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Chapter 23 : Regulation of Vesicle Formation

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Abstract:

This chapter addresses the regulation of outer membrane vesicles (OMVs) production in gram-negative bacteria; however, a brief section is dedicated to summarizing current knowledge of gram-positive membrane vesicles (MVs). To understand the molecular mechanisms of OMV formation, it is important to first review the structural differences between the cell envelopes of Gram-negative and Gram-positive bacteria. Despite intense interest and research in the field since the discovery of OMVs, the molecular mechanism of OMV formation has not been completely elucidated. Three main models for the mechanism of OMV formation have been proposed, which are not mutually exclusive. Processes regulated by quorum sensing (QS) include production of secondary metabolites and virulence factors, light production, biofilm formation, and OMV formation. The contribution of OMVs to biofilm structures is discussed in the chapter; however, specifically within the host, the propensity to form microcolonies and the role OMVs play during infection may reveal novel biofilm-related regulatory mechanisms of OMV formation within the host. Through the combined efforts of many investigators over the course of decades of research, much light has been shed on the highly conserved process of bacterial MV formation, though several questions remain unanswered. Regulatory schemes for OMV formation are actively being determined, and some of the future progress could be derived from collaboration with other research areas like QS and regulatory RNAs.

Citation: Wessel A, Palmer G, Whiteley M. 2013. Regulation of Vesicle Formation, p 441-464. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch23
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Figure 1

Two papers published in 1966 and 1967 give visible evidence of bacterial membrane blebbing. (A) An electron micrograph of lysine-limited cells, illustrating the OM blebbing away from the IM (at arrows). g, extracellular globule, presumably an OMV; m, intracytoplasmic membranous organelle. Reprinted from the ( ) with permission of the publisher. (B) Exponential-phase grown in peptone water, exhibiting multiple areas of membrane blebbing. Reprinted from the ( ) with permission of the publisher. doi:10.1128/9781555818524.ch23f1

Citation: Wessel A, Palmer G, Whiteley M. 2013. Regulation of Vesicle Formation, p 441-464. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch23
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Image of Figure 2
Figure 2

The three models of OMV formation. The cell envelope contains an OM with an outer leaflet of LPS. In models 1 and 2, LPS is hexa-acylated to illustrate a common structure, while in model 3, LPS is penta-acylated to illustrate a common structure. In model 1, the membrane can bleb in areas where the OM is not well anchored to the PG. In model 2, pressure on the OM caused by accumulation of proteins in the periplasmic space is relieved by membrane blebbing (figure adapted from ). In model 3, charge-charge repulsion of LPS and PQS insertion is shown. In , in areas containing large amounts of B band LPS, charge-charge interactions induce curvature of the membrane. Membrane curvature is additionally enhanced by PQS preferentially inserting into the outer leaflet of the OM. doi:10.1128/9781555818524.ch23f2

Citation: Wessel A, Palmer G, Whiteley M. 2013. Regulation of Vesicle Formation, p 441-464. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch23
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Image of Figure 3
Figure 3

vesicles released upon the beginning of septation (black arrows), as the PG and cytoplasmic membrane grow inward toward the center of the cell (white arrows). Scale bar, 100 nm. Reprinted from the ( ) with permission of the publisher. doi:10.1128/9781555818524.ch23f3

Citation: Wessel A, Palmer G, Whiteley M. 2013. Regulation of Vesicle Formation, p 441-464. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch23
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Figure 4

Thin-section TEM of producing nanopods, an organelle which secretes OMVs. (A) Cell-attached nanopods (white arrows) can be up to 6 μm in length. Scale bar, 200 nm. (B) The cell-nanopod junction. Scale bar, 100 nm. Reprinted from ( ) with permission of the publisher. doi:10.1128/9781555818524.ch23f4

Citation: Wessel A, Palmer G, Whiteley M. 2013. Regulation of Vesicle Formation, p 441-464. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch23
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Figure 5

Protein banding patterns of OM proteins (OM) and OMVs (Ves) from HB101 and ETEC strains, with varying growth conditions. OM and Ves (0.5 μg) were applied to 12.5% SDS-PAGE gels and silver stained. Banding patterns for Ves look similar to the OM protein banding; however, some proteins appear to be preferentially sorted into OMVs. Molecular mass standards are indicated on the left, in kilodaltons. Reprinted from ( ) with permission of the publisher. doi:10.1128/9781555818524.ch23f5

Citation: Wessel A, Palmer G, Whiteley M. 2013. Regulation of Vesicle Formation, p 441-464. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch23
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Figure 6

TEM of OMVs produced in biofilms. (A and B) (b) infects in the lumen of the intestine, producing what appears to be OMVs (omv), in the presence of extracellular material (em). Scale bar, 0.5 μm. Reprinted from ( ) with permission of the publisher. (C) TEM of a biofilm isolated from a domestic bathroom drain, indicating the presence of OMVs between cells (arrows), as well as blebbing off the cell surface (arrows). Scale bar, 1 μm. Reprinted from ( ) with permission of the publisher. doi:10.1128/9781555818524.ch23f6

Citation: Wessel A, Palmer G, Whiteley M. 2013. Regulation of Vesicle Formation, p 441-464. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch23
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Figure 7

Production of MVs is not limited to Gram-negative bacteria. (A) A thin-section TEM of the gram-positive bacterium . MV formation occurs at the cell surface (arrows), and a secreted MV is shown nearby (arrowhead). Scale bar, 100 nm. Reprinted from ( ) with permission of the publisher. (B) The Gram-positive bacterium (Ba) produces MVs within macrophages (MØ). A disrupted phagosome (P) double membrane is visible (two dashed arrows), and a vesicle is present in the macrophage cytoplasm (solid arrow). Scale bar, 500 nm. Reprinted from ( ) with permission of the publisher. doi:10.1128/9781555818524.ch23f7

Citation: Wessel A, Palmer G, Whiteley M. 2013. Regulation of Vesicle Formation, p 441-464. In Vasil M, Darwin A (ed), Regulation of Bacterial Virulence. ASM Press, Washington, DC. doi: 10.1128/9781555818524.ch23
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