Plastin and spectrin cooperate to stabilize the actomyosin cortex during cytokinesis

Sobral, Ana Filipa; Chan, Fung‐Yi; Norman, Michael; Osório, Daniel S.; Dias, Alexandra; Ferreira, Vanessa; Barbosa, Daniel José; Cheerambathur, Dhanya K.; Gassmann, Reto; Belmonte, Julio M.; Carvalho, Alexandra T. P.

doi:10.1016/j.cub.2021.09.055

Cited by 22 publications

(29 citation statements)

References 70 publications

(128 reference statements)

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“…However, the breadth of anillin could also reflect differences in other mechanisms that have been experimentally shown to facilitate ingression by promoting the alignment of actin filaments. These mechanisms include cortical flows in the axial and equatorial axis, and the distribution of actin cross-linkers [93][94][95][96][97][98]. Future studies are required to test these models and to reveal how anillin localization affects ring closure kinetics.…”

Section: Discussionmentioning

confidence: 99%

Cytokinetic diversity in mammalian cells is revealed by the characterization of endogenous anillin, Ect2 and RhoA

et al. 2022

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Cytokinesis is required to physically separate the daughter cells at the end of mitosis. This crucial process requires the assembly and ingression of an actomyosin ring, which must occur with high fidelity to avoid aneuploidy and cell fate changes. Most of our knowledge of mammalian cytokinesis was generated using over-expressed transgenes in HeLa cells. Over-expression can introduce artefacts, while HeLa are cancerous human cells that have lost their epithelial identity, and the mechanisms controlling cytokinesis in these cells could be vastly different from other cell types. Here, we tagged endogenous anillin, Ect2 and RhoA with mNeonGreen and characterized their localization during cytokinesis for the first time in live human cells. Comparing anillin localization in multiple cell types revealed cytokinetic diversity with differences in the duration and symmetry of ring closure, and the timing of cortical recruitment. Our findings show that the breadth of anillin correlates with the rate of ring closure, and support models where cell size or ploidy affects the cortical organization, and intrinsic mechanisms control the symmetry of ring closure. This work highlights the need to study cytokinesis in more diverse cell types, which will be facilitated by the reagents generated for this study.

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Section: Discussionmentioning

confidence: 99%

Cytokinetic diversity in mammalian cells is revealed by the characterization of endogenous anillin, Ect2 and RhoA

et al. 2022

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“…After depolymerization of F-actin by Latrunculin A treatment in Drosophila cells, anillin and the RLC of myosin II enrich in circular foci that evolve into linear structures and these structures also form independently of each other (D’Avino et al ., 2008; Hickson and O’Farrell, 2008; Oegema et al ., 2000). In the C. elegans zygote, NMY-2 also forms circular foci after Latrunculin A addition (Michaux et al, 2018; Sobral et al, 2021). However, whether ANI-1 is also present in those circular NMY-2 foci and whether linear structures still form after F-actin depolymerization has not been investigated in C. elegans .…”

Section: Resultsmentioning

confidence: 99%

Anillin forms linear structures and facilitates furrow ingression after septin and formin depletion

Lebedev

Chan

Bellessem

et al. 2022

Preprint

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During cytokinesis a contractile ring consisting of unbranched filamentous actin (F-actin) and myosin II filaments assembles and constricts at the cell equator. Unbranched F-actin is de novo generated by formin and without formin cleavage furrow ingression fails. In C. elegans depletion of septin restores cleavage furrow ingression in formin (CYK-1) mutants. How the cleavage furrow ingresses without a detectable unbranched F-actin ring is not known. We report, that in this setting anillin (ANI-1) is essential for furrow ingression and forms a meshwork of linear structures, which circumferentially align around the cell equator. Although equatorial ANI-1 recruitment is facilitated by septins, the formation of linear ANI-1 structures is septin independent. Analysis of ANI-1 deletion mutants reveals that its disordered linker region is required for linear structure formation and furrow ingression. We also found that myosin II (NMY-2) decorates linear ANI-1 structures and promotes their circumferential alignment. NMY-2 also interacts with various lipids and forms membrane localized clusters in absence of F-actin and anillin binding. This suggests that NMY-2 represents an independent link between the F-actin / ANI-1 network and the plasma membrane. Collectively, our data reveals a compensatory mechanism, mediated by ANI-1 linear structures and membrane-bound NMY-2, that promotes furrow formation and ingression when formins are depleted and therefore unbranched F-actin polymerization is compromised.

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“…Indeed, the correct integration of cell shape regulation, cortical mechanics and Hippo signaling effectors is disrupted in the spectrin-deficient Drosophila retina, which lacks the required apical spectrin accumulation to correctly develop the regular array of hexagonal ommatidia [42, 43]. Moreover, dual spectrin/plastin inhibition results in cytokinesis failure due to disorganization and collapse of the equatorial actomyosin network in C. elegans [44]. Altogether, these observations point to the capacity of spectrin to create dense buffering reservoirs in cortical regions characterized by low mechanical stress, by adopting the ultimately packed periodic topology.…”

Section: Discussionmentioning

confidence: 99%

Mechanically induced topological transition of spectrin regulates its distribution in the mammalian cortex

Ghisleni

Bonilla-Quintana

Crestani

et al. 2023

Preprint

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The cell cortex is a dynamic assembly formed by the plasma membrane and the underlying cytoskeleton. As the main determinant of cell shape, the cortex ensures its integrity during passive deformation or active response by adapting cytoskeleton topologies with poorly understood mechanisms. The spectrin meshwork ensures such adaptation in erythrocytes and neurons by adopting dramatically different organizations. Erythrocytes rely on triangular-like lattices of spectrin tetramers, which in neurons are organized in parallel and periodic arrays. Since spectrin is ubiquitously expressed, we exploited Expansion Microscopy to discover that these two distinct topologies can co-exist in other mammalian cells such as fibroblasts. We show through biophysical measurements and computational modeling that spectrin provides coverage of the cortex and, with the intervention of actomyosin, erythroid-like lattices can dynamically transition into condensates that resemble neuron-like periodic arrays fenced by actin stress fibers. Spectrin condensates experience lower mechanical stress and turnover despite displaying an extension close to the contour length of the tetramer. Our study sheds light on the adaptive properties of spectrin, which ensures protection of the cortex by undergoing mechanically induced topological transitions.

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Plastin and spectrin cooperate to stabilize the actomyosin cortex during cytokinesis

Cited by 22 publications

References 70 publications

Cytokinetic diversity in mammalian cells is revealed by the characterization of endogenous anillin, Ect2 and RhoA

Cytokinetic diversity in mammalian cells is revealed by the characterization of endogenous anillin, Ect2 and RhoA

Anillin forms linear structures and facilitates furrow ingression after septin and formin depletion

Mechanically induced topological transition of spectrin regulates its distribution in the mammalian cortex

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