A distal enhancer at risk locus 11q13.5 promotes suppression of colitis by T

Acetylation Alleles Animals Chromosomes, Human, Pair 11 / genetics Chromosomes, Mammalian / genetics Colitis / genetics Enhancer Elements, Genetic / genetics Female Forkhead Transcription Factors / metabolism Genetic Predisposition to Disease / genetics Histones / metabolism Humans Membrane Proteins / genetics Mice Synteny / genetics T-Lymphocytes, Regulatory / immunology

Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
07 2020
Historique:
received: 27 03 2019
accepted: 10 03 2020
pubmed: 6 6 2020
medline: 15 9 2020
entrez: 6 6 2020
Statut: ppublish

Résumé

Genetic variations underlying susceptibility to complex autoimmune and allergic diseases are concentrated within noncoding regulatory elements termed enhancers

Identifiants

DOI: 10.1038/s41586-020-2296-7 PMID: 32499651 PMC: PMC7116706
pubmed: 32499651
doi: 10.1038/s41586-020-2296-7
pii: 10.1038/s41586-020-2296-7
pmc: PMC7116706
mid: EMS113482
doi:

Substances chimiques

Forkhead Transcription Factors 0
Foxp3 protein, mouse 0
Histones 0
LRRC32 protein, human 0
Lrrc32 protein, mouse 0
Membrane Proteins 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

447-452

Subventions

Organisme : NHGRI NIH HHS
ID : RM1 HG007735
Pays : United States
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/B/000C0407
Pays : United Kingdom
Organisme : NIAID NIH HHS
ID : U19 AI142733
Pays : United States
Organisme : Medical Research Council
ID : MR/N014995/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S024468/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 206194
Pays : United Kingdom
Organisme : NHGRI NIH HHS
ID : P50 HG007735
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI121920
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/S024468/2
Pays : United Kingdom
Organisme : Wellcome Trust
ID : WT206194
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 105663/Z/14/Z
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/N007794/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BBS/E/B/000C0409
Pays : United Kingdom
Organisme : Medical Research Council
ID : MC_UU_00014/5
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 208363/Z/17/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 105663
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Références

Maurano, M. T. et al. Systematic localization of common disease-associated variation in regulatory DNA. Science 337, 1190–1195 (2012).
pubmed: 22955828 pmcid: 3771521
de Lange, K. M. et al. Genome-wide association study implicates immune activation of multiple integrin genes in inflammatory bowel disease. Nat. Genet. 49, 256–261 (2017).
pubmed: 28067908 pmcid: 5289481 doi: 10.1038/ng.3760
Anderson, C. A. et al. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat. Genet. 43, 246–252 (2011).
pubmed: 21297633 pmcid: 3084597 doi: 10.1038/ng.764
Onengut-Gumuscu, S. et al. Fine mapping of type 1 diabetes susceptibility loci and evidence for colocalization of causal variants with lymphoid gene enhancers. Nat. Genet. 47, 381–386 (2015).
pubmed: 25751624 pmcid: 4380767 doi: 10.1038/ng.3245
Ferreira, M. A. et al. Identification of IL6R and chromosome 11q13.5 as risk loci for asthma. Lancet 378, 1006–1014 (2011).
pubmed: 21907864 pmcid: 3517659 doi: 10.1016/S0140-6736(11)60874-X
Ferreira, M. A. et al. Shared genetic origin of asthma, hay fever and eczema elucidates allergic disease biology. Nat. Genet. 49, 1752–1757 (2017).
pubmed: 29083406 pmcid: 5989923 doi: 10.1038/ng.3985
Paternoster, L. et al. Meta-analysis of genome-wide association studies identifies three new risk loci for atopic dermatitis. Nat. Genet. 44, 187–192 (2012).
doi: 10.1038/ng.1017
Kundaje, A. et al. Integrative analysis of 111 reference human epigenomes. Nature 518, 317–330 (2015).
pubmed: 25693563 pmcid: 4530010 doi: 10.1038/nature14248
Sakaguchi, S., Yamaguchi, T., Nomura, T. & Ono, M. Regulatory T cells and immune tolerance. Cell 133, 775–787 (2008).
pubmed: 18510923 doi: 10.1016/j.cell.2008.05.009
Josefowicz, S. Z., Lu, L. F. & Rudensky, A. Y. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30, 531–564 (2012).
pubmed: 22224781 pmcid: 6066374 doi: 10.1146/annurev.immunol.25.022106.141623
Kitagawa, Y. et al. Guidance of regulatory T cell development by Satb1-dependent super-enhancer establishment. Nat. Immunol. 18, 173–183 (2017).
pubmed: 27992401 doi: 10.1038/ni.3646
Boschetti, G. et al. Gut inflammation in mice triggers proliferation and function of mucosal Foxp3
doi: 10.1093/ecco-jcc/jjw125
Worthington, J. J. et al. Integrin αvβ8-mediated TGF-β activation by effector regulatory T cells is essential for suppression of T-cell-mediated inflammation. Immunity 42, 903–915 (2015).
pubmed: 25979421 pmcid: 4448149 doi: 10.1016/j.immuni.2015.04.012
Tran, D. Q. et al. GARP (LRRC32) is essential for the surface expression of latent TGF-β on platelets and activated FOXP3
pubmed: 19651619 doi: 10.1073/pnas.0901944106 pmcid: 2726354
Wang, R., Wan, Q., Kozhaya, L., Fujii, H. & Unutmaz, D. Identification of a regulatory T cell specific cell surface molecule that mediates suppressive signals and induces Foxp3 expression. PLoS ONE 3, e2705 (2008).
pubmed: 18628982 pmcid: 2442191 doi: 10.1371/journal.pone.0002705
Dedobbeleer, O., Stockis, J., van der Woning, B., Coulie, P. G. & Lucas, S. Active TGF-β1 released from GARP/TGF-β1 complexes on the surface of stimulated human B lymphocytes increases class-switch recombination and production of IgA. J. Immunol. 199, 391–396 (2017).
pubmed: 28607112 pmcid: 5502319 doi: 10.4049/jimmunol.1601882
Wallace, C. H. et al. B lymphocytes confer immune tolerance via cell surface GARP–TGF-β complex. JCI Insight 3, e99863 (2018).
pmcid: 5928869 doi: 10.1172/jci.insight.99863
Vermeersch, E. et al. The role of platelet and endothelial GARP in thrombosis and hemostasis. PLoS One 12, e0173329 (2017).
pubmed: 28278197 pmcid: 5344406 doi: 10.1371/journal.pone.0173329
O’Connor, M. N. et al. Functional genomics in zebrafish permits rapid characterization of novel platelet membrane proteins. Blood 113, 4754–4762 (2009).
pubmed: 19109564 pmcid: 2680375 doi: 10.1182/blood-2008-06-162693
Arvey, A. et al. Genetic and epigenetic variation in the lineage specification of regulatory T cells. eLife 4, e07571 (2015).
pubmed: 26510014 pmcid: 4623597 doi: 10.7554/eLife.07571
Schmidl, C. et al. The enhancer and promoter landscape of human regulatory and conventional T-cell subpopulations. Blood 123, e68–e78 (2014).
pubmed: 24671953 doi: 10.1182/blood-2013-02-486944
Oh, H. et al. An NF-κB transcription-factor-dependent lineage-specific transcriptional program promotes regulatory T cell identity and function. Immunity 47, 450–465 (2017).
pubmed: 28889947 pmcid: 5679261 doi: 10.1016/j.immuni.2017.08.010
Changelian, P. S. et al. Prevention of organ allograft rejection by a specific Janus kinase 3 inhibitor. Science 302, 875–878 (2003).
pubmed: 14593182 doi: 10.1126/science.1087061
Edwards, J. P. et al. Regulation of the expression of GARP/latent TGF-β1 complexes on mouse T cells and their role in regulatory T cell and T
pubmed: 23645881 doi: 10.4049/jimmunol.1300199
Eschborn, M. et al. Activated glycoprotein A repetitions predominant (GARP)-expressing regulatory T cells inhibit allergen-induced intestinal inflammation in humanized mice. J. Allergy Clin. Immunol. 136, 159–168 (2015).
pubmed: 26145987 doi: 10.1016/j.jaci.2015.04.020
Salem, M. et al. GARP dampens cancer immunity by sustaining function and accumulation of regulatory T cells in the colon. Cancer Res. 79, 1178–1190 (2019).
pubmed: 30674536 pmcid: 6420855 doi: 10.1158/0008-5472.CAN-18-2623
Chen, L. et al. Genetic drivers of epigenetic and transcriptional variation in human immune cells. Cell 167, 1398–1414 (2016).
pubmed: 27863251 pmcid: 5119954 doi: 10.1016/j.cell.2016.10.026
Mumbach, M. R. et al. Enhancer connectome in primary human cells identifies target genes of disease-associated DNA elements. Nat. Genet. 49, 1602–1612 (2017).
pubmed: 28945252 pmcid: 5805393 doi: 10.1038/ng.3963
Rao, S. S. et al. A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping. Cell 159, 1665–1680 (2014).
pubmed: 25497547 pmcid: 5635824 doi: 10.1016/j.cell.2014.11.021
Simeonov, D. R. et al. Discovery of stimulation-responsive immune enhancers with CRISPR activation. Nature 549, 111–115 (2017).
pubmed: 28854172 pmcid: 5675716 doi: 10.1038/nature23875
De Cuyper, I. M. et al. A novel flow cytometry-based platelet aggregation assay. Blood 121, e70–e80 (2013).
pubmed: 23303822 doi: 10.1182/blood-2012-06-437723
Asseman, C., Mauze, S., Leach, M. W., Coffman, R. L. & Powrie, F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190, 995–1004 (1999).
pubmed: 10510089 pmcid: 2195650 doi: 10.1084/jem.190.7.995
Picelli, S. et al. Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9, 171–181 (2014).
pubmed: 24385147
Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y. & Greenleaf, W. J. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat. Methods 10, 1213–1218 (2013).
pubmed: 24097267 pmcid: 3959825
Pollard, K. S., Hubisz, M. J., Rosenbloom, K. R. & Siepel, A. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res. 20, 110–121 (2010).
pubmed: 19858363 pmcid: 2798823 doi: 10.1101/gr.097857.109
Browning, B. L., Zhou, Y. & Browning, S. R. A one-penny imputed genome from next-generation reference panels. Am. J. Hum. Genet. 103, 338–348 (2018).
pubmed: 30100085 pmcid: 6128308 doi: 10.1016/j.ajhg.2018.07.015
Schmidl, C., Rendeiro, A. F., Sheffield, N. C. & Bock, C. ChIPmentation: fast, robust, low-input ChIP-seq for histones and transcription factors. Nat. Methods 12, 963–965 (2015).
pubmed: 26280331 pmcid: 4589892 doi: 10.1038/nmeth.3542
Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
pubmed: 18798982 pmcid: 2592715 doi: 10.1186/gb-2008-9-9-r137
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
doi: 10.1093/bioinformatics/btt656 pubmed: 24227677
Delaneau, O. et al. A complete tool set for molecular QTL discovery and analysis. Nat. Commun. 8, 15452 (2017).
pubmed: 28516912 pmcid: 5454369 doi: 10.1038/ncomms15452
Giambartolomei, C. et al. Bayesian test for colocalisation between pairs of genetic association studies using summary statistics. PLoS Genet. 10, e1004383 (2014).
pubmed: 24830394 pmcid: 4022491 doi: 10.1371/journal.pgen.1004383
Bossini-Castillo, L. et al. Immune disease variants modulate gene expression in regulatory CD4+ T cells and inform drug targets. Preprint at bioRxiv https://doi.org/10.1101/654632 (2019).
Perez-Pinera, P. et al. RNA-guided gene activation by CRISPR–Cas9-based transcription factors. Nat. Methods 10, 973–976 (2013).
pubmed: 23892895 pmcid: 3911785 doi: 10.1038/nmeth.2600
Chen, X. et al. Functional interrogation of primary human T cells via CRISPR genetic editing. J. Immunol. 201, 1586–1598 (2018).
pubmed: 30021769 doi: 10.4049/jimmunol.1701616
Demenais, F. et al. Multiancestry association study identifies new asthma risk loci that colocalize with immune-cell enhancer marks. Nat. Genet. 50, 42–53 (2018).
pubmed: 29273806 doi: 10.1038/s41588-017-0014-7

Auteurs

Rabab Nasrallah (R)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.

Charlotte J Imianowski (CJ)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK. cji27@cam.ac.uk.
Department of Pathology, University of Cambridge, Cambridge, UK. cji27@cam.ac.uk.

Lara Bossini-Castillo (L)

Immune Genomics Group, Wellcome Sanger Institute, Cambridge, UK.

Francis M Grant (FM)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.

Mikail Dogan (M)

The Jackson Laboratory, Farmington, CT, USA.

Lindsey Placek (L)

The Jackson Laboratory, Farmington, CT, USA.

Lina Kozhaya (L)

The Jackson Laboratory, Farmington, CT, USA.

Paula Kuo (P)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.
Department of Pathology, University of Cambridge, Cambridge, UK.

Firas Sadiyah (F)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.
Department of Pathology, University of Cambridge, Cambridge, UK.

Sarah K Whiteside (SK)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.
Department of Pathology, University of Cambridge, Cambridge, UK.

Maxwell R Mumbach (MR)

Howard Hughes Medical Institute and Center for Personal Dynamic Regulomes, Stanford University School of Medicine, Stanford, CA, USA.

Dafni Glinos (D)

Immune Genomics Group, Wellcome Sanger Institute, Cambridge, UK.

Panagiota Vardaka (P)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.
Department of Pathology, University of Cambridge, Cambridge, UK.

Carly E Whyte (CE)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.

Teresa Lozano (T)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.

Toshitsugu Fujita (T)

Chromatin Biochemistry Research Group, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan.
Department of Biochemistry and Genome Biology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.

Hodaka Fujii (H)

Chromatin Biochemistry Research Group, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan.
Department of Biochemistry and Genome Biology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan.
ORCID: 0000-0003-1296-4256

Adrian Liston (A)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.

Simon Andrews (S)

Bioinformatics Group, The Babraham Institute, Cambridge, UK.
ORCID: 0000-0002-5006-3507

Adeline Cozzani (A)

Inserm UMR1277/CNRS9020, Institut pour la Recherche sur le Cancer de Lille, Lille, France.

Jie Yang (J)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK.
Department of Pathology, University of Cambridge, Cambridge, UK.

Suman Mitra (S)

Inserm UMR1277/CNRS9020, Institut pour la Recherche sur le Cancer de Lille, Lille, France.

Enrico Lugli (E)

Humanitas Clinical and Research Center, Milan, Italy.
ORCID: 0000-0002-1964-7678

Howard Y Chang (HY)

Howard Hughes Medical Institute and Center for Personal Dynamic Regulomes, Stanford University School of Medicine, Stanford, CA, USA.
ORCID: 0000-0002-9459-4393

Derya Unutmaz (D)

The Jackson Laboratory, Farmington, CT, USA.

Gosia Trynka (G)

Immune Genomics Group, Wellcome Sanger Institute, Cambridge, UK. gosia@sanger.ac.uk.
Open Targets, Wellcome Genome Campus, Cambridge, UK. gosia@sanger.ac.uk.
ORCID: 0000-0002-6955-9529

Rahul Roychoudhuri (R)

Laboratory of Lymphocyte Signalling and Development, The Babraham Institute, Cambridge, UK. rr257@cam.ac.uk.
Department of Pathology, University of Cambridge, Cambridge, UK. rr257@cam.ac.uk.

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Classifications MeSH

questionsmedicales.fr › Métabolisme › Acylation › Acétylation › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Gènes › Allèles › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Eucaryotes › Animaux › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Chromosomes › Chromosomes de mammifère › Chromosomes humains › Chromosomes humains 6-12 et X › Chromosomes humains de la paire 11 › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Chromosomes › Chromosomes de mammifère › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Maladies de l'appareil digestif › Maladies gastro-intestinales › Maladies intestinales › Maladies du côlon › Colite › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Composants de génome › Gènes › Composants de gène › Éléments de régulation transcriptionnelle › Éléments activateurs (génétique) › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Facteurs de transcription à motif hélice ailée › Facteurs de transcription Forkhead › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Phénomènes génétiques › Génotype › Prédisposition génétique à une maladie › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Histone › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Rodentia › Muridae › Murinae › Souris › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Phénomènes génétiques › Similitude de séquences › Similitude de séquences d'acides nucléiques › Synténie › A distal enhancer at risk locus 11q13.5...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Leucocytes › Agranulocytes › Lymphocytes › Lymphocytes T › Sous-populations de lymphocytes T › Lymphocytes T régulateurs › A distal enhancer at risk locus 11q13.5...