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. 2023 May;78(5):1292-1306.
doi: 10.1111/all.15640. Epub 2023 Jan 19.

Staphylococcus aureus causes aberrant epidermal lipid composition and skin barrier dysfunction

Jihyun Kim  1   2 , Byung Eui Kim  1   2 , Evgeny Berdyshev  3 , Irina Bronova  3 , Lianghua Bin  1 , Jaewoong Bae  4 , Seokjin Kim  4 , Hye-Young Kim  5 , Un Ha Lee  6 , Myoung Shin Kim  6 , Hyunmi Kim  2 , Jinyoung Lee  2 , Clifton F Hall  1 , Jessica Hui-Beckman  1 , Yunhee Chang  7 , Anna Sofia Bronoff  1 , Dasom Hwang  7 , Hae-Young Lee  7 , Elena Goleva  1 , Kangmo Ahn  2 , Donald Y M Leung  1
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Staphylococcus aureus causes aberrant epidermal lipid composition and skin barrier dysfunction

Jihyun Kim et al. Allergy. 2023 May.

Abstract

Background: Staphylococcus (S) aureus colonization is known to cause skin barrier disruption in atopic dermatitis (AD) patients. However, it has not been studied how S. aureus induces aberrant epidermal lipid composition and skin barrier dysfunction.

Methods: Skin tape strips (STS) and swabs were obtained from 24 children with AD (6.0 ± 4.4 years) and 16 healthy children (7.0 ± 4.5 years). Lipidomic analysis of STS samples was performed by mass spectrometry. Skin levels of methicillin-sensitive and methicillin-resistant S. aureus (MSSA and MRSA) were evaluated. The effects of MSSA and MRSA were evaluated in primary human keratinocytes (HEKs) and organotypic skin cultures.

Results: AD and organotypic skin colonized with MRSA significantly increased the proportion of lipid species with nonhydroxy fatty acid sphingosine ceramide with palmitic acid ([N-16:0 NS-CER], sphingomyelins [16:0-18:0 SM]), and lysophosphatidylcholines [16:0-18:0 LPC], but significantly reduced the proportion of corresponding very long-chain fatty acids (VLCFAs) species (C22-28) compared to the skin without S. aureus colonization. Significantly increased transepidermal water loss (TEWL) was found in MRSA-colonized AD skin. S. aureus indirectly through interleukin (IL)-1β, tumor necrosis factor (TNF)-α, IL-6, and IL-33 inhibited expression of fatty acid elongase enzymes (ELOVL3 and ELOVL4) in HEKs. ELOVL inhibition was more pronounced by MRSA and resulted in TEWL increase in organotypic skin.

Conclusion: Aberrant skin lipid profiles and barrier dysfunction are associated with S. aureus colonization in AD patients. These effects are attributed to the inhibition of ELOVLs by S. aureus-induced IL-1β, TNF-α, IL-6, and IL-33 seen in keratinocyte models and are more prominent in MRSA than MSSA.

Keywords: Staphylococcus aureus; atopic dermatitis; ceramides; elongase; skin barrier.

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References

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