mDia1 Assembles a Linear F-Actin Coat at Membrane Invaginations To Drive Listeria monocytogenes Cell-to-Cell Spreading

Dhanda, Aaron S.; Vogl, A. Wayne; Ness, Fern; Innocenti, Metello; Guttman, Julian A.

doi:10.1128/mbio.02939-21

Cited by 6 publications

(8 citation statements)

References 84 publications

(127 reference statements)

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“…While these proteins have been examined at intercellular spreading events, their localizations at S. flexneri membrane protrusions and/or membrane invaginations are not easily ascertainable. Fortunately, as shown above, our mixed-cell assays (Dhanda et al, 2019;Dhanda et al, 2020;Dhanda, Vogl, Ness, et al, 2021;Dhanda, Yang, Kooner, & Guttman, 2021) provide a way to clearly visualize these proteins at the precise sites of cell-to-cell spreading. Furthermore, many of these factors remain unexplored at S. flexneri comet/rocket tails.…”

Section: Examination Of Host Clathrin Proteins and Endocytic Lipid Sp...mentioning

confidence: 89%

“…Evidence for this comes from studies showing that the actin polymerization necessary for L. monocytogenes initial invasion and enteropathogenic Escherichia coli (EPEC) pedestal formation follows (and requires) clathrin (Veiga et al, 2007). Conversely, we recently showed that caveolin accumulation around L. monocytogenes membrane invaginations requires (and follows) mDia1-mediated actin polymerization at the structures (Dhanda, Vogl, Ness, et al, 2021). However, whether or not F-actin accumulates around S. flexneri membrane invaginations prior to caveolin/clathrin or is a consequence of their presence remains to be seen.…”

Section: Discussionmentioning

confidence: 99%

“…Our previously optimized mixed‐cell assay (Dhanda et al, 2019; Dhanda et al, 2020; Dhanda, Vogl, Ness, et al, 2021; Dhanda, Yang, & Guttman, 2021; Dhanda, Yang, Kooner, & Guttman, 2021) was utilized to examine host factors at S. flexneri comet/rocket tails, membrane protrusions, and membrane invaginations. The major advantage of this assay is that it allows us to examine a fluorescent fusion protein of the host factor of interest solely within comet/rocket tail‐ and membrane protrusion‐forming cells or membrane invagination‐forming cells.…”

Section: Methodsmentioning

confidence: 99%

“…Unfortunately, in the context of S. flexneri infections, there remains lesser analysis on the content of the bacterial actin‐rich structures formed and in particular a dearth of information about the endocytic‐like membrane invaginations. Recently, our group has reported on several new and diverse L. monocytogenes membrane invagination components, of which many are endocytic or cytoskeletal in nature (Dhanda et al, 2020; Dhanda, Vogl, Ness, et al, 2021; Dhanda, Yang, & Guttman, 2021; Dhanda, Yang, Kooner, & Guttman, 2021). Of these proteins, only a handful have been examined during S. flexneri infections.…”

Section: Introductionmentioning

confidence: 99%

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Localization of host endocytic and actin‐associated proteins during Shigella flexneri intracellular motility and intercellular spreading

Dhanda

Guttman

2022

The Anatomical Record

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Shigella flexneri (S. flexneri), the causative agent of bacillary dysentery, uses an effector‐mediated strategy to hijack host cells and cause disease. To propagate and spread within human tissues, S. flexneri bacteria commandeer the host actin cytoskeleton to generate slender actin‐rich comet tails to move intracellularly, and later, plasma membrane actin‐based protrusions to move directly between adjacent host cells. To facilitate intercellular bacterial spreading, large micron‐sized endocytic‐like membrane invaginations form at the periphery of neighboring host cells that come into contact with S. flexneri‐containing membrane protrusions. While S. flexneri comet tails and membrane protrusions consist primarily of host actin cytoskeletal proteins, S. flexneri membrane invaginations remain poorly understood with only clathrin and the clathrin adapter epsin‐1 localized to the structures. Tangentially, we recently reported that Listeria monocytogenes, another actin‐hijacking pathogen, exploits an assortment of caveolar and actin‐bundling proteins at their micron‐sized membrane invaginations formed during their cell‐to‐cell movement. Thus, to further characterize the S. flexneri disease process, we set out to catalog the distribution of a variety of actin‐associated and caveolar proteins during S. flexneri actin‐based motility and cell‐to‐cell spreading. Here we show that actin‐associated proteins found at L. monocytogenes comet tails and membrane protrusions mimic those present at S. flexneri comet tails with the exception of α‐actinins 1 and 4, which were shed from S. flexneri membrane protrusions. We also demonstrate that all known host endocytic components found at L. monocytogenes membrane invaginations are also present at those formed during S. flexneri infections.

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Section: Examination Of Host Clathrin Proteins and Endocytic Lipid Sp...mentioning

confidence: 89%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Localization of host endocytic and actin‐associated proteins during Shigella flexneri intracellular motility and intercellular spreading

Dhanda

Guttman

2022

The Anatomical Record

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“…This mode of elongation imposes frequent interactions between FH1 and the barbed end, which would likely reduce the probability of formins to lag behind the barbed end. In addition, active formins are thought to be anchored to membranes 28 , which should restrict further their ability to diffuse along the core of actin filaments.…”

Section: Discussionmentioning

confidence: 99%

Direct observation of the conformational states of formin mDia1 at actin filament barbed ends and along the filament

Maufront

Guichard

Cao

et al. 2023

MBoC

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The fine regulation of actin polymerization is essential to control cell motility, architecture and to perform essential cellular functions. Formins are key regulators of actin filament assembly, known to processively elongate filament barbed ends and increase their polymerization rate. Different models have been extrapolated to describe the molecular mechanism governing the processive motion of formin FH2 domains at polymerizing barbed ends. Using negative stain electron microscopy, we directly identified for the first time two conformations of the mDia1 formin FH2 domains in interaction with the barbed ends of actin. These conformations agree with the speculated open and closed conformations of the “stair stepping” modelproposed by Otomo and colleagues(Otomo et al., 2005). We observed the FH2 dimers to be in the open conformation for 79% of the data, interacting with the two terminal actin subunits of the barbed end, while they interact with three actin subunits in the closed conformation. In addition, we identified single FH2 dimers encircling the core of actin filaments, providing structural information for mDia1 away from the barbed end, and showing that mDia1 formins are able to explore the core of actin filaments by spontaneously departing from barbed ends.

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Transmembrane formins as active cargoes of membrane trafficking

Cvrčková,

Ghosh,

Kočová

2024

Journal of Experimental Botany

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Formins are a large, evolutionarily old family of plant cytoskeletal regulators whose roles include actin capping and nucleation, as well as modulation of microtubule dynamics. The plant class I formin clade is characterized by a unique domain organization, as most of its members are transmembrane proteins with possible cell wall-binding motifs exposed to the extracytoplasmic space – a structure that appears to be a synapomorphy of the plant kingdom. While such transmembrane formins are traditionally considered mainly as plasmalemma-localized proteins contributing to the organization of the cell cortex, we review, from a cell biology perspective, the growing evidence that they can also, at least temporarily, reside (and in some cases also function) in endomembranes including secretory and endocytotic pathway compartments, the endoplasmic reticulum, the nuclear envelope and the tonoplast. Based on this evidence, we propose that class I formins may thus serve as “active cargoes” of membrane trafficking, i.e. membrane-embedded proteins that modulate the fate of endo- or exocytotic compartments while being transported by them.

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mDia1 Assembles a Linear F-Actin Coat at Membrane Invaginations To Drive Listeria monocytogenes Cell-to-Cell Spreading

Cited by 6 publications

References 84 publications

Localization of host endocytic and actin‐associated proteins during Shigella flexneri intracellular motility and intercellular spreading

Localization of host endocytic and actin‐associated proteins during Shigella flexneri intracellular motility and intercellular spreading

Direct observation of the conformational states of formin mDia1 at actin filament barbed ends and along the filament

Transmembrane formins as active cargoes of membrane trafficking

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