Myosin II dynamics and cortical flow during contractile ring formation in <i>Dictyostelium</i> cells

Yumura, Shigehiko

doi:10.1083/jcb.200011013

Cited by 110 publications

(113 citation statements)

References 45 publications

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“…At late anaphase, cortical myosin II begins sliding along the cortex from the polar to equatorial regions to form the contractile ring at the future cleavage site. This strongly suggests that cortical flow is responsible for concentrating myosin II at the cleavage plane, as has been documented recently during cytokinesis in Dictyostelium (Yumura, 2001). At the end of this reorganization, the myosin ring contracts, providing the force that pulls the cleavage furrow inward.…”

Section: Myosin II and Cytokinesismentioning

confidence: 72%

Reassessing the Role and Dynamics of Nonmuscle Myosin II during Furrow Formation in EarlyDrosophilaEmbryos

Royou

Field

Sisson

et al. 2004

MBoC

280

293

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The early Drosophila embryo undergoes two distinct membrane invagination events believed to be mechanistically related to cytokinesis: metaphase furrow formation and cellularization. Both involve actin cytoskeleton rearrangements, and both have myosin II at or near the forming furrow. Actin and myosin are thought to provide the force driving membrane invagination; however, membrane addition is also important. We have examined the role of myosin during these events in living embryos, with a fully functional myosin regulatory light-chain-GFP chimera. We find that furrow invagination during metaphase and cellularization occurs even when myosin activity has been experimentally perturbed. In contrast, the basal closure of the cellularization furrows and the first cytokinesis after cellularization are highly dependent on myosin. Strikingly, when ingression of the cellularization furrow is experimentally inhibited by colchicine treatment, basal closure still occurs at the appropriate time, suggesting that it is regulated independently of earlier cellularization events. We have also identified a previously unrecognized reservoir of particulate myosin that is recruited basally into the invaginating furrow in a microfilament-independent and microtubule-dependent manner. We suggest that cellularization can be divided into two distinct processes: furrow ingression, driven by microtubule mediated vesicle delivery, and basal closure, which is mediated by actin/myosin based constriction. INTRODUCTIONCytokinesis is the final step of cell division, required for the equal partitioning of the newly separated genetic material into two sister cells. Conventional animal cell cytokinesis is characterized by the assembly of an actin-myosin-based structure called the contractile ring, positioned midway between the two spindle poles, which drives the formation of a cleavage furrow. Despite its importance, many aspects of cytokinesis remain obscure. For example, although it is now well established that the cleavage plane can be specified by the central spindle or by astral microtubules (reviewed in Glotzer, 2001;Straight and Field, 2000), it is not known how microtubules trigger the assembly of the contractile ring or if they are required for regulating the contractile force.During the early phase of Drosophila embryogenesis, the embryo undergoes 13 rounds of nuclear division in the absence of cytokinesis. However, two kinds of membrane invagination events believed to be mechanistically related to conventional cytokinesis take place: metaphase furrow formation and cellularization. Metaphase furrows, or pseudocleavage furrows, form transiently during the 10th to 13th mitotic cycles of the cortical syncytial divisions. At interphase, actin is concentrated in cortical caps above each nucleus, but with entry into mitosis, the actin cytoskeleton reorganizes from caps to rings at the base of shallow furrows surrounding each developing spindle (Zalokar and Erk, 1976;Foe and Alberts, 1983;Karr and Alberts, 1986;Foe et al., 2000). These furrows fo...

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Section: Myosin II and Cytokinesismentioning

confidence: 72%

Reassessing the Role and Dynamics of Nonmuscle Myosin II during Furrow Formation in EarlyDrosophilaEmbryos

Royou

Field

Sisson

et al. 2004

MBoC

280

293

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“…Our understanding of heavy chain phosphorylation comes primarily from studies on the slime mold Dictyostelium discoideum, where phosphorylation of the tail region by a family of heavy chain kinases inhibits filament formation (Egelhoff et al, 1993;Sabry et al, 1997;Yumura and Uyeda, 1997;Zang and Spudich, 1998;Yumura et al, 2005). The expression of nonphosphorylatable heavy chain mutants results in abnormally high myosin II recruitment to the cell equator, whereas expression of myosin II heavy chains containing amino acid substitutions that mimic the phosphorylated state prevents recruitment to the contractile ring (Sabry et al, 1997;Yumura, 2001). These phosphorylation sites reside in a C-terminal extension of myosin heavy chain that is required for proper cytokinesis in Dictyostelium (O'Halloran and Spudich, 1990) but is absent from myosin II in animal cells.…”

Section: Introductionmentioning

confidence: 99%

A Global, Myosin Light Chain Kinase-dependent Increase in Myosin II Contractility Accompanies the Metaphase–Anaphase Transition in Sea Urchin Eggs

Lucero

Stack

Bresnick

et al. 2006

MBoC

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Myosin II is the force-generating motor for cytokinesis, and although it is accepted that myosin contractility is greatest at the cell equator, the temporal and spatial cues that direct equatorial contractility are not known. Dividing sea urchin eggs were placed under compression to study myosin II-based contractile dynamics, and cells manipulated in this manner underwent an abrupt, global increase in cortical contractility concomitant with the metaphase-anaphase transition, followed by a brief relaxation and the onset of furrowing. Prefurrow cortical contractility both preceded and was independent of astral microtubule elongation, suggesting that the initial activation of myosin II preceded cleavage plane specification. The initial rise in contractility required myosin light chain kinase but not Rho-kinase, but both signaling pathways were required for successful cytokinesis. Last, mobilization of intracellular calcium during metaphase induced a contractile response, suggesting that calcium transients may be partially responsible for the timing of this initial contractile event. Together, these findings suggest that myosin II-based contractility is initiated at the metaphaseanaphase transition by Ca 2؉ -dependent myosin light chain kinase (MLCK) activity and is maintained through cytokinesis by both MLCK-and Rho-dependent signaling. Moreover, the signals that initiate myosin II contractility respond to specific cell cycle transitions independently of the microtubule-dependent cleavage stimulus. INTRODUCTIONAt its most fundamental level, cytokinesis in animal cells is brought about by regional differences in cortical contractility that drives partitioning of the cytoplasm into two daughter cells (Wang, 2005). Force generation is accomplished by the transient assembly of a contractile ring, and recent genetic and proteomic approaches have significantly increased our knowledge of ring components and regulatory molecules (Echard et al., 2004;Eggert et al., 2004;Skop et al., 2004). Studies in yeast using green fluorescent protein-tagged ring components have demonstrated that ring components are recruited to the division site in a hierarchical manner that involves the progressive assembly of more complex structures (Lippincott and Li, 1998;Wu et al., 2003;Wu and Pollard, 2005). In contrast, the temporal sequence in which ring components are recruited to the division site in animal cells is not as well resolved; thus, it remains unclear whether the contractile ring assembles in a similar sequential manner. Moreover, it is not known how ring assembly is coordinated in space and time with chromosome segregation. Thus, although great advances have been made in our understanding of the contractile ring itself, fundamental gaps remain in our understanding of the spatiotemporal regulation of cytokinesis.The mechanical nature of cytokinesis was appreciated by early cell biologists (Wilson, 1928;Rappaport, 1996), and for decades investigators have taken advantage of the large size and regular geometry of echinoderm eggs to st...

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“…Follow-up studies showed the presence of myosin, some assembled into minifilaments, located in the furrow region and associated with actin filaments of mixed polarity (Fujiwara and Pollard 1976;Mabuchi and Okuno 1977;Sanger and Sanger 1980;Yumura et al 1984;Maupin and Pollard 1986). Many of these essential conclusions have been confirmed by live-cell imaging with fluorescently labeled actin and myosin in diverse animal species and fungi (Bi et al 1998;Bezanilla et al 2000;Yumura 2001;Murthy and Wadsworth 2005).…”

Section: Contractile Ringmentioning

confidence: 69%

Cytokinesis in Metazoa and Fungi

Glotzer

2016

Cold Spring Harb Perspect Biol

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SUMMARYCell division-cytokinesis-involves large-scale rearrangements of the entire cell. Primarily driven by cytoskeletal proteins, cytokinesis also depends on topological rearrangements of the plasma membrane, which are coordinated with nuclear division in both space and time. Despite the fundamental nature of the process, different types of eukaryotic cells show variations in both the structural mechanisms of cytokinesis and the regulatory controls. In animal cells and fungi, a contractile actomyosin-based structure plays a central, albeit flexible, role. Here, the underlying molecular mechanisms are summarized and integrated and common themes are highlighted.

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Myosin II dynamics and cortical flow during contractile ring formation in Dictyostelium cells

Cited by 110 publications

References 45 publications

Reassessing the Role and Dynamics of Nonmuscle Myosin II during Furrow Formation in EarlyDrosophilaEmbryos

Reassessing the Role and Dynamics of Nonmuscle Myosin II during Furrow Formation in EarlyDrosophilaEmbryos

A Global, Myosin Light Chain Kinase-dependent Increase in Myosin II Contractility Accompanies the Metaphase–Anaphase Transition in Sea Urchin Eggs

Cytokinesis in Metazoa and Fungi

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