Release of Gram‐Negative Outer‐Membrane Proteins into Human Serum and Septic Rat Blood and Their Interactions with Immunoglobulin in Antiserum to<i>Escherichia coli</i>J5

Hellman, Judith; Loiselle, Paul M.; Zanzot, E M; Allaire, Jennifer E.; Tehan, Megan M.; Boyle, Lenora A.; Kurnick, James T.; Warren, H. Shaw

doi:10.1086/315302

Cited by 51 publications

(43 citation statements)

References 60 publications

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“…In a series of studies of E. coli infection, LPS and OM protein-containing bacterial fragments were isolated from the serum of septic rats (52)(53)(54). E. coli cells grown in culture with serum were found to shed OM material with the same composition as the material shed in vivo (55).…”

Section: Vesiculation Observed During Infectionmentioning

confidence: 99%

Virulence and Immunomodulatory Roles of Bacterial Outer Membrane Vesicles

Ellis

Kuehn

2010

Microbiol Mol Biol Rev

807

736

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SUMMARY Outer membrane (OM) vesicles are ubiquitously produced by Gram-negative bacteria during all stages of bacterial growth. OM vesicles are naturally secreted by both pathogenic and nonpathogenic bacteria. Strong experimental evidence exists to categorize OM vesicle production as a type of Gram-negative bacterial virulence factor. A growing body of data demonstrates an association of active virulence factors and toxins with vesicles, suggesting that they play a role in pathogenesis. One of the most popular and best-studied pathogenic functions for membrane vesicles is to serve as natural vehicles for the intercellular transport of virulence factors and other materials directly into host cells. The production of OM vesicles has been identified as an independent bacterial stress response pathway that is activated when bacteria encounter environmental stress, such as what might be experienced during the colonization of host tissues. Their detection in infected human tissues reinforces this theory. Various other virulence factors are also associated with OM vesicles, including adhesins and degradative enzymes. As a result, OM vesicles are heavily laden with pathogen-associated molecular patterns (PAMPs), virulence factors, and other OM components that can impact the course of infection by having toxigenic effects or by the activation of the innate immune response. However, infected hosts can also benefit from OM vesicle production by stimulating their ability to mount an effective defense. Vesicles display antigens and can elicit potent inflammatory and immune responses. In sum, OM vesicles are likely to play a significant role in the virulence of Gram-negative bacterial pathogens.

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Section: Vesiculation Observed During Infectionmentioning

confidence: 99%

Virulence and Immunomodulatory Roles of Bacterial Outer Membrane Vesicles

Ellis

Kuehn

2010

Microbiol Mol Biol Rev

807

736

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“…During infections caused by Neisseria meningitidis, in which the disease pathology is characterized by life-threatening sepsis, the production of endotoxic (LPS-containing) MVs in the bloodstream has been observed, and it likely contributes to pathogenesis of sepsis through Toll-like receptor (TLR)-and nucleotide-binding oligomerization domain-containing protein (NOD)-like receptor (NLR)-mediated inflammatory cytokine production (62,88). Complementary to direct microscopic observation of MV release, complexes containing OM proteins and LPS have been isolated from blood during experimental sepsis (28), suggesting that this material may be vesicular in nature and could persist in vivo separately from parent bacteria. In addition, systemic effects of heart disease may be promoted by MVs from the oral pathogen Porphyromonas gingivalis, as MVs have been shown to aggregate platelets in vitro (80).…”

Section: Functional Significance Of Membrane Vesiclesmentioning

confidence: 99%

Membrane Vesicle Release in Bacteria, Eukaryotes, and Archaea: a Conserved yet Underappreciated Aspect of Microbial Life

2012

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ABSTRACTInteraction of microbes with their environment depends on features of the dynamic microbial surface throughout cell growth and division. Surface modifications, whether used to acquire nutrients, defend against other microbes, or resist the pressures of a host immune system, facilitate adaptation to unique surroundings. The release of bioactive membrane vesicles (MVs) from the cell surface is conserved across microbial life, in bacteria, archaea, fungi, and parasites. MV production occurs not onlyin vitrobut alsoin vivoduring infection, underscoring the influence of these surface organelles in microbial physiology and pathogenesis through delivery of enzymes, toxins, communication signals, and antigens recognized by the innate and adaptive immune systems. Derived from a variety of organisms that span kingdoms of life and called by several names (membrane vesicles, outer membrane vesicles [OMVs], exosomes, shedding microvesicles, etc.), the conserved functions and mechanistic strategies of MV release are similar, including the use of ESCRT proteins and ESCRT protein homologues to facilitate these processes in archaea and eukaryotic microbes. Although forms of MV release by different organisms share similar visual, mechanistic, and functional features, there has been little comparison across microbial life. This underappreciated conservation of vesicle release, and the resulting functional impact throughout the tree of life, explored in this review, stresses the importance of vesicle-mediated processes throughout biology.

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“…uter membrane vesicles (OMVs) are ubiquitously produced by all Gram-negative bacteria studied to date (1)(2)(3)(4)(5)(6)(7)(8). They are defined as outer membrane (OM) buds entrapping periplasmic content in the lumen (9).…”

mentioning

confidence: 99%

Synthetic Effect between Envelope Stress and Lack of Outer Membrane Vesicle Production in Escherichia coli

Schwechheimer

Kuehn

2013

Journal of Bacteriology

109

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Outer membrane vesicles (OMVs) are composed of outer membrane and periplasmic components and are ubiquitously secreted by Gram-negative bacteria. OMVs can disseminate virulence factors for pathogenic bacteria as well as serve as an envelope stress response. From a transposon mutant screen for OMV phenotypes, it was discovered that an nlpA mutant of Escherichia coli produces fewer OMVs than the wild type, whereas a degP mutant produces higher levels of OMVs. NlpA is an inner-membrane-anchored lipoprotein that has a minor role in methionine import. DegP is a periplasmic chaperone/protease for misfolded envelope proteins that is critical when cells are heat shocked. To reveal how these proteins contribute to OMV production, the mutations were combined and the double mutant analyzed. The ⌬nlpA ⌬degP strain displayed a high-temperature growth defect that corresponded to the production of fewer OMVs than produced by the ⌬degP strain. This phenotype also pertained to other undervesiculation mutations in a ⌬degP background. The hypovesiculation phenotype of ⌬nlpA in the wild-type strain as well as in the degP deletion strain was found to be a stationary-phase phenomenon. The periplasm of the ⌬nlpA ⌬degP strain was determined to contain significantly more protein in stationary phase than the wild type. Additionally, misfolded DegP substrate outer membrane porins were detected in ⌬degP mutant-derived OMVs. These data suggest that an accumulation of envelope proteins resulting from decreased vesiculation was toxic and contributed to the growth defect. We conclude that OMV production contributes to relieve the envelope of accumulated toxic proteins and that NlpA plays an important role in the production of vesicles in stationary phase.

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Release of Gram‐Negative Outer‐Membrane Proteins into Human Serum and Septic Rat Blood and Their Interactions with Immunoglobulin in Antiserum toEscherichia coliJ5

Cited by 51 publications

References 60 publications

Virulence and Immunomodulatory Roles of Bacterial Outer Membrane Vesicles

Virulence and Immunomodulatory Roles of Bacterial Outer Membrane Vesicles

Membrane Vesicle Release in Bacteria, Eukaryotes, and Archaea: a Conserved yet Underappreciated Aspect of Microbial Life

Synthetic Effect between Envelope Stress and Lack of Outer Membrane Vesicle Production in Escherichia coli

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