The cell wall component lipoteichoic acid of &lt;i&gt;Staphylococcus aureus&lt;/i&gt; induces chemokine gene expression in bovine mammary epithelial cells

Kiku, Yoshio; Nagasawa, Yoji; Tanabe, Fuyuko; Sugawara, Kazue; Watanabe, Atsushi; Hata, Enjô; Ozawa, Tomomi; Nakajima, Kazuyuki; Arai, Toshiro; Hayashi, Tomohito

doi:10.1292/jvms.15-0706

Cited by 20 publications

(23 citation statements)

References 28 publications

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“…PGN and LTA are the major cell wall lysis components [29]. They can stimulate the bovine mammary gland to produce proinflammatory factors and then induce mastitis and reduce lactation [7,[30][31][32]. However, their proinflammatory activity is weaker than that of LPS [2][3][4], a cell wall lysis component of gram-negative bacteria like E. coli.…”

Section: Discussionmentioning

confidence: 99%

“…The weak and persistent proinflammatory activity of LTA and PGN mainly causes subclinical and chronic mastitis [2][3][4] which is difficult to detect and cure. Previous studies have reported the effects of LTA and LTA + PGN on gene expression profiling of bovine mammary epithelial cells, and mainly focused on the proinflammatory activity of PGN and LTA [5][6][7]. However, the epigenetic modification mechanisms of the inflammation induced by PGN and LTA remain poorly understood, and the direct effects of PGN and LTA, alone or combined, on lactation of bovine mammary epithelial cells and the inherent epigenetic mechanisms receive little attention.…”

Section: Introductionmentioning

confidence: 99%

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PGN and LTA from Staphylococcus aureus Induced Inflammation and Decreased Lactation through Regulating DNA Methylation and Histone H3 Acetylation in Bovine Mammary Epithelial Cells

Sun

Dong

et al. 2020

Toxins

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Staphylococcus aureus (S. aureus) and Escherichia coli (E. coli) are the most common pathogens of mastitis, and S. aureus generally causes subclinical mastitis which is more persistent and resistant to treatment. Peptidoglycan (PGN) and lipoteichoic acid (LTA) are cell wall components of S. aureus. Although the roles of PGN and LTA in causing inflammation are well studied, the epigenetic mechanisms of the effects of PGN and LTA on the inflammation and lactation remain poorly understood. This study characterized the gene expression profiling by RNA sequencing and investigated DNA methylation and histone acetylation in relation to inflammation and lactation in the immortalized bovine mammary epithelial cell line (MAC-T). The cells were cultured for 24 h with neither PGN nor LTA (CON), PGN (30 µg/mL), LTA (30 µg/mL), and PGN (30 µg/mL) + LTA (30 µg/mL), respectively. The number of differentially expressed genes (DEGs) and the expression of proinflammatory factors including interleukin (IL)-1β, IL-6, IL-8, chemokine (C-X-C motif) ligand (CXCL)1, and CXCL6 of the treatments increased in the following order: CON < PGN < LTA < PGN + LTA, and the DEGs mainly enriched on the cytokine-cytokine receptor interaction and chemokine signaling pathway. LTA and PGN + LTA induced hypomethylation of global DNA by suppressing DNA methyltransferase (DNMT) activity. PGN and LTA, alone or combined, decreased the mRNA expression of casein genes (CSN1S1, CSN2, and CSN3) and the expression of two caseins (CSN2 and CSN3), and reduced histone H3 acetylation by suppressing histone acetyltransferase (HAT) activity and promoting histone deacetylase (HDAC) activity. Collectively, this study revealed that PGN and LTA induced inflammation probably due to decreasing DNA methylation through regulating DNMT activity, and decreased lactation possibly through reducing histone H3 acetylation by regulating HAT and HDAC activity in bovine mammary epithelial cells. Key Contribution:In the present study, we demonstrated for the first time that PGN and LTA promoted the expression of proinflammatory factors probably due to inducing DNA hypomethylation by suppressing DNMT activity, whereas PGN and LTA decreased the gene expression of caseins perhaps through reducing histone H3 acetylation by suppressing HAT or/and promoting HDAC activity.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

PGN and LTA from Staphylococcus aureus Induced Inflammation and Decreased Lactation through Regulating DNA Methylation and Histone H3 Acetylation in Bovine Mammary Epithelial Cells

Sun

Dong

et al. 2020

Toxins

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“…Prototheca zopfii GT-II induced more IL-8 mRNA in bMECs compared to GT-I-inoculated or uninfected cells. Increased levels of IL-8 mRNA in murine MECs and bovine MECs induced by P. zopfii GT-II demonstrated that mammary epithelial cells are an important source of IL-8 and that this chemokine is key during protothecal mastitis, perhaps by recruiting leukocytes, as demonstrated by its chemoattractant role in Staphylococcus aureus infection in bMECs 35,36 . Depolarization of mitochondrial transmembrane (ΔΨm) causes the release of cytochrome-c, which may initiate caspase cascade.…”

Section: Discussionmentioning

confidence: 99%

Prototheca zopfii genotype II induces mitochondrial apoptosis in models of bovine mastitis

Shahid

Cobo

Chen

et al. 2020

Sci Rep

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Prototheca zopfii is an alga increasingly isolated from bovine mastitis. of the two genotypes of P. zopfii (genotype i and ii (Gt-i and-ii)), P. zopfii Gt-ii is the genotype associated with acute mastitis and decreased milk production, although its pathogenesis is not well known. the objective was to determine inflammatory and apoptotic roles of P. zopfii Gt-ii in cultured mammary epithelial cells (from cattle and mice) and murine macrophages and using a murine model of mastitis. Prototheca zopfii Gt-ii (but not Gt-i) invaded bovine and murine mammary epithelial cells (Mecs) and induced apoptosis, as determined by the terminal deoxynucleotidyl transferase mediated deoxyuridine triphosphate nick end labeling assay. this P. zopfii Gt-ii driven apoptosis corresponded to mitochondrial pathways; mitochondrial transmembrane resistance (ΔΨm) was altered and modulation of mitochondrionmediated apoptosis regulating genes changed (increased transcriptional Bax, cytochrome-c and Apaf-1 and downregulated Bcl-2), whereas caspase-9 and-3 expression increased. Apoptotic effects by P. zopfii Gt-ii were more pronounced in macrophages compared to Mecs. in a murine mammary infection model, P. zopfii GT-II replicated in the mammary gland and caused severe inflammation with infiltration of macrophages and neutrophils and upregulation of pro-inflammatory genes (TNF-α, IL-1β and Cxcl-1) and also apoptosis of epithelial cells. thus, we concluded P. zopfii Gt-ii is a mastitis-causing pathogen that triggers severe inflammation and also mitochondrial apoptosis.

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“…S. aureus (BM1006 [ 16 ], SA003 [ 17 ] and JE2 [ 18 ]), S. epidermidis (ATCC14990) [ 19 ], Bacillus atrophaeus (ATCC9372) [ 20 ], and E. coli (JM109) [ 21 ] were used in the present study. BM1006 was isolated from the bulk milk of dairy cattle, and SA003 originated from the milk of dairy cattle suffering from mastitis.…”

Section: Methodsmentioning

confidence: 99%

Identification of a novel mechanism of action of bovine IgG antibodies specific for Staphylococcus aureus

Furukawa

Yoneyama

Hata

et al. 2018

Vet Res

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Staphylococcus aureus is a major pathogen that causes subclinical mastitis associated with huge economic losses to the dairy industry. A few vaccines for bovine mastitis are available, and they are expected to induce the production of S. aureus-specific antibodies that prevent bacterial adherence to host cells or promote opsonization by phagocytes. However, the efficacy of such vaccines are still under debate; therefore, further research focusing on improving the current vaccines by seeking additional mechanisms of action is required to reduce economic losses due to mastitis in the dairy industry. Here, we generated S. aureus-specific bovine IgG antibodies (anti-S. aureus) that directly inhibited bacterial growth in vitro. Inhibition depended on specificity for anti-S. aureus, not the interaction between Protein A and the fragment crystallizable region of the IgG antibodies or bacterial agglutination. An in vitro culture study using S. aureus strain JE2 and its deletion mutant JE2ΔSrtA, which lacks the gene encoding sortase A, revealed that the effect of anti-S. aureus was sortase-A-independent. Sortase A is involved in the synthesis of cell-wall-associated proteins. Thus, other surface molecules, such as membrane proteins, cell surface polysaccharides, or both, may trigger the inhibition of bacterial growth by anti-S. aureus. Together, our findings contribute insights into developing new strategies to further improve the available mastitis vaccine by designing a novel antigen on the surface of S. aureus to induce inhibitory signals that prevent bacterial growth.Electronic supplementary materialThe online version of this article (10.1186/s13567-018-0517-y) contains supplementary material, which is available to authorized users.

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The cell wall component lipoteichoic acid of <i>Staphylococcus aureus</i> induces chemokine gene expression in bovine mammary epithelial cells

Cited by 20 publications

References 28 publications

PGN and LTA from Staphylococcus aureus Induced Inflammation and Decreased Lactation through Regulating DNA Methylation and Histone H3 Acetylation in Bovine Mammary Epithelial Cells

PGN and LTA from Staphylococcus aureus Induced Inflammation and Decreased Lactation through Regulating DNA Methylation and Histone H3 Acetylation in Bovine Mammary Epithelial Cells

Prototheca zopfii genotype II induces mitochondrial apoptosis in models of bovine mastitis

Identification of a novel mechanism of action of bovine IgG antibodies specific for Staphylococcus aureus

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