A positive-feedback-based mechanism for constriction rate acceleration during cytokinesis in Caenorhabditis elegans

Khaliullin, Renat N.; Green, Rebecca A.; Shi, Linda Z.; Gomez-Cavazos, J Sebastian; Berns, Michael W.; Desai, Arshad; Oegema, Karen

doi:10.7554/elife.36073

Cited by 79 publications

(118 citation statements)

References 87 publications

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“…Therefore, we conclude that GCK-1/CCM-3 are novel components of negative feedback in the cytokinetic ring. These findings advance the growing body of work showing that contractile networks in cells are not only activated by positive regulation, but also contain structural "brakes" and regulatory time-delayed negative feedback important for turnover and dynamics (Bement et al, 2015;Bischof et al, 2017;Dorn et al, 2016;Goryachev et al, 2016;Khaliullin et al, 2018;Michaux et al, 2018;Nishikawa et al, 2017).…”

Section: Introductionsupporting

confidence: 69%

Novel cytokinetic ring components drive negative feedback in cortical contractility

Rehain-Bell

Werner

Doshi

et al. 2019

Preprint

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Actomyosin-driven cortical contractility is a hallmark of many biological processes. While most attention has been given to the positive regulation of contractility, it is becoming increasingly appreciated that contractility is also limited by negative regulation and mechanical brakes. The cytokinetic ring is an actomyosin contractile structure whose assembly and constriction are activated by the small GTPase RhoA. Here we describe the role of two novel cytokinetic ring components GCK-1 and CCM-3 in inhibiting contractility in the cytokinetic ring. GCK-1 and CCM-3 co-localize with essential cytokinetic ring proteins such as active RhoA, the scaffold protein anillin and non-muscle myosin II (NMM-II) during anaphase. GCK-1 and CCM-3 are interdependent for their localization and require active RhoA and anillin but not NMM-II for their recruitment to the cytokinetic furrow. Partial depletion of either GCK-1 or CCM-3 leads to an increase of active RhoA, anillin and NMM-II in the cytokinetic furrow and increased rates of furrow ingression. Furthermore, GCK-1 and CCM-3 localize to actomyosin foci during pulsed contractility of the cortical cytoskeleton during zygote polarization. Depletion of GCK-1 or CCM-3 leads to an increase in both cortical contractility and baseline active RhoA levels. Together, our findings suggest that GCK-1 and CCM-3 limit contractility during zygote polarization and

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Section: Introductionsupporting

confidence: 69%

Novel cytokinetic ring components drive negative feedback in cortical contractility

Rehain-Bell

Werner

Doshi

et al. 2019

Preprint

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“…Just before cytokinesis, cells expand and microridges dissolve back into pegs; during cytokinesis, cells contract dramatically and microridges rapidly re-form (Lam et al, 2015) . These new microridges are initially oriented predominantly perpendicular to the cytokinetic furrow, consistent with the observation that, during cytokinesis, furrow ingression drives polarized cortical flow towards the furrow (Khaliullin et al, 2018;Cao and Wang, 1990;DeBiasio et al, 1996) .…”

Section: Discussionsupporting

confidence: 86%

Cortical contraction drives the 3D patterning of epithelial cell surfaces

Loon

Erofeev

Maryshev

et al. 2019

Preprint

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SUMMARYMicroridges, elongated 3D protrusions arranged in maze-like patterns on zebrafish skin cells, form by the accretion of simple precursor projections. Modeling and in vivo experiments showed that cortical contractions promote the coalescence of precursors into microridges by reducing membrane tension. ABSTRACTCellular protrusions create complex cell surface topographies, but biomechanical mechanisms regulating their formation and arrangement are largely unknown. To study how protrusions form, we focused on the morphogenesis of microridges, elongated actin-based structures projecting from the apical surfaces of zebrafish skin cells that are arranged in labyrinthine patterns. Microridges form by accreting simple finger-like precursors. Live imaging demonstrated that microridge morphogenesis is linked to apical constriction. A non-muscle myosin II (NMII) reporter revealed pulsatile contractions of the actomyosin cortex; inhibiting NMII demonstrated that contractions are required for apical constriction and microridge formation. A biomechanical model suggested that contraction reduces surface tension to permit the fusion of precursors into microridges. Indeed, reducing surface tension with hyperosmolar media promoted microridge formation. In anisotropically stretched cells, microridges formed by precursor fusion along the stretch axis, which computational modeling explained as a consequence of stretch-induced cortical flow. Collectively, our results demonstrate how contraction within the 2D plane of the cortex patterns 3D cell surfaces.

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“…3d). Using the same data, the cortical flow along the cell periphery was computed in individual embryos by one-dimensional particle image velocimetry (PIV), which gave comparable values to the anterior-posterior component of the flow velocity obtained by two-dimensional PIV (Khaliullin et al, 2018;Reymann et al, 2016;. The average across embryos was displayed as a kymograph in which the green signal indicates flow from the anterior to the posterior, and the magenta indicates flow from the posterior to the anterior (Fig.…”

mentioning

confidence: 97%

“…Nonmuscle myosin II is a major component of the cortical actomyosin network and the cytokinetic contractile ring, and is crucial for animal cell cytokinesis. Myosin dynamics in dividing C. elegans embryos has previously been studied, but data are limited to a low temporal resolution (>~10 s) for a 3D volume (Carvalho et al, 2009;Jordan et al, 2016;Khaliullin et al, 2018) or, at higher temporal resolution, to the cell surface (Reymann et al, 2016;Werner et al, 2007). To examine the rapid dynamics of myosin II on the mitotic spindle and astral microtubules, we performed fast time-lapse recording (~every second) of GFP-tagged nonmuscle myosin II, expressed from the endogenous locus (nmy-2(cp13)) (Dickinson et al, 2013), imaging a 2 µm thick z-section at the embryo midplane with 0.5 µm z-steps.…”

mentioning

confidence: 99%

“…In various cell types, including C. elegans embryos (Dechant and Glotzer, 2003;Khaliullin et al, 2018;Werner et al, 2007), echinoderm embryos (Dassow et al, 2009Foe and Dassow, 2008), silkworm spermatocytes (Chen et al, 2008), and mammalian cultured cells (Murthy and Wadsworth, 2008), evidence has been accumulating for the suppression of the contractility of the polar cortexes by radial arrays of astral microtubules (polar relaxation). The polar relaxation contributes to furrow formation often by promoting the flow of the actomyosin network within the cell cortex (cortical flow) (Chen et al, 2008;Dan, 1954;Khaliullin et al, 2018;Murthy and Wadsworth, 2008;Werner et al, 2007), which contributes to the assembly of the actomyosin contractile ring (DeBiasio et al, 1996;Reymann et al, 2016;Salbreux et al, 2009;Turlier et al, 2014;Zhou and Wang, 2008), and also by releasing cytoplasmic hydrostatic pressure, which otherwise destabilizes the furrow (Sedzinski et al, 2011). The local reduction of the cortical contractility upon removal of NMY-2 from the cortex (Fig.…”

mentioning

confidence: 99%

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Polar relaxation by dynein-mediated removal of cortical myosin II

Chapa-y-Lazo

Hamanaka

Wray

et al. 2019

Preprint

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Nearly 6 decades ago, Lewis Wolpert proposed the relaxation of the polar cell cortex by the radial arrays of astral microtubules as a mechanism for cleavage furrow induction (White and Borisy, 1983;Wolpert, 1960). While this mechanism has remained controversial (Rappaport, 1996), recent work has provided evidence for polar relaxation by astral microtubules (Chen et al., 2008; Dechant and Glotzer, 2003; Foe and Dassow, 2008;Murthy and Wadsworth, 2008;Werner et al., 2007), although its molecular mechanisms remain elusive. Here, using C. elegans embryos, we show that polar relaxation is achieved through dynein-mediated removal of myosin II from the polar cortexes. Mutants that position centrosomes closer to the polar cortex accelerated furrow induction whereas suppression of dynein activity delayed furrowing. We provide evidence that dynein-mediated removal of myosin II from the polar cortexes triggers cortical flow towards the cell equator, which induces the assembly of the actomyosin contractile ring. These studies for the first time provide a molecular basis for the aster-dependent polar relaxation, which works in parallel with equatorial stimulation to promote robust cytokinesis. Results and DiscussionDuring animal cell cytokinesis, cleavage by constriction of an actomyosin contractile ring is spatially coupled to chromosome segregation by the mitotic apparatus (D'Avino et al., 2015;Green et al., 2012). The best-understood mechanism for spatial coupling is chemical signaling via activation of Rho GTPase at the cell equator by the central spindle, which is mediated by centralspindlin, a microtubule-

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A positive-feedback-based mechanism for constriction rate acceleration during cytokinesis in Caenorhabditis elegans

Cited by 79 publications

References 87 publications

Novel cytokinetic ring components drive negative feedback in cortical contractility

Novel cytokinetic ring components drive negative feedback in cortical contractility

Cortical contraction drives the 3D patterning of epithelial cell surfaces

Polar relaxation by dynein-mediated removal of cortical myosin II

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