Cytoplasmic streaming drifts the polarity cue and enables posteriorization of the<i>Caenorhabditis elegans</i>zygote at the side opposite of sperm entry

Kimura, Kenji; Kimura, Asako

doi:10.1091/mbc.e20-01-0058

Cited by 19 publications

(18 citation statements)

References 35 publications

(63 reference statements)

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“…A similar mechanism of MT-dependent cytoplasmic streaming exists in the C. elegans zygote, but here the alignment of MTs relies on the endoplasmic reticulum [32][33][34]. This meiotic cytoplasmic streaming (MeiCS) influences the position of the sperm-derived pronucleus (PN) and associated centrosomes (PN/centrosome complex), which will determine the antero-posterior axis (AP axis) of the C. elegans embryo [35][36][37][38].…”

Section: Introductionmentioning

confidence: 94%

Going with the flow: insights fromCaenorhabditis eleganszygote polarization

Gubieda

Packer

Squires

et al. 2020

Phil. Trans. R. Soc. B

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Cell polarity is the asymmetric distribution of cellular components along a defined axis. Polarity relies on complex signalling networks between conserved patterning proteins, including the PAR ( par titioning defective) proteins, which become segregated in response to upstream symmetry breaking cues. Although the mechanisms that drive the asymmetric localization of these proteins are dependent upon cell type and context, in many cases the regulation of actomyosin cytoskeleton dynamics is central to the transport, recruitment and/or stabilization of these polarity effectors into defined subcellular domains. The transport or advection of PAR proteins by an actomyosin flow was first observed in the Caenorhabditis elegan s zygote more than a decade ago. Since then a multifaceted approach, using molecular methods, high-throughput screens, and biophysical and computational models, has revealed further aspects of this flow and how polarity regulators respond to and modulate it. Here, we review recent findings on the interplay between actomyosin flow and the PAR patterning networks in the polarization of the C. elegans zygote. We also discuss how these discoveries and developed methods are shaping our understanding of other flow-dependent polarizing systems. This article is part of a discussion meeting issue ‘Contemporary morphogenesis’.

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Section: Introductionmentioning

confidence: 94%

Going with the flow: insights fromCaenorhabditis eleganszygote polarization

Gubieda

Packer

Squires

et al. 2020

Phil. Trans. R. Soc. B

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“…adjacent to the male pronucleus, towards the cell cortex (Wallenfang and Seydoux, 2000;Kimura and Kimura, 2020;Bienkowska and Cowan, 2012). We capture the impact of these interactions by a drag coefficient between the male pronucleus and the cortical layer (d, see SI: Equation 18 and SI: subsubsection 2.1.2).…”

Section: A Mathematical Model Accounts For Ap Axis Convergencementioning

confidence: 99%

“…Cytoplasmic flows, in turn, could transport the male pronucleus (Kimura and Kimura, 2020;Mittasch et al, 2018) towards the closest tip. We refer to this scenario as the cytoplasmic flow-dependent mechanism.…”

mentioning

confidence: 99%

Axis convergence inC. elegansembryos

Bhatnagar¹,

Nestler

Groß

et al. 2023

Preprint

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Embryos develop in a surrounding that guides key aspects of their development. For example, the anteroposterior (AP) body axis is always aligned with the geometric long axis of the surrounding eggshell in fruit flies and worms. The mechanisms that ensure convergence of the AP axis with the long axis of the eggshell remain unresolved. We investigate axis convergence in early C. elegans development, where the nascent AP axis, when misaligned, actively re-aligns to converge with the long axis of the egg. Here, we identify two physical mechanisms that underlie axis convergence. First, bulk cytoplasmic flows, driven by actomyosin cortical flows, can directly reposition the AP axis. Second, active forces generated within the pseudocleavage furrow, a transient actomyosin structure similar to a contractile ring, can drive a mechanical re-orientation such that it becomes positioned perpendicular to the long axis of the egg. This in turn ensures AP axis convergence. Numerical simulations, together with experiments that either abolish the pseudocleavage furrow or change the shape of the egg, demonstrate that the pseudocleavage furrow-dependent mechanism is the key driver of axis convergence. We conclude that active force generation within the actomyosin cortical layer drives axis convergence in the early nematode.

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“…Consistent with the role of centrosomes in polarity induction, SB in cortical contractility will occur from the cortex closest to the position of the centrosomes in the zygote (Bienkowska and Cowan, 2012 ). Even in mutant zygotes with the centrosomes located near the maternal pronucleus during meiosis, SB is always triggered from the cortex proximally to the centrosomes, which results in the establishment of a reversed pattern of cortical flow and PAR distribution (Goldstein and Hird, 1996 ; Kimura and Kimura, 2020 ). These findings indicate that zygote polarization is induced by centrosomes.…”

Section: Induction Of Sb By the Centrosomementioning

confidence: 99%

“…During cytoplasmic streaming, kinesin-1 transports a network of endoplasmic reticula toward the plus end of the microtubule (Kimura et al, 2017 ). If by chance cytoplasmic streaming moves the centrosome–pronucleus complex away from the sperm-entry site toward the opposite pole, where the maternal pronucleus is generally located, the centrosome can induce SB at the cortex opposite to the sperm-entry site (Kimura and Kimura, 2020 ). These observations confirmed that the position of the centrosome at the time of SB, but not the sperm-entry site, specifies the anteroposterior axis.…”

Section: Ensuring the Position Of The Centrosome For Efficient Sbmentioning

confidence: 99%

Mechanochemical Control of Symmetry Breaking in the Caenorhabditis elegans Zygote

Gan

Motegi

2021

Front. Cell Dev. Biol.

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Cell polarity is the asymmetric organization of cellular components along defined axes. A key requirement for polarization is the ability of the cell to break symmetry and achieve a spatially biased organization. Despite different triggering cues in various systems, symmetry breaking (SB) usually relies on mechanochemical modulation of the actin cytoskeleton, which allows for advected movement and reorganization of cellular components. Here, the mechanisms underlying SB in Caenorhabditis elegans zygote, one of the most popular models to study cell polarity, are reviewed. A zygote initiates SB through the centrosome, which modulates mechanics of the cell cortex to establish advective flow of cortical proteins including the actin cytoskeleton and partitioning defective (PAR) proteins. The chemical signaling underlying centrosomal control of the Aurora A kinase–mediated cascade to convert the organization of the contractile actomyosin network from an apolar to polar state is also discussed.

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Cytoplasmic streaming drifts the polarity cue and enables posteriorization of theCaenorhabditis eleganszygote at the side opposite of sperm entry

Cited by 19 publications

References 35 publications

Going with the flow: insights fromCaenorhabditis eleganszygote polarization

Going with the flow: insights fromCaenorhabditis eleganszygote polarization

Axis convergence inC. elegansembryos

Mechanochemical Control of Symmetry Breaking in the Caenorhabditis elegans Zygote

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