Biological Effect of Streptococcus pyogenes-Released Extracellular Vesicles on Human Monocytic Cells, Induction of Cytotoxicity, and Inflammatory Response

Murase, Kazunori; Aikawa, Chihiro; Nozawa, Takashi; Nakatake, Ayako; Sakamoto, Kuniyo; Kikuchi, Taisei; Nakagawa, Ichirô

doi:10.3389/fcimb.2021.711144

Cited by 11 publications

(9 citation statements)

References 56 publications

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“…The study of gram-positive bacteria-derived vesicles is rapidly expanding and suggests a newfound pathogenicity of oral bacterial infection. Recently, various reports disclosed that MVs from gram-positive bacteria enclosed many virulence-related proteins such as streptolysin O and NAD-glycohydrolase in Streptococcus pyogenesis [45] and lipoproteins in Staphylococcus aureus [46] and Streptococcus pneumoniae [47]. MVs play roles in intercellular communication involving biofilm formation, nutrition acquisition and quorum sensing [9,[47][48][49].…”

Section: Discussionmentioning

confidence: 99%

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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Section: Discussionmentioning

confidence: 99%

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

et al. 2021

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“…EMV production has been reported in S . pyogenes [ 22 – 25 ]. It is negatively regulated by the CovRS, a two-component system that controls the expression of 15% of S .…”

Section: Discussionmentioning

confidence: 99%

A Streptococcus pyogenes DegV protein regulates the membrane lipid content and limits the formation of extracellular vesicles

et al. 2023

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Membranes contain lipids that are composed of fatty acids (FA) and a polar head. Membrane homeostasis is crucial for optimal bacterial growth and interaction with the environment. Bacteria synthesize their FAs via the FASII pathway. Gram-positive bacteria can incorporate exogenous FAs which need to be phosphorylated to become substrate of the lipid biosynthetic pathway. In many species including staphylococci, streptococci and enterococci, this phosphorylation is carried out by the Fak complex, which is composed of two subunits, FakA and FakB. FakA is the kinase. FakB proteins are members of the DegV family, proteins known to bind FAs. Two or three FakB types have been identified depending on the bacterial species and characterized by their affinity for saturated and/or unsaturated FAs. Some species such as Streptococcus pyogenes, which causes a wide variety of diseases ranging from mild non-invasive to severe invasive infections, possess an uncharacterized additional DegV protein. We identify here this DegV member as a fourth FakB protein, named FakB4. The fakB4 gene is co-regulated with FASII genes suggesting an interaction with endogenous fatty acids. fakB4 deletion has no impact on membrane phospholipid composition nor on the percentage of other major lipids. However, the fakB4 mutant strain produced more lipids and more extracellular membrane vesicles than the wild-type strain. This suggests that FakB4 is involved in endogenous FA binding and controls FA storage or catabolism resulting in a limitation of extracellular FA release via membrane vesicles.

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“…Interestingly, we found that the averaged diameter of 103 + -EVs (130 nm) is slightly bigger than 103 − -EVs (105 nm) ( Figure 1 ). The size of EVs in Gram-positive bacterial varies between different bacterial strains [ 34 , 35 , 36 , 37 ], throughout various stages of bacterial growth [ 38 ], and environmental conditions [ 27 , 39 , 40 ]. As the reports that the size distribution of EVs of the invasive Streptococcus pyogenes strains SSI-1 were 1.31 times bigger than the non-invasive Streptococcus pyogenes strains JRS4 [ 37 ].…”

Section: Discussionmentioning

confidence: 99%

“…The size of EVs in Gram-positive bacterial varies between different bacterial strains [ 34 , 35 , 36 , 37 ], throughout various stages of bacterial growth [ 38 ], and environmental conditions [ 27 , 39 , 40 ]. As the reports that the size distribution of EVs of the invasive Streptococcus pyogenes strains SSI-1 were 1.31 times bigger than the non-invasive Streptococcus pyogenes strains JRS4 [ 37 ]. The bigger size of EVs means it can carry more active molecules including virulence factor.…”

Section: Discussionmentioning

confidence: 99%

Rhodococcus equi-Derived Extracellular Vesicles Promoting Inflammatory Response in Macrophage through TLR2-NF-κB/MAPK Pathways

Hao

et al. 2022

IJMS

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Rhodococcus equi (R. equi) is a Gram-positive coccobacillus that causes pneumonia in foals of less than 3 months, which have the ability of replication in macrophages. The ability of R. equi persist in macrophages is dependent on the virulence plasmid pVAPA. Gram-positive extracellular vesicles (EVs) carry a variety of virulence factors and play an important role in pathogenic infection. There are few studies on R. equi-derived EVs (R. equi-EVs), and little knowledge regarding the mechanisms of how R. equi-EVs communicate with the host cell. In this study, we examine the properties of EVs produced by the virulence strain R. equi 103+ (103+-EVs) and avirulenct strain R. equi 103− (103−-EVs). We observed that 103+-EVs and 103−-EVs are similar to other Gram-positive extracellular vesicles, which range from 40 to 260 nm in diameter. The 103+-EVs or 103−-EVs could be taken up by mouse macrophage J774A.1 and cause macrophage cytotoxicity. Incubation of 103+-EVs or 103−-EVs with J774A.1 cells would result in increased expression levels of IL-1β, IL-6, and TNF-α. Moreover, the expression of TLR2, p-NF-κB, p-p38, and p-ERK were significantly increased in J774A.1 cells stimulated with R. equi-EVs. In addition, we presented that the level of inflammatory factors and expression of TLR2, p-NF-κB, p-p38, and p-ERK in J774A.1 cells showed a significant decreased when incubation with proteinase K pretreated-R. equi-EVs. Overall, our data indicate that R. equi-derived EVs are capable of mediating inflammatory responses in macrophages via TLR2-NF-κB/MAPK pathways, and R. equi-EVs proteins were responsible for TLR2-NF-κB/MAPK mediated inflammatory responses in macrophage. Our study is the first to reveal potential roles for R. equi-EVs in immune response in R. equi-host interactions and to compare the differences in macrophage inflammatory responses mediated by EVs derived from virulent strain R. equi and avirulent strain R. equi. The results of this study have improved our knowledge of the pathogenicity of R. equi.

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Biological Effect of Streptococcus pyogenes-Released Extracellular Vesicles on Human Monocytic Cells, Induction of Cytotoxicity, and Inflammatory Response

Cited by 11 publications

References 56 publications

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

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

A Streptococcus pyogenes DegV protein regulates the membrane lipid content and limits the formation of extracellular vesicles

Rhodococcus equi-Derived Extracellular Vesicles Promoting Inflammatory Response in Macrophage through TLR2-NF-κB/MAPK Pathways

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