Actin turnover maintains actin filament homeostasis during cytokinetic ring contraction

Chew, Ting Gang; Huang, Junqi; Palani, Saravanan; Sommese, Ruth F.; Kamnev, Anton; Hatano, Tomoyuki; Gu, Ying; Oliferenko, Snezhana; Sivaramakrishnan, Sivaraj; Balasubramanian, Mohan K.

doi:10.1083/jcb.201701104

Cited by 43 publications

(62 citation statements)

References 43 publications

(69 reference statements)

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“…A similar trend was observed when Jas-stabilized wild-type, myo2-S1, and cdc3-124 myo2-S1 ghosts were incubated with ATP even at the lower temperature of 24°C ( Figure 4C). This is similar to our previous observations with cell ghosts of the well characterized temperature-sensitive myo2-E1 allele, rings from which fail to contract upon ATP addition, even at the permissive temperature of 24°C (Mishra, Kashiwazaki et al 2013, Palani, Chew et al 2017). In addition, we found that Jasstabilized actomyosin rings in cell ghosts prepared from cdc3-124 myo2-S2 (which suppresses cdc3-124, but less well compared to myo2-S1) also underwent very slow ATP-dependent contraction at 34°C ( Figure S2B and C) and at 24°C ( Figure S2D).…”

Section: S1 Cellssupporting

confidence: 92%

“…Previous work has shown that single actin filaments and networks of actin filaments are broken and disassembled by myosin II through buckling (Murrell andGardel 2012, Vogel, Petrasek et al 2013). Previous work in S. japonicus has shown that isolated cytokinetic rings break into a series of clusters in a myosin II dependent manner, which is reversed and normal contraction upon ATP addition ensues, when the isolated cytokinetic rings are pre-incubated with Jasplakinolide (Chew, Huang et al 2017). Our work may provide in vivo evidence for a role for myosin II in actin filament disassembly and turnover, also consistent with the work in cytokinetic mammalian cells (Murthy and Wadsworth 2005).…”

Section: Myo2-s1 Suppresses Direct Pharmacological Perturbation Of Thsupporting

confidence: 88%

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Genetic interaction between profilin and myosin II reveals a potential role for myosin II in actin filament disassemblyin vivo

Zambon

Palani

Jadhav

et al. 2020

Preprint

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The actin cytoskeleton plays a variety of roles in eukaryotic cell physiology, ranging from cell polarity and migration to cytokinesis. Key to the function of the actin cytoskeleton is the mechanisms that control its assembly, stability, and turnover. Through genetic analyses in fission yeast, we found that, myo2-S1 (myo2-G515D), a myosin II mutant allele was capable of rescuing lethality caused by compromise of mechanisms involved in actin cable / ring assembly and stability. The mutation in myo2-S1 affects the activation loop of Myosin II, which is involved in physical interaction with subdomain 1 of actin and in stimulating the ATPase activity of Myosin.Consistently, actomyosin rings in myo2-S1 cell ghosts were severely compromised in contraction upon ATP addition, suggesting that Myo2-S1p was defective in actin binding and / or motor activity. These studies strongly suggest a role for Myo2p in actin cytoskeletal disassembly and turnover, and that compromise of this activity leads to genetic suppression of mutants defective in actin cable assembly / stability. Introduction:Actin is a highly conserved cytoskeletal polymer forming protein that is key to a vast array of physiological processes in the three domains of life. In eukaryotes, the actin cytoskeleton plays essential roles in cell polarity, morphogenesis, migration, and cytokinesis (Pollard and Wu 2010, Cheffings, Burroughs et al. 2016, Misu, Takebayashi et al. 2017, Rottner, Faix et al. 2017, Skruber, Read et al. 2018. A balance of factors that control filament nucleation and stability and those that promote its disassembly exquisitely regulates the functions of the actin cytoskeleton (Lee and Dominguez 2010). Over the past three decades, the fission yeast Schizosaccharomyces pombe has emerged as an attractive organism for the study of the actin cytoskeleton and its role in cell polarity and division (Pollard and Wu 2010, Cheffings, Burroughs et al. 2016, Chiou, Balasubramanian et al. 2017. This is particularly due to the fact that many of the actin cytoskeletal proteins can be characterized through easily identifiable lethal mutant phenotypes (Wertman, Drubin et al. 1992, Holtzman, Wertman et al. 1994, Balasubramanian, McCollum et al. 1998). In fission yeast, theArp2/3 complex nucleates actin patches (Pelham and Chang 2001, Sirotkin, Berro et al. 2010), whereas linear actin cables and cytokinetic actomyosin rings are assembled by formins For3 (actin cables) (Feierbach and Chang 2001) and Cdc12p (cytokinetic actomyosin rings) (Chang, Drubin et al. 1997) and the actin-binding protein Cdc3-profilin (Balasubramanian, Hirani et al. 1994). The coiled-coil actin binding protein Cdc8 tropomyosin ensures stability of actin cables and actomyosin rings (Liu and Bretscher 1989, Balasubramanian, Helfman et al. 1992, Gunning, Hardeman et al. 2015). The fission yeast actin cytoskeleton undergoes dramatic disassembly and turnover (Kovar, Sirotkin et al. 2011). Treatment of cells with the actin polymerization inhibitor latrunculin A causes complete loss of actin cables...

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Section: S1 Cellssupporting

confidence: 92%

Section: Myo2-s1 Suppresses Direct Pharmacological Perturbation Of Thsupporting

confidence: 88%

Genetic interaction between profilin and myosin II reveals a potential role for myosin II in actin filament disassemblyin vivo

Zambon

Palani

Jadhav

et al. 2020

Preprint

Self Cite

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“…Rapid filament turnover may be important for local network homeostasis -i.e. to maintain uniform filament density and prevent local tearing and/or clumping of contractile ring components (Chew et al, 2017). At the same time, filament turnover provides an effective way to dissipate local resistance to the rapid remodeling of actin networks that underlies flow and filament realignment (McFadden et al, 2017).…”

Section: Discussionmentioning

confidence: 99%

Existing actin filaments orient new filament growth to provide structural memory of filament alignment during cytokinesis

Munro

2020

Preprint

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During cytokinesis, animal cells rapidly remodel the equatorial cortex to build an aligned array of actin filaments called the contractile ring. Local reorientation of filaments by equatorial contraction is thought to underlie the emergence of filament alignment during ring assembly.Here, combining single molecule analysis and modeling in one-cell C. elegans embryos, we show that filaments turnover is far too fast for reorientation of single filaments by equatorial contraction/cortex compression to explain the observed alignment, even if favorably oriented filaments are selectively stabilized. Instead, by tracking single Formin/CYK-1::GFP speckles to monitor local filament assembly, we identify a mechanism that we call filament-guided filament assembly (FGFA), in which existing filaments serve as templates to guide/orient the growth of new filaments. We show that FGFA sharply increases the effective lifetime of filament orientation, providing structural memory that allows slow equatorial contraction to build and maintain highly aligned filament arrays, despite rapid turnover of individual filaments.

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“…Actin turnover during ring contraction is important for actin filament homeostasis and proper contraction, as shown in cytokinesis models including NRK cells and Schizosaccharomyces japonicus (S. japonicus ; Guha et al, ; Chew et al, ) as well as in wound healing models such as Drosophila embryos (Kobb et al, ). Mathematical modeling of the node model of S. pombe cytokinetic ring contraction also suggests that protein turnover is required to stabilize the ring, as myosin aggregation could decrease contractile tension and cause the ring to fracture (Thiyagarajan et al, ).…”

Section: Maintaining a Dynamically Stable Cr During Assembly And Contmentioning

confidence: 99%

“…In Dictyostelium cytokinesis, which does not involve a standard CR, actin crosslinkers dynacortin and fimbrin interact with myosin II to create differentials in stiffness and contractility between the equator and the poles that modulate the shape of the cell (Zhang and Robinson, 2005;Reichl et al, 2008;Descovich et al, 2018) Actin turnover. Actin turnover during ring contraction is important for actin filament homeostasis and proper contraction, as shown in cytokinesis models including NRK cells and Schizosaccharomyces japonicus (S. japonicus; Guha et al, 2005;Chew et al, 2017) as well as in wound healing models such as Drosophila embryos (Kobb et al, 2017). Mathematical modeling of the node model of S. pombe cytokinetic ring contraction also suggests that protein turnover is required to stabilize the ring, as myosin aggregation could decrease contractile tension and cause the ring to fracture (Thiyagarajan et al, 2017).…”

Section: Actin Dynamicsmentioning

confidence: 99%

Regulation and Assembly of Actomyosin Contractile Rings in Cytokinesis and Cell Repair

Dekraker

Boucher

Mandato

2018

The Anatomical Record

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Cytokinesis and single‐cell wound repair both involve contractile assemblies of filamentous actin (F‐actin) and myosin II organized into characteristic ring‐like arrays. The assembly of these actomyosin contractile rings (CRs) is specified spatially and temporally by small Rho GTPases, which trigger local actin polymerization and myosin II contractility via a variety of downstream effectors. We now have a much clearer view of the Rho GTPase signaling cascade that leads to the formation of CRs, but some factors involved in CR positioning, assembly, and function remain poorly understood. Recent studies show that this regulation is multifactorial and goes beyond the long‐established Ca2+‐dependent processes. There is substantial evidence that the Ca2+‐independent changes in cell shape, tension, and plasma membrane composition that characterize cytokinesis and single‐cell wound repair also regulate CR formation. Elucidating the regulation and mechanistic properties of CRs is important to our understanding of basic cell biology and holds potential for therapeutic applications in human disease. In this review, we present a primer on the factors influencing and regulating CR positioning, assembly, and contraction as they occur in a variety of cytokinetic and single‐cell wound repair models. Anat Rec, 301:2051–2066, 2018. © 2018 Wiley Periodicals, Inc.

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Actin turnover maintains actin filament homeostasis during cytokinetic ring contraction

Abstract: Many cytokinetic actomyosin ring components undergo dynamic turnover, but its function is unclear. Chew et al. show that continuous actin polymerization ensures crucial F-actin homeostasis during ring contraction, without which ring proteins organize into noncontractile clusters.

Cited by 43 publications

References 43 publications

Genetic interaction between profilin and myosin II reveals a potential role for myosin II in actin filament disassemblyin vivo

Genetic interaction between profilin and myosin II reveals a potential role for myosin II in actin filament disassemblyin vivo

Existing actin filaments orient new filament growth to provide structural memory of filament alignment during cytokinesis

Regulation and Assembly of Actomyosin Contractile Rings in Cytokinesis and Cell Repair

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