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. 2024 Jan 12:14:1328055.
doi: 10.3389/fmicb.2023.1328055. eCollection 2023.

Slightly acidic electrolyzed water inhibits inflammation induced by membrane vesicles of Staphylococcus aureus

Yuko Shimamura  1 , Yukino Oura  1 , Madoka Tsuchiya  1 , Yuka Yamanashi  1 , Asako Ogasawara  1 , Minami Oishi  1 , Misaki Komuro  2 , Kuniaki Sasaki  2 , Shuichi Masuda  1
Affiliations

Slightly acidic electrolyzed water inhibits inflammation induced by membrane vesicles of Staphylococcus aureus

Yuko Shimamura et al. Front Microbiol. .

Abstract

Staphylococcus aureus grows in the skin of patients with atopic dermatitis and the associated symptoms are induced by membrane vesicles (MVs). This study explored the effects of slightly acidic electrolyzed water (SAEW) on the expression of virulence factors of S. aureus and MV-induced inflammation to uncover the potential of SAEW as a new treatment method for atopic dermatitis. Expression levels of genes related to virulence factors in S. aureus was assessed and S. aureus-derived MVs were characterized. Moreover, expression level of MV-induced Type I allergic reaction-related genes in RBL2H3 cells was also assessed. Significantly decreased staphylococcal enterotoxin A production and decreased virulence factor-related gene expression were observed after culturing S. aureus in broth supplemented with SAEW at ratios of 1, 2, and 5 per broth. MVs prepared by culturing S. aureus in SAEW-supplemented broth exhibited altered particle size and markedly reduced staphylococcal enterotoxin A content under all addition conditions; moreover, those obtained at a ratio of 1:5 (broth:SAEW) exhibited a reduction in the expression of several proteins associated with hemolytic activity and free iron uptake. The MVs prepared in SAEW-supplemented broth also exhibited remarkably reduced allergy-related gene expression levels in rat cell lines derived from basophilic leukemia-2H3 cells. Overall, SAEW is expected to suppress atopic dermatitis symptoms through the alteration of the properties of S. aureus-derived MVs.

Keywords: Staphylococcus aureus; atopic dermatitis; inflammation; membrane vesicles; slightly acidic electrolyzed water.

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Conflict of interest statement

The authors declare that this study received funding from Morinaga Milk Industry Co., Ltd. The funder was not involved in the study design, collection, analysis, interpretation of data, the writing of this article or the decision to submit it for publication.

Figures

FIGURE 1
FIGURE 1
Effect of SAEW on the growth of Staphylococcus aureus. S. aureus growth was measured by optical density at 660 nm. The control used was sterile water instead of SAEW. *Indicates p < 0.05 compared to the control (n = 3).
FIGURE 2
FIGURE 2
Effect of SAEW on virulence factor gene expression levels in S. aureus. (A) SEA gene (sea). (B) β-hemolysin gene (hlb). (C) RNAIII. (D) biofilm formation gene (icaA). S. aureus was added to the BHI broth:SAEW mixing ratios of 1:1 and 1:2 and incubated statically at 37°C for 6 h. The control used was sterile water instead of SAEW. The expression level of each gene in the control is shown as a relative value of 1. *Indicates p < 0.05 compared to the control (n = 3).
FIGURE 3
FIGURE 3
Effect of SAEW on the particle size of S. aureus-derived membrane vesicles (MVs). (A) TEM analysis of MVs. (B) Particle size distribution of MVs. The control (BHI broth:SAEW = 1:0) used was sterile water instead of SAEW.
FIGURE 4
FIGURE 4
Effect of SAEW on staphylococcal enterotoxin A (SEA) content of culture supernatants and MVs of S. aureus. (A) SEA content of S. aureus-derived MVs analyzed by SDS-PAGE and visualized by western blotting analysis. (B) Measurement of SEA in S. aureus-derived MVs. (C) SEA production in the culture supernatant of S. aureus analyzed by SDS-PAGE and visualized by western blotting. (D) Measurement of SEA production in the culture supernatant of S. aureus. The control used was sterile water instead of SAEW. M: Pre-stained protein marker, and PC: positive control (SEA protein). Adjustments to the contrast and brightness were made using Adobe Photoshop to enable better visibility without altering the relationship between the SAEW images and the control images. The SEA in the control is shown as a relative value of 1. *Indicates p < 0.05 compared to the control (n = 3).
FIGURE 5
FIGURE 5
Effect of SAEW on cargo proteins of S. aureus-derived MVs. (A) Cargo protein concentration in S. aureus-derived MVs. (B) Cargo proteins in MVs obtained from supernatants after different SAEW mixing ratios. The control (BHI broth:SAEW = 1:0) used was sterile water instead of SAEW. Arrows (white): decreasing, arrows (filled): increasing. Bands indicated by arrows were subjected to nano-LC–MS/MS analysis. (C) Measurement of cargo proteins decreased or increased in S. aureus-derived MVs. Proteins 1 and 2 correspond to the bands in Figure 5B with the BHI broth:SAEW mixing ratio of 1:5. *p < 0.05 compared to the control (n = 3).
FIGURE 6
FIGURE 6
Effect of SAEW on S. aureus-derived MV-induced type I allergic reaction. S. aureus-derived MVs were exposed to IgE-sensitized RBL-2H3 cells. (A) Type I allergy-related gene expression induced by S. aureus-derived MVs. MVs obtained by culturing S. aureus in broth without SAEW. The control used was phosphate-buffered saline instead of MVs. (B) Effect of SAEW on S. aureus-derived MV-induced type I allergic reactions. MVs: MVs obtained by culturing S. aureus in broth without SAEW, MVs + SAEW: MVs obtained by culturing S. aureus in broth with SAEW. *Indicates p < 0.05 compared to the control (n = 3).
FIGURE 7
FIGURE 7
Effects of SAEW on the virulence factors of S. aureus and MVs. (A) S. aureus cultured with SAEW reduced SEA production and decreased the expression of virulence factor-related genes. (B) MVs from SAEW-supplemented broth displayed altered particle sizes, and markedly reduced contents of SEA and cargo proteins. Allergy-related gene expression in RBL-2H3 cells was substantially reduced in MVs obtained from the SAEW-treated broth.
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