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RNA‐sequencing of paired tape‐strips and skin biopsies in atopic dermatitis reveals key differences
Background Skin tape‐strips and biopsies are widely used methods for investigating the skin in atopic dermatitis (AD). Biopsies are more commonly used but can cause scarring and pain, whereas tape‐strips are noninvasive but sample less tissue. The study evaluated the performance of skin tape‐strips...
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Published in: | Allergy (Copenhagen) 2024-06, Vol.79 (6), p.1548-1559 |
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creator | Fritz, Blaine Halling, Anne‐Sofie Cort, Isabel Díaz‐Pinés Christensen, Maria Oberländer Rønnstad, Amalie Thorsti Møller Olesen, Caroline Meyer Knudgaard, Mette Hjorslev Zachariae, Claus Heegaard, Steffen Thyssen, Jacob P. Bjarnsholt, Thomas |
description | Background
Skin tape‐strips and biopsies are widely used methods for investigating the skin in atopic dermatitis (AD). Biopsies are more commonly used but can cause scarring and pain, whereas tape‐strips are noninvasive but sample less tissue. The study evaluated the performance of skin tape‐strips and biopsies for studying AD.
Methods
Whole‐transcriptome RNA‐sequencing was performed on paired tape‐strips and biopsies collected from lesional and non‐lesional skin from AD patients (n = 7) and non‐AD controls (n = 5). RNA yield, mapping efficiency, and differentially expressed genes (DEGs) for the two methods (tape‐strip/biopsy) and presence of AD (AD/non‐AD) were compared.
Results
Tape‐strips demonstrated a lower RNA yield (22 vs. 4596 ng) and mapping efficiency to known genes (28% vs. 93%) than biopsies. Gene‐expression profiles of paired tape‐strips and biopsies demonstrated a medium correlation (R2 = 0.431). Tape‐strips and biopsies demonstrated systematic differences in measured expression levels of 6483 genes across both AD and non‐AD samples. Tape‐strips preferentially detected many itch (CCL3/CCL4/OSM) and immune‐response (CXCL8/IL4/IL5/IL22) genes as well as markers of epidermal dendritic cells (CD1a/CD207), while certain cytokines (IL18/IL37), skin‐barrier genes (KRT2/FLG2), and dermal fibroblasts markers (COL1A/COL3A) were preferentially detected by biopsies. Tape‐strips identified more DEGs between AD and non‐AD (3157 DEGs) then biopsies (44 DEGs). Tape‐strips also detected higher levels of bacterial mRNA than biopsies.
Conclusions
This study concludes that tape‐strips and biopsies each demonstrate respective advantages for measuring gene‐expression changes in AD. Thus, the specific skin layers and genes of interest should be considered before selecting either method.
Tape strips yielded a lower yield of RNA and fewer sequences mapping to known genes than biopsies. Paired sampling from the same skin (AD or no AD) identified differential detection of thousands of genes between tape strips and biopsies. Tape strips performed better than biopsies for identifying differentially expressed genes in AD. |
doi_str_mv | 10.1111/all.16086 |
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fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2956682786</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2956682786</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3486-3d36c43d2a433118dc1e032d8f99aad080467e408ccff60c4b2fe96e2a12f4f43</originalsourceid><addsrcrecordid>eNp1kM9OGzEQhy1URELaAy-ALPXSHhb8b732MUKlIEVUquBsOfYYOdnsbu0NKDceoc_Ik9Q0lANS5zIj-9OnmR9CJ5Sc0VLntm3PqCRKHqAp5VpVWuv6A5oSSupK1FxN0HHOK0JIwzQ5QhOuRNPUNZui-5838-en3xl-baFzsbvHfcCDjQk8Hu0AL39jikPGtvM4r2OHl7EfcoSMy2zHfogOe0gbO8YxZpzgAWyb8Rp22McQIBUv5I_oMJRn-PTaZ-ju8tvtxVW1-PH9-mK-qBwXSlbcc-kE98wKzilV3lEgnHkVtLbWE0WEbEAQ5VwIkjixZAG0BGYpCyIIPkNf9t4h9eWkPJpNzA7a1nbQb7NhupZSsUbJgn5-h676berKdoYTybgkNWWF-rqnXOpzThDMkOLGpp2hxLykb0r65m_6hT19NW6XG_Bv5L-4C3C-Bx5jC7v_m8x8sdgr_wCcZpB_</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>3062360512</pqid></control><display><type>article</type><title>RNA‐sequencing of paired tape‐strips and skin biopsies in atopic dermatitis reveals key differences</title><source>Wiley-Blackwell Read & Publish Collection</source><creator>Fritz, Blaine ; Halling, Anne‐Sofie ; Cort, Isabel Díaz‐Pinés ; Christensen, Maria Oberländer ; Rønnstad, Amalie Thorsti Møller ; Olesen, Caroline Meyer ; Knudgaard, Mette Hjorslev ; Zachariae, Claus ; Heegaard, Steffen ; Thyssen, Jacob P. ; Bjarnsholt, Thomas</creator><creatorcontrib>Fritz, Blaine ; Halling, Anne‐Sofie ; Cort, Isabel Díaz‐Pinés ; Christensen, Maria Oberländer ; Rønnstad, Amalie Thorsti Møller ; Olesen, Caroline Meyer ; Knudgaard, Mette Hjorslev ; Zachariae, Claus ; Heegaard, Steffen ; Thyssen, Jacob P. ; Bjarnsholt, Thomas</creatorcontrib><description>Background
Skin tape‐strips and biopsies are widely used methods for investigating the skin in atopic dermatitis (AD). Biopsies are more commonly used but can cause scarring and pain, whereas tape‐strips are noninvasive but sample less tissue. The study evaluated the performance of skin tape‐strips and biopsies for studying AD.
Methods
Whole‐transcriptome RNA‐sequencing was performed on paired tape‐strips and biopsies collected from lesional and non‐lesional skin from AD patients (n = 7) and non‐AD controls (n = 5). RNA yield, mapping efficiency, and differentially expressed genes (DEGs) for the two methods (tape‐strip/biopsy) and presence of AD (AD/non‐AD) were compared.
Results
Tape‐strips demonstrated a lower RNA yield (22 vs. 4596 ng) and mapping efficiency to known genes (28% vs. 93%) than biopsies. Gene‐expression profiles of paired tape‐strips and biopsies demonstrated a medium correlation (R2 = 0.431). Tape‐strips and biopsies demonstrated systematic differences in measured expression levels of 6483 genes across both AD and non‐AD samples. Tape‐strips preferentially detected many itch (CCL3/CCL4/OSM) and immune‐response (CXCL8/IL4/IL5/IL22) genes as well as markers of epidermal dendritic cells (CD1a/CD207), while certain cytokines (IL18/IL37), skin‐barrier genes (KRT2/FLG2), and dermal fibroblasts markers (COL1A/COL3A) were preferentially detected by biopsies. Tape‐strips identified more DEGs between AD and non‐AD (3157 DEGs) then biopsies (44 DEGs). Tape‐strips also detected higher levels of bacterial mRNA than biopsies.
Conclusions
This study concludes that tape‐strips and biopsies each demonstrate respective advantages for measuring gene‐expression changes in AD. Thus, the specific skin layers and genes of interest should be considered before selecting either method.
Tape strips yielded a lower yield of RNA and fewer sequences mapping to known genes than biopsies. Paired sampling from the same skin (AD or no AD) identified differential detection of thousands of genes between tape strips and biopsies. Tape strips performed better than biopsies for identifying differentially expressed genes in AD.</description><identifier>ISSN: 0105-4538</identifier><identifier>ISSN: 1398-9995</identifier><identifier>EISSN: 1398-9995</identifier><identifier>DOI: 10.1111/all.16086</identifier><identifier>PMID: 38477552</identifier><language>eng</language><publisher>Denmark: Blackwell Publishing Ltd</publisher><subject>Adult ; Atopic dermatitis ; biopsies ; Biopsy ; Dendritic cells ; Dermatitis ; Dermatitis, Atopic - genetics ; Dermatitis, Atopic - pathology ; Female ; Gene Expression Profiling ; Gene mapping ; Genes ; Humans ; inflammation ; Male ; Middle Aged ; RNA sequencing ; Sequence Analysis, RNA ; Skin - metabolism ; Skin - pathology ; Skin diseases ; Surgical Tape ; tape‐strips ; Transcriptome ; Transcriptomes</subject><ispartof>Allergy (Copenhagen), 2024-06, Vol.79 (6), p.1548-1559</ispartof><rights>2024 The Authors. published by European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.</rights><rights>2024 The Authors. Allergy published by European Academy of Allergy and Clinical Immunology and John Wiley & Sons Ltd.</rights><rights>2024. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3486-3d36c43d2a433118dc1e032d8f99aad080467e408ccff60c4b2fe96e2a12f4f43</cites><orcidid>0000-0001-7177-1054 ; 0000-0003-3770-1743 ; 0000-0001-9949-9726 ; 0000-0002-2085-894X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38477552$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fritz, Blaine</creatorcontrib><creatorcontrib>Halling, Anne‐Sofie</creatorcontrib><creatorcontrib>Cort, Isabel Díaz‐Pinés</creatorcontrib><creatorcontrib>Christensen, Maria Oberländer</creatorcontrib><creatorcontrib>Rønnstad, Amalie Thorsti Møller</creatorcontrib><creatorcontrib>Olesen, Caroline Meyer</creatorcontrib><creatorcontrib>Knudgaard, Mette Hjorslev</creatorcontrib><creatorcontrib>Zachariae, Claus</creatorcontrib><creatorcontrib>Heegaard, Steffen</creatorcontrib><creatorcontrib>Thyssen, Jacob P.</creatorcontrib><creatorcontrib>Bjarnsholt, Thomas</creatorcontrib><title>RNA‐sequencing of paired tape‐strips and skin biopsies in atopic dermatitis reveals key differences</title><title>Allergy (Copenhagen)</title><addtitle>Allergy</addtitle><description>Background
Skin tape‐strips and biopsies are widely used methods for investigating the skin in atopic dermatitis (AD). Biopsies are more commonly used but can cause scarring and pain, whereas tape‐strips are noninvasive but sample less tissue. The study evaluated the performance of skin tape‐strips and biopsies for studying AD.
Methods
Whole‐transcriptome RNA‐sequencing was performed on paired tape‐strips and biopsies collected from lesional and non‐lesional skin from AD patients (n = 7) and non‐AD controls (n = 5). RNA yield, mapping efficiency, and differentially expressed genes (DEGs) for the two methods (tape‐strip/biopsy) and presence of AD (AD/non‐AD) were compared.
Results
Tape‐strips demonstrated a lower RNA yield (22 vs. 4596 ng) and mapping efficiency to known genes (28% vs. 93%) than biopsies. Gene‐expression profiles of paired tape‐strips and biopsies demonstrated a medium correlation (R2 = 0.431). Tape‐strips and biopsies demonstrated systematic differences in measured expression levels of 6483 genes across both AD and non‐AD samples. Tape‐strips preferentially detected many itch (CCL3/CCL4/OSM) and immune‐response (CXCL8/IL4/IL5/IL22) genes as well as markers of epidermal dendritic cells (CD1a/CD207), while certain cytokines (IL18/IL37), skin‐barrier genes (KRT2/FLG2), and dermal fibroblasts markers (COL1A/COL3A) were preferentially detected by biopsies. Tape‐strips identified more DEGs between AD and non‐AD (3157 DEGs) then biopsies (44 DEGs). Tape‐strips also detected higher levels of bacterial mRNA than biopsies.
Conclusions
This study concludes that tape‐strips and biopsies each demonstrate respective advantages for measuring gene‐expression changes in AD. Thus, the specific skin layers and genes of interest should be considered before selecting either method.
Tape strips yielded a lower yield of RNA and fewer sequences mapping to known genes than biopsies. Paired sampling from the same skin (AD or no AD) identified differential detection of thousands of genes between tape strips and biopsies. Tape strips performed better than biopsies for identifying differentially expressed genes in AD.</description><subject>Adult</subject><subject>Atopic dermatitis</subject><subject>biopsies</subject><subject>Biopsy</subject><subject>Dendritic cells</subject><subject>Dermatitis</subject><subject>Dermatitis, Atopic - genetics</subject><subject>Dermatitis, Atopic - pathology</subject><subject>Female</subject><subject>Gene Expression Profiling</subject><subject>Gene mapping</subject><subject>Genes</subject><subject>Humans</subject><subject>inflammation</subject><subject>Male</subject><subject>Middle Aged</subject><subject>RNA sequencing</subject><subject>Sequence Analysis, RNA</subject><subject>Skin - metabolism</subject><subject>Skin - pathology</subject><subject>Skin diseases</subject><subject>Surgical Tape</subject><subject>tape‐strips</subject><subject>Transcriptome</subject><subject>Transcriptomes</subject><issn>0105-4538</issn><issn>1398-9995</issn><issn>1398-9995</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><recordid>eNp1kM9OGzEQhy1URELaAy-ALPXSHhb8b732MUKlIEVUquBsOfYYOdnsbu0NKDceoc_Ik9Q0lANS5zIj-9OnmR9CJ5Sc0VLntm3PqCRKHqAp5VpVWuv6A5oSSupK1FxN0HHOK0JIwzQ5QhOuRNPUNZui-5838-en3xl-baFzsbvHfcCDjQk8Hu0AL39jikPGtvM4r2OHl7EfcoSMy2zHfogOe0gbO8YxZpzgAWyb8Rp22McQIBUv5I_oMJRn-PTaZ-ju8tvtxVW1-PH9-mK-qBwXSlbcc-kE98wKzilV3lEgnHkVtLbWE0WEbEAQ5VwIkjixZAG0BGYpCyIIPkNf9t4h9eWkPJpNzA7a1nbQb7NhupZSsUbJgn5-h676berKdoYTybgkNWWF-rqnXOpzThDMkOLGpp2hxLykb0r65m_6hT19NW6XG_Bv5L-4C3C-Bx5jC7v_m8x8sdgr_wCcZpB_</recordid><startdate>202406</startdate><enddate>202406</enddate><creator>Fritz, Blaine</creator><creator>Halling, Anne‐Sofie</creator><creator>Cort, Isabel Díaz‐Pinés</creator><creator>Christensen, Maria Oberländer</creator><creator>Rønnstad, Amalie Thorsti Møller</creator><creator>Olesen, Caroline Meyer</creator><creator>Knudgaard, Mette Hjorslev</creator><creator>Zachariae, Claus</creator><creator>Heegaard, Steffen</creator><creator>Thyssen, Jacob P.</creator><creator>Bjarnsholt, Thomas</creator><general>Blackwell Publishing Ltd</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7T5</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7177-1054</orcidid><orcidid>https://orcid.org/0000-0003-3770-1743</orcidid><orcidid>https://orcid.org/0000-0001-9949-9726</orcidid><orcidid>https://orcid.org/0000-0002-2085-894X</orcidid></search><sort><creationdate>202406</creationdate><title>RNA‐sequencing of paired tape‐strips and skin biopsies in atopic dermatitis reveals key differences</title><author>Fritz, Blaine ; Halling, Anne‐Sofie ; Cort, Isabel Díaz‐Pinés ; Christensen, Maria Oberländer ; Rønnstad, Amalie Thorsti Møller ; Olesen, Caroline Meyer ; Knudgaard, Mette Hjorslev ; Zachariae, Claus ; Heegaard, Steffen ; Thyssen, Jacob P. ; Bjarnsholt, Thomas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3486-3d36c43d2a433118dc1e032d8f99aad080467e408ccff60c4b2fe96e2a12f4f43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adult</topic><topic>Atopic dermatitis</topic><topic>biopsies</topic><topic>Biopsy</topic><topic>Dendritic cells</topic><topic>Dermatitis</topic><topic>Dermatitis, Atopic - genetics</topic><topic>Dermatitis, Atopic - pathology</topic><topic>Female</topic><topic>Gene Expression Profiling</topic><topic>Gene mapping</topic><topic>Genes</topic><topic>Humans</topic><topic>inflammation</topic><topic>Male</topic><topic>Middle Aged</topic><topic>RNA sequencing</topic><topic>Sequence Analysis, RNA</topic><topic>Skin - metabolism</topic><topic>Skin - pathology</topic><topic>Skin diseases</topic><topic>Surgical Tape</topic><topic>tape‐strips</topic><topic>Transcriptome</topic><topic>Transcriptomes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fritz, Blaine</creatorcontrib><creatorcontrib>Halling, Anne‐Sofie</creatorcontrib><creatorcontrib>Cort, Isabel Díaz‐Pinés</creatorcontrib><creatorcontrib>Christensen, Maria Oberländer</creatorcontrib><creatorcontrib>Rønnstad, Amalie Thorsti Møller</creatorcontrib><creatorcontrib>Olesen, Caroline Meyer</creatorcontrib><creatorcontrib>Knudgaard, Mette Hjorslev</creatorcontrib><creatorcontrib>Zachariae, Claus</creatorcontrib><creatorcontrib>Heegaard, Steffen</creatorcontrib><creatorcontrib>Thyssen, Jacob P.</creatorcontrib><creatorcontrib>Bjarnsholt, Thomas</creatorcontrib><collection>Wiley Open Access</collection><collection>Wiley Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Allergy (Copenhagen)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fritz, Blaine</au><au>Halling, Anne‐Sofie</au><au>Cort, Isabel Díaz‐Pinés</au><au>Christensen, Maria Oberländer</au><au>Rønnstad, Amalie Thorsti Møller</au><au>Olesen, Caroline Meyer</au><au>Knudgaard, Mette Hjorslev</au><au>Zachariae, Claus</au><au>Heegaard, Steffen</au><au>Thyssen, Jacob P.</au><au>Bjarnsholt, Thomas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>RNA‐sequencing of paired tape‐strips and skin biopsies in atopic dermatitis reveals key differences</atitle><jtitle>Allergy (Copenhagen)</jtitle><addtitle>Allergy</addtitle><date>2024-06</date><risdate>2024</risdate><volume>79</volume><issue>6</issue><spage>1548</spage><epage>1559</epage><pages>1548-1559</pages><issn>0105-4538</issn><issn>1398-9995</issn><eissn>1398-9995</eissn><abstract>Background
Skin tape‐strips and biopsies are widely used methods for investigating the skin in atopic dermatitis (AD). Biopsies are more commonly used but can cause scarring and pain, whereas tape‐strips are noninvasive but sample less tissue. The study evaluated the performance of skin tape‐strips and biopsies for studying AD.
Methods
Whole‐transcriptome RNA‐sequencing was performed on paired tape‐strips and biopsies collected from lesional and non‐lesional skin from AD patients (n = 7) and non‐AD controls (n = 5). RNA yield, mapping efficiency, and differentially expressed genes (DEGs) for the two methods (tape‐strip/biopsy) and presence of AD (AD/non‐AD) were compared.
Results
Tape‐strips demonstrated a lower RNA yield (22 vs. 4596 ng) and mapping efficiency to known genes (28% vs. 93%) than biopsies. Gene‐expression profiles of paired tape‐strips and biopsies demonstrated a medium correlation (R2 = 0.431). Tape‐strips and biopsies demonstrated systematic differences in measured expression levels of 6483 genes across both AD and non‐AD samples. Tape‐strips preferentially detected many itch (CCL3/CCL4/OSM) and immune‐response (CXCL8/IL4/IL5/IL22) genes as well as markers of epidermal dendritic cells (CD1a/CD207), while certain cytokines (IL18/IL37), skin‐barrier genes (KRT2/FLG2), and dermal fibroblasts markers (COL1A/COL3A) were preferentially detected by biopsies. Tape‐strips identified more DEGs between AD and non‐AD (3157 DEGs) then biopsies (44 DEGs). Tape‐strips also detected higher levels of bacterial mRNA than biopsies.
Conclusions
This study concludes that tape‐strips and biopsies each demonstrate respective advantages for measuring gene‐expression changes in AD. Thus, the specific skin layers and genes of interest should be considered before selecting either method.
Tape strips yielded a lower yield of RNA and fewer sequences mapping to known genes than biopsies. Paired sampling from the same skin (AD or no AD) identified differential detection of thousands of genes between tape strips and biopsies. Tape strips performed better than biopsies for identifying differentially expressed genes in AD.</abstract><cop>Denmark</cop><pub>Blackwell Publishing Ltd</pub><pmid>38477552</pmid><doi>10.1111/all.16086</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-7177-1054</orcidid><orcidid>https://orcid.org/0000-0003-3770-1743</orcidid><orcidid>https://orcid.org/0000-0001-9949-9726</orcidid><orcidid>https://orcid.org/0000-0002-2085-894X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Atopic dermatitis biopsies Biopsy Dendritic cells Dermatitis Dermatitis, Atopic - genetics Dermatitis, Atopic - pathology Female Gene Expression Profiling Gene mapping Genes Humans inflammation Male Middle Aged RNA sequencing Sequence Analysis, RNA Skin - metabolism Skin - pathology Skin diseases Surgical Tape tape‐strips Transcriptome Transcriptomes |
title | RNA‐sequencing of paired tape‐strips and skin biopsies in atopic dermatitis reveals key differences |
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