Cytokinesis through biochemical–mechanical feedback loops

Department of Cell Biology, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA.
Seminars in Cell and Developmental Biology (Impact Factor: 6.27). 12/2010; 21(9):866-73. DOI: 10.1016/j.semcdb.2010.08.003
Source: PubMed


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.

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    • "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 rearrangement [Eggert et al., 2006; Barr and Gruneberg, 2007; Werner and Glotzer, 2008; Atilla-Gokcumen et al., 2010; Sagona and Stenmark, 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 . "
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    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.
    Cytoskeleton 11/2012; 69(11). DOI:10.1002/cm.21067 · 3.12 Impact Factor
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    • "Note: the dashed arrows and asterisk (*) denote that the interaction between 14-3-3 and microtubules has been characterized in interphase cells, but due to the sparse nature of astral microtubules in Dictyostelium cells, this interaction has not been fully characterized in mitotic cells. [Data are compiled from [Robinson and Spudich, 2000; Reichl et al., 2008; Surcel et al., 2010; Zhou et al., 2010; Kee et al., 2012]. "
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    ABSTRACT: Cytokinesis shape change occurs through the interfacing of three modules, cell mechanics, myosin II-mediated contractile stress generation and sensing, and a control system of regulatory proteins, which together ensure flexibility and robustness. This integrated system then defines the stereotypical shape changes of successful cytokinesis, which occurs under a diversity of mechanical contexts and environmental conditions. © 2012 Wiley Periodicals, Inc.
    Cytoskeleton 10/2012; 69(10):700-9. DOI:10.1002/cm.21045 · 3.12 Impact Factor
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    • "Further, the 14-3-3 protein was similarly required to maintain normal microtubule structure, indicating that 14-3-3 acts at a nexus between the microtubule and cortical networks. Finally, because the myosin II distribution is exquisitely sensitive to mechanical stress and given these various modes of cross-talk, the entire contractile and microtubule networks are poised to be governed through feedback loops (Surcel et al. 2010). "
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    ABSTRACT: Recent work shows that cytokinesis and other cellular morphogenesis events are tuned by an interplay among biochemical signals, cell shape, and cellular mechanics. In cytokinesis, this includes cross-talk between the cortical cytoskeleton and the mitotic spindle in coordination with cell cycle control, resulting in characteristic changes in cellular morphology and mechanics through metaphase and cytokinesis. The changes in cellular mechanics affect not just overall cell shape, but also mitotic spindle morphology and function. This review will address how these principles apply to oocytes undergoing the asymmetric cell divisions of meiosis I and II. The biochemical signals that regulate cell cycle timing during meiotic maturation and egg activation are crucial for temporal control of meiosis. Spatial control of the meiotic divisions is also important, ensuring that the chromosomes are segregated evenly and that meiotic division is clearly asymmetric, yielding two daughter cells - oocyte and polar body - with enormous volume differences. In contrast to mitotic cells, the oocyte does not undergo overt changes in cell shape with its progression through meiosis, but instead maintains a relatively round morphology with the exception of very localized changes at the time of polar body emission. Placement of the metaphase-I and -II spindles at the oocyte periphery is clearly important for normal polar body emission, although this is likely not the only control element. Here, consideration is given to how cellular mechanics could contribute to successful mammalian female meiosis, ultimately affecting egg quality and competence to form a healthy embryo.
    Molecular Reproduction and Development 10/2011; 78(10-11):769-77. DOI:10.1002/mrd.21358 · 2.53 Impact Factor
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