Genomic programming of IRF4-expressing human Langerhans cells

Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in skin, but the genomic states and transcription factors (TF) regulating these context-specific responses are unclear. Bulk and single-cell transcriptional profiling demonstrates that human migratory LCs are robustly progr...

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Published inNature communications Vol. 11; no. 1; p. 313
Main Authors Sirvent, Sofia, Vallejo, Andres F., Davies, James, Clayton, Kalum, Wu, Zhiguo, Woo, Jeongmin, Riddell, Jeremy, Chaudhri, Virendra K., Stumpf, Patrick, Nazlamova, Liliya Angelova, Wheway, Gabrielle, Rose-Zerilli, Matthew, West, Jonathan, Pujato, Mario, Chen, Xiaoting, Woelk, Christopher H., MacArthur, Ben, Ardern-Jones, Michael, Friedmann, Peter S., Weirauch, Matthew T., Singh, Harinder, Polak, Marta E.
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 16.01.2020
Nature Publishing Group
Nature Portfolio
Subjects
13/106
13/31
13/89
38/39
38/91
631/250/21
631/250/2502
631/250/2504/133
631/250/2504/133/1593
Activator protein 1
Antigen presentation
Antigen Presentation - genetics
Antigen processing
Antigens
Attenuation
Basic-Leucine Zipper Transcription Factors - metabolism
Cell Movement
Chromatin
CRISPR
CRISPR-Cas Systems
Cytokines
Cytokines - metabolism
Editing
Epidermis
ETS protein
Gene Editing
Gene expression
Gene Expression Profiling
Genes
Genomics
Histocompatibility Antigens Class I
Histocompatibility Antigens Class II
Humanities and Social Sciences
Humans
Immunogenicity
Inflammation
Inflammatory response
Interferon regulatory factor 4
Interferon Regulatory Factors - genetics
Interferon Regulatory Factors - metabolism
Langerhans cells
Langerhans Cells - immunology
Langerhans Cells - metabolism
Major histocompatibility complex
Maturation
multidisciplinary
NF-kappa B - metabolism
NF-κB protein
Oxidative stress
Proto-Oncogene Proteins - metabolism
PU.1 protein
Regulatory sequences
Repressor Proteins - metabolism
Science
Science (multidisciplinary)
Skin
Trans-Activators - metabolism
Transcription factors
Transcription, Genetic
Transcriptional Activation
Tumor necrosis factor
Up-Regulation
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Abstract Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in skin, but the genomic states and transcription factors (TF) regulating these context-specific responses are unclear. Bulk and single-cell transcriptional profiling demonstrates that human migratory LCs are robustly programmed for MHC-I and MHC-II antigen presentation. Chromatin analysis reveals enrichment of ETS-IRF and AP1-IRF composite regulatory elements in antigen-presentation genes, coinciding with expression of the TFs, PU.1, IRF4 and BATF3 but not IRF8. Migration of LCs from the epidermis is accompanied by upregulation of IRF4, antigen processing components and co-stimulatory molecules. TNF stimulation augments LC cross-presentation while attenuating IRF4 expression. CRISPR-mediated editing reveals IRF4 to positively regulate the LC activation programme, but repress NF2EL2 and NF-kB pathway genes that promote responsiveness to oxidative stress and inflammatory cytokines. Thus, IRF4-dependent genomic programming of human migratory LCs appears to enable LC maturation while attenuating excessive inflammatory and immunogenic responses in the epidermis. Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in the skin. Here the authors show, by transcriptomic, epigenetic and CRISPR editing analyses, that during LC migration and maturation the transcription factor IRF4 regulates expression of antigen presentation and co-stimulatory gene modules while attenuating inflammatory response genes.
AbstractList Abstract Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in skin, but the genomic states and transcription factors (TF) regulating these context-specific responses are unclear. Bulk and single-cell transcriptional profiling demonstrates that human migratory LCs are robustly programmed for MHC-I and MHC-II antigen presentation. Chromatin analysis reveals enrichment of ETS-IRF and AP1-IRF composite regulatory elements in antigen-presentation genes, coinciding with expression of the TFs, PU.1, IRF4 and BATF3 but not IRF8. Migration of LCs from the epidermis is accompanied by upregulation of IRF4, antigen processing components and co-stimulatory molecules. TNF stimulation augments LC cross-presentation while attenuating IRF4 expression. CRISPR-mediated editing reveals IRF4 to positively regulate the LC activation programme, but repress NF2EL2 and NF-kB pathway genes that promote responsiveness to oxidative stress and inflammatory cytokines. Thus, IRF4-dependent genomic programming of human migratory LCs appears to enable LC maturation while attenuating excessive inflammatory and immunogenic responses in the epidermis.
Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in skin, but the genomic states and transcription factors (TF) regulating these context-specific responses are unclear. Bulk and single-cell transcriptional profiling demonstrates that human migratory LCs are robustly programmed for MHC-I and MHC-II antigen presentation. Chromatin analysis reveals enrichment of ETS-IRF and AP1-IRF composite regulatory elements in antigen-presentation genes, coinciding with expression of the TFs, PU.1, IRF4 and BATF3 but not IRF8. Migration of LCs from the epidermis is accompanied by upregulation of IRF4, antigen processing components and co-stimulatory molecules. TNF stimulation augments LC cross-presentation while attenuating IRF4 expression. CRISPR-mediated editing reveals IRF4 to positively regulate the LC activation programme, but repress NF2EL2 and NF-kB pathway genes that promote responsiveness to oxidative stress and inflammatory cytokines. Thus, IRF4-dependent genomic programming of human migratory LCs appears to enable LC maturation while attenuating excessive inflammatory and immunogenic responses in the epidermis.
Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in skin, but the genomic states and transcription factors (TF) regulating these context-specific responses are unclear. Bulk and single-cell transcriptional profiling demonstrates that human migratory LCs are robustly programmed for MHC-I and MHC-II antigen presentation. Chromatin analysis reveals enrichment of ETS-IRF and AP1-IRF composite regulatory elements in antigen-presentation genes, coinciding with expression of the TFs, PU.1, IRF4 and BATF3 but not IRF8. Migration of LCs from the epidermis is accompanied by upregulation of IRF4, antigen processing components and co-stimulatory molecules. TNF stimulation augments LC cross-presentation while attenuating IRF4 expression. CRISPR-mediated editing reveals IRF4 to positively regulate the LC activation programme, but repress NF2EL2 and NF-kB pathway genes that promote responsiveness to oxidative stress and inflammatory cytokines. Thus, IRF4-dependent genomic programming of human migratory LCs appears to enable LC maturation while attenuating excessive inflammatory and immunogenic responses in the epidermis.Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in the skin. Here the authors show, by transcriptomic, epigenetic and CRISPR editing analyses, that during LC migration and maturation the transcription factor IRF4 regulates expression of antigen presentation and co-stimulatory gene modules while attenuating inflammatory response genes.
Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in skin, but the genomic states and transcription factors (TF) regulating these context-specific responses are unclear. Bulk and single-cell transcriptional profiling demonstrates that human migratory LCs are robustly programmed for MHC-I and MHC-II antigen presentation. Chromatin analysis reveals enrichment of ETS-IRF and AP1-IRF composite regulatory elements in antigen-presentation genes, coinciding with expression of the TFs, PU.1, IRF4 and BATF3 but not IRF8. Migration of LCs from the epidermis is accompanied by upregulation of IRF4, antigen processing components and co-stimulatory molecules. TNF stimulation augments LC cross-presentation while attenuating IRF4 expression. CRISPR-mediated editing reveals IRF4 to positively regulate the LC activation programme, but repress NF2EL2 and NF-kB pathway genes that promote responsiveness to oxidative stress and inflammatory cytokines. Thus, IRF4-dependent genomic programming of human migratory LCs appears to enable LC maturation while attenuating excessive inflammatory and immunogenic responses in the epidermis. Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in the skin. Here the authors show, by transcriptomic, epigenetic and CRISPR editing analyses, that during LC migration and maturation the transcription factor IRF4 regulates expression of antigen presentation and co-stimulatory gene modules while attenuating inflammatory response genes.
Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in the skin. Here the authors show, by transcriptomic, epigenetic and CRISPR editing analyses, that during LC migration and maturation the transcription factor IRF4 regulates expression of antigen presentation and co-stimulatory gene modules while attenuating inflammatory response genes.
ArticleNumber 313
Author Ardern-Jones, Michael
Clayton, Kalum
Rose-Zerilli, Matthew
Weirauch, Matthew T.
West, Jonathan
Nazlamova, Liliya Angelova
Davies, James
Woo, Jeongmin
MacArthur, Ben
Singh, Harinder
Stumpf, Patrick
Polak, Marta E.
Wu, Zhiguo
Riddell, Jeremy
Chen, Xiaoting
Friedmann, Peter S.
Sirvent, Sofia
Vallejo, Andres F.
Pujato, Mario
Woelk, Christopher H.
Wheway, Gabrielle
Chaudhri, Virendra K.
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/31949143$$D View this record in MEDLINE/PubMed
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SSID ssj0000391844
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Snippet Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in skin, but the genomic states and transcription factors (TF) regulating these...
Abstract Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in skin, but the genomic states and transcription factors (TF) regulating...
Langerhans cells (LC) can prime tolerogenic as well as immunogenic responses in the skin. Here the authors show, by transcriptomic, epigenetic and CRISPR...
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StartPage 313
SubjectTerms 13/106
13/31
13/89
38/39
38/91
631/250/21
631/250/2502
631/250/2504/133
631/250/2504/133/1593
Activator protein 1
Antigen presentation
Antigen Presentation - genetics
Antigen processing
Antigens
Attenuation
Basic-Leucine Zipper Transcription Factors - metabolism
Cell Movement
Chromatin
CRISPR
CRISPR-Cas Systems
Cytokines
Cytokines - metabolism
Editing
Epidermis
ETS protein
Gene Editing
Gene expression
Gene Expression Profiling
Genes
Genomics
Histocompatibility Antigens Class I
Histocompatibility Antigens Class II
Humanities and Social Sciences
Humans
Immunogenicity
Inflammation
Inflammatory response
Interferon regulatory factor 4
Interferon Regulatory Factors - genetics
Interferon Regulatory Factors - metabolism
Langerhans cells
Langerhans Cells - immunology
Langerhans Cells - metabolism
Major histocompatibility complex
Maturation
multidisciplinary
NF-kappa B - metabolism
NF-κB protein
Oxidative stress
Proto-Oncogene Proteins - metabolism
PU.1 protein
Regulatory sequences
Repressor Proteins - metabolism
Science
Science (multidisciplinary)
Skin
Trans-Activators - metabolism
Transcription factors
Transcription, Genetic
Transcriptional Activation
Tumor necrosis factor
Up-Regulation
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Title Genomic programming of IRF4-expressing human Langerhans cells
URI https://link.springer.com/article/10.1038/s41467-019-14125-x
https://www.ncbi.nlm.nih.gov/pubmed/31949143
https://www.proquest.com/docview/2342378092
https://search.proquest.com/docview/2341622228
https://pubmed.ncbi.nlm.nih.gov/PMC6965086
https://doaj.org/article/b437083920e842f086e6d17c31b3b048
Volume 11
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