Cited by 101T-cell and B-cell ImmunologyGenomics and Chromatin DynamicsDevelopmental Biology and Gene Regulation

The DOI matches its Crossref record; 163 of the 228 references it cites were found in a registry or an index; 189 of the 244 sources its claims cite were checked for support.

Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development

Open access

Abstract

PU.1 is an ETS-family transcription factor that plays a broad range of roles in hematopoiesis. A direct regulator of myeloid, dendritic-cell, and B cell functional programs, and a well-known antagonist of terminal erythroid cell differentiation, it is also expressed in the earliest stages of T-cell development of each cohort of intrathymic pro-T cells. Its expression in this context appears to give T-cell precursors initial, transient access to myeloid and dendritic cell developmental competence and therefore to represent a source of antagonism or delay of T-cell lineage commitment. However, it has remained uncertain until recently why T-cell development is also intensely dependent upon PU.1. Here, we review recent work that sheds light on the molecular biology of PU.1 action across the genome in pro-T cells and identifies the genes that depend on PU.1 for their correct regulation. This work indicates modes of chromatin engagement, pioneering, and cofactor recruitment ("coregulator theft") by PU.1 as well as gene network interactions that not only affect specific target genes but also have system-wide regulatory consequences, amplifying the impact of PU.1 beyond its own direct binding targets. The genes directly regulated by PU.1 also suggest a far-reaching transformation of cell biology and signaling potential between the early stages of T-cell development when PU.1 is expressed and when it is silenced. These cell-biological functions can be important to distinguish fetal from adult T-cell development and have the potential to illuminate aspects of thymic function that have so far remained the most mysterious.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

PU.1 is transiently expressed in early pro-T cells, where it acts as a pioneer/cofactor-redistributing transcription factor that supports proliferation, delays commitment, and maintains a myeloid/dendritic-competence window constrained by Notch signaling. Its role is ontogenically scaled: largely dispensable in first-wave fetal T cells but important for later fetal and adult T-cell development.

Key findings

  • PU.1 binds >30,000 genomic sites in the earliest pro-T cells, declining to ~5,000 sites by T-lineage commitment; its motifs are highly enriched at chromatin sites that lose accessibility during commitment, and acute PU.1 deletion leaves many of these sites less open.
  • Within the T-cell pathway, PU.1 slows differentiation while supporting proliferation: PU.1-disrupted precursors underwent fewer cycles and a larger fraction progressed to DN3 over the same absolute time; high-confidence targets include activated genes such as Mef2c, Lmo2, Bcl11a, and Hhex, and repressed genes such as E2f2.
  • PU.1 directly regulates many signaling/cell-biology genes—cytokine receptors, chemokine receptors, tyrosine kinases, G-protein-coupled receptors, adhesion and cytoskeletal molecules—more than transcription factor genes, and can repress indirectly by “coregulator theft,” redistributing Runx1 and Satb1 away from other functional sites.
  • Ontogeny: first-wave fetal T cells tolerate ~5-fold reduced PU.1 almost unchanged, whereas later fetal hematopoietic stem/progenitor cells show severe T-cell defects; the PU.1 phase lasts >10 days in young adult thymocytes but may last only 1–2 days in many first-wave fetal thymocytes.

Methods

  • Review/synthesis of recent mouse T-cell development studies, mostly postnatal thymus or late fetal progenitors, using primary pro-T cells, OP9-DL1/DL4 stromal co-cultures, and the Scid.adh.2C2 pro-T-like cell line.
  • Gain- and loss-of-function perturbations: retroviral PU.1 overexpression, Cre-mediated Spi1 deletion, Cas9/sgRNA Spi1 disruption, and dominant-negative PU.1-ENG; readouts include ChIP-seq, ATAC-seq, transcriptome, proteomics, and GO/PANTHER pathway analyses.
  • High-confidence PU.1 target genes were defined as those showing reciprocal responses in gain- and loss-of-function perturbations within the DN2a–DN2b developmental interval.

Limitations

  • Stated: biochemical mechanisms of PU.1/Notch effects remain to be fully defined; PU.1 small-molecule inhibitors have not yet been tested in normal T-cell development; long PU.1 protein half-life and asynchronous deletion make loss-of-function effects weak at <2 days and confounded by developmental progression at later timepoints.
  • Stated: gain-of-function overexpression can inhibit Notch signaling and produce nonlinear, switch-like transdifferentiation, so some effects may be high-dose artifacts; Scid.adh.2C2 cells do not fully restore the ETP/DN2a chromatin landscape.
  • Evident: the review is largely based on mouse systems and in vitro cultures, which the authors note may lack normal thymic environmental molecules; PU.1-high early stages are rare and difficult to study directly in vivo.

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Integrity signals

Registry

Crossref · 10.3389/fimmu.2019.00228

Cites

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  • The paper relies on this without support.

    Developmentally potent transcription factors often transform a cell's identity by positively or negatively regulating the expression of other transcription factors.

    “Developmentally potent transcription factors often transform a cell's identity by positively or negatively regulating the expression of other transcription factors.”
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  1. Petrovick, 1998, Multiple functional domains of AML1: PU, 3915

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Metadata

Authors
Rothenberg, E. V., Hosokawa, H., & Ungerbäck, J.
Affiliations
California Institute of Technology (US)
Corresponding author
Rothenberg, Ellen V.
Venue
Frontiers in Immunology
Published
2019-02-20
Volume
10
Pages
228-228
ISSN
1664-3224 (ISSN-L)
OpenAlex
W2915813447
Cited by
99
References
228
Citations by year
2026: 11 · 2025: 16 · 2024: 15 · 2023: 16 · 2022: 9 · 2021: 16 · 2020: 9 · 2019: 7
FWCI
3.28
Type
journal article
Language
en
Open access
Locations
  • Frontiers in Immunology (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (submittedVersion, cc-by)
  • PubMed Central (submittedVersion, cc-by)
  • CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • U.S. Public Health Service (R01AI095943, R01HD076915)
  • Manpei Suzuki Diabetes Foundation
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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
PU.1, ETS transcription factors, T cell development, pro-T cells, T cell lineage commitment, coregulator recruitment, gene regulatory networks, thymus
MeSH terms
Proto-Oncogene Protein Spi-1, Animals, Cell Differentiation, Hematopoiesis, Humans, Proto-Oncogene Proteins, T-Lymphocytes, Transcription, Genetic, Trans-Activators, Hematopoietic Stem Cell Transplantation, Cell Lineage, Gene Regulatory Networks

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