Molecular Mechanisms of Membrane Trafficking. What do we Learn from Dictyostelium discoideum?

Neuhaus, Eva M.; Soldati, Thierry

doi:10.1016/s1434-4610(99)70026-x

Cited by 13 publications

(14 citation statements)

References 88 publications

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“…Dictyostelium cells can use both macropinocytosis of liquid medium and phagocytosis of bacteria to grow. As a genetically tractable professional phagocyte, Dictyostelium has been well used for studies on phagosome maturation, and the pathways involved are highly conserved with those in mammalian macrophages (33)(34)(35). Much less is known about macropinosome maturation, but the large and frequent macropinosomes formed by laboratory strains of Dictyostelium make it ideal for investigations (2).…”

Section: Significancementioning

confidence: 99%

WASH drives early recycling from macropinosomes and phagosomes to maintain surface phagocytic receptors

Buckley

Gopaldass

Bosmani

et al. 2016

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

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Macropinocytosis is an ancient mechanism that allows cells to harvest nutrients from extracellular media, which also allows immune cells to sample antigens from their surroundings. During macropinosome formation, bulk plasma membrane is internalized with all its integral proteins. It is vital for cells to salvage these proteins before degradation, but the mechanisms for sorting them are not known. Here we describe the evolutionarily conserved recruitment of the WASH (WASP and SCAR homolog) complex to both macropinosomes and phagosomes within a minute of internalization. Using Dictyostelium, we demonstrate that WASH drives protein sorting and recycling from macropinosomes and is thus essential to maintain surface receptor levels and sustain phagocytosis. WASH functionally interacts with the retromer complex at both early and late phases of macropinosome maturation, but mediates recycling via retromer-dependent and -independent pathways. WASH mutants consequently have decreased membrane levels of integrins and other surface proteins. This study reveals an important pathway enabling cells to sustain macropinocytosis without bulk degradation of plasma membrane components.phagocytosis | macropinocytosis | WASH | Dictyostelium | trafficking

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Section: Significancementioning

confidence: 99%

WASH drives early recycling from macropinosomes and phagosomes to maintain surface phagocytic receptors

Buckley

Gopaldass

Bosmani

et al. 2016

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

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“…Class-1 myosins localize to cortical regions of high actin turnover during cell migration, associate with cell-cell junctions, bind endocytic vesicles, and support the formation and maintenance of actin-rich protrusive structures during endocytosis (Kim and Flavell, 2008). The eukaryotic model system Dictyostelium discoideum has been used extensively to study class-1 myosins in processes of the endocytic pathway and cell movement (Falk et al, 2003;Jung et al, 1996;Neuhaus and Soldati, 1999). Of the seven class-1 myosins produced in D. discoideum, the longtailed members myosin-1B, myosin-1C and myosin-1D have been implicated in the management of cortical tension during endocytosis Morita et al, 1996); they are important for efficient cell motility (Wessels et al, 1991;Jung et al, 1996), and essential for the recycling of plasma membrane components from endosomes back to the cell surface (Neuhaus and Soldati, 2000).…”

Section: Introductionmentioning

confidence: 99%

Myosin-1C associates with microtubules and stabilizes the mitotic spindle during cell division

Rump

Scholz

Thiel

et al. 2011

Journal of Cell Science

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SummaryThe mitotic spindle in eukaryotic cells is composed of a bipolar array of microtubules (MTs) and associated proteins that are required during mitosis for the correct partitioning of the two sets of chromosomes to the daughter cells. In addition to the well-established functions of MT-associated proteins (MAPs) and MT-based motors in cell division, there is increasing evidence that the F-actin-based myosin motors are important mediators of F-actin-MT interactions during mitosis. Here, we report the functional characterization of the long-tailed class-1 myosin myosin-1C from Dictyostelium discoideum during mitosis. Our data reveal that myosin-1C binds to MTs and has a role in maintenance of spindle stability for accurate chromosome separation. Both myosin-1C motor function and taildomain-mediated MT-F-actin interactions are required for the cell-cycle-dependent relocalization of the protein from the cell periphery to the spindle. We show that the association of myosin-1C with MTs is mediated through the tail domain. The myosin-1C tail can inhibit kinesin motor activity, increase the stability of MTs, and form crosslinks between MTs and F-actin. These data illustrate that myosin-1C is involved in the regulation of MT function during mitosis in D. discoideum.

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“…Laboratory strains have phagocytosis rates 2-fold to 10-fold higher than those observed in macrophages or neutrophils (Thilo, 1985), and the molecular mechanisms of endocytic membrane trafficking have been well investigated in recent years (for review, see Maniak, 1999;Neuhaus and Soldati, 1999;Maniak, 2001;Rupper and Cardelli, 2001), revealing a striking degree of similarity to higher eukaryotes. After uptake and release of the cytoskeletal coat of actin and coronin, particles progress through the endolysosomal pathway.…”

Section: Introductionmentioning

confidence: 99%

High-Resolution Dissection of Phagosome Maturation Reveals Distinct Membrane Trafficking Phases

Gotthardt¹,

Warnatz²,

Henschel

et al. 2002

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113

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Molecular mechanisms of endocytosis in the genetically and biochemically tractable professional phagocyte Dictyostelium discoideum reveal a striking degree of similarity to higher eukaryotic cells. Pulse-chase feeding with latex beads allowed purification of phagosomes at different stages of maturation. Gentle ATP stripping of an actin meshwork entrapping contaminating organelles resulted in a 10-fold increase in yield and purity, as confirmed by electron microscopy. Temporal profiling of signaling, cytoskeletal, and trafficking proteins resulted in a complex molecular fingerprint of phagosome biogenesis and maturation. First, nascent phagosomes were associated with coronin and rapidly received a lysosomal glycoprotein, LmpB. Second, at least two phases of delivery of lysosomal hydrolases (cathepsin D [CatD] and cysteine protease [CPp34]) were accompanied by removal of plasma membrane components (PM4C4 and biotinylated surface proteins). Third, a phase of late maturation, preparing for final exocytosis of undigested material, included quantitative recycling of hydrolases and association with vacuolin. Also, lysosomal glycoproteins of the Lmp family showed distinct trafficking kinetics. The delivery and recycling of CatD was directly visualized by confocal microscopy. This heavy membrane traffic of cargos was precisely accompanied by regulatory proteins such as the Rab7 GTPases and the endosomal SNAREs Vti1 and VAMP7. This initial molecular description of phagocytosis demonstrates the feasibility of a comprehensive analysis of phagosomal lipids and proteins in genetically modified strains.

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Molecular Mechanisms of Membrane Trafficking. What do we Learn from Dictyostelium discoideum?

Cited by 13 publications

References 88 publications

WASH drives early recycling from macropinosomes and phagosomes to maintain surface phagocytic receptors

WASH drives early recycling from macropinosomes and phagosomes to maintain surface phagocytic receptors

Myosin-1C associates with microtubules and stabilizes the mitotic spindle during cell division

High-Resolution Dissection of Phagosome Maturation Reveals Distinct Membrane Trafficking Phases

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