segregation. During mitotic exit, however, centrosomes are deformed and fractured by those same forces, which is a key step in centrosome disassembly. How the functional material properties of centrosomes change throughout th...

Descripción completa

Detalles Bibliográficos
Autores principales: Mittasch, Matthäus, Tran, Vanna M., Rios, Manolo U., Fritsch, Anatol W., Enos, Stephen J., Ferreira Gomes, Beatriz, Bond, Alec, Kreysing, Moritz, Woodruff, Jeffrey B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Rockefeller University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7147112/
https://www.ncbi.nlm.nih.gov/pubmed/32050025
http://dx.doi.org/10.1083/jcb.201912036
_version_ 1783520354469150720
author Mittasch, Matthäus
Tran, Vanna M.
Rios, Manolo U.
Fritsch, Anatol W.
Enos, Stephen J.
Ferreira Gomes, Beatriz
Bond, Alec
Kreysing, Moritz
Woodruff, Jeffrey B.
author_facet Mittasch, Matthäus
Tran, Vanna M.
Rios, Manolo U.
Fritsch, Anatol W.
Enos, Stephen J.
Ferreira Gomes, Beatriz
Bond, Alec
Kreysing, Moritz
Woodruff, Jeffrey B.
author_sort Mittasch, Matthäus
collection PubMed
description Centrosomes must resist microtubule-mediated forces for mitotic chromosome segregation. During mitotic exit, however, centrosomes are deformed and fractured by those same forces, which is a key step in centrosome disassembly. How the functional material properties of centrosomes change throughout the cell cycle, and how they are molecularly tuned, remain unknown. Here, we used optically induced flow perturbations to determine the molecular basis of centrosome strength and ductility in C. elegans embryos. We found that both properties declined sharply at anaphase onset, long before natural disassembly. This mechanical transition required PP2A phosphatase and correlated with inactivation of PLK-1 (Polo kinase) and SPD-2 (Cep192). In vitro, PLK-1 and SPD-2 directly protected centrosome scaffolds from force-induced disassembly. Our results suggest that, before anaphase, PLK-1 and SPD-2 respectively confer strength and ductility to the centrosome scaffold so that it can resist microtubule-pulling forces. In anaphase, centrosomes lose PLK-1 and SPD-2 and transition to a weak, brittle state that enables force-mediated centrosome disassembly.
format Online
Article
Text
id pubmed-7147112
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Rockefeller University Press
record_format MEDLINE/PubMed
spelling pubmed-71471122020-04-14 Regulated changes in material properties underlie centrosome disassembly during mitotic exit Mittasch, Matthäus Tran, Vanna M. Rios, Manolo U. Fritsch, Anatol W. Enos, Stephen J. Ferreira Gomes, Beatriz Bond, Alec Kreysing, Moritz Woodruff, Jeffrey B. J Cell Biol Article Centrosomes must resist microtubule-mediated forces for mitotic chromosome segregation. During mitotic exit, however, centrosomes are deformed and fractured by those same forces, which is a key step in centrosome disassembly. How the functional material properties of centrosomes change throughout the cell cycle, and how they are molecularly tuned, remain unknown. Here, we used optically induced flow perturbations to determine the molecular basis of centrosome strength and ductility in C. elegans embryos. We found that both properties declined sharply at anaphase onset, long before natural disassembly. This mechanical transition required PP2A phosphatase and correlated with inactivation of PLK-1 (Polo kinase) and SPD-2 (Cep192). In vitro, PLK-1 and SPD-2 directly protected centrosome scaffolds from force-induced disassembly. Our results suggest that, before anaphase, PLK-1 and SPD-2 respectively confer strength and ductility to the centrosome scaffold so that it can resist microtubule-pulling forces. In anaphase, centrosomes lose PLK-1 and SPD-2 and transition to a weak, brittle state that enables force-mediated centrosome disassembly. Rockefeller University Press 2020-02-12 /pmc/articles/PMC7147112/ /pubmed/32050025 http://dx.doi.org/10.1083/jcb.201912036 Text en © 2020 Mittasch et al. https://creativecommons.org/licenses/by/4.0/This article is available under a Creative Commons License (Attribution 4.0 International, as described at https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Mittasch, Matthäus
Tran, Vanna M.
Rios, Manolo U.
Fritsch, Anatol W.
Enos, Stephen J.
Ferreira Gomes, Beatriz
Bond, Alec
Kreysing, Moritz
Woodruff, Jeffrey B.
Regulated changes in material properties underlie centrosome disassembly during mitotic exit
title Regulated changes in material properties underlie centrosome disassembly during mitotic exit
title_full Regulated changes in material properties underlie centrosome disassembly during mitotic exit
title_fullStr Regulated changes in material properties underlie centrosome disassembly during mitotic exit
title_full_unstemmed Regulated changes in material properties underlie centrosome disassembly during mitotic exit
title_short Regulated changes in material properties underlie centrosome disassembly during mitotic exit
title_sort regulated changes in material properties underlie centrosome disassembly during mitotic exit
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7147112/
https://www.ncbi.nlm.nih.gov/pubmed/32050025
http://dx.doi.org/10.1083/jcb.201912036
work_keys_str_mv AT mittaschmatthaus regulatedchangesinmaterialpropertiesunderliecentrosomedisassemblyduringmitoticexit
AT tranvannam regulatedchangesinmaterialpropertiesunderliecentrosomedisassemblyduringmitoticexit
AT riosmanolou regulatedchangesinmaterialpropertiesunderliecentrosomedisassemblyduringmitoticexit
AT fritschanatolw regulatedchangesinmaterialpropertiesunderliecentrosomedisassemblyduringmitoticexit
AT enosstephenj regulatedchangesinmaterialpropertiesunderliecentrosomedisassemblyduringmitoticexit
AT ferreiragomesbeatriz regulatedchangesinmaterialpropertiesunderliecentrosomedisassemblyduringmitoticexit
AT bondalec regulatedchangesinmaterialpropertiesunderliecentrosomedisassemblyduringmitoticexit
AT kreysingmoritz regulatedchangesinmaterialpropertiesunderliecentrosomedisassemblyduringmitoticexit
AT woodruffjeffreyb regulatedchangesinmaterialpropertiesunderliecentrosomedisassemblyduringmitoticexit