Regulatory T cells inhibit acute IFN-γ synthesis without blocking T-helper cell type 1 (Th1) differentiation via a compartmentalized requirement for IL-10

Sojka, Dorothy K.; Fowell, Deborah J.

doi:10.1073/pnas.1110566108

Cited by 94T-cell and B-cell ImmunologyPsoriasis: Treatment and PathogenesisIL-33, ST2, and ILC Pathways

Regulatory T cells inhibit acute IFN-γ synthesis without blocking T-helper cell type 1 (Th1) differentiation via a compartmentalized requirement for IL-10

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Sojka, Dorothy K., Fowell, Deborah J.·2011·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.1110566108PMC PMC3215041

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Abstract

CD4 + CD25 + Forkhead box P3 (Foxp3) + regulatory T cells (Tregs) control immune responses to self and foreign antigens in secondary lymphoid organs and at tissue sites of inflammation. Tregs can modify the function of many immune cells and have been proposed to block early proliferation, differentiation, and effector function. Acute ablation of Tregs has revealed rapid cytokine production immediately after Treg removal, suggesting that Tregs may regulate effector function acutely rather than regulating the programming for immune function. We developed in vitro and in vivo models that enabled the direct test of Treg regulation of T-helper cell type 1 (Th1) differentiation. CD28 signaling is known to abrogate Treg suppression of IL-2 secretion and proliferation, but our studies show that Treg suppression of IFN-γ during Th1 priming proceeds despite enhanced CD28 signaling. Importantly, during Th1 differentiation, Tregs inhibited early IFN-γ transcription without disrupting expression of Th1-specific T-box transcription factor (Tbet) and Th1 programming. Acute shutoff of effector cytokine production by Tregs was selective for IFN-γ but not TNF-α and was independent of TGF-β and Epstein-Barr virus-induced gene 3. In vivo, Tregs potently controlled CD4 IFN-γ and CD4 effector cell expansion in the lymph node (four- to fivefold reduction) but not Th1 programming, independent of IL-10. Tregs additionally reduced CD4 IFN-γ in the inflamed dermis (twofold reduction) dependent on their production of IL-10. We propose a model for Treg inhibition of effector function based on acute cytokine regulation. Interestingly, Tregs used different regulatory mechanisms to regulate IFN-γ (IL-10–dependent or –independent) subject to the target T-cell stage of activation and its tissue location.

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Treg depletion is expected to promote a chronic low-grade inflammatory milieu characterized by elevated interferon γ, and such a cytokine environment is well-suited to sustain T-bet+ ABC-like populations.
“their depletion is expected to promote a chronic low-grade inflammatory milieu characterized by elevated interferon γ [69], such a cytokine environment is well-suited to sustain T-bet+ ABC-like populations [70].”
From PLCγ2 deficiency compromises systemic immune tolerance and erodes myelin homeostasis while enhancing oxidative metabolism in the mouse brain (2026) · cites this paper as [69]
The Abstract and Discussion report that Tregs suppress IFN-γ and that IFN-γ can be produced rapidly after Treg depletion. They address acute cytokine regulation, not a chronic low-grade inflammatory milieu. The ABC-like population claim is attached to a different citation and is not assessed here. (LLM, conf=0.86)
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Authors: Sojka, D. K., & Fowell, D. J.
Affiliations: University of Rochester Medicine (US)
ORCID: Sojka, Dorothy K.
Fowell, Deborah J.
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2011-10-24
Volume: 108
Issue: 45
Pages: 18336-18341
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.1110566108
PMC: PMC3215041
OpenAlex: W2077926649
Cited by: 93
References: 41
Citations by year: 2026: 3 · 2025: 8 · 2024: 7 · 2023: 4 · 2022: 3 · 2021: 5 · 2020: 7 · 2019: 6 · 2018: 3 · 2017: 7 · 2016: 4 · 2015: 4 · 2014: 12 · 2013: 10 · 2012: 10
FWCI: 4.52
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Allergy and Infectious Diseases (R01AI070826)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Keywords: regulatory T cells, Foxp3, interferon-gamma, Th1 differentiation, IL-10, CD28 signaling, Treg suppressive function, cytokine regulation, T-bet, CD4+ T cells, lymph nodes, TNF-α, TGF-beta
MeSH terms: Animals, Cell Compartmentation, Cell Differentiation, Flow Cytometry, T-Lymphocytes, Helper-Inducer, Interferon-gamma, Mice, Inbred BALB C, Mice, Inbred C57BL, Interleukin-10, Cell Lineage, T-Lymphocytes, Regulatory, Mice

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Regulatory T cells inhibit acute IFN-γ synthesis without blocking T-helper cell type 1 (Th1) differentiation via a compartmentalized requirement for IL-10

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