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Quorum sensing between bacterial species on the skin protects against epidermal injury in atopic dermatitis.

ABSTRACT: Colonization of the skin by Staphylococcus aureus is associated with exacerbation of atopic dermatitis (AD), but any direct mechanism through which dysbiosis of the skin microbiome may influence the development of AD is unknown. Here, we show that proteases and phenol-soluble modulin ? (PSM?) secreted by S. aureus lead to endogenous epidermal proteolysis and skin barrier damage that promoted inflammation in mice. We further show that clinical isolates of different coagulase-negative staphylococci (CoNS) species residing on normal skin produced autoinducing peptides that inhibited the S. aureus agr system, in turn decreasing PSM? expression. These autoinducing peptides from skin microbiome CoNS species potently suppressed PSM? expression in S. aureus isolates from subjects with AD without inhibiting S. aureus growth. Metagenomic analysis of the AD skin microbiome revealed that the increase in the relative abundance of S. aureus in patients with active AD correlated with a lower CoNS autoinducing peptides to S. aureus ratio, thus overcoming the peptides' capacity to inhibit the S. aureus agr system. Characterization of a S. hominis clinical isolate identified an autoinducing peptide (SYNVCGGYF) as a highly potent inhibitor of S. aureus agr activity, capable of preventing S. aureus-mediated epithelial damage and inflammation on murine skin. Together, these findings show how members of the normal human skin microbiome can contribute to epithelial barrier homeostasis by using quorum sensing to inhibit S. aureus toxin production.

SUBMITTER: Williams MR

PROVIDER: S-EPMC7106486 | biostudies-literature | 2019 May

REPOSITORIES: biostudies-literature

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Quorum sensing between bacterial species on the skin protects against epidermal injury in atopic dermatitis.

Williams Michael R MR Costa Stephen K SK Zaramela Livia S LS Khalil Shadi S Todd Daniel A DA Winter Heather L HL Sanford James A JA O'Neill Alan M AM Liggins Marc C MC Nakatsuji Teruaki T Cech Nadja B NB Cheung Ambrose L AL Zengler Karsten K Horswill Alexander R AR Gallo Richard L RL

Science translational medicine 20190501 490

Colonization of the skin by <i>Staphylococcus aureus</i> is associated with exacerbation of atopic dermatitis (AD), but any direct mechanism through which dysbiosis of the skin microbiome may influence the development of AD is unknown. Here, we show that proteases and phenol-soluble modulin α (PSMα) secreted by <i>S. aureus</i> lead to endogenous epidermal proteolysis and skin barrier damage that promoted inflammation in mice. We further show that clinical isolates of different coagulase-negativ ...[more]

PMID: 31043573

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Project description:IntroductionAtopic dermatitis is a common skin disease characterized by altered cutaneous immunity in which patients often exhibit lower skin microbiota diversity compared to healthy skin and are prone to colonization by Staphylococcus aureus. Apple cider vinegar has been shown to have antibacterial effects; however, its effects on the skin microbiome have not previously been well-described.ObjectivesWe aimed to examine the effects of topical dilute apple cider vinegar soaks on Staphylococcus aureus abundance, skin bacterial microbiome composition, and skin bacterial microbiome diversity in atopic dermatitis participants compared to healthy skin.MethodsEleven subjects with atopic dermatitis and 11 healthy controls were enrolled in this randomized, non-blinded, single-institution, split-arm pilot study. Subjects soaked one forearm in dilute apple cider vinegar (0.5% acetic acid) and the other forearm in tap water for 10 minutes daily. Skin bacteria samples were collected from subjects' volar forearms before and after 14 days of treatment. 16S sequencing was used to analyze Staphylococcus aureus abundance and skin bacterial microbiome composition, and alpha diversity of microbiota were determined using Shannon diversity index.ResultsThere was no difference in skin bacterial microbiome in atopic dermatitis subjects after 2 weeks of daily water or apple cider vinegar treatments (p = 0.056 and p = 0.22, respectively), or in mean abundance of S. aureus on apple cider vinegar-treated forearms (p = 0.60). At 2 weeks, the skin bacterial microbiomes of healthy control subjects were not significantly different from the skin bacterial microbiome of atopic dermatitis subjects (p = 0.14, 0.21, 0.12, and 0.05).ConclusionsOur results suggest that daily soaks in 0.5% apple cider vinegar are not an effective method of altering the skin bacterial microbiome in atopic dermatitis. Further studies are needed to explore the effects of different concentrations of apple cider vinegar on skin microflora and disease severity.Trial numberUVA IRB-HSR #19906.

Project description:BACKGROUND:Atopic dermatitis (AD) is associated with itch, skin inflammation and barrier disruption, and scratching, all of which may be associated with skin pain. OBJECTIVE:To characterize the patient burden of skin pain in AD. METHODS:We performed a prospective dermatology practice-based study using questionnaires and evaluation by a dermatologist. RESULTS:Overall, 305 patients (age range, 13-97 years) were included in the study, with 564 encounters. The cohort included 195 females (63.9%) and 193 whites (63.7%). The mean (SD) age at enrollment was 42.3 (18.1) years, and the mean (SD) age of patient-reported AD onset was 29.6 (31.9) years. At baseline, 144 patients (42.7%) reported skin pain in the past week, with 42 (13.8%) reporting severe or very severe pain. Twenty-four (16.8%) thought the skin pain was part of their itch, 16 (11.2%) from scratching, and 77 (72.0%) from both. Patients with skin pain were more likely to describe their itch using terms that resembled neuropathic pain. Prevalence of skin pain was increased in patients with vs without excoriations (72.6% vs 57.6%; ?2 test P?=?.02) but not other morphologic characteristics. Skin pain severity was most strongly correlated with the Patient-Oriented Eczema Measure (Spearman ??=?0.54), followed by ItchyQOL (??=?0.52), 5-dimensions of itch scale (??=?0.47), Dermatology Life Quality Index (??=?0.45), numeric rating scale for itch (??=?0.43) and sleep (??=?0.36), Patient Health Questionnaire 9 (??=?0.36), patient-reported global AD severity (??=?0.34), Eczema Area and Severity Index (??=?0.23), and objective Scoring AD index (??=?0.20) (P?<?.001 for all). Patients with both severe itch and pain vs those with only one or neither symptom being severe had significant increases in all these measures. CONCLUSION:Skin pain is a common and burdensome symptom in AD. Skin pain severity should be assessed with itch severity in AD patients and may be an important end point for monitoring treatment response.

Dataset Information

Quorum sensing between bacterial species on the skin protects against epidermal injury in atopic dermatitis.

Publications

Quorum sensing between bacterial species on the skin protects against epidermal injury in atopic dermatitis.

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