Cited by 491T-cell and B-cell ImmunologyCancer Immunotherapy and BiomarkersImmunotherapy and Immune Responses

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Treg-expressed CTLA-4 depletes CD80/CD86 by trogocytosis, releasing free PD-L1 on antigen-presenting cells

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Tekguc, Murat, Wing, James Badger, Osaki, Motonao, Long, Jia, Sakaguchi, Shimon·2021·Proceedings of the National Academy of Sciences

DOI 10.1073/pnas.2023739118PMC PMC8325248

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Abstract

Significance Immunosuppressive Tregs constitutively express CTLA-4, an immune checkpoint receptor. Addressing the role of CTLA-4 in Treg-suppressive function, we show that Treg-expressed CTLA-4, even in the absence of its cytoplasmic portion, promoted the conjugation of Tregs and antigen-presenting cells (APCs), leading to CTLA-4–dependent trogocytosis of CD80/CD86 and concomitant transfer of membrane fragments from APCs to the Treg cell surface. The depletion or blockade of CD80 by trogocytosis or solubilized CTLA-4, respectively, increased free PD-L1 by disrupting cis-CD80/PD-L1 heterodimers on APCs. Thus, Tregs can exert dual suppressive effects through the limitation of CD80/CD86 and up-regulation of free PD-L1 on APCs. Cancer immunotherapy with anti–CTLA-4 and anti–PD-1/PD-L1 blocking antibodies may enhance tumor immunity by hindering this Treg-mediated immune suppression.

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Understanding the role of regulatory T cell-derived small extracellular vesicles in suppression of anti-tumor immune response: Key to advancing cancer immunotherapy
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“Co ‑ stimulatory interactions between APC and Treg were also frequently observed, including CD80_CD28, CD86_CD28 35,36 and ICOSLG_ICOS 37 , whichmay contribute to Treg ‑ mediated immune evasion.”
The Role of MicroRNAs in Treg‐Derived Extracellular Vesicles: A Narrative Review Focusing on Immune‐Related Diseases
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“Tregs exert suppressive effects via contact-dependent pathways (CTLA-4, PD-1/PD-L1, and CD25) [17, 24, 25] and cytokines (IL-10, TGF-β , and IL-35) [26 – 30], and by modulating extracellular adenosine (CD39/CD73) and cAMP [31 – 33].”
Reversing chemoresistance in ovarian cancer: network pharmacology reveals how hydroxychloroquine/sulfasalazine duotherapy remodels tumor inflammatory–immune microenvironment
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“Treg in ﬁ ltration predicts poor prognosis (68), synergistically enhancing immune evasion (69).”
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Influential
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“The inhibitory molecule (and exhaustion marker) CTLA-4 binds to CD80/86 and limits their surface expression on antigen-presenting cells, thereby depleting the CD28mediated costimulatory signaling in T cells to reduce their effector functions and contribution to the inflammatory environment.(14,15) Consistently, the ex…”
Background
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“For instance, CD80 and CD86 are significant indicators of clinical pathological grading and prognosis and are promising targets for immunotherapy [35].”
BackgroundMethodInfluential
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CTLA-4 regulates PD-L1-PD-1 interactions via transendocytosis of CD80Preprint
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BackgroundResultInfluential
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Background
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Convergence, plasticity, and tissue residence of regulatory T cell response via TCR repertoire prismPreprint
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“In addition to the CTLA-4 transendocytosis model, an alternative model of trogocytosis has also been proposed, in which CD80 and CD86 plus other membrane proteins such as CD40 and MHC class II are concomitantly transferred from APCs to the T R cell surface in a CTLA-4-dependent manner ( 56 ).”
Low expression of PRRG2 in kidney renal clear cell carcinoma: an immune infiltration-associated prognostic biomarker
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“CTLA4, a T-cell co-stimulatory molecule, primarily functions by binding with co-stimulatory molecules CD80/CD86, thereby inhibiting T-cell activity and weakening immune response [42], ultimately promoting tumor growth and metastasis [43].”
Background
Convergence, plasticity, and tissue residence of regulatory T cell response via TCR repertoire prismPreprint
Nakonechnaya, T. O., Moltedo, B., Putintseva, E. V., Leyn, S., Bolotin, D. A., Britanova, O. V., Shugay, M., & Chudakov, D. M. (2024) · eLife · doi:10.7554/elife.89382.2
Rigid, bivalent CTLA-4 binding to CD80 is required to disrupt the cis CD80 / PD-L1 interactionPreprint
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“…M monensin) and incubated for 8 hr at 37 � C. Intracellular interferon (IFN)- c levels from the mouse splenic CD8 þ or CD4 þ T-cells were characterized using an earlier-described flow cytometry protocol [with minor modification] (Latanova et al. 2018; Prompetchara et al. 2021; Tekguc et al. 2021).”
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Kawakami, R., Kitagawa, Y., & Sakaguchi, S. (2024) · Elsevier eBooks · doi:10.1016/b978-0-128-24465-4.00067-3
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Inducing and regulating human naive CD4+ T cell proliferation by different antigen presenting cells
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The role of prostanoids in regulatory T cells and their implications in inflammatory diseases and cancers
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Authors: Tekguc, M., Wing, J. B., Osaki, M., Long, J., & Sakaguchi, S.
Affiliations: Laboratory of Experimental Immunology, World Premier International (WPI) Immunology Frontier Research Center (IFReC), Osaka University, Suita 565-0871, Japan;
Immunology Frontier Research Center, The University of Osaka (JP)
Kyoto University (JP)
Corresponding author: Sakaguchi, Shimon
ORCID: Tekguc, Murat
Wing, James Badger
Osaki, Motonao
Long, Jia
Sakaguchi, Shimon
Venue: Proceedings of the National Academy of Sciences
Publisher: National Academy of Sciences
Published: 2021-07-23
Volume: 118
Issue: 30
ISSN: 0027-8424 (ISSN-L)
1091-6490
DOI: 10.1073/pnas.2023739118
PMC: PMC8325248
OpenAlex: W3185714107
Cited by: 490
References: 53
Citations by year: 2026: 116 · 2025: 123 · 2024: 114 · 2023: 72 · 2022: 61 · 2021: 4
FWCI: 23.46
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.pnas.org/site/aboutpnas/licenses.xhtml (vor, 184 d)
Locations: Proceedings of the National Academy of Sciences (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
OUKA (Osaka University Knowledge Archive) (Osaka University) (submittedVersion)
Funders: MEXT | Japan Society for the Promotion of Science (16H06295, 18K07175)
MEXT | JST | Core Research for Evolutional Science and Technology (JP 19gm0010005)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords: regulatory T cells, CTLA-4, trogocytosis, CD80, CD86, PD-L1, antigen-presenting cells, immune checkpoint, cancer immunotherapy
MeSH terms: Trogocytosis, Animals, Antigen-Presenting Cells, Dendritic Cells, Female, Lymphocyte Activation, Mice, Inbred BALB C, Mice, Inbred C57BL, B7-1 Antigen, Mice, Knockout, T-Lymphocytes, Regulatory, Mice, B7-2 Antigen, B7-H1 Antigen, CTLA-4 Antigen

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Treg-expressed CTLA-4 depletes CD80/CD86 by trogocytosis, releasing free PD-L1 on antigen-presenting cells

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