Advanced search
Publication Cover
OncoImmunology Volume 13, 2024 - Issue 1
Submit an article Journal homepage
1,067
Views
0
CrossRef citations to date
0
Altmetric
Original Research

Lymphatic endothelial cell-mediated accumulation of CD177+Treg cells suppresses antitumor immunity in human esophageal squamous cell carcinoma

Min Maa Chronic Disease Laboratory, School of Medicine South China University of Technology, Guangzhou, China;b Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Liang Lic Medical Research Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0003-0745-2571View further author information
ORCID Icon,
Shu-Han Yangb Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Chuan Huanga Chronic Disease Laboratory, School of Medicine South China University of Technology, Guangzhou, China;b Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Weitao Zhuangd Department of Thoracic Surgery, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Shujie Huangd Department of Thoracic Surgery, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Xin Xiad Department of Thoracic Surgery, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Yong Tangd Department of Thoracic Surgery, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Zijun Lie Guangdong Provincial Institute of Geriatrics, Concord Medical Center, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Zhi-Bin Zhaoc Medical Research Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Qingyun Chenc Medical Research Institute, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaView further author information
,
Guibin Qiaod Department of Thoracic Surgery, Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaCorrespondence[email protected]
View further author information
&
Zhe-Xiong Liana Chronic Disease Laboratory, School of Medicine South China University of Technology, Guangzhou, China;b Guangdong Provincial People’s Hospital (Guangdong Academy of Medical Sciences), Southern Medical University, Guangzhou, ChinaCorrespondence[email protected]
ORCID Iconhttps://orcid.org/0000-0002-9525-1421View further author information
ORCID Icon show all
Article: 2327692 | Received 06 Oct 2023, Accepted 04 Mar 2024, Published online: 20 Mar 2024

References

  • Lu CL, Lang H-C, Luo J-C, Liu C-C, Lin H-C, Chang F-Y, Lee S-D. Increasing trend of the incidence of esophageal squamous cell carcinoma, but not adenocarcinoma, in Taiwan. Cancer Causes Control. 2010;21(2):269–16. doi:10.1007/s10552-009-9458-0.
  • Zheng S, Liu B, Guan X. The role of tumor microenvironment in invasion and metastasis of esophageal squamous cell carcinoma. Front Oncol. 2022;12:911285. doi:10.3389/fonc.2022.911285.
  • Vinay DS, Ryan EP, Pawelec G, Talib WH, Stagg J, Elkord E, Lichtor T, Decker WK, Whelan RL, Kumara HMCS. et al. Immune evasion in cancer: mechanistic basis and therapeutic strategies. Semin Cancer Biol. 2015;35:S185–S198. doi:10.1016/j.semcancer.2015.03.004.
  • Wing JB, Tanaka A, Sakaguchi S. Human FOXP3(+) regulatory T cell heterogeneity and function in autoimmunity and cancer. Immunity. 2019;50(2):302–316. doi:10.1016/j.immuni.2019.01.020.
  • Villarreal DO, L’Huillier A, Armington S, Mottershead C, Filippova EV, Coder BD, Petit RG, Princiotta MF. Targeting CCR8 induces protective antitumor immunity and enhances vaccine-induced responses in colon cancer. Cancer Res. 2018;78(18):5340–5348. doi:10.1158/0008-5472.CAN-18-1119.
  • Kamada T, Togashi Y, Tay C, Ha D, Sasaki A, Nakamura Y, Sato E, Fukuoka S, Tada Y, Tanaka A. et al. PD-1 + regulatory T cells amplified by PD-1 blockade promote hyperprogression of cancer. Proc Natl Acad Sci U S A. 2019;116(20):9999–10008. doi:10.1073/pnas.1822001116.
  • Fourcade J, Sun Z, Chauvin J-M, Ka M, Davar D, Pagliano O, Wang H, Saada S, Menna C, Amin R. et al. CD226 opposes TIGIT to disrupt Tregs in melanoma. JCI Insight. 2018;3(14). doi:10.1172/jci.insight.121157.
  • Jie HB, Gildener-Leapman N, Li J, Srivastava RM, Gibson SP, Whiteside TL, Ferris RL. Intratumoral regulatory T cells upregulate immunosuppressive molecules in head and neck cancer patients. Br J Cancer. 2013;109(10):2629–2635. doi:10.1038/bjc.2013.645.
  • Miquelotti LB, Sari MHM, Ferreira LM. Immunotherapy in cancer management: a literature review of clinical efficacy of pembrolizumab in the non-small cell lung cancer treatment. Adv Pharm Bull. 2023;13(1):88–95. doi:10.34172/apb.2023.007.
  • Stafford M, Kaczmar J. The neoadjuvant paradigm reinvigorated: a review of pre-surgical immunotherapy in HNSCC. Cancers Head Neck. 2020;5(1):4. doi:10.1186/s41199-020-00052-8.
  • Steven A, Fisher SA, Robinson BW. Immunotherapy for lung cancer. Respirology. 2016;21(5):821–33. doi:10.1111/resp.12789.
  • Debien V, De Caluwé A, Wang X, Piccart-Gebhart M, Tuohy VK, Romano E, Buisseret L. Immunotherapy in breast cancer: an overview of current strategies and perspectives. NPJ Breast Cancer. 2023;9(1):7. doi:10.1038/s41523-023-00508-3.
  • Shi MW, Huang J, Sun Y. Neoadjuvant immunotherapy for head and neck squamous cell carcinoma: expecting its application in temporal bone squamous cell carcinoma. Curr Med Sci. 2023;43(2):213–222. doi:10.1007/s11596-023-2700-2.
  • Zhang X, Zhang C, Hou H, Zhang Y, Jiang P, Zhou H, Wang L, Zhou N, Zhang X. Neoadjuvant PD-1 blockade plus chemotherapy versus chemotherapy alone in locally advanced stage II-III gastric cancer: a single-centre retrospective study. Transl Oncol. 2023;31:101657. doi:10.1016/j.tranon.2023.101657.
  • Yang Y, Li H, Chen X, Qin J, Li Y, Shen Y, Zhang R, Kang X, Wang Z, Zheng Q. et al. Comparison of neoadjuvant nab-paclitaxel plus immunotherapy versus paclitaxel plus immunotherapy for esophageal squamous cell carcinoma. Thorac Cancer. 2023;14(7):700–708. doi:10.1111/1759-7714.14795.
  • Wang K, Liang Y, Huang J, Xie X, Wu D, Chen B, Wang K, Shen Z, Li Y, Wang W. et al. A propensity score–matched analysis of neoadjuvant chemoimmunotherapy versus surgery alone for locally advanced esophageal squamous cell carcinoma. J Surg Oncol. 2023;128(2):207–217. doi:10.1002/jso.27277.
  • Ge F, Huo Z, Cai X, Hu Q, Chen W, Lin G, Zhong R, You Z, Wang R, Lu Y. et al. Evaluation of clinical and safety outcomes of neoadjuvant immunotherapy combined with chemotherapy for patients with resectable esophageal cancer: a systematic review and meta-analysis. JAMA Netw Open. 2022;5(11):e2239778. doi:10.1001/jamanetworkopen.2022.39778.
  • Yilmaz M, Akovali B. Hyperprogression after nivolumab for melanoma: a case report. J Oncol Pharm Pract. 2020;26(1):244–251. doi:10.1177/1078155219845436.
  • Wakiyama H, Kato T, Furusawa A, Okada R, Inagaki F, Furumoto H, Fukushima H, Okuyama S, Choyke PL, Kobayashi H. et al. Treg-dominant tumor microenvironment is responsible for hyperprogressive disease after PD-1 blockade therapy. Cancer Immunol Res. 2022;10(11):1386–1397. doi:10.1158/2326-6066.CIR-22-0041.
  • Kashef J, Franz CM. Quantitative methods for analyzing cell-cell adhesion in development. Dev Biol. 2015;401(1):165–174. doi:10.1016/j.ydbio.2014.11.002.
  • Zhang X, Peng L, Luo Y, Zhang S, Pu Y, Chen Y, Guo W, Yao J, Shao M, Fan W. et al. Dissecting esophageal squamous-cell carcinoma ecosystem by single-cell transcriptomic analysis. Nat Commun. 2021;12(1):5291. doi:10.1038/s41467-021-25539-x.
  • Zheng L, Qin S, Si W, Wang A, Xing B, Gao R, Ren X, Wang L, Wu X, Zhang J. et al. Pan-cancer single-cell landscape of tumor-infiltrating T cells. Science. 2021;374(6574):abe6474. doi:10.1126/science.abe6474.
  • Luoma AM, Suo S, Wang Y, Gunasti L, Porter CBM, Nabilsi N, Tadros J, Ferretti AP, Liao S, Gurer C. et al. Tissue-resident memory and circulating T cells are early responders to pre-surgical cancer immunotherapy. Cell. 2022;185(16):2918–2935 e29. doi:10.1016/j.cell.2022.06.018.
  • Hao Y, Hao S, Andersen-Nissen E, Mauck WM, Zheng S, Butler A, Lee MJ, Wilk AJ, Darby C, Zager M. et al. Integrated analysis of multimodal single-cell data. Cell. 2021;184(13):3573–3587 e29. doi:10.1016/j.cell.2021.04.048.
  • Stuart T, Butler A, Hoffman P, Hafemeister C, Papalexi E, Mauck WM, Hao Y, Stoeckius M, Smibert P, Satija R. Comprehensive Integration of single-cell data. Cell. 2019;177(7):1888–1902 e21. doi:10.1016/j.cell.2019.05.031.
  • Butler A, Hoffman P, Smibert P, Papalexi E, Satija R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat Biotechnol. 2018;36(5):411–420. doi:10.1038/nbt.4096.
  • Wu T, Hu E, Xu S, Chen M, Guo P, Dai Z, Feng T, Zhou L, Tang W, Zhan L. et al. clusterProfiler 4.0: a universal enrichment tool for interpreting omics data. Innov. 2021;2(3):100141. doi:10.1016/j.xinn.2021.100141.
  • Yu G, Wang L-G, Han Y, He Q-Y. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics. 2012;16(5):284–287. doi:10.1089/omi.2011.0118.
  • Trapnell C, Cacchiarelli D, Grimsby J, Pokharel P, Li S, Morse M, Lennon NJ, Livak KJ, Mikkelsen TS, Rinn JL. et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat Biotechnol. 2014;32(4):381–386. doi:10.1038/nbt.2859.
  • Borcherding N, Bormann NL, Kraus G. scRepertoire: an R-based toolkit for single-cell immune receptor analysis. F1000Res. 2020;9:47. doi:10.12688/f1000research.22139.1.
  • Liu W, Xie L, He Y-H, Wu Z-Y, Liu L-X, Bai X-F, Deng D-X, Xu X-E, Liao L-D, Lin W. et al. Large-scale and high-resolution mass spectrometry-based proteomics profiling defines molecular subtypes of esophageal cancer for therapeutic targeting. Nat Commun. 2021;12(1):4961. doi:10.1038/s41467-021-25202-5.
  • Gerner MC, Ziegler LS, Schmidt RLJ, Krenn M, Zimprich F, Uyanik‐Ünal K, Konstantopoulou V, Derdak S, Del Favero G, Schwarzinger I. et al. The TGF-b/SOX4 axis and ROS-driven autophagy co-mediate CD39 expression in regulatory T-cells. FASEB J. 2020;34(6):8367–8384. doi:10.1096/fj.201902664.
  • Watanabe N, Mo F, Zheng R, Ma R, Bray VC, van Leeuwen DG, Sritabal-Ramirez J, Hu H, Wang S, Mehta B. et al. Feasibility and preclinical efficacy of CD7-unedited CD7 CAR T cells for T cell malignancies. Mol Ther. 2023;31(1):24–34. doi:10.1016/j.ymthe.2022.09.003.
  • Zheng Y, Josefowicz SZ, Kas A, Chu T-T, Gavin MA, Rudensky AY. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature. 2007;445(7130):936–940. doi:10.1038/nature05563.
  • Bai M, Grieshaber-Bouyer R, Wang J, Schmider AB, Wilson ZS, Zeng L, Halyabar O, Godin MD, Nguyen HN, Levescot A. et al. CD177 modulates human neutrophil migration through activation-mediated integrin and chemoreceptor regulation. Blood. 2017;130(19):2092–2100. doi:10.1182/blood-2017-03-768507.
  • Kim MC, Borcherding N, Ahmed KK, Voigt AP, Vishwakarma A, Kolb R, Kluz PN, Pandey G, De U, Drashansky T. et al. CD177 modulates the function and homeostasis of tumor-infiltrating regulatory T cells. Nat Commun. 2021;12(1):5764. doi:10.1038/s41467-021-26091-4.
  • Plitas G, Konopacki C, Wu K, Bos PD, Morrow M, Putintseva E, Chudakov D, Rudensky A. Regulatory T cells exhibit distinct features in human breast cancer. Immunity. 2016;45(5):1122–1134. doi:10.1016/j.immuni.2016.10.032.
  • Zheng Y, Chen Z, Han Y, Han L, Zou X, Zhou B, Hu R, Hao J, Bai S, Xiao H. et al. Immune suppressive landscape in the human esophageal squamous cell carcinoma microenvironment. Nat Commun. 2020;11(1):6268. doi:10.1038/s41467-020-20019-0.
  • Lowther DE, Goods BA, Lucca LE, Lerner BA, Raddassi K, van Dijk D, Hernandez AL, Duan X, Gunel M, Coric V. et al. PD-1 marks dysfunctional regulatory T cells in malignant gliomas. JCI Insight. 2016;1(5):1(5. doi:10.1172/jci.insight.85935.
  • Sawant DV, Yano H, Chikina M, Zhang Q, Liao M, Liu C, Callahan DJ, Sun Z, Sun T, Tabib T. et al. Adaptive plasticity of IL-10(+) and IL-35(+) T(reg) cells cooperatively promotes tumor T cell exhaustion. Nat Immunol. 2019;20(6):724–735. doi:10.1038/s41590-019-0346-9.
  • Fridman WH, Meylan M, Petitprez F, Sun C-M, Italiano A, Sautès-Fridman C. B cells and tertiary lymphoid structures as determinants of tumour immune contexture and clinical outcome. Nat Rev Clin Oncol. 2022;19(7):441–457. doi:10.1038/s41571-022-00619-z.
  • Chen L, He Q, Zhai Y, Deng M. Single-cell RNA-seq data semi-supervised clustering and annotation via structural regularized domain adaptation. Bioinformatics. 2021;37(6):775–784. doi:10.1093/bioinformatics/btaa908.
  • Kumagai S, Koyama S, Itahashi K, Tanegashima T, Lin Y-T, Togashi Y, Kamada T, Irie T, Okumura G, Kono H. et al. Lactic acid promotes PD-1 expression in regulatory T cells in highly glycolytic tumor microenvironments. Cancer Cell. 2022;40(2):201–218 e9. doi:10.1016/j.ccell.2022.01.001.
  • Sachs UJ, Andrei-Selmer CL, Maniar A, Weiss T, Paddock C, Orlova VV, Choi EY, Newman PJ, Preissner KT, Chavakis T. et al. The neutrophil-specific antigen CD177 is a counter-receptor for platelet endothelial cell adhesion molecule-1 (CD31). J Biol Chem. 2007;282(32):23603–12. doi:10.1074/jbc.M701120200.
  • Saito T, Nishikawa H, Wada H, Nagano Y, Sugiyama D, Atarashi K, Maeda Y, Hamaguchi M, Ohkura N, Sato E. et al. Two FOXP3(+)CD4(+) T cell subpopulations distinctly control the prognosis of colorectal cancers. Nat Med. 2016;22(6):679–684. doi:10.1038/nm.4086.
  • Whiteside SK, Grant FM, Gyori DS, Conti AG, Imianowski CJ, Kuo P, Nasrallah R, Sadiyah F, Lira SA, Tacke F. et al. CCR8 marks highly suppressive Treg cells within tumours but is dispensable for their accumulation and suppressive function. Immunology. 2021;163(4):512–520. doi:10.1111/imm.13337.
  • Kidani Y, Nogami W, Yasumizu Y, Kawashima A, Tanaka A, Sonoda Y, Tona Y, Nashiki K, Matsumoto R, Hagiwara M. et al. CCR8-targeted specific depletion of clonally expanded Treg cells in tumor tissues evokes potent tumor immunity with long-lasting memory. Proc Natl Acad Sci USA. 2022;119(7). doi:10.1073/pnas.2114282119.
  • Zhu J, Wang Y, Li D, Zhang H, Guo Z, Yang X. Interleukin-35 promotes progression of prostate cancer and inhibits anti-tumour immunity. Cancer Cell Int. 2020;20(1):487. doi:10.1186/s12935-020-01583-3.
  • Dieterich LC, Tacconi C, Ducoli L, Detmar M. Lymphatic vessels in cancer. Physiol Rev. 2022;102(4):1837–1879. doi:10.1152/physrev.00039.2021.
  • Bayat B, Werth S, Sachs UJH, Newman DK, Newman PJ, Santoso S. Neutrophil transmigration mediated by the neutrophil-specific antigen CD177 is influenced by the endothelial S536N dimorphism of platelet endothelial cell adhesion molecule-1. J Immunol. 2010;184(7):3889–3896. doi:10.4049/jimmunol.0903136.
  • Marski M, Kandula S, Turner JR, Abraham C. CD18 is required for optimal development and function of CD4+CD25+ T regulatory cells. J Immunol. 2005;175(12):7889–7897. doi:10.4049/jimmunol.175.12.7889.
  • Singh K, Gatzka M, Peters T, Borkner L, Hainzl A, Wang H, Sindrilaru A, Scharffetter-Kochanek K. Reduced CD18 levels drive regulatory T cell conversion into Th17 cells in the CD18hypo PL/J mouse model of psoriasis. J Immunol. 2013;190(6):2544–2553. doi:10.4049/jimmunol.1202399.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.