Myosin II localization during cytokinesis occurs by a mechanism that does not require its motor domain

Zang, Ji-Hong; Spudich, James A.

doi:10.1073/pnas.95.23.13652

Cited by 94 publications

(89 citation statements)

References 33 publications

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“…Myosin II is the force-generating motor for cytokinesis and is subject to regulation by both heavy and regulatory light chain phosphorylation (Matsumura et al, 2001;Matsumura, 2005). 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).…”

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

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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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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

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Bresnick

et al. 2006

MBoC

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“…Zang and Spudich had shown that the actin-binding motor (head and neck) domain of DdMII is not required for localization of the tail domain to the cleavage furrow, implying that any required sequence for cleavage-furrow localization resides in the tail domain (Zang and Spudich, 1998). The results of Shu et al imply further that if there is a required sequence it is probably within the relatively small region of the tail required for polymerization (Shu et al, 1999).…”

Section: Expression Of Chimeric Myosins and Cell Growth In Suspensionmentioning

confidence: 99%

“…For example, myosins with mutations in the motor domain of the heavy chain that eliminate ATPase activity but have no effect on polymerization competence (Yumura and Uyeda, 1997a) and polymerization-competent myosin rods devoid of the motor domain (Zang and Spudich, 1998) localize properly to the cleavage furrow but neither protein supports cytokinesis. On the other hand, myosin with mutations in the tail domain that prevent polymerization but have no effect on catalytic activity (Egelhoff et al, 1993) and catalytically active but polymerization incompetent heavy meromyosin (De Lozanne and Spudich, 1987;Fukui et al, 1990) fail to localize to the cleavage furrow and support neither cytokinesis, capping of ConA receptors nor full development.…”

Section: Introductionmentioning

confidence: 99%

Tail chimeras ofDictyosteliummyosin II support cytokinesis and other myosin II activities but not full development

Shu

Liu

Parent

et al. 2002

Journal of Cell Science

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IntroductionClass II myosins consist of two identical heavy chains and two pairs of light chains (Sellers, 1999). Because the cellular slime mold Dictyostelium discoideum contains only a single myosin II heavy chain gene (De Lozanne et al., 1985;Warrick et al., 1986), Dictyostelium myosin II heavy chain-null cells provide an excellent system for determining the biological roles of myosin II and the abilities of mutant myosin II heavy chains to substitute for wild-type heavy chain. In this way, it has been shown that Dictyostelium myosin II (DdMII) is required for cytokinesis and growth of vegetative amoeboid cells in suspension culture, for development and differentiation beyond the mound stage, the first developmental stage, (Knecht and Loomis, 1987;De Lozanne and Spudich, 1987;Manstein et al., 1989) and for capping of concanavalin A (ConA) receptors [(Pasternak et al., 1989b;Fukui et al., 1990) but see AguadoVelasco and Bretscher, for a contrary view (Aguado-Velasco and Bretscher, 1997)]. DdMII heavy chain-null cells are motile and capable of cAMP-induced chemotaxis but both motility and chemotaxis in a spatial gradient of cAMP are impaired compared to wild-type cells (De Lozanne and Spudich, 1987;Wessels et al., 1988;Peters et al., 1988). Null cells can phagocytose bacteria but at the time the experiments described in this paper were carried out phagocytosis by null cells had not been quantified.Cytokinesis in suspension culture, capping of ConA receptors and full development of Dictyostelium to fruiting bodies depend on both the actin-dependent MgATPase activity of DdMII and its ability to form filaments. For example, myosins with mutations in the motor domain of the heavy chain that eliminate ATPase activity but have no effect on polymerization competence (Yumura and Uyeda, 1997a) and polymerization-competent myosin rods devoid of the motor domain (Zang and Spudich, 1998) localize properly to the cleavage furrow but neither protein supports cytokinesis. On the other hand, myosin with mutations in the tail domain that prevent polymerization but have no effect on catalytic activity (Egelhoff et al., 1993) and catalytically active but polymerization incompetent heavy meromyosin (De Lozanne and Spudich, 1987;Fukui et al., 1990) Recently, we showed that the actin-activated MgATPase activity of myosin chimeras in which the tail domain of Dictyostelium myosin II heavy chain is replaced by the tail domain of either Acanthamoeba or chicken smooth muscle myosin II is unregulated and about 20 times higher than wild-type myosin. The Acanthamoeba chimera forms short bipolar filaments similar to, but shorter than, filaments of Dictyostelium myosin and the smooth muscle chimera forms much larger side-polar filaments. We now find that the Acanthamoeba chimera expressed in myosin null cells localizes to the periphery of vegetative amoeba similarly to wild-type myosin but the smooth muscle chimera is heavily concentrated in a single cortical patch. Despite their different tail sequences and filament structures and different...

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“…It is known that recruitment of myosin II into the central cortical layer of a dividing cell is independent of its binding to actin (Yumura and Uyeda, 1997;Zang and Spudich, 1998). Consequently, it can be postulated that a population of binding sites for myosin II exists in this region, probably anchored to the cell plasma membrane.…”

Section: Myosin II Filaments As a Mechanical Lensmentioning

confidence: 99%

“…Bars,10mm. pose that cortical myosin II mini-filaments act as linkages between actin filaments and the cell plasma membrane. Actin-binding activity of myosin II is known to be essential for its full functionality, since truncated molecules that lack the actin-binding activity cannot rescue the cytokinesis defect in myosin II-null cells (Yumura and Uyeda, 1997;Zang and Spudich, 1998). Also, dynamic shuffling of myosin II between cortical and cytoplasmic populations seems to be of crucial importance for its function, since mutant cells that express the triple-alanine construct have a strong cytokinesis defect (Egelhoff et al, 1993).…”

Section: Myosin II Filaments As a Mechanical Lensmentioning

confidence: 99%

Advances in Cytokinesis Research. On the Mechanism of Cleavage Furrow Ingression in Dictyostelium.

Weber

2001

Cell Struct. Funct.

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ABSTRACT. The ability of Dictyostelium cells to divide without myosin II in a cell cycle-coupled manner has opened two questions about the mechanism of cleavage furrow ingression. First, are there other possible functions for myosin II in this process except for generating contraction of the furrow by a sliding filament mechanism? Second, what could be an alternative mechanical basis for the furrowing? Using aberrant changes of the cell shape and anomalous localization of the actin-binding protein cortexillin I during asymmetric cytokinesis in myosin IIdeficient cells as clues, it is proposed that myosin II filaments act as a mechanical lens in cytokinesis. The mechanical lens serves to focus the forces that induce the furrowing to the center of the midzone, a cortical region where cortexillins are enriched in dividing cells. Additionally, continual disassembly of a filamentous actin meshwork at the midzone is a prerequisite for normal ingression of the cleavage furrow and a successful cytokinesis. If this process is interrupted, as it occurs in cells that lack cortexillins, an overassembly of filamentous actin at the midzone obstructs the normal cleavage. Disassembly of the crosslinked actin network can generate entropic contractile forces in the cortex, and may be considered as an alternative mechanism for driving ingression of the cleavage furrow. Instead of invoking different types of cytokinesis that operate under attached and unattached conditions in Dictyostelium, it is anticipated that these cells use a universal multifaceted mechanism to divide, which is only moderately sensitive to elimination of its constituent mechanical processes.Key words: cytokinesis/cell division/mechanical lens/actin disassembly/bending stiffness/cortexillin Since the discovery of myosin II-independent mitotic cell division in Dictyostelium discoideum (Neujahr et al., 1997a), several attempts have been undertaken to clarify its mechanism and relate it to the classical model of cytokinesis, which is based on the concept of contractile ring Uyeda et al., 2000). Basic assumption in these propositions is that cytokinesis in wild-type Dictyostelium cells is driven by contraction of a contractile ring, an annular structure that assembles at the central zone of a dividing cell and consists of actin and myosin II filaments. Thus, cells that express myosin II are assumed to divide primarily by the standard sliding-filament mechanism, and this mode of cell division was termed cytokinesis A. It was argued that myosin II-null cells use a different mechanism to divide by a process termed cytokinesis B, apparently not used by wild-type cells. In this view, cytokinesis B depends on expansion of the polar regions of a dividing cell, which induces a passive ingression at the cleavage furrow by drawing the cytoplasmic material out of the midzone (Uyeda et al., 2000). Traction forces between the ventral cell surface and a substratum are viewed as necessary in order to support the polar expansion. A sufficient magnitude of the traction forces and t...

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Myosin II localization during cytokinesis occurs by a mechanism that does not require its motor domain

Cited by 94 publications

References 33 publications

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

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

Tail chimeras ofDictyosteliummyosin II support cytokinesis and other myosin II activities but not full development

Advances in Cytokinesis Research. On the Mechanism of Cleavage Furrow Ingression in Dictyostelium.

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