Myosin-1c Couples Assembling Actin to Membranes to Drive Compensatory Endocytosis

Sokac, Anna Marie; Schietroma, Cataldo; Gundersen, Cameron B.; Bement, William M.

doi:10.1016/j.devcel.2006.09.002

Cited by 72 publications

(77 citation statements)

References 37 publications

(51 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

138

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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

138

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“…In addition, mutations in Myosin IA, Myosin IC, and Myosin IF are associated with hereditary hearing loss (Chen et al 2001;Donaudy et al 2003;Zadro et al 2009). In vertebrates, each class I myosin is expressed in various cell types and has distinct functions that depend on their cellular context (Gillespie 2004;Philimonenko et al 2004;Sokac et al 2006). Even so, these multiple class I myosins are predicted to have overlapping functions, as found in yeast and Dictyostelium (Tyska et al 2005;Nambiar et al 2009;Chen et al 2012), complicating the understanding of their in vivo roles (Kim and Flavell 2008).…”

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confidence: 99%

“…Myosin IA is thought to maintain brush border structure and membrane tension and to power the release of vesicles from the tips of microvilli (Tyska et al 2005;McConnell et al 2009;Nambiar et al 2009), while Myosin IB regulates the actin-dependent post-Golgi trafficking of cargo (Almeida et al 2011). Myosin IC is involved in vesicle transport both in the fertilized egg of Xenopus and in mammalian cells (Bose et al 2002;Sokac et al 2006;Fan et al 2012) and regulates ion channels in the hair cells of the inner ear (Gillespie and Cyr 2004). Interestingly, an isoform of Myosin IC localizes to the nucleus and contributes to transcription (Pestic-Dragovich et al 2000;Philimonenko et al 2004), and Myosin IF is involved in neutrophil migration (Kim et al 2006).…”

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confidence: 99%

Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development inDrosophila

et al. 2015

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The class I myosin genes are conserved in diverse organisms, and their gene products are involved in actin dynamics, endocytosis, and signal transduction. Drosophila melanogaster has three class I myosin genes, Myosin 31DF (Myo31DF), Myosin 61F (Myo61F), and Myosin 95E (Myo95E). Myo31DF, Myo61F, and Myo95E belong to the Myosin ID, Myosin IC, and Myosin IB families, respectively. Previous loss-of-function analyses of Myo31DF and Myo61F revealed important roles in left-right (LR) asymmetric development and enterocyte maintenance, respectively. However, it was difficult to elucidate their roles in vivo, because of potential redundant activities. Here we generated class I myosin double and triple mutants to address this issue. We found that the triple mutant was viable and fertile, indicating that all three class I myosins were dispensable for survival. A loss-of-function analysis revealed further that Myo31DF and Myo61F, but not Myo95E, had redundant functions in promoting the dextral LR asymmetric development of the male genitalia. Myo61F overexpression is known to antagonize the dextral activity of Myo31DF in various Drosophila organs. Thus, the LR-reversing activity of overexpressed Myo61F may not reflect its physiological function. The endogenous activity of Myo61F in promoting dextral LR asymmetric development was observed in the male genitalia, but not the embryonic gut, another LR asymmetric organ. Thus, Myo61F and Myo31DF, but not Myo95E, play tissue-specific, redundant roles in LR asymmetric development. Our studies also revealed differential colocalization of the class I myosins with filamentous (F)-actin in the brush border of intestinal enterocytes.KEYWORDS myosin I; Myosin 31DF; Myosin 61F; Myosin 95E; left-right asymmetry T HE class I myosin genes encode myosin heavy chains, which are conserved in phylogenetically diverse organisms (Sellers 2000;Krendel and Mooseker 2005). The class I myosins are nonfilamentous, actin-based motor proteins and were the first discovered unconventional myosin proteins. These myosins are involved in a variety of cellular processes, such as cell migration, cell adhesion, and cell growth, through their regulation of actin dynamics, endocytosis, and signal transduction (Osherov and May 2000;Krendel and Mooseker 2005;Kim and Flavell 2008;McConnell and Tyska 2010).The structure of the myosin I heavy chains is evolutionarily conserved and composed of head (or motor), neck, and tail domains ( Figure 1A) (Coluccio 1997;Barylko et al. 2000). The head domain binds to filamentous (F)-actin and adenosine triphosphate (ATP), a common feature of myosin proteins ( Figure 1A) (Mermall et al. 1998); the neck domain possesses one or more IQ motifs, which directly interact with calmodulin or calmodulin-related myosin light chains (Coluccio 1997;Barylko et al. 2000), and the tail domains are divided into short and long types. Short tails contain a single tail homology 1 (TH1) domain, which is rich in basic residues and thought to interact with plasma membranes (Coluccio 1997;Barylko...

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“…It consists of a motor domain, a neck or lever arm domain (three or four IQ repeats each of which binds a calmodulin), and a cargo-binding domain (4)(5)(6). In adipocytes Myo1c facilitates glucose transporter recycling in response to insulin (7,8), and in amphibian oocytes Myo1c mediates exocytosis (9). In the specialized cells of the inner ear, there is considerable evidence that Myo1c acts as a mediator of adaptation of mechanoelectrical transduction in stereocilia (10,11).…”

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confidence: 99%

Calcium sensitivity of the cross-bridge cycle of Myo1c, the adaptation motor in the inner ear

Adamek

Coluccio

Geeves

2008

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

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The class I myosin Myo1c is a mediator of adaptation of mechanoelectrical transduction in the stereocilia of the inner ear. Adaptation, which is strongly affected by Ca 2؉ , permits hair cells under prolonged stimuli to remain sensitive to new stimuli. Using a Myo1c fragment (motor domain and one IQ domain with associated calmodulin), with biochemical and kinetic properties similar to those of the native molecule, we have performed a thorough analysis of the biochemical cross-bridge cycle. We show that, although the steady-state ATPase activity shows little calcium sensitivity, individual molecular events of the cross-bridge cycle are calcium-sensitive. Of significance is a 7-fold inhibition of the ATP hydrolysis step and a 10-fold acceleration of ADP release in calcium. These changes result in an acceleration of detachment of the cross-bridge and a lengthening of the lifetime of the detached M-ATP state. These data support a model in which slipping adaptation, which reduces tip-link tension and allows the transduction channels to close after an excitatory stimulus, is mediated by Myo1c and modulated by the calcium transient. molecular motor ͉ myosin M yosins are actin-based molecular motors that support a variety of cellular functions including muscle contraction and cell migration. There are at least two dozen classes in the myosin superfamily based on analysis of sequences in the catalytic domain (1). Myo1c is a class I myosin that is widely expressed in vertebrate tissues (2, 3). It consists of a motor domain, a neck or lever arm domain (three or four IQ repeats each of which binds a calmodulin), and a cargo-binding domain (4-6). In adipocytes Myo1c facilitates glucose transporter recycling in response to insulin (7,8), and in amphibian oocytes Myo1c mediates exocytosis (9). In the specialized cells of the inner ear, there is considerable evidence that Myo1c acts as a mediator of adaptation of mechanoelectrical transduction in stereocilia (10, 11).Neighboring stereocilia on the hair cells of the inner ear are connected by extracellular tip links that are attached to transduction channels, which in turn are attached to an adaptation-motor complex consisting of Myo1c molecules. The prevailing model for mechanotransduction is that deflection of the stereocilia by sound or motion affects tip-link tension and causes opening or closing of transduction channels through which potassium and calcium ions pass (5, 12, 13). Myo1c sets the transducer sensitivity by moving along the core bundle of actin filaments in the stereocilia until the resting tension in the tip link is at a point where the channels are poised just below the threshold tension required to open the channels (Fig. 1). During an excitatory stimulus, movement of the stereocilia increases tip-link tension, opening the channels. Fig. 1 illustrates how in adaptation the motor/transducer complex responds to increased tension by slipping down the actin cytoskeleton thereby reducing tip-link tension. Alternatively, reduced tension causes Myo1c to ascend the ac...

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Myosin-1c Couples Assembling Actin to Membranes to Drive Compensatory Endocytosis

Cited by 72 publications

References 37 publications

Control of cell membrane tension by myosin-I

Control of cell membrane tension by myosin-I

Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development inDrosophila

Calcium sensitivity of the cross-bridge cycle of Myo1c, the adaptation motor in the inner ear

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