Cited by 352T-cell and B-cell ImmunologyCancer Immunotherapy and BiomarkersImmune cells in cancer

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PD-1hi Identifies a Novel Regulatory B-cell Population in Human Hepatoma That Promotes Disease Progression

Xiao, Xiao, Lao, Xiang-Ming, Chen, Min-Min, Liu, Rui-Xian, Wei, Yuan, Ouyang, Fang-Zhu, Chen, Dong-Ping, Zhao, Xiao-Yu, Zhao, Qiyi, Li, Xue-Feng, Liu, Chuan-Lu, Zheng, Limin, Kuang, Dong-Ming·2016·Cancer Discovery

DOI 10.1158/2159-8290.cd-15-1408

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Abstract

UNLABELLED: B cells often constitute abundant cellular components in human tumors. Regulatory B cells that are functionally defined by their ability to produce IL10 downregulate inflammation and control T-cell immunity. Here, we identified a protumorigenic subset of B cells that constitutively expressed higher levels of programmed cell death-1 (PD-1) and constituted ∼10% of all B cells in advanced-stage hepatocellular carcinoma (HCC). These PD-1(hi) B cells exhibited a unique CD5(hi)CD24(-/+)CD27(hi/+)CD38(dim) phenotype different from the phenotype of conventional CD24(hi)CD38(hi) peripheral regulatory B cells. TLR4-mediated BCL6 upregulation was crucial for PD-1(hi) B-cell induction by HCC environmental factors, and that effect was abolished by IL4-elicited STAT6 phosphorylation. Importantly, upon encountering PD-L1(+) cells or undergoing PD-1 triggering, PD-1(hi) B cells acquired regulatory functions that suppressed tumor-specific T-cell immunity and promoted cancer growth via IL10 signals. Our findings provide significant new insights for human cancer immunosuppression and anticancer therapies regarding PD-1/PD-L1. SIGNIFICANCE: We identify a novel protumorigenic PD-1(hi) B-cell subset in human HCC that exhibits a phenotype distinct from that of peripheral regulatory B cells. TLR4-mediated BCL6 upregulation is critical for induction of PD-1(hi) B cells, which operate via IL10-dependent pathways upon interacting with PD-L1 to cause T-cell dysfunction and foster disease progression. Cancer Discov; 6(5); 546-59. ©2016 AACR.See related commentary by Ren et al., p. 477This article is highlighted in the In This Issue feature, p. 461.

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Authors: Xiao, X., Lao, X.-M., Chen, M.-M., Liu, R.-X., Wei, Y., Ouyang, F.-Z., Chen, D.-P., Zhao, X.-Y., Zhao, Q., Li, X.-F., Liu, C.-L., Zheng, L., & Kuang, D.-M.
Affiliations: 1Key Laboratory of Gene Engineering of the Ministry of Education, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
Sun Yat-sen University Cancer Center (CN)
Sun Yat-sen University (CN)
ORCID: Lao, Xiang-Ming
Chen, Dong-Ping
Zhao, Qiyi
Zheng, Limin
Kuang, Dong-Ming
Venue: Cancer Discovery
Publisher: American Association for Cancer Research (AACR)
Published: 2016-05-01
Volume: 6
Issue: 5
Pages: 546-559
ISSN: 2159-8274 (ISSN-L)
2159-8290
DOI: 10.1158/2159-8290.cd-15-1408
OpenAlex: W2295125580
Cited by: 352
References: 46
Citations by year: 2026: 23 · 2025: 42 · 2024: 37 · 2023: 35 · 2022: 46 · 2021: 57 · 2020: 35 · 2019: 34 · 2018: 20 · 2017: 13 · 2016: 10
FWCI: 15.44
Type: journal article
Language: en
Open access: closed
Locations: Cancer Discovery (publishedVersion)
PubMed (publishedVersion)
Funders: National Natural Science Foundation of China (81422036, 31470855, 81171982)
Guangdong Natural Science Funds for Distinguished Young Scholars (S2013050014639)
Doctoral Dissertation of PR China (201230)
Fundamental Research Funds for the Central Universities (15lgjc09)
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 › Immune cells in cancer
Keywords: regulatory B cells, hepatocellular carcinoma, PD-L1, TLR4, BCL6, IL-10, STAT6, tumor immunosuppression, T cell suppression, B-cell phenotype, cancer immunotherapy
MeSH terms: Animals, Disease Models, Animal, Flow Cytometry, Hepatitis B, Hepatitis C, Carcinoma, Hepatocellular, Humans, Liver Neoplasms, Neoplasm Staging, Phenotype, Protein Binding, Recurrence, Signal Transduction, Biomarkers, Gene Expression, Immunophenotyping, Cytokines, Lymphocytes, Tumor-Infiltrating, Disease Progression, Cell Line, Tumor, STAT6 Transcription Factor, Mice, Proto-Oncogene Proteins c-bcl-6, Immunomodulation, B-Lymphocytes, Regulatory, B7-H1 Antigen, Programmed Cell Death 1 Receptor, Heterografts

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PD-1hi Identifies a Novel Regulatory B-cell Population in Human Hepatoma That Promotes Disease Progression

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