Cited by 211T-cell and B-cell ImmunologyGenomics and Chromatin DynamicsPsoriasis: Treatment and Pathogenesis

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The Transcription Factor Runx3 Establishes Chromatin Accessibility of cis-Regulatory Landscapes that Drive Memory Cytotoxic T Lymphocyte Formation

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Wang, Dapeng, Diao, Huitian, Getzler, Adam J., Rogal, Walter, Frederick, Megan A., Milner, Justin, Yu, Bingfei, Crotty, Shane, Goldrath, Ananda W., Pipkin, Matthew E.·2018·Immunity

DOI 10.1016/j.immuni.2018.03.028PMC PMC6750808

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Abstract

T cell receptor (TCR) stimulation of naive CD8+ T cells initiates reprogramming of cis-regulatory landscapes that specify effector and memory cytotoxic T lymphocyte (CTL) differentiation. We mapped regions of hyper-accessible chromatin in naive cells during TCR stimulation and discovered that the transcription factor (TF) Runx3 promoted accessibility to memory CTL-specific cis-regulatory regions before the first cell division and was essential for memory CTL differentiation. Runx3 was specifically required for accessibility to regions highly enriched with IRF, bZIP and Prdm1-like TF motifs, upregulation of TFs Irf4 and Blimp1, and activation of fundamental CTL attributes in early effector and memory precursor cells. Runx3 ensured that nascent CTLs differentiated into memory CTLs by preventing high expression of the TF T-bet, slowing effector cell proliferation, and repressing terminal CTL differentiation. Runx3 overexpression enhanced memory CTL differentiation during iterative infections. Thus, Runx3 governs chromatin accessibility during TCR stimulation and enforces the memory CTL developmental program.

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Authors: Wang, D., Diao, H., Getzler, A. J., Rogal, W., Frederick, M. A., Milner, J., Yu, B., Crotty, S., Goldrath, A. W., & Pipkin, M. E.
Affiliations: Scripps Research Institute (US)
University of California San Diego (US)
La Jolla Institute for Immunology (US)
Corresponding author: Pipkin, Matthew E.
ORCID: Wang, Dapeng
Diao, Huitian
Getzler, Adam J.
Frederick, Megan A.
Milner, Justin
Yu, Bingfei
Crotty, Shane
Goldrath, Ananda W.
Pipkin, Matthew E.
Venue: Immunity
Publisher: Elsevier BV
Published: 2018-04
Volume: 48
Issue: 4
Pages: 659-674.e6
ISSN: 1074-7613 (ISSN-L)
DOI: 10.1016/j.immuni.2018.03.028
PMC: PMC6750808
OpenAlex: W2800450153
Cited by: 201
References: 55
Citations by year: 2026: 16 · 2025: 29 · 2024: 19 · 2023: 31 · 2022: 29 · 2021: 32 · 2020: 27 · 2019: 12 · 2018: 6
FWCI: 9.24
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 382 d)
Locations: Immunity (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: NIH (R01 AI095634, NIH U19 AI109976)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
Keywords: RUNX3, chromatin accessibility, cis-regulatory elements, T cell differentiation, T cell receptor stimulation, naive T cells, IRF4, Blimp-1, T-bet, effector T cells, transcription factor binding motifs, terminal differentiation
MeSH terms: Positive Regulatory Domain I-Binding Factor 1, Interferon Regulatory Factor-4, Animals, Binding Sites, Cell Differentiation, Cell Line, Chlorocebus aethiops, Chromatin, Enzyme Activation, Female, Cricetinae, Humans, Immunologic Memory, Male, Mice, Inbred C57BL, Receptors, Antigen, T-Cell, T-Lymphocytes, Cytotoxic, Vero Cells, Mice, Knockout, Cell Proliferation, Core Binding Factor Alpha 3 Subunit, Interferon Regulatory Factors, Mice

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The Transcription Factor Runx3 Establishes Chromatin Accessibility of cis-Regulatory Landscapes that Drive Memory Cytotoxic T Lymphocyte Formation

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