A disassembly-driven mechanism explains F-actin-mediated chromosome transport in starfish oocytes

While contraction of sarcomeric actomyosin assemblies is well understood, this is not the case for disordered networks of actin filaments (F-actin) driving diverse essential processes in animal cells. For example, at the onset of meiosis in starfish oocytes a contractile F-actin network forms in the...

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Bibliographic Details
Published in:eLife 2018-01, Vol.7
Main Authors: Bun, Philippe, Dmitrieff, Serge, Belmonte, Julio M, Nédélec, François J, Lénárt, Péter
Format: Article
Language:English
Subjects:
Actin
actin dynamics
Actins - metabolism
Actomyosin
Aneuploidy
Animals
Biological Transport
Cell adhesion & migration
Cell Biology
Cell division
Chromosomes
Chromosomes - metabolism
Computer applications
Computer Simulation
Contractility
Contraction
cytoskeleton
Embryogenesis
Filaments
Mathematical models
Meiosis
Models, Biological
Myosin
oocyte meiosis
Oocytes
Oocytes - physiology
Patiria miniata
Polymerization
Starfish
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Summary:While contraction of sarcomeric actomyosin assemblies is well understood, this is not the case for disordered networks of actin filaments (F-actin) driving diverse essential processes in animal cells. For example, at the onset of meiosis in starfish oocytes a contractile F-actin network forms in the nuclear region transporting embedded chromosomes to the assembling microtubule spindle. Here, we addressed the mechanism driving contraction of this 3D disordered F-actin network by comparing quantitative observations to computational models. We analyzed 3D chromosome trajectories and imaged filament dynamics to monitor network behavior under various physical and chemical perturbations. We found no evidence of myosin activity driving network contractility. Instead, our observations are well explained by models based on a disassembly-driven contractile mechanism. We reconstitute this disassembly-based contractile system revealing a simple architecture that robustly drives chromosome transport to prevent aneuploidy in the large oocyte, a prerequisite for normal embryonic development.
ISSN:2050-084X
2050-084X
DOI:10.7554/elife.31469