Priming of transcriptional memory responses via the chromatin accessibility landscape in T cells.
Identifieur interne : 000F98 ( PubMed/Corpus ); précédent : 000F97; suivant : 000F99Priming of transcriptional memory responses via the chromatin accessibility landscape in T cells.
Auteurs : Wen Juan Tu ; Kristine Hardy ; Christopher R. Sutton ; Robert Mccuaig ; Jasmine Li ; Jenny Dunn ; Abel Tan ; Vedran Brezar ; Melanie Morris ; Gareth Denyer ; Sau Kuen Lee ; Stephen J. Turner ; Nabila Seddiki ; Corey Smith ; Rajiv Khanna ; Sudha RaoSource :
- Scientific reports [ 2045-2322 ] ; 2017.
Abstract
Memory T cells exhibit transcriptional memory and "remember" their previous pathogenic encounter to increase transcription on re-infection. However, how this transcriptional priming response is regulated is unknown. Here we performed global FAIRE-seq profiling of chromatin accessibility in a human T cell transcriptional memory model. Primary activation induced persistent accessibility changes, and secondary activation induced secondary-specific opening of previously less accessible regions associated with enhanced expression of memory-responsive genes. Increased accessibility occurred largely in distal regulatory regions and was associated with increased histone acetylation and relative H3.3 deposition. The enhanced re-stimulation response was linked to the strength of initial PKC-induced signalling, and PKC-sensitive increases in accessibility upon initial stimulation showed higher accessibility on re-stimulation. While accessibility maintenance was associated with ETS-1, accessibility at re-stimulation-specific regions was linked to NFAT, especially in combination with ETS-1, EGR, GATA, NFκB, and NR4A. Furthermore, NFATC1 was directly regulated by ETS-1 at an enhancer region. In contrast to the factors that increased accessibility, signalling from bHLH and ZEB family members enhanced decreased accessibility upon re-stimulation. Interplay between distal regulatory elements, accessibility, and the combined action of sequence-specific transcription factors allows transcriptional memory-responsive genes to "remember" their initial environmental encounter.
DOI: 10.1038/srep44825
PubMed: 28317936
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Priming of transcriptional memory responses via the chromatin accessibility landscape in T cells.</title><author><name sortKey="Tu, Wen Juan" sort="Tu, Wen Juan" uniqKey="Tu W" first="Wen Juan" last="Tu">Wen Juan Tu</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Hardy, Kristine" sort="Hardy, Kristine" uniqKey="Hardy K" first="Kristine" last="Hardy">Kristine Hardy</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Sutton, Christopher R" sort="Sutton, Christopher R" uniqKey="Sutton C" first="Christopher R" last="Sutton">Christopher R. Sutton</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Mccuaig, Robert" sort="Mccuaig, Robert" uniqKey="Mccuaig R" first="Robert" last="Mccuaig">Robert Mccuaig</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Jasmine" sort="Li, Jasmine" uniqKey="Li J" first="Jasmine" last="Li">Jasmine Li</name><affiliation><nlm:affiliation>Department of Microbiology, Biomedical Discovery Institute, Monash University, Clayton, Victoria 3800, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Dunn, Jenny" sort="Dunn, Jenny" uniqKey="Dunn J" first="Jenny" last="Dunn">Jenny Dunn</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Tan, Abel" sort="Tan, Abel" uniqKey="Tan A" first="Abel" last="Tan">Abel Tan</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Brezar, Vedran" sort="Brezar, Vedran" uniqKey="Brezar V" first="Vedran" last="Brezar">Vedran Brezar</name><affiliation><nlm:affiliation>INSERM U955 Eq16 Faculte de medicine Henri Mondor and Universite Paris-Est, Creteil/Vaccine Research Institute, Creteil 94010, France.</nlm:affiliation></affiliation></author><author><name sortKey="Morris, Melanie" sort="Morris, Melanie" uniqKey="Morris M" first="Melanie" last="Morris">Melanie Morris</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Denyer, Gareth" sort="Denyer, Gareth" uniqKey="Denyer G" first="Gareth" last="Denyer">Gareth Denyer</name><affiliation><nlm:affiliation>School of Molecular Bioscience, The University of Sydney, Sydney, NSW, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Lee, Sau Kuen" sort="Lee, Sau Kuen" uniqKey="Lee S" first="Sau Kuen" last="Lee">Sau Kuen Lee</name><affiliation><nlm:affiliation>QIMR Berghofer Centre for Immunotherapy and Vaccine Development QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Turner, Stephen J" sort="Turner, Stephen J" uniqKey="Turner S" first="Stephen J" last="Turner">Stephen J. Turner</name><affiliation><nlm:affiliation>Department of Microbiology, Biomedical Discovery Institute, Monash University, Clayton, Victoria 3800, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Seddiki, Nabila" sort="Seddiki, Nabila" uniqKey="Seddiki N" first="Nabila" last="Seddiki">Nabila Seddiki</name><affiliation><nlm:affiliation>INSERM U955 Eq16 Faculte de medicine Henri Mondor and Universite Paris-Est, Creteil/Vaccine Research Institute, Creteil 94010, France.</nlm:affiliation></affiliation></author><author><name sortKey="Smith, Corey" sort="Smith, Corey" uniqKey="Smith C" first="Corey" last="Smith">Corey Smith</name><affiliation><nlm:affiliation>QIMR Berghofer Centre for Immunotherapy and Vaccine Development QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Khanna, Rajiv" sort="Khanna, Rajiv" uniqKey="Khanna R" first="Rajiv" last="Khanna">Rajiv Khanna</name><affiliation><nlm:affiliation>QIMR Berghofer Centre for Immunotherapy and Vaccine Development QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Rao, Sudha" sort="Rao, Sudha" uniqKey="Rao S" first="Sudha" last="Rao">Sudha Rao</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2017">2017</date><idno type="RBID">pubmed:28317936</idno><idno type="pmid">28317936</idno><idno type="doi">10.1038/srep44825</idno><idno type="wicri:Area/PubMed/Corpus">000F98</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">000F98</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Priming of transcriptional memory responses via the chromatin accessibility landscape in T cells.</title><author><name sortKey="Tu, Wen Juan" sort="Tu, Wen Juan" uniqKey="Tu W" first="Wen Juan" last="Tu">Wen Juan Tu</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Hardy, Kristine" sort="Hardy, Kristine" uniqKey="Hardy K" first="Kristine" last="Hardy">Kristine Hardy</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Sutton, Christopher R" sort="Sutton, Christopher R" uniqKey="Sutton C" first="Christopher R" last="Sutton">Christopher R. Sutton</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Mccuaig, Robert" sort="Mccuaig, Robert" uniqKey="Mccuaig R" first="Robert" last="Mccuaig">Robert Mccuaig</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Li, Jasmine" sort="Li, Jasmine" uniqKey="Li J" first="Jasmine" last="Li">Jasmine Li</name><affiliation><nlm:affiliation>Department of Microbiology, Biomedical Discovery Institute, Monash University, Clayton, Victoria 3800, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Dunn, Jenny" sort="Dunn, Jenny" uniqKey="Dunn J" first="Jenny" last="Dunn">Jenny Dunn</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Tan, Abel" sort="Tan, Abel" uniqKey="Tan A" first="Abel" last="Tan">Abel Tan</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Brezar, Vedran" sort="Brezar, Vedran" uniqKey="Brezar V" first="Vedran" last="Brezar">Vedran Brezar</name><affiliation><nlm:affiliation>INSERM U955 Eq16 Faculte de medicine Henri Mondor and Universite Paris-Est, Creteil/Vaccine Research Institute, Creteil 94010, France.</nlm:affiliation></affiliation></author><author><name sortKey="Morris, Melanie" sort="Morris, Melanie" uniqKey="Morris M" first="Melanie" last="Morris">Melanie Morris</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Denyer, Gareth" sort="Denyer, Gareth" uniqKey="Denyer G" first="Gareth" last="Denyer">Gareth Denyer</name><affiliation><nlm:affiliation>School of Molecular Bioscience, The University of Sydney, Sydney, NSW, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Lee, Sau Kuen" sort="Lee, Sau Kuen" uniqKey="Lee S" first="Sau Kuen" last="Lee">Sau Kuen Lee</name><affiliation><nlm:affiliation>QIMR Berghofer Centre for Immunotherapy and Vaccine Development QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Turner, Stephen J" sort="Turner, Stephen J" uniqKey="Turner S" first="Stephen J" last="Turner">Stephen J. Turner</name><affiliation><nlm:affiliation>Department of Microbiology, Biomedical Discovery Institute, Monash University, Clayton, Victoria 3800, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Seddiki, Nabila" sort="Seddiki, Nabila" uniqKey="Seddiki N" first="Nabila" last="Seddiki">Nabila Seddiki</name><affiliation><nlm:affiliation>INSERM U955 Eq16 Faculte de medicine Henri Mondor and Universite Paris-Est, Creteil/Vaccine Research Institute, Creteil 94010, France.</nlm:affiliation></affiliation></author><author><name sortKey="Smith, Corey" sort="Smith, Corey" uniqKey="Smith C" first="Corey" last="Smith">Corey Smith</name><affiliation><nlm:affiliation>QIMR Berghofer Centre for Immunotherapy and Vaccine Development QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Khanna, Rajiv" sort="Khanna, Rajiv" uniqKey="Khanna R" first="Rajiv" last="Khanna">Rajiv Khanna</name><affiliation><nlm:affiliation>QIMR Berghofer Centre for Immunotherapy and Vaccine Development QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</nlm:affiliation></affiliation></author><author><name sortKey="Rao, Sudha" sort="Rao, Sudha" uniqKey="Rao S" first="Sudha" last="Rao">Sudha Rao</name><affiliation><nlm:affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Scientific reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Memory T cells exhibit transcriptional memory and "remember" their previous pathogenic encounter to increase transcription on re-infection. However, how this transcriptional priming response is regulated is unknown. Here we performed global FAIRE-seq profiling of chromatin accessibility in a human T cell transcriptional memory model. Primary activation induced persistent accessibility changes, and secondary activation induced secondary-specific opening of previously less accessible regions associated with enhanced expression of memory-responsive genes. Increased accessibility occurred largely in distal regulatory regions and was associated with increased histone acetylation and relative H3.3 deposition. The enhanced re-stimulation response was linked to the strength of initial PKC-induced signalling, and PKC-sensitive increases in accessibility upon initial stimulation showed higher accessibility on re-stimulation. While accessibility maintenance was associated with ETS-1, accessibility at re-stimulation-specific regions was linked to NFAT, especially in combination with ETS-1, EGR, GATA, NFκB, and NR4A. Furthermore, NFATC1 was directly regulated by ETS-1 at an enhancer region. In contrast to the factors that increased accessibility, signalling from bHLH and ZEB family members enhanced decreased accessibility upon re-stimulation. Interplay between distal regulatory elements, accessibility, and the combined action of sequence-specific transcription factors allows transcriptional memory-responsive genes to "remember" their initial environmental encounter.</div></front></TEI><pubmed><MedlineCitation Status="In-Data-Review" Owner="NLM"><PMID Version="1">28317936</PMID><DateCreated><Year>2017</Year><Month>03</Month><Day>20</Day></DateCreated><DateRevised><Year>2017</Year><Month>03</Month><Day>23</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2045-2322</ISSN><JournalIssue CitedMedium="Internet"><Volume>7</Volume><PubDate><Year>2017</Year><Month>Mar</Month><Day>20</Day></PubDate></JournalIssue><Title>Scientific reports</Title><ISOAbbreviation>Sci Rep</ISOAbbreviation></Journal><ArticleTitle>Priming of transcriptional memory responses via the chromatin accessibility landscape in T cells.</ArticleTitle><Pagination><MedlinePgn>44825</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/srep44825</ELocationID><Abstract><AbstractText>Memory T cells exhibit transcriptional memory and "remember" their previous pathogenic encounter to increase transcription on re-infection. However, how this transcriptional priming response is regulated is unknown. Here we performed global FAIRE-seq profiling of chromatin accessibility in a human T cell transcriptional memory model. Primary activation induced persistent accessibility changes, and secondary activation induced secondary-specific opening of previously less accessible regions associated with enhanced expression of memory-responsive genes. Increased accessibility occurred largely in distal regulatory regions and was associated with increased histone acetylation and relative H3.3 deposition. The enhanced re-stimulation response was linked to the strength of initial PKC-induced signalling, and PKC-sensitive increases in accessibility upon initial stimulation showed higher accessibility on re-stimulation. While accessibility maintenance was associated with ETS-1, accessibility at re-stimulation-specific regions was linked to NFAT, especially in combination with ETS-1, EGR, GATA, NFκB, and NR4A. Furthermore, NFATC1 was directly regulated by ETS-1 at an enhancer region. In contrast to the factors that increased accessibility, signalling from bHLH and ZEB family members enhanced decreased accessibility upon re-stimulation. Interplay between distal regulatory elements, accessibility, and the combined action of sequence-specific transcription factors allows transcriptional memory-responsive genes to "remember" their initial environmental encounter.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Tu</LastName><ForeName>Wen Juan</ForeName><Initials>WJ</Initials><AffiliationInfo><Affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hardy</LastName><ForeName>Kristine</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Sutton</LastName><ForeName>Christopher R</ForeName><Initials>CR</Initials><AffiliationInfo><Affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>McCuaig</LastName><ForeName>Robert</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Li</LastName><ForeName>Jasmine</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Department of Microbiology, Biomedical Discovery Institute, Monash University, Clayton, Victoria 3800, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiology &Immunology, The Doherty Institute for Infection and Immunity, University of Melbourne, Victoria 3010, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Dunn</LastName><ForeName>Jenny</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tan</LastName><ForeName>Abel</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Brezar</LastName><ForeName>Vedran</ForeName><Initials>V</Initials><AffiliationInfo><Affiliation>INSERM U955 Eq16 Faculte de medicine Henri Mondor and Universite Paris-Est, Creteil/Vaccine Research Institute, Creteil 94010, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Morris</LastName><ForeName>Melanie</ForeName><Initials>M</Initials><AffiliationInfo><Affiliation>Faculty of Education, Science, Technology &Mathematics, University of Canberra, Canberra, Australian Capital Territory 2617, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Denyer</LastName><ForeName>Gareth</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>School of Molecular Bioscience, The University of Sydney, Sydney, NSW, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lee</LastName><ForeName>Sau Kuen</ForeName><Initials>SK</Initials><AffiliationInfo><Affiliation>QIMR Berghofer Centre for Immunotherapy and Vaccine Development QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Tumour Immunology Laboratory, Department of Immunology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Turner</LastName><ForeName>Stephen J</ForeName><Initials>SJ</Initials><AffiliationInfo><Affiliation>Department of Microbiology, Biomedical Discovery Institute, Monash University, Clayton, Victoria 3800, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Microbiology &Immunology, The Doherty Institute for Infection and Immunity, University of Melbourne, Victoria 3010, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Seddiki</LastName><ForeName>Nabila</ForeName><Initials>N</Initials><AffiliationInfo><Affiliation>INSERM U955 Eq16 Faculte de medicine Henri Mondor and Universite Paris-Est, Creteil/Vaccine Research Institute, Creteil 94010, France.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Smith</LastName><ForeName>Corey</ForeName><Initials>C</Initials><AffiliationInfo><Affiliation>QIMR Berghofer Centre for Immunotherapy and Vaccine Development QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Tumour Immunology Laboratory, Department of Immunology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Khanna</LastName><ForeName>Rajiv</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>QIMR Berghofer Centre for Immunotherapy and Vaccine Development QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Tumour Immunology Laboratory, Department of Immunology, QIMR Berghofer Medical Research Institute, Brisbane, Queensland, Australia.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Rao</LastName><ForeName>Sudha</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Faculty of Education, Science, 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