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Cited by 61T-cell and B-cell ImmunologyDevelopmental Biology and Gene RegulationGenomics and Chromatin Dynamics

Forging T-Lymphocyte Identity

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Rothenberg, Ellen V., Ungerbäck, Jonas, Champhekar, Ameya·2016·Advances in Immunology
DOI 10.1016/bs.ai.2015.09.002PMC PMC4747653
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Abstract

T-lymphocyte development branches off from other lymphoid developmental programs through its requirement for sustained environmental signals through the Notch pathway. In the thymus, Notch signaling induces a succession of T-lineage regulatory factors that collectively create the T-cell identity through distinct steps. This process involves both the staged activation of T-cell identity genes and the staged repression of progenitor-cell-inherited regulatory genes once their roles in self-renewal and population expansion are no longer needed. With the recent characterization of innate lymphoid cells (ILCs) that share transcriptional regulation programs extensively with T-cell subsets, T-cell identity can increasingly be seen as defined in modular terms, as the processes selecting and actuating effector function are potentially detachable from the processes generating and selecting clonally unique T-cell receptor structures. The developmental pathways of different classes of T cells and ILCs are distinguished by the numbers of prerequisites of gene rearrangement, selection, and antigen contact before the cells gain access to nearly common regulatory mechanisms for choosing effector function. Here, the major classes of transcription factors that interact with Notch signals during T-lineage specification are discussed in terms of their roles in these programs, the evidence for their spectra of target genes at different stages, and their cross-regulatory and cooperative actions with each other. Specific topics include Notch modulation of PU.1 and GATA-3, PU.1-Notch competition, the relationship between PU.1 and GATA-3, and the roles of E proteins, Bcl11b, and GATA-3 in guiding acquisition of T-cell identity while avoiding redirection to an ILC fate.

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  • The transition at commitment includes general downregulation of phase 1 genes and major reorganization of active chromatin and chromatin interactions genome-wide.

    “This is part of a general downregulation of stem/progenitor associated regulatory genes (“phase 1 genes”) (34, 43) and a major reorganization of active chromatin and chromatin interactions, genome-wide, that occurs during this transition (44).”

    From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [34]

  • The progression of cells through T-cell commitment involves the ordered downregulation of a substantial set of progenitor-specific Phase 1 transcription factors concomitant with the upregulation of T-lineage affiliated factors.

    “It has become clear that the progression of cells through T-cell commitment involves the ordered downregulation of a substantial set of progenitor-specific transcription factors, called “Phase 1” factors in this context, concomitant with the upregulation of T-lineage affiliated factors (34, 65, 84, 121, 122).”

    From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [34]

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References 243 · Cited by 61

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Authors
Rothenberg, E. V., Ungerbäck, J., & Champhekar, A.
Affiliations
  • California Institute of Technology (US)
  • Linköping University (SE)
  • University of California, Los Angeles (US)
Corresponding author
Rothenberg, Ellen V.
ORCID
Venue
Advances in Immunology
Publisher
Elsevier
Published
2016
Volume
129
Pages
109-174
ISSN
0065-2776 (ISSN-L)
DOI
10.1016/bs.ai.2015.09.002
PMC
PMC4747653
OpenAlex
W2273843457
Cited by
61
References
243
Citations by year
2025: 2 · 2024: 2 · 2023: 3 · 2022: 6 · 2021: 9 · 2020: 14 · 2019: 8 · 2018: 10 · 2017: 5 · 2016: 2
FWCI
13.22
Type
book chapter
Language
en
Open access
Licence
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations
  • Advances in immunology (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • CaltechAUTHORS (California Institute of Technology) (submittedVersion)
Funders
  • Linköpings Universitet
  • Vetenskapsrådet
  • U.S. Public Health Service
  • National Heart, Lung, and Blood Institute (HL119102, R01HL119102)
  • National Institute of Allergy and Infectious Diseases (R56AI083514, R01AI083514, R01AI095943, AI083514, AI095943)
  • Eunice Kennedy Shriver National Institute of Child Health and Human Development (R01HD076915, HD076915)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords
T cell development, Notch signaling, thymus, transcription factors, PU.1, GATA3, E protein, BCL11B, innate lymphoid cells, transcriptional regulation, effector function, T-cell receptor gene rearrangement, gene repression
MeSH terms
Animals, Cell Differentiation, Gene Expression Regulation, Humans, Transcription Factors, Transcription, Genetic, Signal Transduction, T-Lymphocyte Subsets, Receptors, Notch, Precursor Cells, T-Lymphoid, Cellular Microenvironment

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