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12 Bacterial Manipulation of the Host Cell Cytoskeleton

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12 Bacterial Manipulation of the Host Cell Cytoskeleton, Page 1 of 2

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Abstract:

This chapter illustrates several modes of bacterial manipulation of the host cell cytoskeleton using a few well-studied examples and explores interactions of various pathogenic bacteria with the actin cytoskeleton of both phagocytic and nonphagocytic host cells. These interactions are generally mediated by specific bacterial gene products, virulence factors, whose sole function is to mimic or interfere with normal host cell signals, in this case, those that regulate actin filament dynamics. A section focuses on the ability of to invade epithelial cells by a process that triggers global changes in the cellular actin cytoskeleton that result in membrane ruffles and macropinocytosis. Importantly, both zipper and trigger uptake mechanisms proceed using energy derived from the host cell. The cytoskeletal and membrane rearrangements that are responsible for bacterial invasion require no energetic input from the bacterium once the type III secretion apparatus is made (for the trigger mechanism of uptake); they invade by persuasion rather than by force. The chapter further focuses on four well-characterized cytoskeletal manipulators: YopE, YopH, YopT, and YpkA/YopO. Intracellular motility allows pathogens to spread directly from the cytoplasm of one cell into the cytoplasm of an adjacent cell. The many processes used by bacterial pathogens of cellular invasion, inhibition of internalization, cellular adhesion, and intercellular spread may appear diverse, but they are linked by common molecules: the components of the host cell cytoskeleton. In becoming better pathogens, these bacteria have come to a highly evolved appreciation of the subtlety required to regulate it.

Citation: Robbins J, Baldwin D, McCallum S, Theriot J. 2004. 12 Bacterial Manipulation of the Host Cell Cytoskeleton, p 275-297. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch12

Key Concept Ranking

Bacterial Proteins
0.6895651
Type III Secretion System
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Type IV Secretion Systems
0.41127893
0.6895651
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Figures

Image of Figure 12.1
Figure 12.1

Schematic diagram of host cell actin rearrangements caused by bacterial pathogens. Some pathogens induce their own uptake by nonphagocytic epithelial cells, initiating signal transduction cascades that result in polymerization of actin filaments under the host cell plasma membrane. For some pathogens, including and , tight adhesion of the bacterium to the cell surface followed by modest actin polymerization only in the immediate neighborhood of bacterial attachment, the “zipper” form of induced phagocytosis, allows the bacterium to be taken up by the cells. For others, such as and , the host cell throws up a large ruffling membrane that folds over and traps the bacteria in a membranebound compartment. This is called the “trigger” form of induced phagocytosis. Macrophages normally phagocytose foreign particles, including bacterial invaders, but species are able to prevent phagocytosis by injecting virulence factors into the host cell cytoplasm that disrupt actin cytoskeletal structures. In contrast, enteropathogenic colonize the surface of epithelial cells without being internalized, building a dense “pedestal” of actin filaments that raises them up from the cell surface. and are able to escape from their vacuoles and nucleate the polymerization of actin filaments at their surfaces while growing in host cell cytoplasm. This results in the formation of a dense tail structure that pushes the bacteria through the cytoplasm. At the interface between neighboring epithelial cells, the actin-rich tail pushes the bacteria out into a membrane-bound protrusion, which can be taken up by the second cell, allowing direct cytoplasm-to-cytoplasm transmission.

Citation: Robbins J, Baldwin D, McCallum S, Theriot J. 2004. 12 Bacterial Manipulation of the Host Cell Cytoskeleton, p 275-297. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch12
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Image of Figure 12.2
Figure 12.2

The “trigger” mechanism of bacterial invasion. Eight frames from a video sequence, recorded at 10-s intervals, show the large actin-rich ruffle formed when serovar Typhimurium encounters a Henle epithelial cell in culture. Folding in of the ruffle forms numerous spacious vacuoles, visible as white circles in the later frames. Scale bar is 10 μm.

Citation: Robbins J, Baldwin D, McCallum S, Theriot J. 2004. 12 Bacterial Manipulation of the Host Cell Cytoskeleton, p 275-297. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch12
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Image of Figure 12.3
Figure 12.3

Actin tail formation and movement of in cytoplasmic extract. Eight frames from a video sequence are shown, recorded at 10-s intervals with phase-contrast images on the top and direct actin fluorescence on the bottom.

Citation: Robbins J, Baldwin D, McCallum S, Theriot J. 2004. 12 Bacterial Manipulation of the Host Cell Cytoskeleton, p 275-297. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch12
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Image of Figure 12.4
Figure 12.4

Schematic diagram of the interactions between ActA protein and host cell cytoskeletal factors. The C terminus is anchored in the bacterial membrane. The N-terminal third of the protein mediates dimerization and also mediates nucleation of actin filaments by the Arp2/3 complex. The activated Arp2/3 complex binds to the sides of preexisting filaments to nucleate branches. Filaments nucleated close together can be efficiently cross-linked by α-actinin. A second host protein complex that includes VASP tetramers and profilin associates with the proline-rich repeats in the central region of ActA. This interaction serves to accelerate the rate of actin filament elongation.

Citation: Robbins J, Baldwin D, McCallum S, Theriot J. 2004. 12 Bacterial Manipulation of the Host Cell Cytoskeleton, p 275-297. In Cossart P, Boquet P, Normark S, Rappuoli R (ed), Cellular Microbiology, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555817633.ch12
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