TCF-1 promotes chromatin interactions across topologically associating domains in T cell progenitors

Wang, Wenliang; Chandra, Aditi; Goldman, Naomi; Yoon, Susan A.; Ferrari, Emily K.; Nguyen, Son C.; Joyce, Eric F.; Vahedi, Golnaz

doi:10.1038/s41590-022-01232-z

Cited by 50 publications

(25 citation statements)

References 79 publications

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“…Within the larger hierarchical structures, we found that innate and adaptive lymphocytes share high proportions of compartments and TADs that are largely stable throughout effector and memory differentiation. In support of our findings, previous studies in lymphocyte development suggest that higher-order structures are established as early as the common lymphoid progenitor (CLP) stage, with relatively little changes occurring after the CLP and during acute inflammatory response, consistent with the idea that the higher-order structures may be acting as a scaffold to facilitate cell type-specific functions 7,20,31,32 . However, how these larger structures are established during lymphocyte development and antiviral responses, and what factors shape the higher-order structures within innate and adaptive lymphocytes, warrant further investigation.…”

Section: Discussionsupporting

confidence: 91%

“…Therefore, to determine how the chromatin of innate and adaptive lymphocytes are rewired beyond the 1D genome, we subjected both Ly49H + NK cells and MCMV-specific CD8 + T cells at different time points following MCMV infection to HiC (Supp. during the development of various cell types 7,20 , it is unclear whether the A/B compartments of mature lymphocytes undergo similar changes during cell state transitions. To this end, we analyzed the A/B compartments from Ly49H + NK cells sorted from day 0, 2, 7, and 35 PI, as well as naïve CD8 + T cells (day 0) and MCMV-specific M45 H2-Db+ CD8 + T cells from day 7 and 35 PI.…”

Section: Innate Lymphocytes Undergo Coordinated Histone Remodeling Du...mentioning

confidence: 99%

“…5B). Indeed, these transcriptions factors have been implicated in regulating CD8 + T and NK cell development and functions 24,25 , and TCF7 itself has been shown to enforce chromatin interactions during T cell development by colocalizing with CTCF and recruiting NIPBL 20,26 .…”

Section: Chromatin Interactions Of Naïve Innate Versus Adaptive Lymph...mentioning

confidence: 99%

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3D Chromatin Dynamics during Innate and Adaptive Immune Memory Acquisition

Santosa

Lau

Şahin³

et al. 2023

Preprint

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Immune cells responding to pathogens undergo molecular changes that are intimately linked to genome organization. Recent work has demonstrated that natural killer (NK) and CD8+ T cells experience substantial transcriptomic and epigenetic rewiring during their differentiation from naive to effector to memory cells. Whether these molecular adaptations are accompanied by changes in three-dimensional (3D) chromatin architecture is unknown. In this study, we combine histone profiling, ATAC-seq, RNA-seq and high-throughput chromatin capture (HiC) assay to investigate the dynamics of one-dimensional (1D) and 3D chromatin during the differentiation of innate and adaptive lymphocytes. To this end, we discovered a coordinated 1D and 3D epigenetic remodeling during innate immune memory differentiation, and demonstrate that effector CD8+ T cells adopt an NK-like architectural program that is maintained in memory cells. Altogether, our study reveals the dynamic nature of the 1D and 3D genome during the formation of innate and adaptive immunological memory.

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Section: Discussionsupporting

confidence: 91%

Section: Innate Lymphocytes Undergo Coordinated Histone Remodeling Du...mentioning

confidence: 99%

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3D Chromatin Dynamics during Innate and Adaptive Immune Memory Acquisition

Santosa

Lau

Şahin³

et al. 2023

Preprint

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“…As PU.1 expression declines when pro-T cells progress from ETP to DN2b stages, many PU.1 binding sites lose chromatin accessibility; this supports a pivotal role of PU.1 in maintaining the Phase 1-preferential open chromatin regions (48). By contrast, many of the long-range loops near the T-identity genes appear to be dependent on other factors, which include TCF1, Bcl11b, and E2A (136,158,162). Thus, the epigenetic dynamics modulating gene network action are affected by both current trans-acting transcription factor activity and baseline cisregulatory chromatin states.…”

Section: Constraints On Network State Changes By Three-dimensional (3...mentioning

confidence: 98%

Multi-modular structure of the gene regulatory network for specification and commitment of murine T cells

Shin

Rothenberg

2023

Front. Immunol.

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T cells develop from multipotent progenitors by a gradual process dependent on intrathymic Notch signaling and coupled with extensive proliferation. The stages leading them to T-cell lineage commitment are well characterized by single-cell and bulk RNA analyses of sorted populations and by direct measurements of precursor-product relationships. This process depends not only on Notch signaling but also on multiple transcription factors, some associated with stemness and multipotency, some with alternative lineages, and others associated with T-cell fate. These factors interact in opposing or semi-independent T cell gene regulatory network (GRN) subcircuits that are increasingly well defined. A newly comprehensive picture of this network has emerged. Importantly, because key factors in the GRN can bind to markedly different genomic sites at one stage than they do at other stages, the genes they significantly regulate are also stage-specific. Global transcriptome analyses of perturbations have revealed an underlying modular structure to the T-cell commitment GRN, separating decisions to lose “stem-ness” from decisions to block alternative fates. Finally, the updated network sheds light on the intimate relationship between the T-cell program, which depends on the thymus, and the innate lymphoid cell (ILC) program, which does not.

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“…Wang et al demonstrated that TCF-1 and CTCF co-occupy recombined TAD boundaries during T-cell development, weakening the insulation between adjacent neighbors and enhancing the interaction between regulatory elements and target genes located on previously insulating domains. The promotion of chromatin interactions mediated by TCF-1 is associated with the deposition of the active enhancer marker H3K27ac and the recruitment of NIPBL [ 27 ]. What is more, Bansal et al indicated that in medullary thymic epithelial cells (mTECs), the transcription factor Aire controls immune tolerance by driving abundant gene expression and has broad effects on the organization of 3D chromatin structure [ 28 ].…”

Section: Protein Partners Of Ctcfmentioning

confidence: 99%

CTCF and Its Partners: Shaper of 3D Genome during Development

Sun

Zhang

Cao

2022

Genes

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The 3D genome organization and its dynamic modulate genome function, playing a pivotal role in cell differentiation and development. CTCF and cohesin, acting as the core architectural components involved in chromatin looping and genome folding, can also recruit other protein or RNA partners to fine-tune genome structure during development. Moreover, systematic screening for partners of CTCF has been performed through high-throughput approaches. In particular, several novel protein and RNA partners, such as BHLHE40, WIZ, MAZ, Aire, MyoD, YY1, ZNF143, and Jpx, have been identified, and these partners are mostly implicated in transcriptional regulation and chromatin remodeling, offering a unique opportunity for dissecting their roles in higher-order chromatin organization by collaborating with CTCF and cohesin. Here, we review the latest advancements with an emphasis on features of CTCF partners and also discuss the specific functions of CTCF-associated complexes in chromatin structure modulation, which may extend our understanding of the functions of higher-order chromatin architecture in developmental processes.

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TCF-1 promotes chromatin interactions across topologically associating domains in T cell progenitors

Cited by 50 publications

References 79 publications

3D Chromatin Dynamics during Innate and Adaptive Immune Memory Acquisition

3D Chromatin Dynamics during Innate and Adaptive Immune Memory Acquisition

Multi-modular structure of the gene regulatory network for specification and commitment of murine T cells

CTCF and Its Partners: Shaper of 3D Genome during Development

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