Signaling sphingolipids are biomarkers for atopic dermatitis prone to disseminated viral infections
Life-threatening viral diseases such as eczema herpeticum (EH) and eczema vaccinatum (EV) occur in <5% of individuals with atopic dermatitis (AD). The diagnosis of AD, however, excludes all individuals with AD from smallpox vaccination. We sought to identify circulatory and skin lipid biomarkers...
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| Published in | Journal of allergy and clinical immunology Vol. 150; no. 3; pp. 640 - 648 |
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| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
01.09.2022
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Life-threatening viral diseases such as eczema herpeticum (EH) and eczema vaccinatum (EV) occur in <5% of individuals with atopic dermatitis (AD). The diagnosis of AD, however, excludes all individuals with AD from smallpox vaccination.
We sought to identify circulatory and skin lipid biomarkers associated with EH and EV.
Stratum corneum and plasma samples from 15 subjects with AD and a history of EH, 13 age- and gender-matched subjects with AD and without EH history, and 13 healthy nonatopic (NA) controls were analyzed by liquid chromatography tandem mass spectrometry for sphingolipid content. Sphingosine-1-phosphate (S1P) and ceramide levels were validated in plasma samples from the Atopic Dermatitis Vaccinia Network/Atopic Dermatitis Research Network repository (12 NA, 12 AD, 23 EH) and plasma from 7 subjects with EV and 7 matched subjects with AD. S1P lyase was downregulated in human primary keratinocytes to evaluate its effect on herpes simplex virus 1 (HSV-1) replication in vitro.
The stratum corneum of patients with EH demonstrated significantly higher levels of free sphingoid bases than those in patients who were NA, indicating enhanced sphingolipid turnover in keratinocytes (P < .05). Plasma from 2 independent cohorts of patients with EH had a significantly increased S1P/ceramide ratio in subjects with EH versus those with AD and or who were NA (P < .01). The S1P level in plasma from subjects with EV was twice the level in plasma from subjects with AD (mean = 1,533 vs 732 pmol/mL; P < .001). Downregulation of S1P lyase expression with silencing RNA led to an increased S1P level and doubled HSV-1 titer in keratinocytes.
Our data point to long-term abnormalities in the S1P signaling system as a biomarker for previous disseminated viral diseases and a potential treatment target in recurring infections. |
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| AbstractList | Life-threatening viral diseases such as eczema herpeticum (EH) and eczema vaccinatum (EV) occur in <5% of individuals with atopic dermatitis (AD). The diagnosis of AD, however, excludes all individuals with AD from smallpox vaccination.
We sought to identify circulatory and skin lipid biomarkers associated with EH and EV.
Stratum corneum and plasma samples from 15 subjects with AD and a history of EH, 13 age- and gender-matched subjects with AD and without EH history, and 13 healthy nonatopic (NA) controls were analyzed by liquid chromatography tandem mass spectrometry for sphingolipid content. Sphingosine-1-phosphate (S1P) and ceramide levels were validated in plasma samples from the Atopic Dermatitis Vaccinia Network/Atopic Dermatitis Research Network repository (12 NA, 12 AD, 23 EH) and plasma from 7 subjects with EV and 7 matched subjects with AD. S1P lyase was downregulated in human primary keratinocytes to evaluate its effect on herpes simplex virus 1 (HSV-1) replication in vitro.
The stratum corneum of patients with EH demonstrated significantly higher levels of free sphingoid bases than those in patients who were NA, indicating enhanced sphingolipid turnover in keratinocytes (P < .05). Plasma from 2 independent cohorts of patients with EH had a significantly increased S1P/ceramide ratio in subjects with EH versus those with AD and or who were NA (P < .01). The S1P level in plasma from subjects with EV was twice the level in plasma from subjects with AD (mean = 1,533 vs 732 pmol/mL; P < .001). Downregulation of S1P lyase expression with silencing RNA led to an increased S1P level and doubled HSV-1 titer in keratinocytes.
Our data point to long-term abnormalities in the S1P signaling system as a biomarker for previous disseminated viral diseases and a potential treatment target in recurring infections. Life-threatening viral diseases such as eczema herpeticum (EH) and eczema vaccinatum (EV) occur in <5% of individuals with atopic dermatitis (AD). The diagnosis of AD, however, excludes all individuals with AD from smallpox vaccination.BACKGROUNDLife-threatening viral diseases such as eczema herpeticum (EH) and eczema vaccinatum (EV) occur in <5% of individuals with atopic dermatitis (AD). The diagnosis of AD, however, excludes all individuals with AD from smallpox vaccination.We sought to identify circulatory and skin lipid biomarkers associated with EH and EV.OBJECTIVESWe sought to identify circulatory and skin lipid biomarkers associated with EH and EV.Stratum corneum and plasma samples from 15 subjects with AD and a history of EH, 13 age- and gender-matched subjects with AD and without EH history, and 13 healthy nonatopic (NA) controls were analyzed by liquid chromatography tandem mass spectrometry for sphingolipid content. Sphingosine-1-phosphate (S1P) and ceramide levels were validated in plasma samples from the Atopic Dermatitis Vaccinia Network/Atopic Dermatitis Research Network repository (12 NA, 12 AD, 23 EH) and plasma from 7 subjects with EV and 7 matched subjects with AD. S1P lyase was downregulated in human primary keratinocytes to evaluate its effect on herpes simplex virus 1 (HSV-1) replication in vitro.METHODSStratum corneum and plasma samples from 15 subjects with AD and a history of EH, 13 age- and gender-matched subjects with AD and without EH history, and 13 healthy nonatopic (NA) controls were analyzed by liquid chromatography tandem mass spectrometry for sphingolipid content. Sphingosine-1-phosphate (S1P) and ceramide levels were validated in plasma samples from the Atopic Dermatitis Vaccinia Network/Atopic Dermatitis Research Network repository (12 NA, 12 AD, 23 EH) and plasma from 7 subjects with EV and 7 matched subjects with AD. S1P lyase was downregulated in human primary keratinocytes to evaluate its effect on herpes simplex virus 1 (HSV-1) replication in vitro.The stratum corneum of patients with EH demonstrated significantly higher levels of free sphingoid bases than those in patients who were NA, indicating enhanced sphingolipid turnover in keratinocytes (P < .05). Plasma from 2 independent cohorts of patients with EH had a significantly increased S1P/ceramide ratio in subjects with EH versus those with AD and or who were NA (P < .01). The S1P level in plasma from subjects with EV was twice the level in plasma from subjects with AD (mean = 1,533 vs 732 pmol/mL; P < .001). Downregulation of S1P lyase expression with silencing RNA led to an increased S1P level and doubled HSV-1 titer in keratinocytes.RESULTSThe stratum corneum of patients with EH demonstrated significantly higher levels of free sphingoid bases than those in patients who were NA, indicating enhanced sphingolipid turnover in keratinocytes (P < .05). Plasma from 2 independent cohorts of patients with EH had a significantly increased S1P/ceramide ratio in subjects with EH versus those with AD and or who were NA (P < .01). The S1P level in plasma from subjects with EV was twice the level in plasma from subjects with AD (mean = 1,533 vs 732 pmol/mL; P < .001). Downregulation of S1P lyase expression with silencing RNA led to an increased S1P level and doubled HSV-1 titer in keratinocytes.Our data point to long-term abnormalities in the S1P signaling system as a biomarker for previous disseminated viral diseases and a potential treatment target in recurring infections.CONCLUSIONSOur data point to long-term abnormalities in the S1P signaling system as a biomarker for previous disseminated viral diseases and a potential treatment target in recurring infections. In patients with a history of eczema vaccinatum and eczema herpeticum, sphingolipid homeostasis is substantially perturbed in favor of S1P-mediated signaling and persists for many years after the last disease episode. |
| Author | David, Gloria Vang, Kathryn A. Leung, Donald Y.M. Goleva, Elena Streib, Joanne E. Richers, Brittany N. Villarreal, Miguel Hanifin, Jon Bronoff, Anna Sofia Beck, Lisa Taylor, Patricia Johnson, Keli Berdyshev, Evgeny Bronova, Irina Slifka, Mark K. |
| AuthorAffiliation | 3 Rho Federal Systems Division, Inc., Durham, NC, USA 2 University of Rochester Medical Center, Rochester, NY, USA 1 National Jewish Health, Denver, CO, USA 4 Oregon Health & Science University, Portland, OR, USA |
| AuthorAffiliation_xml | – name: 2 University of Rochester Medical Center, Rochester, NY, USA – name: 1 National Jewish Health, Denver, CO, USA – name: 3 Rho Federal Systems Division, Inc., Durham, NC, USA – name: 4 Oregon Health & Science University, Portland, OR, USA |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/35304160$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1007_s12016_022_08953_x crossref_primary_10_1016_j_jaci_2022_09_031 crossref_primary_10_1016_j_jaci_2023_02_013 crossref_primary_10_1177_07487304231220695 crossref_primary_10_1016_j_jaci_2024_01_014 crossref_primary_10_1016_j_anai_2024_02_004 crossref_primary_10_1016_j_xjidi_2024_100279 crossref_primary_10_1111_bph_17393 crossref_primary_10_1016_j_antiviral_2024_105942 crossref_primary_10_3390_cells12192352 |
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| Copyright | 2022 American Academy of Allergy, Asthma & Immunology Copyright © 2022 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved. |
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| Keywords | ADRN AD EH ADVN NS SPHK NJH eczema herpeticum S1P/ceramide ratio human primary keratinocytes stratum corneum CER EV ceramide HSV-1 SGPL1 NA S1P FTY720 S1P lyase sphingosine-1-phosphate plasma Eczema vaccinatum |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 E.B. developed mass spectrometric approaches for the analysis of tape strip samples for lipid components, performed sample processing and data analysis, supervised the entire workflow of sample mass spectrometric processing, reviewed data, and wrote the manuscript. I.B. performed sample processing and data analysis. A.S.B. performed skin tape strip sample processing and data analysis. E.G. coordinated the sample processing and interaction between research sites, performed experiments with keratinocytes, reviewed the data, and coauthored the manuscript. D.Y.M.L. conceptually designed and coauthored the protocol, reviewed data, and coauthored the manuscript. K.A.V. assisted with real time PCR assays and analysis. B.N.R. performed skin tape strip sample processing. J.E.S. oversaw interaction between study sites and provided logistical support. P.T. was involved in patient enrollment, clinical visits assessments and skin biopsy and STS sampling at NJH. L.B. oversaw ADRN plasma samples registry. M.K.S. and J.H. were involved in the enrollment and characterization of EV and AD patients at OHSU. Author contributions |
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| Snippet | Life-threatening viral diseases such as eczema herpeticum (EH) and eczema vaccinatum (EV) occur in <5% of individuals with atopic dermatitis (AD). The... In patients with a history of eczema vaccinatum and eczema herpeticum, sphingolipid homeostasis is substantially perturbed in favor of S1P-mediated signaling... |
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| SubjectTerms | Biomarkers ceramide Ceramides Dermatitis, Atopic - diagnosis Dermatitis, Atopic - genetics eczema herpeticum Eczema vaccinatum Herpesvirus 1, Human human primary keratinocytes Humans Kaposi Varicelliform Eruption - diagnosis Kaposi Varicelliform Eruption - genetics Lyases plasma S1P lyase S1P/ceramide ratio Sphingolipids - analysis sphingosine-1-phosphate stratum corneum |
| Title | Signaling sphingolipids are biomarkers for atopic dermatitis prone to disseminated viral infections |
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