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pmid:33193087
Immune Cell Confrontation in the Papillary Thyroid Carcinoma Microenvironment.
Zhenyu Xie · Xin Li · Yuzhen He · Song Wu · Shiyue Wang · Jianjian Sun · Yuchen He · Yu Lun · Jian Zhang
Frontiers in endocrinology · 2020 doi:10.3389/fendo.2020.570604
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Complete file
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A systematic understanding of immune cell infiltration in PTC is essential for subsequent immune research and new diagnostic and therapeutic strategies.\nMethods: Three different algorithms, single-sample gene set enrichment analysis (ssGSEA), immune cell marker and CIBERSORT, were used to evaluate immune cell infiltration levels (abundance and proportion) in 10 data sets (The Cancer Genome Atlas [TCGA], GSE3467, GSE3678, GSE5364, GSE27155, GSE33630, GSE50901, GSE53157, GSE58545, and GSE60542; a total of 799 PTC and 194 normal thyroid samples). Consensus unsupervised clustering divided PTC patients into low-immunity and high-immunity groups. Weighted gene coexpression network analysis (WGCNA) and gene set enrichment analysis (GSEA) were used to analyze the potential mechanisms causing differences in the immune response.\nResults: Compared with normal tissues, PTC tissues had a higher overall immune level and higher abundance levels and proportions of M2 macrophages, Tregs, monocytes, neutrophils, dendritic cells (DCs), mast cells (MCs), and M0 macrophages. Compared with early PTC, advanced PTC showed higher immune infiltration and higher abundance levels and proportions of M2 macrophages, Tregs, monocytes, neutrophils, DCs, MCs, and M0 macrophages. Compared to the low-immunity group, the high-immunity group exhibited more advanced stages, larger tumor sizes, greater lymph node metastases, higher tall-cell PTCs, lower follicular PTC proportions, more BRAF mutations, and fewer RAS mutations. Epstein-Barr virus (EBV) infection was the most significantly enriched Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway for key module genes.\nConclusions: In human PTC, M2 macrophages, Tregs, monocytes, neutrophils, DCs, MCs, and M0 macrophages appear to play a tumor-promoting role, while M1 macrophages, CD8+ T cells, B cells, NK cells, and T follicular helper (TFH) cells (including eosinophils, γδ T cells, and Th17 cells with weak supporting evidence) appear to play an antitumor role. During the occurrence and development of PTC, the overall immune level was increased, and the abundance and proportion of tumor-promoting immune cells were significantly increased, indicating that immune escape had been aggravated. 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data", "References"], ["B cells", "• In DTCs, B cells were positively correlated with reduced tumor sizes.", "(26)"], ["TAMs", "• Macrophages are present in the immune environment of PTC and are significantly elevated in the BRAF V600E+ group.", "(27)"], ["• The density of macrophages in PTC tissues is significantly higher than that in normal tissues.", "(28, 29),"], ["• Compared with thyroid goiter and follicular adenoma, PTC tumors have significantly higher TAM densities.", "(30)"], ["• The expression of DCs MCs and macrophages in follicular variant of PTC (FVPTC) is higher than that in adenomas and may be involved in tumor development and invasion.", "(31)"], ["• TAM density is positively correlated with PTC stage, tumor size, lymph node metastasis, and distant metastases.", "(24, 29, 30, 32, 33)"], ["• In diffuse sclerosing variants of PTC (DSV-PTC), M2 TAMs are associated with lymphatic invasion.", "(34)"], ["• CXCL16 signaling mediates the effect of macrophages on PTC tumor cell invasion and changes the macrophage phenotype to M2 TAMs in the PTC microenvironment.", "(35)"], ["• In DTCs, TAMs are positively correlated with reduced tumor sizes and a favorable prognosis.", "(26)"], ["", "• High TAM density in PTC is associated with poor survival.", "(28)"], ["DCs", "• DCs are higher in papillary cancer tissues than in normal thyroid tissues, adenomas and other thyroid tumors.", "(36–31)"], ["• Immature DCs (iDCs) in PTC are difficult to induce T cell and NK cell-mediated responses, and they can even suppress immune responses by producing suppressive cytokines such as IL-10 and TGF-β.", "(37)"], ["• Tregs and pDCs together help tumor escape in patients with PTC plus nontoxic goiter (MNG).", "(38)"], ["• The expression of DCs, MCs, and macrophages in FVPTC is higher than that in adenomas and may be involved in tumor development and invasion.", "(31)"], ["• High CD1a+ DC density is associated with improved disease-free survival (DFS) of PTC.", "(39)"], ["• There is no significant correlation between DC density and DFS.", "(36)"], ["• DC immunotherapy can be used in patients with papillary or follicular TC without significant side effects.", "(40)"], ["MCs", "• MCs are recruited into PTC and promote the proliferation, survival and invasion of cancer cells, thereby promoting the growth and aggressiveness of PTC.", "(41)"], ["• Increased MC density in TC correlates with increased aggressiveness.", "(42)"], ["Neutrophils", "• NLR is not significantly increased in patients with PTC.", "(43)"], ["• NLR significantly increased in papillary thyroid microcarcinoma (PTMC) and TC patients.", "(44)"], ["• TC cells can recruit neutrophils by releasing CXCL8/IL-8. Additionally, in human TC samples, neutrophil density is related to tumor size and has a potential tumor-promoting effect.", "(45)"], ["• Elevated neutrophils in PTC can predict bilaterality and lymph node metastasis.", "(46)"], ["• Elevated NLR does not appear to be a reliable indicator of DTC progression.", "(47)"], ["• With the increase in the NLR value of PTC, the histopathological characteristics become worse and the clinical behavior becomes more aggressive.", "(48–49)"], ["• There is no significant association between preoperative NLR and prognostic factors in patients with PTC.", "(48, 50),"], ["• Elevated NLR is associated with a high risk of relapse. After treatment, those patients with low stage and good prognosis of DTC were observed to have a significant decrease in NLR.", "(51–53),"], ["• Higher NLR is associated with higher thyroglobulin levels in DTC, which indicates poorer survival.", "(54)"], ["NK cells", "• Compared with goiter and healthy thyroid, tumor-infiltrating NK cells increase in PTC, while no differences are found in peripheral blood NK cells.", "(55–57),"], ["• In PTC patients, NK cell infiltration is inversely related to the stage of the disease and plays a role of immune surveillance center by killing cancer cells.", "(56, 58–60),"], ["T cells", "• In PTC, CD8+ T cells kill tumor cells through cytotoxicity and are negatively related to tumor size and lymph node metastasis.", "(26, 60–62),"], ["• In PTC patients, CD8+ T cell infiltration is positively correlated with better prognosis.", "(26, 62, 63),"], ["• A study in patients with DTC showed that the combination of CD8+ cells enrichment and Cox-2 overexpression correlates with the highest risk of disease recurrence.", "(64)"], ["• In human PTC, lymphocyte density is associated with improved overall survival and reduced relapse.", "(65, 66),"], ["• In terms of CD4+ cell frequency, no difference was found between PTC and MNG patients.", "(38)"], ["• In DTC, the extent of tumor-infiltrating CD4+ cells does not seem to predict the patient’s prognosis.", "(64)"], ["• Compared with patients with thyroid adenoma, PTC patients have significantly increased CD4+ CD25+ regulatory T cells in the peripheral blood.", "(67)"], ["• Increased Treg infiltration is positively correlated with advanced PTC.", "(58–68)"], ["• FoxP3 expression in PTC is associated with extrathyroidal invasion and distant metastasis but has nothing to do with overall survival.", "(69)"], ["• Compared with healthy controls, Th17 levels in the peripheral blood and tissue samples of patients with PTC increased, and Th17 cells in the peripheral blood were negatively correlated with tumor size.", "(70)"]], "row_count": 41, "column_count": 3, "numeric_cells": 47, "header_rows": 1, "locator": "section[17]/table-wrap[1]#T1"}}, {"id": "asset:table:pmid:33193087:2", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:7ed51c09c4f0f456b16662fdaa0f4339ad746c7774c946a436a792bfbad8ec15", "bytes": 1653, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[22]/table-wrap[1]#T2", "version": null, "note": "Comparison of the clinical parameters between the H-immunity and L-immunity groups in PTC.", "structure": {"pmcid": "PMC7642595", "section_index": 22, "section_title": "Comparison of Clinical Characteristics Between the H-Immunity and L-Immunity Groups", "row_count": 44, "column_count": 4}, "table": {"label": "Table 2", "caption": "Comparison of the clinical parameters between the H-immunity and L-immunity groups in PTC.", "rows": [["Clinical parameters", "H-immunity (n = 293, %)", "L-immunity (n = 209, %)", "p-value"], ["Age (y)", "", "", ""], ["<55", "199 (67.9)", "136 (65.1)", "0.505"], ["≥55", "94 (32.1)", "73 (34.9)"], ["Gender", "", "", ""], ["Female", "215 (73.4)", "152 (72.7)", "0.871"], ["Male", "78 (26.6)", "57 (27.3)"], ["Stage", "", "", ""], ["I", "161 (54.9)", "120 (58.0)", "0.001"], ["II", "19 (6.5)", "33 (15.9)"], ["III", "76 (25.9)", "36 (17.4)"], ["IV", "37 (12.6)", "18 (8.7)"], ["NA", "0", "2", ""], ["Metastasis", "", "", ""], ["M0", "184 (97.9)", "98 (95.1)", "0.199"], ["M1", "4 (2.1)", "5 (4.9)"], ["NA", "105", "106", ""], ["N classification", "", "", ""], ["N0", "123 (43.9)", "106 (61.6)", "<0.001"], ["N1", "157 (56.1)", "66 (38.4)"], ["NA", "13", "37", ""], ["T classification", "", "", ""], ["T1", "87 (29.8)", "56 (26.9)", "0.018"], ["T2", "80 (27.4)", "84 (40.4)"], ["T3", "109 (37.3)", "61 (29.3)"], ["T4", "16 (5.5)", "7 (3.4)"], ["NA", "1", "1", ""], ["Radiation therapy", "", "", ""], ["Yes", "175 (62.7)", "130 (64.0)", "0.767"], ["No", "104 (37.3)", "73 (36.0)"], ["NA", "14", "6", ""], ["Pathological type", "", "", ""], ["Classical", "231 (78.8)", "125 (59.8)", "<0.001"], ["Follicular", "23 (7.8)", "78 (37.3)"], ["Tall cell", "35 (11.9)", "1 (0.5)"], ["Other", "4 (1.4)", "5 (2.4)"], ["BRAF", "", "", ""], ["Wild-type", "63 (22.4)", "132 (65.7)", "<0.001"], ["Mutated", "218 (77.6)", "69 (34.3)"], ["NA", "12", "8", ""], ["RAS", "", "", ""], ["Wild-type", "275 (97.9)", "147 (73.1)", "<0.001"], ["Mutated", "6 (2.1)", "54 (26.9)"], ["NA", "12", "8", ""]], "row_count": 44, "column_count": 4, "numeric_cells": 80, "header_rows": 1, "locator": "section[22]/table-wrap[1]#T2"}}], "gaps": ["asset:data:geo:GSE27155 not downloaded", "asset:data:geo:GSE27155 licence not read", "asset:data:geo:GSE33630 not downloaded", "asset:data:geo:GSE33630 licence not read", "asset:data:geo:GSE3467 not downloaded", "asset:data:geo:GSE3467 licence not read", "asset:data:geo:GSE3678 not 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