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

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Renat N Khaliullin ◽  
Rebecca A Green ◽  
Linda Z Shi ◽  
J Sebastian Gomez-Cavazos ◽  
Michael W Berns ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Positive Feedback ◽  
Rate Increase ◽  
Unit Length ◽  
Cortical Surface ◽  
Contractile Ring ◽  
Exponential Increase ◽  
Rate Acceleration ◽  
Constant Rate ◽  
Ring Constriction

To ensure timely cytokinesis, the equatorial actomyosin contractile ring constricts at a relatively constant rate despite its progressively decreasing size. Thus, the per-unit-length constriction rate increases as ring perimeter decreases. To understand this acceleration, we monitored cortical surface and ring component dynamics during the first cytokinesis of the Caenorhabditis elegans embryo. We found that, per unit length, the amount of ring components (myosin, anillin) and the constriction rate increase with parallel exponential kinetics. Quantitative analysis of cortical flow indicated that the cortex within the ring is compressed along the axis perpendicular to the ring, and the per-unit-length rate of cortical compression increases during constriction in proportion to ring myosin. We propose that positive feedback between ring myosin and compression-driven flow of cortex into the ring drives an exponential increase in the per-unit-length amount of ring myosin to maintain a high ring constriction rate and support this proposal with an analytical mathematical model.

scholarly journals A positive feedback-based mechanism for constriction rate acceleration during cytokinesis in C. elegans

2017 ◽  
Author(s):  
Renat N. Khaliullin ◽  
Rebecca A. Green ◽  
Linda Z. Shi ◽  
J. Sebastian Gomez-Cavazos ◽  
Michael W. Berns ◽  
...  
Keyword(s):  
Positive Feedback ◽  
Cell Biology ◽  
Unit Length ◽  
Mathematical Formulation ◽  
Ring Closure ◽  
Cortical Surface ◽  
Contractile Ring ◽  
Closure Rate ◽  
C Elegans ◽  
Rate Acceleration

ABSTRACTDuring cytokinesis, an equatorial actomyosin contractile ring constricts at a relatively constant overall rate despite its progressively decreasing size. Thus, the per-unit-length rate of ring closure increases as ring perimeter decreases. To understand this acceleration, we monitored cortical surface and ring component dynamics during the first division of the C. elegans embryo. We show that the polar cortex expands during ring constriction to provide the cortical surface area required for division. Polar expansion also allows ring myosin to compress cortical surface along the pole-to-pole axis, leading to a continuous flow of cortical surface into the ring. We propose that feedback between ring myosin and compression-driven cortical flow drives an exponential increase in the amount of ring myosin that maintains the high overall closure rate as ring perimeter decreases. We further show that an analytical mathematical formulation of the proposed feedback, called the Compression Feedback model, recapitulates the experimental observations.IMPACT STATEMENTDuring cytokinesis, positive feedback between myosin motors in the contractile ring and compression-driven cortical flow along the axis perpendicular to the ring drives constriction rate acceleration to ensure timely cell separation.MAJOR SUBJECT AREASCell biology, Computational and Systems Biology

scholarly journals Author response: A positive-feedback-based mechanism for constriction rate acceleration during cytokinesis in Caenorhabditis elegans

2018 ◽  
Author(s):  
Renat N Khaliullin ◽  
Rebecca A Green ◽  
Linda Z Shi ◽  
J Sebastian Gomez-Cavazos ◽  
Michael W Berns ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Positive Feedback ◽  
Author Response ◽  
Rate Acceleration

scholarly journals The ARP2/3 complex prevents excessive formin activity during cytokinesis

2019 ◽  
Vol 30 (1) ◽  
pp. 96-107 ◽  
Author(s):  
Fung-Yi Chan ◽  
Ana M. Silva ◽  
Joana Saramago ◽  
Joana Pereira-Sousa ◽  
Hailey E. Brighton ◽  
...  
Keyword(s):  
Cell Division ◽  
Caenorhabditis Elegans ◽  
Actin Filament ◽  
Ring Formation ◽  
Contractile Ring ◽  
Present Evidence ◽  
Daughter Cells ◽  
Ring Constriction ◽  
Filament Network ◽  
Kinetics Of

Cytokinesis completes cell division by constriction of an actomyosin contractile ring that separates the two daughter cells. Here we use the early Caenorhabditis elegans embryo to explore how the actin filament network in the ring and the surrounding cortex is regulated by the single cytokinesis formin CYK-1 and the ARP2/3 complex, which nucleate nonbranched and branched filaments, respectively. We show that CYK-1 and the ARP2/3 complex are the predominant F-actin nucleators responsible for generating distinct cortical F-actin architectures and that depletion of either nucleator affects the kinetics of cytokinesis. CYK-1 is critical for normal F-actin levels in the contractile ring, and acute inhibition of CYK-1 after furrow ingression slows ring constriction rate, suggesting that CYK-1 activity is required throughout ring constriction. Surprisingly, although the ARP2/3 complex does not localize in the contractile ring, depletion of the ARP2 subunit or treatment with ARP2/3 complex inhibitor delays contractile ring formation and constriction. We present evidence that the delays are due to an excess in formin-nucleated cortical F-actin, suggesting that the ARP2/3 complex negatively regulates CYK-1 activity. We conclude that the kinetics of cytokinesis are modulated by interplay between the two major actin filament nucleators.

scholarly journals CYK-4 regulates Rac, but not Rho, during cytokinesis

2017 ◽  
Vol 28 (9) ◽  
pp. 1258-1270 ◽  
Author(s):  
Yelena Zhuravlev ◽  
Sophia M. Hirsch ◽  
Shawn N. Jordan ◽  
Julien Dumont ◽  
Mimi Shirasu-Hiza ◽  
...  
Keyword(s):  
Alternative Model ◽  
Single Cell Analysis ◽  
Myosin Ii ◽  
Small Gtpases ◽  
Nucleotide Exchange ◽  
Filamentous Actin ◽  
Contractile Ring ◽  
Division Plane ◽  
Ring Constriction

Cytokinesis is driven by constriction of an actomyosin contractile ring that is controlled by Rho-family small GTPases. Rho, activated by the guanine-nucleotide exchange factor ECT-2, is upstream of both myosin-II activation and diaphanous formin-mediated filamentous actin (f-actin) assembly, which drive ring constriction. The role for Rac and its regulators is more controversial, but, based on the finding that Rac inactivation can rescue cytokinesis failure when the GTPase-activating protein (GAP) CYK-4 is disrupted, Rac activity was proposed to be inhibitory to contractile ring constriction and thus specifically inactivated by CYK-4 at the division plane. An alternative model proposes that Rac inactivation generally rescues cytokinesis failure by reducing cortical tension, thus making it easier for the cell to divide when ring constriction is compromised. In this alternative model, CYK-4 was instead proposed to activate Rho by binding ECT-2. Using a combination of time-lapse in vivo single-cell analysis and Caenorhabditis elegans genetics, our evidence does not support this alternative model. First, we found that Rac disruption does not generally rescue cytokinesis failure: inhibition of Rac specifically rescues cytokinesis failure due to disruption of CYK-4 or ECT-2 but does not rescue cytokinesis failure due to disruption of two other contractile ring components, the Rho effectors diaphanous formin and myosin-II. Second, if CYK-4 regulates cytokinesis through Rho rather than Rac, then CYK-4 inhibition should decrease levels of downstream targets of Rho. Inconsistent with this, we found no change in the levels of f-actin or myosin-II at the division plane when CYK-4 GAP activity was reduced, suggesting that CYK-4 is not upstream of ECT-2/Rho activation. Instead, we found that the rescue of cytokinesis in CYK-4 mutants by Rac inactivation was Cdc42 dependent. Together our data suggest that CYK-4 GAP activity opposes Rac (and perhaps Cdc42) during cytokinesis.

scholarly journals The asymmetry of female meiosis reduces the frequency of inheritance of unpaired chromosomes

eLife ◽  
2015 ◽  
Vol 4 ◽  
Author(s):  
Daniel B Cortes ◽  
Karen L McNally ◽  
Paul E Mains ◽  
Francis J McNally
Keyword(s):  
Caenorhabditis Elegans ◽  
X Chromosome ◽  
High Frequency ◽  
Germ Line ◽  
Extra Chromosome ◽  
Polar Body ◽  
Contractile Ring ◽  
Female Meiosis ◽  
Random Segregation ◽  
The Asymmetry

Trisomy, the presence of a third copy of one chromosome, is deleterious and results in inviable or defective progeny if passed through the germ line. Random segregation of an extra chromosome is predicted to result in a high frequency of trisomic offspring from a trisomic parent. Caenorhabditis elegans with trisomy of the X chromosome, however, have far fewer trisomic offspring than expected. We found that the extra X chromosome was preferentially eliminated during anaphase I of female meiosis. We utilized a mutant with a specific defect in pairing of the X chromosome as a model to investigate the apparent bias against univalent inheritance. First, univalents lagged during anaphase I and their movement was biased toward the cortex and future polar body. Second, late-lagging univalents were frequently captured by the ingressing polar body contractile ring. The asymmetry of female meiosis can thus partially correct pre-existing trisomy.

scholarly journals Mitochondrial morphology and activity regulate furrow ingression and contractile ring dynamics in Drosophila cellularization

2020 ◽  
Vol 31 (21) ◽  
pp. 2331-2347
Author(s):  
Sayali Chowdhary ◽  
Somya Madan ◽  
Darshika Tomer ◽  
Manos Mavrakis ◽  
Richa Rikhy
Keyword(s):  
Mitochondrial Fission ◽  
Cell Formation ◽  
Mitochondrial Morphology ◽  
Contractile Ring ◽  
Drosophila Embryogenesis ◽  
Ring Dynamics ◽  
Mitochondrial Distribution ◽  
Ring Constriction

Drp1-regulated mitochondrial fission is essential for mitochondrial distribution across the cell in cellularization during Drosophila embryogenesis. Loss of mitochondrial fission in Drp1 mutant embryos leads to defects in morphogenetic events of cell formation and contractile ring constriction in cellularization.

scholarly journals The chromosomal passenger complex and centralspindlin independently contribute to contractile ring assembly

2011 ◽  
Vol 193 (1) ◽  
pp. 155-169 ◽  
Author(s):  
Lindsay Lewellyn ◽  
Ana Carvalho ◽  
Arshad Desai ◽  
Amy S. Maddox ◽  
Karen Oegema
Keyword(s):  
Contractile Ring ◽  
Chromosomal Passenger Complex ◽  
Ring Assembly ◽  
Assembly Pathway ◽  
Chromosomal Passenger ◽  
Spindle Midzone ◽  
Ring Constriction ◽  
Simultaneous Inhibition ◽  
Control Transformation ◽  
Equatorial Band

The chromosomal passenger complex (CPC) and centralspindlin are conserved cytokinesis regulators that localize to the spindle midzone, which forms between the separating chromosomes. Previous work placed the CPC and centralspindlin in a linear pathway that governs midzone formation. Using Caenorhabditis elegans embryos, we test whether there is a similar linear relationship between centralspindlin and the CPC in contractile ring constriction during cytokinesis. We show that simultaneous inhibition of the CPC kinase Aurora BAIR-2 and the centralspindlin component MKLP1ZEN-4 causes an additive constriction defect. Consistent with distinct roles for the proteins, inhibition of filamentous septin guanosine triphosphatases alleviates constriction defects in Aurora BAIR-2–inhibited embryos, whereas inhibition of Rac does so in MKLP1ZEN-4-inhibited embryos. Centralspindlin and the CPC are not required to enrich ring proteins at the cell equator but instead regulate formation of a compact mature ring. Therefore, in contrast to the linear midzone assembly pathway, centralspindlin and the CPC make independent contributions to control transformation of the sheet-like equatorial band into a ribbon-like contractile ring at the furrow tip.

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