Dictyostelium mutants lacking multiple classic myosin I isoforms reveal combinations of shared and distinct functions.

Jung, Goeh; Wu, Xufeng; Hammer, John A.

doi:10.1083/jcb.133.2.305

Cited by 163 publications

(194 citation statements)

References 59 publications

(176 reference statements)

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“…Experiments performed in multiple eukaryotic model systems have implicated class I myosins in various aspects of membranerelated events including phagocytosis (29)(30)(31)(32)(33), endocytosis (34)(35)(36)(37), exocytosis (38,39), and membrane recycling (40). Although our current data set does not allow us to rule out the possibility that perturbations in membrane trafficking may contribute to the changes in membrane tension observed in our experiments, our results do provide strong support for a model where class I myosins play a direct role in the control of membrane tension, by contributing to adhesion between the plasma membrane and underlying actin cytoskeleton.…”

Section: Discussionmentioning

confidence: 99%

Control of cell membrane tension by myosin-I

Nambiar

McConnell²,

Tyska³

2009

Proc. Natl. Acad. Sci. U.S.A.

166

137

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All cell functions that involve membrane deformation or a change in cell shape (e.g., endocytosis, exocytosis, cell motility, and cytokinesis) are regulated by membrane tension. While molecular contacts between the plasma membrane and the underlying actin cytoskeleton are known to make significant contributions to membrane tension, little is known about the molecules that mediate these interactions. We used an optical trap to directly probe the molecular determinants of membrane tension in isolated organelles and in living cells. Here, we show that class I myosins, a family of membrane-binding, actin-based motor proteins, mediate membrane/cytoskeleton adhesion and thus, make major contributions to membrane tension. These studies show that class I myosins directly control the mechanical properties of the cell membrane; they also position these motor proteins as master regulators of cellular events involving membrane deformation.actin ͉ brush border ͉ cytoskeleton ͉ microvilli ͉ optical trap

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Section: Discussionmentioning

confidence: 99%

Control of cell membrane tension by myosin-I

Nambiar

McConnell²,

Tyska³

2009

Proc. Natl. Acad. Sci. U.S.A.

166

137

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“…To address V-1's role in this actin-based process, we compared the rate of uptake of the nondigestible fluid phase marker TRITC-dextran in WT and V-1-null cells. Of note, the rate of accumulation of this marker within cells during the first ∼60 min after its addition to the medium accurately reports the rate of fluid phase endocytosis because the time interval between the uptake and exoctyosis of nondigestible markers in Dictyostelium, which lack a rapid recycling component, is ∼60 min (41). Fig.…”

Section: Vegetative V-1-null Cells Exhibit a Defect In Macropinocytosmentioning

confidence: 99%

“…At this stage, Dictyostelium amoebae exhibit their highest rate of motility, which is approximately two to four times faster than the rate exhibited by vegetative cells (41,43,44). Ripple-stage cells were then harvested by trituration and allowed to attach at low density on chamber slides for 20 min.…”

Section: Vegetative V-1-null Cells Exhibit a Defect In Macropinocytosmentioning

confidence: 99%

V-1 regulates capping protein activity in vivo

Jung

Alexander

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Capping Protein (CP) plays a central role in the creation of the Arp2/ 3-generated branched actin networks comprising lamellipodia and pseudopodia by virtue of its ability to cap the actin filament barbed end, which promotes Arp2/3-dependent filament nucleation and optimal branching. The highly conserved protein V-1/Myotrophin binds CP tightly in vitro to render it incapable of binding the barbed end. Here we addressed the physiological significance of this CP antagonist in Dictyostelium, which expresses a V-1 homolog that we show is very similar biochemically to mouse V-1. Consistent with previous studies of CP knockdown, overexpression of V-1 in Dictyostelium reduced the size of pseudopodia and the cortical content of Arp2/3 and induced the formation of filopodia. Importantly, these effects scaled positively with the degree of V-1 overexpression and were not seen with a V-1 mutant that cannot bind CP. V-1 is present in molar excess over CP, suggesting that it suppresses CP activity in the cytoplasm at steady state. Consistently, cells devoid of V-1, like cells overexpressing CP described previously, exhibited a significant decrease in cellular F-actin content. Moreover, V-1-null cells exhibited pronounced defects in macropinocytosis and chemotactic aggregation that were rescued by V-1, but not by the V-1 mutant. Together, these observations demonstrate that V-1 exerts significant influence in vivo on major actin-based processes via its ability to sequester CP. Finally, we present evidence that V-1's ability to sequester CP is regulated by phosphorylation, suggesting that cells may manipulate the level of active CP to tune their "actin phenotype."T he addition of Capping Protein (CP) to seed-initiated actin polymerization assays results in the rapid cessation of polymerization because CP binds with very high affinity to the fastgrowing barbed end of the actin filament to block further monomer addition (1). Direct extrapolation of this simple, potent biochemical property would suggest that the cell's content of F-actin should rise and fall as its content of CP is artificially forced to fall and rise, respectively. Indeed, this finding was reported many years ago in Dictyostelium amoeba (2). This simple view of CP's role in regulating actin assembly in vivo falls short of the whole story, however. The additional complexity arises from the critical relationship between CP and the Arp2/3 complex, the major actin nucleating machine that generates the branched actin networks comprising lamellipodia and pseudopodia (3). At the heart of this relationship is the fact that CP increases the rate of Arp2/3-dependent filament nucleation and promotes optimal branching by rapidly capping filaments (4). As a result, CP promotes actin-related proteins 2 and 3 (Arp2/3)-driven actin assembly and motility (4, 5). This effect was evident from early solution experiments focused on defining the function of the Arp2/3 complex (6), verified by in vitro reconstitution of the Arp2/3-dependent motility of Listeria (5), and explained mecha...

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“…Nevertheless, it has been shown that phagocytosis (7) and references therein) as well as part of axonal transport (8) and exocytosis (9) are actin-based movement. Endocytosis in yeast (10), vertebrates (11) and amoebae (12,13), polarized secretion in yeast (14), and fungi (15), vacuole inheritance in yeast (16), contractile vacuole function in amoebae (17), as well as blastoderm cellularization and cytoplasmic transport of particles in Drosophila (18,19), require specific myosin motors. Myosin V has now been shown to power the redistribution of melanosomes in mouse melanocytes (20,21), as well as in fish and Xenopus melanophores (22,23).…”

Section: Soldati Geissler and Schwarzmentioning

confidence: 99%

“…Disruptions of single myosin I genes showed only subtle alterations of cell motility, and multiple disruptions had to be performed to induce stronger phenotypic impairments. Different combinations of double and even triple mutations of myoB, myoC, myoD, or myoA resulted in strains impaired to different extents in macropinocytosis and motility, highlighting the potentially high degree of functional redundancy (12,13,75). It is important to note that in a similar way, disruption of the genes for multiple actin-binding proteins was necessary to reveal strong phe-Exploring the Myosin Repertoire 399 notypic alterations (76), indicating that a certain level of redundancy is probably inherent to components of the actin cytoskeleton and associated vital functions.…”

Section: Phylogenetic Analysis Shows the Newcomer Myok (See "A Potentmentioning

confidence: 99%

Unconventional myosins at the crossroad of signal transduction and cytoskeleton remodeling

1999

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The cytoplasm of eukaryotic cells is a very complex milieu and unraveling how its unique cytoarchitecture is achieved and maintained is a central theme in modern cell biology. It is crucial to understand how organelles and macro-complexes of RNA and/or proteins are transported to and/or maintained at their specific cellular locations. The importance of filamentous-actindirected myosin-powered cargo transport was only recently realized, and after an initial explosion in the identification of new molecules, the field is now concentrating on their functional dissection. Direct connections of myosins to a variety of cellular tasks are now slowly emerging, such as in cytokinesis, phagocytosis, endocytosis, polarized secretion and exocytosis, axonal transport, etc. Unconventional myosins have been identified in a wide variety of organisms, making the presence of actin and

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Dictyostelium mutants lacking multiple classic myosin I isoforms reveal combinations of shared and distinct functions.

Cited by 163 publications

References 59 publications

Control of cell membrane tension by myosin-I

Control of cell membrane tension by myosin-I

V-1 regulates capping protein activity in vivo

Unconventional myosins at the crossroad of signal transduction and cytoskeleton remodeling

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