Polar actomyosin contractility destabilizes the position of the cytokinetic furrow

Sedzinski, Jakub; Biro, Maté; Oswald, Annelie; Tinévez, Jean-Yves; Salbreux, Guillaume; Paluch, Ewa K.

doi:10.1038/nature10286

Cited by 307 publications

(406 citation statements)

References 32 publications

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“…Several in vivo studies provide evidence that cortex-membrane attachment strongly influences contractile processes. For instance, blebbing at the cell poles due to transient detachment of the cortex from the membrane serves to release excess cortical tension during cytokinesis, which is crucial to achieve proper division (14). In early Caenorhabditis elegans embryos, myosin-driven contraction drives long-range cortical flow of actin along the membrane, which is crucial to establish cell polarity and asymmetric cell division (15).…”

Section: P-eif2αmentioning

confidence: 99%

Cell-sized liposomes reveal how actomyosin cortical tension drives shape change

Carvalho

Tsai

Lees

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

106

111

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Significance Animal cells continuously move, divide, and transmit forces by actively reorganizing their internal scaffold or cytoskeleton. Molecular motors pull actin filaments together and generate contraction of the cytoskeleton underneath the cell membrane. We address the detailed mechanism of contraction by using a minimal in vitro assay: a liposome membrane to which we attach actin filaments and molecular motors in a controlled manner. We reproduce contraction like in cells. We show that the scaffold needs to be tightly attached to the membrane for efficient contraction, but, under some conditions, efficient contraction can lead to liposome destruction. These results suggest that cells must precisely control their contractility to remain intact during cellular events.

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Section: P-eif2αmentioning

confidence: 99%

Cell-sized liposomes reveal how actomyosin cortical tension drives shape change

Carvalho

Tsai

Lees

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

106

111

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“…Parameters chosen to model P. polycephalum include a base tube radius of a 0 = 50 µm, wall height h = 0.1a 0 , tube length L = 0.5 cm, contraction frequency ω 0 = 120s, dynamic viscosity of cytoplasm µ = 6.4 · 10 −3 Ns/ m 2 (39), and molecular diffusivity of a smaller molecule (i.e., ATP in cytoplasm) κ = 10 − 10 m 2 /s, resulting in Re = 2ua 0 /ν ∼ 0.0008. To estimate the elastic modulus we used the calculated value of myosin-generated elastic stress T = 50 Pa during Dictyostelium discoideum cleavage (40) and T/E = 1.15 for myosin activity in HeLa cells (41) to estimate E = 44 Pa and a Poisson's ratio of ν = 0.4 (42). Velocity of an elastic wave in tube wall follows using c = E/ρ(1 − ν 2 ).…”

Section: Methodsmentioning

confidence: 99%

Mechanism of signal propagation in Physarum polycephalum

Alim

Andrew

Pringle

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Complex behaviors are typically associated with animals, but the capacity to integrate information and function as a coordinated individual is also a ubiquitous but poorly understood feature of organisms such as slime molds and fungi. Plasmodial slime molds grow as networks and use flexible, undifferentiated body plans to forage for food. How an individual communicates across its network remains a puzzle, but Physarum polycephalum has emerged as a novel model used to explore emergent dynamics. Within P. polycephalum, cytoplasm is shuttled in a peristaltic wave driven by cross-sectional contractions of tubes. We first track P. polycephalum's response to a localized nutrient stimulus and observe a front of increased contraction. The front propagates with a velocity comparable to the flow-driven dispersion of particles. We build a mathematical model based on these data and in the aggregate experiments and model identify the mechanism of signal propagation across a body: The nutrient stimulus triggers the release of a signaling molecule. The molecule is advected by fluid flows but simultaneously hijacks flow generation by causing local increases in contraction amplitude as it travels. The molecule is initiating a feedback loop to enable its own movement. This mechanism explains previously puzzling phenomena, including the adaptation of the peristaltic wave to organism size and P. polycephalum's ability to find the shortest route between food sources. A simple feedback seems to give rise to P. polycephalum's complex behaviors, and the same mechanism is likely to function in the thousands of additional species with similar behaviors. acellular slime mold | transport network | behavior | Taylor dispersion O ne of the great challenges of unraveling biological complexity is understanding what kind of and how much computational power is required for an organism to generate sophisticated behaviors. Behaviors are typically associated with a nervous system, but many organisms without nervous systems integrate information and function as coordinated individuals (1); examples range from the ability of Escherichia coli to move up chemical gradients (2) to the ability of a multicellular fungus to sense and precisely explore unoccupied space (3). A recently published and striking example of a complex behavior involves bacteria within a biofilm: When a Bacillus subtilis biofilm is deprived of nutrients, bacteria are able to grow networks of channels and evaporatively pump flows, creating intricate structures that benefit the entire community (4).Perhaps the archetypal example of an apparently simple organism able to generate sophisticated behaviors is the slime mold Physarum polycephalum, whose behaviors are repeatedly characterized as "intelligent." This slime mold is able to navigate mazes by finding the shortest route between different food sources (5) and has used its ability to reconstruct the transportation maps of major cities (6). The organism can structure its connections to different nutrient sources to optimize its diet...

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“…2g). Polar blebbing is a normal event during cytokinesis (Sedzinski et al, 2011); however, it is very infrequently observed in unstressed embryos (see below). Thus, strong polar blebbing in heat shocked embryos indicates weakened polar cortical tension compared to unstressed embryos.…”

Section: Resultsmentioning

confidence: 99%

Acute heat shock leads to cortical domain internalization and polarity loss in the C. elegans embryo

Singh

Odedra

Lehmann

et al. 2016

Genesis

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Summary: Many developmental processes are inherently robust due to network organization of the participating factors and functional redundancy. The heterogeneity of the factors involved and their connectivity puts these processes at risk of abrupt system collapse under stress. The polarization of the one-cell C. elegans embryo constitutes such an inherently robust process with functional redundancy. However, how polarization is affected by acute stress has not been thoroughly investigated. Here, we report that heat shock (348C, 1 h) triggers a highly reproducible loss of the anterior and collapse of the posterior polarity domains. Temperature-dependent loss of cortical nonmuscle myosin II drastically reduces cortical tension and leads to internalization of large plasma membrane domains including the membrane-associated polarity factor PAR-2. After internalization, plasma membrane vesicles and associated factors cluster around centrosomes and are thereby withdrawn from the polarization process. Transient formation of the posterior polarity domain suggests that microtubule-induced self-organization of this domain is not compromised after heat shock. Hence, our data uncover that the polarization system undergoes a temperature-dependent collapse under acute stress. genesis 54:220-228, 2016. V C 2016Wiley Periodicals, Inc.

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Polar actomyosin contractility destabilizes the position of the cytokinetic furrow

Cited by 307 publications

References 32 publications

Cell-sized liposomes reveal how actomyosin cortical tension drives shape change

Cell-sized liposomes reveal how actomyosin cortical tension drives shape change

Mechanism of signal propagation in Physarum polycephalum

Acute heat shock leads to cortical domain internalization and polarity loss in the C. elegans embryo

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