ArticleImmunity2017
Group 1 Innate Lymphoid Cell Lineage Identity Is Determined by a cis-Regulatory Element Marked by a Long Non-coding RNA.
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Article in Immunity, 2017. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 49 papers.
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49citing papers in PubMed
2.9field-weighted citation impact, top 8% of its field
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Who cites it
49 citing papers in PubMed, 69 citations in OpenAlex.
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Authors and funding
28 authors at 8 institutions in 2 countries.
Walter K MowelDepartment of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Sam J McCrightDepartment of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Jonathan J KotzinDepartment of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Magalie A ColletThe Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA.
Asli UyarThe Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA.
Xin ChenThe Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA; Department of Immunology, University of Connecticut School of Medicine, Farmington, CT 06030, USA.
Alexandra DeLaneyDepartment of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Sean P SpencerDepartment of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Anthony T VirtueDepartment of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
EnJun YangDepartment of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Alejandro VillarinoMolecular Immunology and Inflammation Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, NIH, Bethesda, MD 20892, USA.
Makoto KurachiInstitute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Margaret C DunaginSchool of Engineering and Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA.
Gretchen Harms PritchardDepartment of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Judith SteinDepartment of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA; Howard Hughes Medical Institute, Yale University, New Haven, CT 06510, USA.
Cynthia HughesDepartment of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA; Howard Hughes Medical Institute, Yale University, New Haven, CT 06510, USA.
Diogo Fonseca-PereiraInstituto de Medicina Molecular, Faculdade de Medicina de Lisboa, Av. Prof. Egas Moniz, Edifício Egas Moniz, 1649-028 Lisbon, Portugal.
Henrique Veiga-FernandesInstituto de Medicina Molecular, Faculdade de Medicina de Lisboa, Av. Prof. Egas Moniz, Edifício Egas Moniz, 1649-028 Lisbon, Portugal; Champalimaud Research, Champalimaud Centre for the Unknown, 1400-038 Lisbon, Portugal.
Arjun RajSchool of Engineering and Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA.
Taku KambayashiDepartment of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Igor E BrodskyDepartment of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
John J O'SheaMolecular Immunology and Inflammation Branch, National Institute of Arthritis and Musculoskeletal and Skin Diseases, NIH, Bethesda, MD 20892, USA.
E John WherryInstitute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Microbiology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
Loyal A GoffMcKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University, Baltimore, MD 21205, USA; Department of Neuroscience, Johns Hopkins University, Baltimore, MD 21205, USA.
John L RinnBiological and Biomedical Sciences, Harvard Medical School, Boston, MA 02115, USA; Department of Stem Cell and Regenerative Biology, Harvard University, Cambridge, MA 02138, USA.
Adam WilliamsThe Jackson Laboratory for Genomic Medicine, Farmington, CT 06032, USA; Department of Genetics and Genomic Sciences, University of Connecticut Health Center, Farmington, CT 06032, USA. Electronic address: adam.williams@jax.org.
Richard A FlavellSchool of Engineering and Applied Science, University of Pennsylvania, Philadelphia, PA 19104, USA; Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06520, USA. Electronic address: richard.flavell@yale.edu.
Jorge Henao-MejiaDepartment of Pathology and Laboratory Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Institute for Immunology, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA; Division of Transplant Immunology, Department of Pathology and Laboratory Medicine, Children's Hospital of Philadelphia, University of Pennsylvania, Philadelphia, PA 19104, USA. Electronic address: jhena@mail.med.upenn.edu.
University of Pennsylvania · USJackson Laboratory · USHoward Hughes Medical Institute · USNational Institute of Arthritis and Musculoskeletal and Skin Diseases · USHarvard University · USHospital de Egas Moniz · PTInstituto de Medicina Molecular João Lobo AntunesJohns Hopkins University · US
Funding
Yale Clinical and Translational Science Award (U Component)UL1TR001863 · NCATS · YALE UNIVERSITY · PI John H. Krystal, LUCILA OHNO-MACHADO · 2016 to 2026
$102.9MStat transcription factors in immunoregulation and autoimmune diseaseZIAAR041159 · NIAMS · NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES · PI O'SHEA, JOHN · 2009 to 2025
$49.3MHigh Throughput Next Generation Sequencing: supports genomics and epigenomics research in muscle, skin, bone and autoimmune diseases.ZICAR041207 · NIAMS · NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES · PI DELL'ORSO, STEFANIA · 2016 to 2025
$12.3MHEMATOPOIESIS TRAINING GRANTT32DK007780 · NIDDK · UNIVERSITY OF PENNSYLVANIA · PI TONG, WEI · 1999 to 2023
$6.7MImmune System Development and RegulationT32AI055428 · NIAID · UNIVERSITY OF PENNSYLVANIA · PI ALLMAN, DAVID M, OLIVER, PAULA MARIA · 2003 to 2025
$4.2MA Comprehensive Spatial Picture of Transcription in the NucleusDP2OD008514 · OD · UNIVERSITY OF PENNSYLVANIA · PI RAJ, ARJUN · 2011 to 2011
$2.4MDefining the non-apoptotic role of Caspase-8 activity in anti-bacterial immune defenseR01AI128530 · NIAID · UNIVERSITY OF PENNSYLVANIA · PI BRODSKY, IGOR E · 2017 to 2021
$2.0MRegulation of short-lived myeloid cells by the novel long non-coding RNA MorrbidR01HL136572 · NHLBI · UNIVERSITY OF PENNSYLVANIA · PI HENAO-MEJIA, JORGE · 2017 to 2021
$2.0MModulation of Inflammasome Activation by YersiniaR01AI103062 · NIAID · UNIVERSITY OF PENNSYLVANIA · PI BRODSKY, IGOR E · 2013 to 2016
$1.7MValidation and development of single nucleotide variant RNA FISH in single cells in culture and tissueR33EB019767 · NIBIB · UNIVERSITY OF PENNSYLVANIA · PI RAJ, ARJUN · 2014 to 2016
$1.1MRegulation of adipose tissue inflammation by the miR-181 familyR21DK111755 · NIDDK · UNIVERSITY OF PENNSYLVANIA · PI HENAO-MEJIA, JORGE · 2016 to 2018
$604kIdentifying lincRNAs critical in asthma pathogenesisR21AI110776 · NIAID · YALE UNIVERSITY · PI FLAVELL, RICHARD A, WILLIAMS, ADAM · 2014 to 2015
$458kHoward Hughes Medical InstituteNCATS NIH HHS UL1 TR001863NHLBI NIH HHS R01 HL136572NIAID NIH HHS F31 AI124538NIAID NIH HHS R01 AI103062NIAID NIH HHS R01 AI128530NIAID NIH HHS R21 AI110776NIAID NIH HHS R21 AI128060NIAID NIH HHS T32 AI055428NIBIB NIH HHS R33 EB019767NIDDK NIH HHS F30 DK094708NIDDK NIH HHS R21 DK111755NIDDK NIH HHS T32 DK007780NIH HHS DP2 OD008514
Abstract
Commitment to the innate lymphoid cell (ILC) lineage is determined by Id2, a transcriptional regulator that antagonizes T and B cell-specific gene expression programs. Yet how Id2 expression is regulated in each ILC subset remains poorly understood. We identified a cis-regulatory element demarcated by a long non-coding RNA (lncRNA) that controls the function and lineage identity of group 1 ILCs, while being dispensable for early ILC development and homeostasis of ILC2s and ILC3s. The locus encoding this lncRNA, which we termed Rroid, directly interacted with the promoter of its neighboring gene, Id2, in group 1 ILCs. Moreover, the Rroid locus, but not the lncRNA itself, controlled the identity and function of ILC1s by promoting chromatin accessibility and deposition of STAT5 at the promoter of Id2 in response to interleukin (IL)-15. Thus, non-coding elements responsive to extracellular cues unique to each ILC subset represent a key regulatory layer for controlling the identity and function of ILCs.
Indexed as
Gene Expression RegulationRegulatory Sequences, Nucleic AcidAnimalsCell DifferentiationCell LineageChromatin Assembly and DisassemblyFemaleGene Expression ProfilingGenetic LociHomeostasisImmunity, InnateInhibitor of Differentiation Protein 2Killer Cells, NaturalLymphocytesLymphocyte SubsetsMaleInhibitor of Differentiation Protein 2RNA, Long NoncodingSTAT5 Transcription FactorId2ILC1innate lymphoid cellslineage identitylncRNAtranscriptional regulation
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