Regulatory T-cell and neutrophil extracellular trap interaction contributes to carcinogenesis in non-alcoholic steatohepatitis
Open accessAbstract
Background & aims Regulatory T-cells (Tregs) impair cancer immunosurveillance by creating an immunosuppressive environment that fosters tumor cell survival. Our previous findings demonstrated that neutrophil extracellular traps (NETs), which are involved both in innate and adaptive immunity, are abundant in livers affected by non-alcoholic steatohepatitis (NASH). However, how NETs interact with Tregs in the development of NASH-associated hepatocellular carcinoma (NASH-HCC) is not known.Methods A choline-deficient, high-fat diet+diethylnitrosamine mouse model and the stelic animal model were utilized for NASH-HCC and a western diet mouse model was used for NASH development. Treg depletion was achieved using FoxP3-DTR mice. RNA sequencing was used to explore the mechanism by which NETs could regulate Treg differentiation. Bioenergetic analyses of naïve CD4+ T-cells were assessed by Seahorse.Results Although the absolute number of CD4+ T-cells is lower in NASH livers, the Treg subpopulation is selectively increased. Depleting Tregs dramatically inhibits HCC initiation and progression in NASH. There is a positive correlation between increased NET and hepatic Treg levels. RNA sequencing data reveals that NETs impact gene expression profiles in naïve CD4+ T-cells, with the most differentially expressed genes being those involved in mitochondrial oxidative phosphorylation. By facilitating mitochondrial respiration, NETs can promote Treg differentiation. Metabolic reprogramming of naïve CD4+ T-cells by NETs requires toll-like receptor 4. Blockade of NETs in vivo using Pad4-/- mice or DNase I treatment reduces the activity of Tregs.Conclusions Tregs can suppress immunosurveillance in the premalignant stages of NASH. NETs facilitate the crosstalk between innate and adaptive immunity in NASH by promoting Treg activity through metabolic reprogramming. Therapies targeting NETs and Treg interactions could offer a potential strategy for preventing HCC in patients with NASH.Lay summary Regulatory T-cells (Tregs) can promote tumor development by suppressing cancer immunosurveillance, but their role in carcinogenesis during non-alcoholic steatohepatitis (NASH) progression is unknown. Herein, we discovered that selectively increased intrahepatic Tregs can promote an immunosuppressive environment in NASH livers. Neutrophil extracellular traps (NETs) link innate and adaptive immunity by promoting Treg differentiation via metabolic reprogramming of naïve CD4+ T-cells. This mechanism could be targeted to prevent liver cancer in patients with NASH.
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The function of hepatic regulatory T cells in MASH has been examined only rarely, and the small number of existing studies report contradictory findings, with some suggesting disease worsening and others suggesting a protective homeostatic role.
“In contrast, the role of hepatic Tregs in MASH has been explored only sparingly, and the limited studies available yield conflicting results, some implicating these cells in disease exacerbation, others attributing to them a protective, homeostatic function (18, 19).”
From Regulatory T cells safeguard liver health during metabolic-associated steatohepatitis (2026) · cites this paper as [18]
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Experimental — accuracy not yet measuredRegulatory T (Treg) cells are increased in MASH-induced HCC and promote hepatocarcinogenesis by exerting immunosuppressive function.
“However, regulatory T (Treg) cells, a subset of CD4+ T cells, are increased in MASH-induced HCC and promote hepatocarcinogenesis by exerting immunosuppressive function [14].”
From Single-cell transcriptome reveals the reprogramming of immune microenvironment during the transition from MASH to HCC (2025) · cites this paper as [14]
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“In addition, neutrophil extracellular traps, which are abundant in livers affected by NASH, facilitates mitochondrial oxidative phosphorylation and, thus, differentiation of naïve CD4+ T cells into Tregs, which in turn impairs immunosurveillance of premalignant hepatocytes [24].”
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Regulatory T cells safeguard liver health during metabolic-associated steatohepatitis
Hanna, B. S., Langston, P. K., Marin-Rodero, M., Ramirez, R. N., Wan, M., Benoist, C., & Mathis, D. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2536314123 · Cited by 1 · see citing works
“Our results align with studies showing that ablation of Nr4a1 and Nr4a2 in T cells enhanced liver Treg accumulation and attenuated MASH pathology (19), but contrast with claims of a detrimental role for Tregs in MASH (18, 28).”
- Authors
- Wang, H., Zhang, H., Wang, Y., Brown, Z. J., Xia, Y., Huang, Z., Shen, C., Hu, Z., Beane, J., Ansa-Addo, E. A., Huang, H., Tian, D., & Tsung, A.
- Affiliations
- The Ohio State University Wexner Medical Center (US)
- Tongji Hospital (CN)
- Corresponding author
- Tian, Dean
- Tsung, Allan
- ORCID
- Venue
- Journal of Hepatology
- Publisher
- Elsevier BV
- Published
- 2021-12
- Volume
- 75
- Issue
- 6
- Pages
- 1271-1283
- ISSN
- 0168-8278 (ISSN-L)
- PMC
- PMC12888775
- OpenAlex
- W3191601662
- Cited by
- 398
- References
- 43
- Citations by year
- 2026: 66 · 2025: 92 · 2024: 104 · 2023: 75 · 2022: 53 · 2021: 8
- FWCI
- 22.48
- Type
- journal article
- Language
- en
- Open access
- green
- pmc.ncbi.nlm.nih.gov
- Locations
- Journal of Hepatology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- Funders
- National Institutes of Health (R01-CA214865, R01-GM95566)
- National Cancer Institute (P30 CA016058)
- National Natural Science Foundation of China (81974071)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › Neutrophil, Myeloperoxidase and Oxidative Mechanisms
- Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Keywords
- regulatory T cells, neutrophil extracellular traps, nonalcoholic steatohepatitis, tumor surveillance, immunosuppression, Treg differentiation, metabolic reprogramming, mitochondrial oxidative phosphorylation, TLR4, innate-adaptive immune crosstalk, choline-deficient high-fat diet, diethylnitrosamine
- MeSH terms
- Analysis of Variance, Animals, Disease Models, Animal, Ohio, T-Lymphocytes, Statistics, Nonparametric, Mice, Forkhead Transcription Factors, Carcinogenesis, Extracellular Traps, Non-alcoholic Fatty Liver Disease
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