Control of cell membrane tension by myosin-I

Nambiar, Rajalakshmi; McConnell, Russell E.; Tyska, Matthew J.

doi:10.1073/pnas.0901641106

Cited by 166 publications

(149 citation statements)

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“…Membrane tension is the loading force that growing actin filaments fight in order to protrude the membrane [30]. It was previously demonstrated that inhibiting the function of class I myosins function decreased the membrane tension in fibroblasts [42] and that down-regulation of Myo1g expression in T cells gives the same effect. According to this, it has also been observed that the decrease in membrane tension correlates with an increased protrusion generation in fibroblasts [43] and the uniform peripheral expansion of the leading edge and loss of polarity of migrating neutrophils.…”

Section: Discussionmentioning

confidence: 99%

Myosin 1g regulates cytoskeleton plasticity, cell migration, exocytosis, and endocytosis in B lymphocytes

et al. 2014

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Myosin 1g (Myo1g) is a hematopoietic-specific myosin expressed mainly by lymphocytes. Here, we report the localization of Myo1g in B-cell membrane compartments such as lipid rafts, microvilli, and membrane extensions formed during spreading. By using Myo1g-deficient mouse B cells, we detected abnormalities in the adhesion ability and chemokineinduced directed migration of these lymphocytes. We also assessed a role for Myo1g in phagocytosis and exocytosis processes, as these were also irregular in Myo1g-deficient B cells. Taken together, our results show that Myo1g acts as a main regulator of different membrane/cytoskeleton-dependent processes in B lymphocytes.Keywords: B lymphocyte r Chemotaxis r Cytoskeleton r Exo-endocytosis r Myosin Additional supporting information may be found in the online version of this article at the publisher's web-site IntroductionMyosin I refers to a class of single-headed and actin-dependent molecular motors, which regulates a number of cellular functions, including intracellular transport, formation of cell-surface projections, regulation of the cytoskeleton, and regulation of membranerelated events, which includes exocytosis, endocytosis, and phagocytosis [1][2][3].Members of myosin I family contain a single heavy chain of 110-140 kDa [4,5], are monomeric, and do not form filaments unlike muscular/conventional myosin II. The single heavy chain is divided into the head (or motor), neck, and tail domains. The motor domain contains the ATP-binding (where ATP is adenosine triphosphate) site and the actin-binding site. This domain is Correspondence: Dr. Leopoldo Santos-Argumedo e-mail: lesantos@cinvestav.mx followed by the neck domain, which is involved in the binding of myosin light chains; molecules identified as calmodulin in vertebrate and yeast class I myosins [6]. Following the neck domain is the C-terminal tail region, which is enriched in basic residues and is involved in the binding of membrane phosphoinositides [7,8]. In humans and mice, eight different genes encode the eight heavy chains of class I myosins and are named Myo1a to Myo1h [2].Myosin 1g (Myo1g) is a vertebrate class I myosin, which is highly represented in leukocytes, according to microarray databases [9][10][11]. Immunoblot analyses of different tissues and cell lines recently identified this protein as being an exclusively hematopoietic motor protein [12,13].Mass spectrometric proteomic profiling of lymphocyte proteins indicates that Myo1g is the most abundant class I myosin * These authors contributed equally to this work. 878José L. Maravillas-Montero et al. Eur. J. Immunol. 2014. 44: 877-886 expressed by T lymphocytes [13]. Immunofluorescence assays showed that Myo1g localizes to the plasma membrane linked to phosphatidylinositol 4,5-bisphosphate and phosphatidylinositol 3,4,5-triphosphate [14], is particularly enriched at cell-surface microvilli, and associates in an ATP-releasable manner to the actin cytoskeleton [12,13]. In addition to its localization pattern, it has been proposed that this molecula...

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Section: Discussionmentioning

confidence: 99%

Myosin 1g regulates cytoskeleton plasticity, cell migration, exocytosis, and endocytosis in B lymphocytes

et al. 2014

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“…Expression of an EGFP-tagged Myo1-TH1 in cell lines causes a dominant negative phenotype (28,29), which disrupts the targeting of endogenous class I myosins and confers cellular characteristics similar to those observed in Myo1a and Myo1e KO mice (12,30). By transfecting an EGFP-tagged Myo1c-TH1 construct, we expected to block the function of endogenous Myo1c in the A20 mature mouse B cell line.…”

Section: Extent Of B Cell Spreading Is Dependent Of Myo1c Functionmentioning

confidence: 99%

Myosin 1c Participates in B Cell Cytoskeleton Rearrangements, Is Recruited to the Immunologic Synapse, and Contributes to Antigen Presentation

Maravillas-Montero

Gillespie

Patiño-López

et al. 2011

The Journal of Immunology

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Myosin 1c (Myo1c) is a member of the unconventional class I myosins of vertebrates, which directly link the plasma membrane with the microfilament cortical web. Although this molecular motor has been implicated in cell functions such as cytoskeleton organization, cell motility, nuclear transcription, and endocytosis, its role in hematopoietic cells is largely unknown. In this study, we show that Myo1c is abundantly expressed in murine B lymphocytes and is preferentially located at the plasma membrane, especially in peripheral processes such as microvilli. We observed that this motor concentrates at the growing membrane protrusions generated during B cell spreading and that it is actively recruited to the immune synapse. Interestingly, Myo1c was detected in lipid rafts of B cells and showed strong colocalization with MHC-II, particularly after cross-linking of these molecules. By transfection of a dominant negative form of Myo1c or specific siRNA, we also detected alterations in the spreading and Ag-presenting ability of these cells. The data suggest that Myo1c is involved in the cytoskeleton dynamics and membrane protein anchoring or sorting in B lymphocytes.

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“…The myosin-1 tail contains a tail homology 1 (TH1) domain that interacts with acidic phospholipids and, in some cases, also contains a glycine-and proline-rich TH2 domain that binds filamentous actin and an Src homology 3 domain that forms complexes with proteins that stimulate actin filament assembly (4 -10). Myosin-1 is able to cross-link the plasma membrane to the underlying actin cytoskeleton and plays a direct role in the control of cortical and membrane tension (11,12). These motor proteins can also drive vesicle trafficking, pseudopod retraction, and the uptake of particles and fluids by phagocytosis and micropinocytosis (13-16).…”

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confidence: 99%

Structure of the Single-lobe Myosin Light Chain C in Complex with the Light Chain-binding Domains of Myosin-1C Provides Insights into Divergent IQ Motif Recognition

Langelaan¹,

Liburd²,

Yang

et al. 2016

Journal of Biological Chemistry

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Myosin light chains are key regulators of class 1 myosins and typically comprise two domains, with calmodulin being the archetypal example. They bind IQ motifs within the myosin neck region and amplify conformational changes in the motor domain. A single lobe light chain, myosin light chain C (MlcC), was recently identified and shown to specifically bind to two sequentially divergent IQ motifs of the Dictyostelium myosin-1C. To provide a molecular basis of this interaction, the structures of apo-MlcC and a 2:1 MlcC⅐myosin-1C neck complex were determined. The two non-functional EF-hand motifs of MlcC pack together to form a globular four-helix bundle that opens up to expose a central hydrophobic groove, which interacts with the N-terminal portion of the divergent IQ1 and IQ2 motifs. The N-and C-terminal regions of MlcC make critical contacts that contribute to its specific interactions with the myosin-1C divergent IQ motifs, which are contacts that deviate from the traditional mode of calmodulin-IQ recognition.The class 1 myosins (myosin-1) are a widely expressed family of single-headed, non-filament-forming, membrane-binding myosins (1-3). The myosin-1 heavy chain consists of a highly conserved N-terminal motor domain with sites for binding actin and for ATP hydrolysis, a light chain-binding domain (LCBD) 5 that acts as the motor's lever arm, and a C-terminal tail. The myosin-1 tail contains a tail homology 1 (TH1) domain that interacts with acidic phospholipids and, in some cases, also contains a glycine-and proline-rich TH2 domain that binds filamentous actin and an Src homology 3 domain that forms complexes with proteins that stimulate actin filament assembly (4 -10). Myosin-1 is able to cross-link the plasma membrane to the underlying actin cytoskeleton and plays a direct role in the control of cortical and membrane tension (11,12). These motor proteins can also drive vesicle trafficking, pseudopod retraction, and the uptake of particles and fluids by phagocytosis and micropinocytosis (13-16).The myosin-1 LCBD includes one or more IQ motifs, which are ␣-helical sequences between 18 and 25 residues in length that terminate with a loosely conserved IQXXXRGXXXR consensus sequence (17, 18). IQ motifs bind calmodulin (CaM) or CaM-related light chains (LCs) in the absence of Ca 2ϩ . The LCs stabilize the ␣-helical structure of the LCBD, allowing it to function as a rigid swinging lever arm to amplify ATP-dependent conformational changes that originate within the motor domain (19). The LCs are also important regulatory sites that interact with the motor domain to influence mechanochemical properties such as step size, motility rate, and force sensing (1,20,21).The social amoeba Dictyostelium discoideum has been used extensively to study myosin-1 structure, function, and regulation. The seven Dictyostelium myosin-1 isozymes include three with short tails that contain only a TH1 domain (myosin-1A, -1E, and -1F), three with long tails that have TH1, TH2, and Src homology 3 domains (myosin-1B, -1C, and -1D), and one ...

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Control of cell membrane tension by myosin-I

Cited by 166 publications

References 51 publications

Myosin 1g regulates cytoskeleton plasticity, cell migration, exocytosis, and endocytosis in B lymphocytes

Myosin 1g regulates cytoskeleton plasticity, cell migration, exocytosis, and endocytosis in B lymphocytes

Myosin 1c Participates in B Cell Cytoskeleton Rearrangements, Is Recruited to the Immunologic Synapse, and Contributes to Antigen Presentation

Structure of the Single-lobe Myosin Light Chain C in Complex with the Light Chain-binding Domains of Myosin-1C Provides Insights into Divergent IQ Motif Recognition

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