Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response

By Amanda J. McBroom, M. Kuehn. Molecular Microbiology, 2006

713 citations recorded by the source corpus.

Conditions that impair protein folding in the Gram‐negative bacterial envelope cause stress. The destabilizing effects of stress in this compartment are recognized and countered by a number of signal transduction mechanisms. Data presented here reveal another facet of the complex bacterial stress response, release of outer membrane vesicles. Native vesicles are composed of outer membrane and periplasmic material, and they are released from the bacterial surface without loss of membrane integrity. Here we demonstrate that the quantity of vesicle release correlates directly with the level of protein accumulation in the cell envelope. Accumulation of material occurs under stress, and is exacerbated upon impairment of the normal housekeeping and stress‐responsive mechanisms of the cell. Mutations that cause increased vesiculation enhance bacterial survival upon challenge with stressing agents or accumulation of toxic misfolded proteins. Preferential packaging of a misfolded protein mimic into vesicles for removal indicates that the vesiculation process can act to selectively eliminate unwanted material. Our results demonstrate that production of bacterial outer membrane vesicles is a fully independent, general envelope stress response. In addition to identifying a novel mechanism for alleviating stress, this work provides physiological relevance for vesicle production as a protective mechanism.

Subfields: Infectious Diseases, Microbiology, Public Health, Environmental and Occupational Health

View Paper: https://www.semanticscholar.org/paper/764610dcf936cc1d9afeeae730b869de1f8f3242

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Citations in the corpus

Biological properties of extracellular vesicles and their physiological functions (2015, background): “Misfolded proteins may be sequestered in OMVs and exported out of the cell (661).”
Bacterial outer membrane vesicles mediate cytosolic localization of LPS and caspase-11 activation (2016, positive): “…in genes that encode proteins involved in OMV production such as pepP, ypjA, bolA, and dsbA result in hypovesiculating E. coli strains that minimally produce OMVs without a major growth defect (Kulp and Kuehn, 2010; McBroom and Kuehn, 2007; McBroom et al., 2006; Schwechheimer and Kuehn, 2013).”
Biological Functions and Biogenesis of Secreted Bacterial Outer Membrane Vesicles (2010, background): “coli were better able to survive conditions of envelope stress, using both external (ethanol and polymyxin treatment) and internal (overexpression of a toxic periplasmic protein) stressors (57).”
Outer Membrane Vesicles of a Human Commensal Mediate Immune Regulation and Disease Protection (2012, background): “As attempts to delete OMVs from bacteria have thus far been unsuccessful, as they may be necessary for viability (Deatherage et al., 2009; McBroom and Kuehn, 2007), the in vivo relevance of B.”
Contribution of bacterial outer membrane vesicles to innate bacterial defense (2011, methodology): “coli strain ADA600 carrying a plasmid for kanamycin resistance (MK496) was used in this study (WT) [9], along with a hyper-vesiculating isogenic strain ADA600 ΔyieM (MK1248, made by P1 phage transduction from the Keio collection knockout strain [50]) which does not carry the plasmid but encodes kana”
Effect of NaCl on in vitro plant regeneration from embryogenic callus cultures of 'cv IR 64' indica rice ( Oryza sativa L.) (2011, background): “In Escherichia coli, mutations that caused increased vesiculation enhance bacterial survival upon challenge with stress agents or accumulation of toxic misfolded proteins (McBroom and Kuehn, 2007).”
Membrane Vesicle Release in Bacteria, Eukaryotes, and Archaea: a Conserved yet Underappreciated Aspect of Microbial Life (2012, background): “Accumulation of over184 expressed periplasmic proteins promotes increased MV release, possibly via 185 induction of outward budding of the membrane (59).”
Virulence and Immunomodulatory Roles of Bacterial Outer Membrane Vesicles (2010, background): “The production of vesicles was further demonstrated to be linked to the bacterial stress response (97).”