Roles of membrane vesicles from Streptococcus mutans for the induction of antibodies to glucosyltransferase in mucosal immunity

Nakamura, T.; Iwabuchi, Yusuke; Hirayama, Satoru; Narisawa, Naoki; Takenaga, Fumio; Nakao, Ryoma; Senpuku, Hidenobu

doi:10.1016/j.micpath.2020.104260

Cited by 10 publications

(14 citation statements)

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“…Several studies have now described the utility of EMVs produced by B. anthracis (Rivera et al, 2010), Neisseria meningitidis (Schwechheimer and Kuehn, 2015), S. aureus (Wang et al, 2018), S. pneumoniae (Brown et al, 2015), and S. mutans (Senpuku et al, 2019) as potential delivery vehicles for vaccine antigens. Intranasal immunization of Balb/c mice with S. mutans EMVs in concert with the TLR3 agonist poly(I-C) was an effective method to raise anti-GtfC IgA and IgG antibodies (Nakamura et al, 2020). Thus, comprehensive information regarding the content and characteristics of S. mutans EMVs will be useful in future studies to evaluate their role in induction of protective immunity, and to facilitate studies regarding their specific contributions to mono and mixed species biofilms development.…”

Section: Discussionmentioning

confidence: 99%

The Impacts of Sortase A and the 4′-Phosphopantetheinyl Transferase Homolog Sfp on Streptococcus mutans Extracellular Membrane Vesicle Biogenesis

et al. 2020

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Extracellular membrane vesicles (EMVs) are produced by many Gram-positive organisms, but information regarding vesiculogenesis is incomplete. We used single gene deletions to evaluate the impacts on Streptococcus mutans EMV biogenesis of Sortase A (SrtA), which affects S. mutans EMV composition, and Sfp, a 4phosphopantetheinyl transferase that affects Bacillus subtilis EMV stability. srtA EMVs were notably larger than sfp and wild-type (WT) EMVs. EMV proteins identified from all three strains are known to be involved in cell wall biogenesis and cell architecture, bacterial adhesion, biofilm cell density and matrix development, and microbial competition. Notably, the AtlA autolysin was not processed to its mature active form in the srtA mutant. Proteomic and lipidomic analyses of all three strains revealed multiple dissimilarities between vesicular and corresponding cytoplasmic membranes (CMs). A higher proportion of EMV proteins are predicted substrates of the general secretion pathway (GSP). Accordingly, the GSP component SecA was identified as a prominent EMV-associated protein. In contrast, CMs contained more multi-pass transmembrane (TM) protein substrates of co-translational transport machineries than EMVs. EMVs from the WT, but not the mutant strains, were enriched in cardiolipin compared to CMs, and all EMVs were over-represented in polyketide flavonoids. EMVs and CMs were rich in long-chain saturated, monounsaturated, and polyunsaturated fatty acids, except for sfp EMVs that contained exclusively polyunsaturated fatty acids. Lipoproteins were less prevalent in EMVs of all three strains compared to their CMs. This study provides insight into biophysical characteristics of S. mutans EMVs and indicates discrete partitioning of protein and lipid components between EMVs and corresponding CMs of WT, srtA, and sfp strains.

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Section: Discussionmentioning

confidence: 99%

The Impacts of Sortase A and the 4′-Phosphopantetheinyl Transferase Homolog Sfp on Streptococcus mutans Extracellular Membrane Vesicle Biogenesis

et al. 2020

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“…Subsequently, proteins were transferred onto Immobilon PVDF membranes (Millipore, Bedford, MA, USA) and blocked with 2.5% skim milk in Tris-buffered saline with Tween 20 (TBST: 50 mM Tris, 2.7 mM KCl, 0.138 M NaCl, 0.05% Tween 20, pH 7.6) for 1 h at room temperature. The membranes were probed with mousederived anti-MV antisera [19] diluted 1:15,000 in 1.25% skim milk/TBST for 1 h at room temperature. Horseradish peroxidase (HRP)-labeled anti-goat secondary antibody (Merck kGaA) was used to detect the antibodies.…”

Section: Sds-page and Western Blottingmentioning

confidence: 99%

“…A relationship has also been found between biofilm formation and the MVs from pathogens such as the Francisella species, Pseudomonas aeruginosa, Vibrio cholerae, and Helicobacter pylori [16][17][18]. The MVs from S. mutans contain Gtfs, bacterial cell surface protein antigen (PAc), and a glucan-binding protein, which are components of S. mutans associated with the development of dental caries [10,11,19]. Among Gtfs, GtfC is mainly bound to MVs, and the MVs are used for the adhesion and biofilm formation of other early adherent bacteria and core bacteria in oral biofilms on the tooth surface, such as Streptococcus mitis, Streptococcus oralis, Actinomyces naeslundii, and Fusobacterium nucleatum [11,19].…”

Section: Introductionmentioning

confidence: 99%

“…The MVs from S. mutans contain Gtfs, bacterial cell surface protein antigen (PAc), and a glucan-binding protein, which are components of S. mutans associated with the development of dental caries [10,11,19]. Among Gtfs, GtfC is mainly bound to MVs, and the MVs are used for the adhesion and biofilm formation of other early adherent bacteria and core bacteria in oral biofilms on the tooth surface, such as Streptococcus mitis, Streptococcus oralis, Actinomyces naeslundii, and Fusobacterium nucleatum [11,19]. The MVs of S. mutans bind to the acquired pellicle on the tooth surface by the ability of PAc, and as a result, GtfC may be guided to the tooth surface; subsequently, GtfC synthesizes water-soluble glucan and waterinsoluble glucan on the tooth surface in a sugar-containing environment [19][20][21][22].…”

Section: Introductionmentioning

confidence: 99%

“…Among Gtfs, GtfC is mainly bound to MVs, and the MVs are used for the adhesion and biofilm formation of other early adherent bacteria and core bacteria in oral biofilms on the tooth surface, such as Streptococcus mitis, Streptococcus oralis, Actinomyces naeslundii, and Fusobacterium nucleatum [11,19]. The MVs of S. mutans bind to the acquired pellicle on the tooth surface by the ability of PAc, and as a result, GtfC may be guided to the tooth surface; subsequently, GtfC synthesizes water-soluble glucan and waterinsoluble glucan on the tooth surface in a sugar-containing environment [19][20][21][22]. It has been suggested that MVs utilize water-soluble glucans and water-insoluble glucans to support the binding of early adherent bacteria to the tooth surface [11].…”

Section: Introductionmentioning

confidence: 99%

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Effects of pH on the Properties of Membrane Vesicles Including Glucosyltransferase in Streptococcus mutans

et al. 2021

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Streptococcus mutans releases membrane vesicles (MVs) and induces MV-dependent biofilm formation. Glucosyltransferases (Gtfs) are bound to MVs and contribute to the adhesion and glucans-dependent biofilm formation of early adherent bacteria on the tooth surface. The biofilm formation of S. mutans may be controlled depending on whether the initial pH tends to be acidic or alkaline. In this study, the characteristics and effects of MVs extracted from various conditions {(initial pH 6.0 and 8.0 media prepared with lactic acid (LA) and acetic acid (AA), and with NaOH (NO), respectively)} on the biofilm formation of S. mutans and early adherent bacteria were investigated. The quantitative changes in glucans between primary pH 6.0 and 8.0 conditions were observed, associated with different activities affecting MV-dependent biofilm formation. The decreased amount of Gtfs on MVs under the initial pH 6.0 conditions strongly guided low levels of MV-dependent biofilm formation. However, in the initial pH 6.0 and 8.0 solutions prepared with AA and NO, the MVs in the biofilm appeared to be formed by the expression of glucans and/or extracellular DNA. These results suggest that the environmental pH conditions established by acid and alkaline factors determine the differences in the local pathogenic activities of biofilm development in the oral cavity.

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Inhibitory effect of the combination of xylitol and funoran on Streptococcus mutans biofilm formation on the uncoated surface

et al. 2022

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Roles of membrane vesicles from Streptococcus mutans for the induction of antibodies to glucosyltransferase in mucosal immunity

Cited by 10 publications

References 59 publications

The Impacts of Sortase A and the 4′-Phosphopantetheinyl Transferase Homolog Sfp on Streptococcus mutans Extracellular Membrane Vesicle Biogenesis

The Impacts of Sortase A and the 4′-Phosphopantetheinyl Transferase Homolog Sfp on Streptococcus mutans Extracellular Membrane Vesicle Biogenesis

Effects of pH on the Properties of Membrane Vesicles Including Glucosyltransferase in Streptococcus mutans

Inhibitory effect of the combination of xylitol and funoran on Streptococcus mutans biofilm formation on the uncoated surface

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