Literature Review of articles inCytokinesisDictyosteliumMyosinsActinCytoplasm

Cytokinesis through biochemical–mechanical feedback loops

Article · Literature Review · December 2010with64 Reads
DOI: 10.1016/j.semcdb.2010.08.003 · Source: PubMed
Abstract
Cytokinesis is emerging as a control system defined by interacting biochemical and mechanical modules, which form a system of feedback loops. This integrated system accounts for the regulation and kinetics of cytokinesis furrowing and demonstrates that cytokinesis is a whole-cell process in which the global and equatorial cortices and cytoplasm are active players in the system. Though originally defined in Dictyostelium, features of the control system are recognizable in other organisms, suggesting a universal mechanism for cytokinesis regulation and contractility.
    • Dictyostelium discoideum serves as a model organism helping to understand biological phenomena like motility, chemotaxis, phagocytosis and cytokinesis (Unal and Steinert, 2006;CalvoGarrido et al., 2010;Surcel et al., 2010;Cai and Devreotes, 2011). The amoeba belongs to the evolutionary supergroup of Amoebozoa (Adl et al., 2012), and it likely is its beststudied representative.
    [Show abstract] [Hide abstract] ABSTRACT: Transposable elements, identified in all eukaryotes, are mobile genetic units that can change their genomic position. Transposons usually employ an excision and reintegration mechanism, by which they change position, but not copy number. In contrast, retrotransposons amplify via RNA intermediates, increasing their genomic copy number. Hence, they represent a particular threat to the structural and informational integrity of the invaded genome. The social amoeba Dictyostelium discoideum, model organism of the evolutionary Amoebozoa supergroup, features a haploid, gene-dense genome that offers limited space for damage-free transposition. Several of its contemporary retrotransposons display intrinsic integration preferences, for example by inserting next to transfer RNA genes or other retroelements. Likely, any retrotransposons that invaded the genome of the amoeba in a non-directed manner were lost during evolution, as this would result in decreased fitness of the organism. Thus, the positional preference of the Dictyostelium retroelements might represent a domestication of the selfish elements. Likewise, the reduced danger of such domesticated transposable elements led to their accumulation, and they represent about 10% of the current genome of D. discoideum. To prevent the uncontrolled spreading of retrotransposons, the amoeba employs control mechanisms including RNA interference and heterochromatization. Here, we review TRE5-A, DIRS-1 and Skipper-1, as representatives of the three retrotransposon classes in D. discoideum, which make up 5.7% of the Dictyostelium genome. We compile open questions with respect to their mobility and cellular regulation, and suggest strategies, how these questions might be addressed experimentally.
    Full-text · Article · Oct 2017
    • We will consider Rho-dependent signaling pathways in D. discoideum cytokinesis following current models that consider distinct polar and equatorial processes (Fig. 3(A)). For a discussion on the biomechanical aspects implicating most of the elements considered later the reader is referred to the excellent review of (Surcel et al., 2010). Rac1, RacC, and RacE emerge as the main Rho GTPases involved in regulating cytokinesis but signaling pathways have been delineated to some extent for Rac1 and RacE only.
    [Show abstract] [Hide abstract] ABSTRACT: Small GTPases of the Rho family are ubiquitous molecular switches involved in the regulation of most actin cytoskeleton dependent processes and many other processes not directly linked to actin. D. discoideum is a well-established model organism for studies of the actin cytoskeleton and its regulation by signal transduction pathways. D. discoideum is equipped with a complex repertoire of Rho signaling components, with 20 Rho GTPases, more than 100 regulators (including exchange factors, GTPase activating proteins and guanine nucleotide dissociation inhibitors), and nearly 80 effectors or components of effector complexes. In this review we examine the knowledge accumulated to date about proteins involved in Rho-regulated signaling pathways in D. discoideum, with an emphasis on functional studies. We integrate the information about individual components into defined signaling pathways, with a focus on three extensively investigated processes: chemotaxis, vesicle trafficking, and cytokinesis.
    Chapter · Dec 2016
    • The dramatic actomyosin arrays and balanced contractility of ZO KD cells were intriguing. In situations ranging from cytokinesis to apical constriction or convergent extension, actomyosin assembly is driven in part by positive feedback loops and can in turn be terminated by negative feedback (Surcel et al., 2010; Levayer and Lecuit, 2012). We thus explored whether internally generated signals downstream of ZO KD were sufficient for myosin recruitment or whether it was enhanced by feedback loops instigated by neighboring cells pulling on one another.
    [Show abstract] [Hide abstract] ABSTRACT: Morphogenesis requires dynamic coordination between cell–cell adhesion and the cytoskeleton to allow cells to change shape and move without losing tissue integrity. We used genetic tools and superresolution microscopy in a simple model epithelial cell line to define how the molecular architecture of cell–cell zonula adherens (ZA) is modified in response to elevated contractility, and how these cells maintain tissue integrity. We previously found that depleting zonula occludens 1 (ZO-1) family proteins in MDCK cells induces a highly organized contractile actomyosin array at the ZA. We find that ZO knockdown elevates contractility via a Shroom3/Rho-associated, coiled-coil containing protein kinase (ROCK) pathway. Our data suggest that each bicellular border is an independent contractile unit, with actin cables anchored end-on to cadherin complexes at tricellular junctions. Cells respond to elevated contractility by increasing junctional afadin. Although ZO/afadin knockdown did not prevent contractile array assembly, it dramatically altered cell shape and barrier function in response to elevated contractility. We propose that afadin acts as a robust protein scaffold that maintains ZA architecture at tricellular junctions.
    Full-text · Article · Apr 2016
    • Regulated cell shape changes in the presence of internal and external disturbances, for example during cell division and cell motility, are a result of interlinked biochemical and mechanical feedback loops [32]. In this study, we have developed a biomechanical feedback model that explains the entire cellular response to a mechanical disturbance.
    [Show abstract] [Hide abstract] ABSTRACT: Cells undergo controlled changes in morphology in response to intracellular and extracellular signals. These changes require a means for sensing and interpreting the signalling cues, for generating the forces that act on the cell's physical material, and a control system to regulate this process. Experiments on Dictyostelium amoebae have shown that force-generating proteins can localize in response to external mechanical perturbations. This mechanosensing, and the ensuing mechanical feedback, plays an important role in minimizing the effect of mechanical disturbances in the course of changes in cell shape, especially during cell division, and likely in other contexts, such as during three-dimensional migration. Owing to the complexity of the feedback system, which couples mechanical and biochemical signals involved in shape regulation, theoretical approaches can guide further investigation by providing insights that are difficult to decipher experimentally. Here, we present a computational model that explains the different mechanosensory and mechanoresponsive behaviours observed in Dictyostelium cells. The model features a multiscale description of myosin II bipolar thick filament assembly that includes cooperative and force-dependent myosin-actin binding, and identifies the feedback mechanisms hidden in the observed mechanoresponsive behaviours of Dictyostelium cells during micropipette aspiration experiments. These feedbacks provide a mechanistic explanation of cellular retraction and hence cell shape regulation. © 2015 The Author(s).
    Full-text · Article · Aug 2015
    • This mechanosensitivity allows for mechanical stresses acting at the surface of the cortex to drive myosin II and cortexillin I accumulation in a cooperative manner that is dependent on myosin II mechanochemistry (Ren et al., 2009; Luo et al., 2012). This stress sensitivity acts independently of the mitotic spindle in postmetaphase cells and may help drive myosin II to the cleavage furrow cortex in three-dimensional culture and tissue environments, as well as in some asymmetric cell divisions (Cabernard et al., 2010; Ou et al., 2010; Surcel et al., 2010; Kee et al., 2012). Other mechanisms for promoting myosin II cleavage furrow cortex accumulation are believed to involve signals directly emanating from the mitotic spindle.
    [Show abstract] [Hide abstract] ABSTRACT: How myosin II localizes to the cleavage furrow in Dictyostelium and metazoan cells remains largely unknown despite significant advances in understanding its regulation. We designed a genetic selection using cDNA library suppression of 3xAsp myosin II to identify factors involved in myosin cleavage furrow accumulation. The 3xAsp mutant is deficient in bipolar thick filament assembly, fails to accumulate at the cleavage furrow, cannot rescue myoII-null cytokinesis, and has impaired mechanosensitive accumulation. Eleven genes suppressed this dominant cytokinesis deficiency when 3xAsp was expressed in WT cells. 3xAsp myosin II's localization to the cleavage furrow was rescued by constructs encoding rcdBB, mmsdh, RMD1, actin, one novel protein, and a 14-3-3 hairpin. Further characterization showed that RMD1 is required for myosin II cleavage furrow accumulation, acting parallel with mechanical stress. Analysis of several mutant strains revealed that different thresholds of myosin II activity are required for daughter cell symmetry than for furrow ingression dynamics. Finally, an engineered myosin II with a longer lever arm (2xELC), producing a highly mechanosensitive motor, could also partially suppress the intragenic 3xAsp. Overall, myosin II accumulation is the result of multiple parallel and partially redundant pathways that comprise a cellular contractility control system.
    Full-text · Article · Dec 2014
    • C ytokinesis is the last step of cell division, leading to the physical separation of the sister cells. In animal cells, it relies on complex and coordinated cell shape changes associated with membrane and cytoskeleton rear- rangement [Eggert et al., 2006; Barr and Gruneberg, 2007; Werner and Glotzer, 2008; Atilla-Gokcumen et al., 2010; Surcel et al., 2010; Fededa and Gerlich, 2012]. First, a plasma membrane cleavage furrow ingresses at the cell equator, which requires the contraction of an actomyosin II cortical network .
    [Show abstract] [Hide abstract] ABSTRACT: Phosphoinositides [Phosphatidylinositol (PtdIns), phosphatidylinositol 3-monophosphate (PtdIns3P), phosphatidylinositol 4-monophosphate (PtdIns4P), phosphatidylinositol 5-monophosphate (PtdIns5P), phosphatidylinositol 3,4-bisphosphate (PtdIns(3,4)P(2) ), phosphatidylinositol 3,5-bisphosphate (PtdIns(3,5)P(2) ), phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P(2) ), and phosphatidylinositol 3,4,5-trisphosphate (PtdIns(3,4,5)P(3) )] are lowly abundant acidic lipids found at the cytosolic leaflet of the plasma membrane and intracellular membranes. Initially discovered as precursors of second messengers in signal transduction, phosphoinositides are now known to directly or indirectly control key cellular functions, such as cell polarity, cell migration, cell survival, cytoskeletal dynamics, and vesicular traffic. Phosphoinositides actually play a central role at the interface between membranes and cytoskeletons and contribute to the identity of the cellular compartments by recruiting specific proteins. Increasing evidence indicates that several phosphoinositides, particularly PtdIns(4,5)P(2) , are essential for cytokinesis, notably after furrow ingression. The present knowledge about the specific phosphoinositides and phosphoinositide modifying-enzymes involved in cytokinesis will be first presented. The review of the current data will then show that furrow stability and cytokinesis abscission require that both phosphoinositide production and hydrolysis are regulated in space and time. Finally, I will further discuss recent mechanistic insights on how phosphoinositides regulate membrane trafficking and cytoskeletal remodeling for successful furrow ingression and intercellular bridge abscission. This will highlight unanticipated connections between cytokinesis and enzymes implicated in human diseases, such as the Lowe syndrome. © 2012 Wiley Periodicals, Inc.
    Article · Nov 2012
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April 2017 · The Journal of Cell Biology · Impact Factor: 9.83
    The cell cortex is essential to maintain animal cell shape, and contractile forces generated within it by nonmuscle myosin II (NMY-2) drive cellular morphogenetic processes such as cytokinesis. The role of actin cross-linking proteins in cortical dynamics is still incompletely understood. Here, we show that the evolutionarily conserved actin bundling/cross-linking protein plastin is... [Show full abstract]
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