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

Bun, Philippe; Dmitrieff, Serge; Belmonte, Julio M.; Nédélec, François; Lénárt, Péter

doi:10.7554/elife.31469

Cited by 31 publications

(38 citation statements)

References 73 publications

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“…4B) (Mori et al, 2014). These data thus allow us to conclude that the F-actin patches are nucleated by the Arp2/3 complex, while filaments of the F-actin network are polymerized by other factors, likely formins (Bun et al, 2018). We have shown previously that the F-actin patches are nucleated around DNA-coated beads (Lénárt et al, 2005).…”

Section: Disassembly Of the F-actin Patches Coordinates Capture By MIsupporting

confidence: 53%

“…mRNAs were dissolved in water (typical concentration 3-5 µg/µl) and injected into the oocytes up to 5% of the oocyte volume. Histone H1 and Utrophin CH domain (UtrCH) (Burkel et al, 2007) were labeled with Alexa fluorophores as described previously (Bun et al, 2018). Phalloidin labeled with the indicated Alexa fluorophores (Invitrogen) was dissolved in methanol, and was then air-dried prior use and dissolved in PBS for microinjection and immunostaining.…”

Section: Live-cell Fluorescent Markersmentioning

confidence: 99%

“…(B) Table summarizing the main parameters used in the model. (C) Chromosome pair-wise velocity analysis to derive the network contraction rate, as described in (Bun et al, 2018). Comparison between experimental data (red) and simulation (grey).…”

Section: Supplemental Figure S6 Details Of the Computer Simulations (A)mentioning

confidence: 99%

“…The specific cellular geometry of oocytes, featuring a large nucleus and a small meiotic spindle challenges chromosome 'search-and-capture'. Indeed, we have shown that in starfish oocytes the known microtubule-driven mechanisms are insufficient, and a contractile actin filament (F-actin) network is additionally required to transport chromosomes to the assembling microtubule spindle (Lénárt et al, 2005;Mori et al, 2011;Bun et al, 2018). The F-actin network forms at nuclear envelope breakdown (NEBD), filling the entire 70-μm diameter nuclear space.…”

Section: Introductionmentioning

confidence: 99%

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F-actin patches nucleated on chromosomes coordinate capture by microtubules in oocyte meiosis

Burdyniuk

Callegari²,

Mori³

et al. 2018

Preprint

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Capture of each and every chromosome by spindle microtubules is essential to prevent chromosome loss and aneuploidy. In somatic cells, astral microtubules search and capture chromosomes forming lateral attachments to kinetochores. However, this mechanism alone is insufficient in large oocytes. We have previously shown that a contractile F-actin network is additionally required to collect chromosomes scattered in the 70-μm starfish oocyte nucleus. How this F-actin-driven mechanism is coordinated with microtubule capture remained unknown. Here, we show that after nuclear envelope breakdown Arp2/3-nucleated F-actin patches form around chromosomes in a Ran-GTPdependent manner, and we propose that these structures sterically block kinetochore-microtubule attachments. Once F-actin-driven chromosome transport is complete, coordinated disassembly of these F-actin patches allows synchronous capture by microtubules. Our observations indicate that this coordination is necessary, as early capture of chromosomes by microtubules would interfere with F-actin-driven transport leading to chromosome loss and formation of aneuploid eggs.All rights reserved. No reuse allowed without permission.

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Section: Disassembly Of the F-actin Patches Coordinates Capture By MIsupporting

confidence: 53%

Section: Live-cell Fluorescent Markersmentioning

confidence: 99%

Section: Supplemental Figure S6 Details Of the Computer Simulations (A)mentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

F-actin patches nucleated on chromosomes coordinate capture by microtubules in oocyte meiosis

Burdyniuk

Callegari²,

Mori³

et al. 2018

Preprint

Self Cite

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show abstract

“…Theoretical work and in vivo experiments suggest that possible sources of the driving force underlying myosin-independent constriction mechanisms depend on actin-crosslinking proteins and actin filament disassembly (16)(17)(18)(19)(20). In microtubule networks, similar force-generating mechanisms, independent of molecular motors, are directly experimentally observed.…”

Section: Introductionmentioning

confidence: 99%

Anillin propels myosin-independent constriction of actin rings

Kučera

Janda

Siahaan

et al. 2020

Preprint

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Constriction of the actin cytokinetic ring is an essential step of cell division. In a generally accepted view, the constriction is driven by relative sliding of actin filaments propelled by myosin motors. However, in multiple organisms, the ring constriction is myosin independent. How actin rings constrict in the absence of motor activity remains unclear. Here, we demonstrate that actin contractility can be propelled by anillin, a diffusible non-motor actin crosslinker, localising to the cytokinetic ring. We in vitro observed the formation and constriction of rings comprising multiple actin filaments bundled by anillin. Rings constricted due to anillin-generated forces maximising the overlap lengths between the filaments. Actin disassembly promoted constriction. We propose that actin crosslinkers, generating forces complementary to molecular motors, contribute to the contractility of diverse actin structures, including the cytokinetic ring.

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Morphogenesis: a focus on marine invertebrates

Dong

2019

Mar Life Sci Technol

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Morphogenesis is a process describing how the shapes of living tissues and bodies are created during development. Living and fossil organisms exhibit enormously diverse tissue architecture and body forms, although the functions of organs are evolutionally conserved. Current knowledge reveals that relatively conserved mechanisms are applied to control development among different species. However, the regulations of morphogenesis are quite diverse in detail. Animals in the ocean display a wide range of diversity of morphology suitable for their seawater environment. Nevertheless, compared with the intensive studies on terrestrial animals, research on marine animal morphogenesis is still insufficient. The increasing genomic data and the recently available gene editing methods, together with the fast development of imaging techniques, quantitative analyses and biophysical models, provide us the opportunities to have a deeper understanding of the principles that drive the diverse morphogenetic processes in marine animals. In this review, we summarize the recent studies of morphogenesis and evolution at molecular, cellular and tissue levels, with a focus on three model marine animals, namely ascidians, sea urchins and sea anemones.

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

Cited by 31 publications

References 73 publications

F-actin patches nucleated on chromosomes coordinate capture by microtubules in oocyte meiosis

F-actin patches nucleated on chromosomes coordinate capture by microtubules in oocyte meiosis

Anillin propels myosin-independent constriction of actin rings

Morphogenesis: a focus on marine invertebrates

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