Staphylococcus epidermidis protease EcpA can be a deleterious component of the skin microbiome in atopic dermatitis
Staphylococcus aureus and Staphylococcus epidermidis are the most abundant bacteria found on the skin of patients with atopic dermatitis (AD). S aureus is known to exacerbate AD, whereas S epidermidis has been considered a beneficial commensal organism. In this study, we hypothesized that S epidermi...
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| Published in | Journal of allergy and clinical immunology Vol. 147; no. 3; pp. 955 - 966.e16 |
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| Main Authors | , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
01.03.2021
Elsevier Limited |
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| Abstract | Staphylococcus aureus and Staphylococcus epidermidis are the most abundant bacteria found on the skin of patients with atopic dermatitis (AD). S aureus is known to exacerbate AD, whereas S epidermidis has been considered a beneficial commensal organism.
In this study, we hypothesized that S epidermidis could promote skin damage in AD by the production of a protease that damages the epidermal barrier.
The protease activity of S epidermidis isolates was compared with that of other staphylococcal species. The capacity of S epidermidis to degrade the barrier and induce inflammation was examined by using human keratinocyte tissue culture and mouse models. Skin swabs from atopic and healthy adult subjects were analyzed for the presence of S epidermidis genomic DNA and mRNA.
S epidermidis strains were observed to produce strong cysteine protease activity when grown at high density. The enzyme responsible for this activity was identified as EcpA, a cysteine protease under quorum sensing control. EcpA was shown to degrade desmoglein-1 and LL-37 in vitro, disrupt the physical barrier, and induce skin inflammation in mice. The abundance of S epidermidis and expression of ecpA mRNA were increased on the skin of some patients with AD, and this correlated with disease severity. Another commensal skin bacterial species, Staphylococcus hominis, can inhibit EcpA production by S epidermidis.
S epidermidis has commonly been regarded as a beneficial skin microbe, whereas S aureus has been considered deleterious. This study suggests that the overabundance of S epidermidis found on some atopic patients can act similarly to S aureus and damage the skin by expression of a cysteine protease.
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| AbstractList | Staphylococcus aureus and Staphylococcus epidermidis are the most abundant bacteria found on the skin of patients with atopic dermatitis (AD). S aureus is known to exacerbate AD, whereas S epidermidis has been considered a beneficial commensal organism.
In this study, we hypothesized that S epidermidis could promote skin damage in AD by the production of a protease that damages the epidermal barrier.
The protease activity of S epidermidis isolates was compared with that of other staphylococcal species. The capacity of S epidermidis to degrade the barrier and induce inflammation was examined by using human keratinocyte tissue culture and mouse models. Skin swabs from atopic and healthy adult subjects were analyzed for the presence of S epidermidis genomic DNA and mRNA.
S epidermidis strains were observed to produce strong cysteine protease activity when grown at high density. The enzyme responsible for this activity was identified as EcpA, a cysteine protease under quorum sensing control. EcpA was shown to degrade desmoglein-1 and LL-37 in vitro, disrupt the physical barrier, and induce skin inflammation in mice. The abundance of S epidermidis and expression of ecpA mRNA were increased on the skin of some patients with AD, and this correlated with disease severity. Another commensal skin bacterial species, Staphylococcus hominis, can inhibit EcpA production by S epidermidis.
S epidermidis has commonly been regarded as a beneficial skin microbe, whereas S aureus has been considered deleterious. This study suggests that the overabundance of S epidermidis found on some atopic patients can act similarly to S aureus and damage the skin by expression of a cysteine protease.
[Display omitted] BackgroundStaphylococcus aureus and Staphylococcus epidermidis are the most abundant bacteria found on the skin of patients with atopic dermatitis (AD). S aureus is known to exacerbate AD, whereas S epidermidis has been considered a beneficial commensal organism.ObjectiveIn this study, we hypothesized that S epidermidis could promote skin damage in AD by the production of a protease that damages the epidermal barrier.MethodsThe protease activity of S epidermidis isolates was compared with that of other staphylococcal species. The capacity of S epidermidis to degrade the barrier and induce inflammation was examined by using human keratinocyte tissue culture and mouse models. Skin swabs from atopic and healthy adult subjects were analyzed for the presence of S epidermidis genomic DNA and mRNA.ResultsS epidermidis strains were observed to produce strong cysteine protease activity when grown at high density. The enzyme responsible for this activity was identified as EcpA, a cysteine protease under quorum sensing control. EcpA was shown to degrade desmoglein-1 and LL-37 in vitro, disrupt the physical barrier, and induce skin inflammation in mice. The abundance of S epidermidis and expression of ecpA mRNA were increased on the skin of some patients with AD, and this correlated with disease severity. Another commensal skin bacterial species, Staphylococcus hominis, can inhibit EcpA production by S epidermidis.ConclusionS epidermidis has commonly been regarded as a beneficial skin microbe, whereas S aureus has been considered deleterious. This study suggests that the overabundance of S epidermidis found on some atopic patients can act similarly to S aureus and damage the skin by expression of a cysteine protease. Staphylococcus aureus and Staphylococcus epidermidis are the most abundant bacteria found on the skin of patients with atopic dermatitis (AD). S aureus is known to exacerbate AD, whereas S epidermidis has been considered a beneficial commensal organism. In this study, we hypothesized that S epidermidis could promote skin damage in AD by the production of a protease that damages the epidermal barrier. The protease activity of S epidermidis isolates was compared with that of other staphylococcal species. The capacity of S epidermidis to degrade the barrier and induce inflammation was examined by using human keratinocyte tissue culture and mouse models. Skin swabs from atopic and healthy adult subjects were analyzed for the presence of S epidermidis genomic DNA and mRNA. S epidermidis strains were observed to produce strong cysteine protease activity when grown at high density. The enzyme responsible for this activity was identified as EcpA, a cysteine protease under quorum sensing control. EcpA was shown to degrade desmoglein-1 and LL-37 in vitro, disrupt the physical barrier, and induce skin inflammation in mice. The abundance of S epidermidis and expression of ecpA mRNA were increased on the skin of some patients with AD, and this correlated with disease severity. Another commensal skin bacterial species, Staphylococcus hominis, can inhibit EcpA production by S epidermidis. S epidermidis has commonly been regarded as a beneficial skin microbe, whereas S aureus has been considered deleterious. This study suggests that the overabundance of S epidermidis found on some atopic patients can act similarly to S aureus and damage the skin by expression of a cysteine protease. Staphylococcus aureus and Staphylococcus epidermidis are the most abundant bacteria found on the skin of patients with atopic dermatitis (AD). S aureus is known to exacerbate AD, whereas S epidermidis has been considered a beneficial commensal organism.BACKGROUNDStaphylococcus aureus and Staphylococcus epidermidis are the most abundant bacteria found on the skin of patients with atopic dermatitis (AD). S aureus is known to exacerbate AD, whereas S epidermidis has been considered a beneficial commensal organism.In this study, we hypothesized that S epidermidis could promote skin damage in AD by the production of a protease that damages the epidermal barrier.OBJECTIVEIn this study, we hypothesized that S epidermidis could promote skin damage in AD by the production of a protease that damages the epidermal barrier.The protease activity of S epidermidis isolates was compared with that of other staphylococcal species. The capacity of S epidermidis to degrade the barrier and induce inflammation was examined by using human keratinocyte tissue culture and mouse models. Skin swabs from atopic and healthy adult subjects were analyzed for the presence of S epidermidis genomic DNA and mRNA.METHODSThe protease activity of S epidermidis isolates was compared with that of other staphylococcal species. The capacity of S epidermidis to degrade the barrier and induce inflammation was examined by using human keratinocyte tissue culture and mouse models. Skin swabs from atopic and healthy adult subjects were analyzed for the presence of S epidermidis genomic DNA and mRNA.S epidermidis strains were observed to produce strong cysteine protease activity when grown at high density. The enzyme responsible for this activity was identified as EcpA, a cysteine protease under quorum sensing control. EcpA was shown to degrade desmoglein-1 and LL-37 in vitro, disrupt the physical barrier, and induce skin inflammation in mice. The abundance of S epidermidis and expression of ecpA mRNA were increased on the skin of some patients with AD, and this correlated with disease severity. Another commensal skin bacterial species, Staphylococcus hominis, can inhibit EcpA production by S epidermidis.RESULTSS epidermidis strains were observed to produce strong cysteine protease activity when grown at high density. The enzyme responsible for this activity was identified as EcpA, a cysteine protease under quorum sensing control. EcpA was shown to degrade desmoglein-1 and LL-37 in vitro, disrupt the physical barrier, and induce skin inflammation in mice. The abundance of S epidermidis and expression of ecpA mRNA were increased on the skin of some patients with AD, and this correlated with disease severity. Another commensal skin bacterial species, Staphylococcus hominis, can inhibit EcpA production by S epidermidis.S epidermidis has commonly been regarded as a beneficial skin microbe, whereas S aureus has been considered deleterious. This study suggests that the overabundance of S epidermidis found on some atopic patients can act similarly to S aureus and damage the skin by expression of a cysteine protease.CONCLUSIONS epidermidis has commonly been regarded as a beneficial skin microbe, whereas S aureus has been considered deleterious. This study suggests that the overabundance of S epidermidis found on some atopic patients can act similarly to S aureus and damage the skin by expression of a cysteine protease. |
| Author | Shafiq, Faiza Hata, Tissa R. Gallo, Richard L. Nakatsuji, Teruaki Kavanaugh, Jeffrey S. Horswill, Alexander R. Cheng, Joyce Y. Williams, Michael R. Higbee, Kyle Cau, Laura Butcher, Anna M. |
| AuthorAffiliation | c Department of Immunology and Microbiology, University of Colorado Anschutz, Medical Campus, Aurora b R&D Department, SILAB, Brive d Department of Veterans Affairs Eastern Colorado Health Care System, Aurora a Department of Dermatology, University of California San Diego e Center for Microbiome Innovation, University of California San Diego |
| AuthorAffiliation_xml | – name: e Center for Microbiome Innovation, University of California San Diego – name: b R&D Department, SILAB, Brive – name: c Department of Immunology and Microbiology, University of Colorado Anschutz, Medical Campus, Aurora – name: d Department of Veterans Affairs Eastern Colorado Health Care System, Aurora – name: a Department of Dermatology, University of California San Diego |
| Author_xml | – sequence: 1 givenname: Laura surname: Cau fullname: Cau, Laura organization: Department of Dermatology, University of California San Diego, San Diego, Calif – sequence: 2 givenname: Michael R. surname: Williams fullname: Williams, Michael R. organization: Department of Dermatology, University of California San Diego, San Diego, Calif – sequence: 3 givenname: Anna M. surname: Butcher fullname: Butcher, Anna M. organization: Department of Dermatology, University of California San Diego, San Diego, Calif – sequence: 4 givenname: Teruaki surname: Nakatsuji fullname: Nakatsuji, Teruaki organization: Department of Dermatology, University of California San Diego, San Diego, Calif – sequence: 5 givenname: Jeffrey S. surname: Kavanaugh fullname: Kavanaugh, Jeffrey S. organization: Department of Immunology and Microbiology, University of Colorado Anschutz, Medical Campus, Aurora, Colo – sequence: 6 givenname: Joyce Y. surname: Cheng fullname: Cheng, Joyce Y. organization: Department of Dermatology, University of California San Diego, San Diego, Calif – sequence: 7 givenname: Faiza surname: Shafiq fullname: Shafiq, Faiza organization: Department of Dermatology, University of California San Diego, San Diego, Calif – sequence: 8 givenname: Kyle surname: Higbee fullname: Higbee, Kyle organization: Department of Dermatology, University of California San Diego, San Diego, Calif – sequence: 9 givenname: Tissa R. surname: Hata fullname: Hata, Tissa R. organization: Department of Dermatology, University of California San Diego, San Diego, Calif – sequence: 10 givenname: Alexander R. surname: Horswill fullname: Horswill, Alexander R. organization: Department of Immunology and Microbiology, University of Colorado Anschutz, Medical Campus, Aurora, Colo – sequence: 11 givenname: Richard L. surname: Gallo fullname: Gallo, Richard L. email: rgallo@ucsd.edu organization: Department of Dermatology, University of California San Diego, San Diego, Calif |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32634452$$D View this record in MEDLINE/PubMed |
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| Keywords | cytokine TEWL TSB AD AMP skin AIP PSM microbiome agr EcpA HEK protease CoNS Staphylococcus epidermidis CFU Atopic dermatitis inflammation DSG-1 qPCR epidermal barrier WT IVL dysbiosis |
| Language | English |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 These authors contributed equally to this work. San Diego, Calif, Brive, France, and Aurora, Colo |
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| PublicationDate | 2021-03-01 |
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| PublicationTitle | Journal of allergy and clinical immunology |
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| Snippet | Staphylococcus aureus and Staphylococcus epidermidis are the most abundant bacteria found on the skin of patients with atopic dermatitis (AD). S aureus is... BackgroundStaphylococcus aureus and Staphylococcus epidermidis are the most abundant bacteria found on the skin of patients with atopic dermatitis (AD). S... |
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| SubjectTerms | Animal models Animals Antibiotics Antimicrobial Cationic Peptides - metabolism Atopic dermatitis Bacteria Bacterial Proteins - metabolism Cathelicidins Cells, Cultured Cysteine Cysteine Proteases - metabolism Cysteine proteinase cytokine Dermatitis Dermatitis, Atopic - microbiology Dermatitis, Atopic - pathology Desmoglein 1 - metabolism DNA, Bacterial - genetics dysbiosis Eczema Enzymes epidermal barrier Experiments Gene expression Human subjects Humans Inflammation Keratinocytes - microbiology Keratinocytes - pathology Mice Mice, Inbred C57BL microbiome Microbiomes Microbiota mRNA Pathogens protease Quorum sensing Severity of Illness Index Skin Skin - microbiology Skin - pathology Skin diseases Staphylococcal Skin Infections - microbiology Staphylococcal Skin Infections - pathology Staphylococcus epidermidis Staphylococcus epidermidis - enzymology Statistical analysis Tissue culture |
| Title | Staphylococcus epidermidis protease EcpA can be a deleterious component of the skin microbiome in atopic dermatitis |
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