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pmid:31612115
Identification of a Nine-Gene Signature and Establishment of a Prognostic Nomogram Predicting Overall Survival of Pancreatic Cancer.
Mengwei Wu · Xiaobin Li · Taiping Zhang · Ziwen Liu · Yupei Zhao
Frontiers in oncology · 2019 doi:10.3389/fonc.2019.00996
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Complete file
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Materials and Methods: Seven datasets of mRNA expression and clinical data were obtained from gene expression omnibus (GEO) database. Level 3 mRNA expression and clinicopathological data were obtained from The Cancer Genome Atlas pancreatic ductal adenocarcinoma (TCGA-PAAD) dataset. Differentially expressed genes (DEGs) between pancreatic tumor and normal tissue were identified by integrated analysis of multiple GEO datasets. Univariate and Lasso Cox regression analyses were applied to identify overall survival-related DEGs and establish a prognostic gene signature whose performance was evaluated by Kaplan-Meier curve, receiver operating characteristic (ROC), Harrell's concordance index (C-index) and calibration curve. GSE62452 and GSE57495 were used for external validation. Gene set enrichment analysis (GSEA) and tumor immunity analysis were applied to elucidate the molecular mechanisms and immune relevance. Multivariate Cox regression analysis was used to identify independent prognostic factors in pancreatic cancer. Finally, a prognostic nomogram was established based on the TCGA PAAD dataset. Results: A nine-gene signature comprising MET, KLK10, COL17A1, CEP55, ANKRD22, ITGB6, ARNTL2, MCOLN3, and SLC25A45 was established to predict overall survival of pancreatic cancer. The ROC curve and C-index indicated good performance of the nine-gene signature at predicting overall survival in the TCGA dataset and external validation datasets relative to classic AJCC staging. The nine-gene signature could classify patients into high- and low-risk groups with distinct overall survival and differentiate tumor from normal tissue. Univariate Cox regression revealed that the nine-gene signature was an independent prognostic factor in pancreatic cancer. The nomogram incorporating the gene signature and clinical prognostic factors was superior to AJCC staging in predicting overall survival. The high-risk group was enriched with multiple oncological signatures and aggressiveness-related pathways and associated with significantly lower levels of CD4+ T cell infiltration. Conclusion: Our study identified a nine-gene signature and established a prognostic nomogram that reliably predict overall survival in pancreatic cancer. 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"reader_status": "available", "identifier": "section[12]/table-wrap[1]#T1", "version": null, "note": "Details of the GEO datasets included in this study.", "structure": {"pmcid": "PMC6776930", "section_index": 12, "section_title": "Identification of DEGs", "row_count": 9, "column_count": 5}, "table": {"label": "Table 1", "caption": "Details of the GEO datasets included in this study.", "rows": [["Datasets", "References", "Platform", "Sample size (tumor/control)", "Application"], ["GSE71729", "Moffitt et al. (9)", "Agilent-014850 whole human genome microarray 4x44K G4112F (Gene Symbol Version; updated July, 2014)", "357 (145/46)", "Identification of DEGs"], ["GSE62165", "Janky et al. (10)", "[HG-U219] affymetrix human genome U219 array", "131 (118/13)", "Identification of DEGs"], ["GSE62452", "Yang et al. (11)", "[HuGene-1_0-st] affymetrix human gene 1.0 ST array [transcript (gene) version]", "130 (69/61)", "Identification of DEGs and validation"], ["GSE28735", "Zhang et al. (12)", "[HuGene-1_0-st] affymetrix human gene 1.0 ST array [transcript (gene) version]", "90 (45/45)", "Identification of DEGs"], ["GSE15471", "Badea et al. (13)", "[HG-U133_Plus_2] affymetrix human genome U133 Plus 2.0 array", "78 (39/39)", "Identification of DEGs"], ["GSE16515", "Pei et al. (14)", "[HG-U133_Plus_2] affymetrix human genome U133 Plus 2.0 array", "52 (36/16)", "Identification of DEGs"], ["GSE32676", "Donahue et al. (15)", "[HG-U133_Plus_2] affymetrix human genome U133 Plus 2.0 array", "32 (25/7)", "Identification of DEGs"], ["GSE57495", "Chen et al. (16)", "Rosetta/Merck human RSTA custom affymetrix 2.0 microarray", "63(63/0)", "Validation"]], "row_count": 9, "column_count": 5, "numeric_cells": 32, "header_rows": 1, "locator": "section[12]/table-wrap[1]#T1"}}, {"id": "asset:table:pmid:31612115:2", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:c9ac17bac8a96e099b15faf1c65d23a189e1057698cedd34d1df0774b0df1f59", "bytes": 3306, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[14]/table-wrap[1]#T2", "version": null, "note": "Clinical features of pancreatic cancer patients in the TCGA Dataset.", "structure": {"pmcid": "PMC6776930", "section_index": 14, "section_title": "Identification of Survival-Related DEGs and Establishment of the Nine-Gene Prognostic Signature", "row_count": 106, "column_count": 2}, "table": {"label": "Table 2", "caption": "Clinical features of pancreatic cancer patients in the TCGA Dataset.", "rows": [["Clinical features", "Mean + SD"], ["Follow-up time (day)", "591.02 ± 479.02"], ["Age", "64.53 ± 10.84"], ["Size (cm)", "3.91 ± 1.70"], ["", "N (%)"], ["Survival status"], ["Alive", "76 (46.06%)"], ["Dead", "89 (53.94%)"], ["Sex"], ["Male", "90 (54.55%)"], ["Female", "75 (45.45%)"], ["Site"], ["Head of pancreas", "128 (77.58%)"], ["Body of pancreas", "14 (8.48%)"], ["Tail of pancreas", "12 (7.27%)"], ["Others", "11 (6.67%)"], ["Subtype"], ["Pancreas-adenocarcinoma ductal type", "140 (84.85%)"], ["Pancreas-adenocarcinoma-other subtype", "25 (15.15%)"], ["Grade"], ["G1", "27 (16.36%)"], ["G2", "89 (53.94%)"], ["G3", "47 (28.48%)"], ["G4", "1 (0.61%)"], ["Not available", "1 (0.61%)"], ["T"], ["T1", "6 (3.64%)"], ["T2", "20 (12.12%)"], ["T3", "134 (81.21%)"], ["T4", "3 (1.82%)"], ["Not available", "2 (1.21%)"], ["N"], ["N0", "45 (27.27%)"], ["N1", "116 (70.30%)"], ["Not available", "4 (2.42%)"], ["M"], ["M0", "74 (44.85%)"], ["M1", "4 (2.42%)"], ["Mx", "87 (52.73%)"], ["AJCC stage"], ["I", "1 (0.61%)"], ["IA", "4 (2.42%)"], ["IB", "13 (7.88%)"], ["IIA", "26 (15.76%)"], ["IIB", "112 (67.88%)"], ["III", "3 (1.82%)"], ["IV", "4 (2.42%)"], ["Not available", "2 (1.21%)"], ["Residual tumor"], ["R0", "96 (58.18%)"], ["R1", "51 (30.91%)"], ["R2", "5 (3.03%)"], ["Not available", "13 (7.88%)"], ["Initial pathologic diagnosis method"], ["Tumor resection", "99 (60.00%)"], ["Tissue biopsy", "35 (21.21%)"], ["Cytology (e.g., Peritoneal or pleural fluid)", "22 (13.33%)"], ["Fine needle aspiration biopsy", "4 (2.42%)"], ["Not available", "5 (3.03%)"], ["Surgical treatment"], ["Whipple", "130 (78.79%)"], ["Distal pancreatectomy", "22 (13.33%)"], ["Distal pancreatectomy and laporoscopy followed by Hand-assisted and splenectomy", "1 (0.61%)"], ["Subtotal pancreatectomy", "2 (1.21%)"], ["Subtotal pancreatectomy and splenectomy and cholecystectomy", "1 (0.61%)"], ["Near total pancreatomy with splenectomy, duodenum perserving", "1 (0.61%)"], ["Radical pancreaticoduodenectomy", "3 (1.82%)"], ["Total pancreatectomy", "2 (1.21%)"], ["Endoscopic retrograde cholangiopancreaticography", "1 (0.61%)"], ["Not available", "2 (1.21%)"], ["History of neoadjuvant treatment"], ["No", "164 (99.39%)"], ["Yes", "1 (0.61%)"], ["History of chemotherapy"], ["No", "51 (30.91%)"], ["Yes", "114 (69.09%)"], ["History of radiation therapy"], ["No", "94 (56.97%)"], ["Yes", "45 (27.27%)"], ["Not available", "26 (15.76%)"], ["History of targeted molecular therapy"], ["No", "41 (24.85%)"], ["Yes", "112 (67.88%)"], ["Not available", "12 (7.27%)"], ["Tobacco smoking history"], ["Lifelong non-smoker", "60 (36.36%)"], ["Current smoker", "18 (10.91%)"], ["Current reformed smoker for >15 years", "27 (16.36%)"], ["Current reformed smoker for ≤15 years", "22 (13.33%)"], ["Current reformed smoker, duration not specified", "7 (4.24%)"], ["Not available", "31 (18.79%)"], ["Alcohol drinking history"], ["No", "61 (36.97%)"], ["Yes", "92 (55.76%)"], ["Not available", "12 (7.27%)"], ["History of chronic pancreatitis"], ["No", "119 (72.12%)"], ["Yes", "13 (7.88%)"], ["Not available", "33 (20.00%)"], ["History of diabetes"], ["No", "102 (61.82%)"], ["Yes", "34 (20.61%)"], ["Not available", "29 (17.58%)"], ["History of prior malignancy"], ["No", "148 (89.70%)"], ["Yes", "17 (10.30)"]], "row_count": 106, "column_count": 2, "numeric_cells": 85, "header_rows": 1, "locator": "section[14]/table-wrap[1]#T2"}}, {"id": "asset:table:pmid:31612115:3", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:7735b8982ca439240eced7ecffd99c48c230de6afcc2382e54ad161de6c6c2d0", "bytes": 2840, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[17]/table-wrap[1]#T3", "version": null, "note": "Baseline characteristics of patients included for univariate and multivariate Cox regression analysis.", "structure": {"pmcid": "PMC6776930", "section_index": 17, "section_title": "Evaluation of Prognostic Factors in PAAD", "row_count": 92, "column_count": 2}, "table": {"label": "Table 3", "caption": "Baseline characteristics of patients included for univariate and multivariate Cox regression analysis.", "rows": [["Clinical features", "Mean + SD"], ["Risk score", "2.06 ± 0.44"], ["Age", "63.59 ± 11.31"], ["Follow-up time (day)", "528.46 ± 371.92"], ["Size (cm)", "3.77 ± 1.44"], ["", "N (%)"], ["Survival status"], ["Alive", "35 (38.46%)"], ["Dead", "56 (61.54%)"], ["Sex"], ["Male", "52 (57.14%)"], ["Female", "39 (42.86%)"], ["Site"], ["Head of pancreas", "74 (81.32%)"], ["Body of pancreas", "5 (5.49%)"], ["Tail of Pancreas", "9 (9.89%)"], ["Others", "3 (3.30%)"], ["Subtype"], ["Pancreas-adenocarcinoma ductal type", "79 (86.81%)"], ["Pancreas-adenocarcinoma-other subtype", "12 (13.19%)"], ["Grade"], ["G1", "9 (9.89%)"], ["G2", "51 (56.04%)"], ["G3", "30 (32.97%)"], ["G4", "1 (1.10%)"], ["T"], ["T1", "4 (4.40%)"], ["T2", "11 (12.09%)"], ["T3", "75 (82.42%)"], ["T4", "1 (1.10%)"], ["N"], ["N0", "26 (28.57%)"], ["N1", "65 (71.43%)"], ["M"], ["M0", "54 (59.34%)"], ["M1", "1 (1.10%)"], ["Mx", "36 (39.56%)"], ["AJCC stage"], ["IA", "3 (3.30%)"], ["IB", "8 (8.79%)"], ["IIA", "14 (15.38%)"], ["IIB", "64 (70.33%)"], ["III", "1 (1.10%)"], ["IV", "1 (1.10%)"], ["Residual tumor"], ["R0", "55 (60.44%)"], ["R1", "34 (37.36%)"], ["R2", "2 (2.20%)"], ["Initial pathologic diagnosis method"], ["Tumor resection", "53 (58.24%)"], ["Tissue biopsy", "23 (25.27%)"], ["Cytology (e.g., Peritoneal or pleural fluid)", "13 (14.29%)"], ["Fine needle aspiration biopsy", "1 (1.10%)"], ["Not available", "1 (1.10%)"], ["Surgical treatment"], ["Whipple", "74 (81.32%)"], ["Distal pancreatectomy", "12 (13.19%)"], ["Distal pancreatectomy and laporoscopy followed by Hand-assisted and splenectomy", "1 (1.10%)"], ["Subtotal pancreatectomy", "1 (1.10%)"], ["Subtotal pancreatectomy and splenectomy and cholecystectomy", "1 (1.10%)"], ["Total pancreatectomy", "1 (1.10%)"], ["Endoscopic retrograde cholangiopancreaticography", "1 (1.10%)"], ["History of neoadjuvant treatment"], ["No", "90 (98.90%)"], ["Yes", "1 (1.10%)"], ["History of chemotherapy", ""], ["No", "25 (27.47%)"], ["Yes", "66 (72.53%)"], ["History of radiation therapy"], ["No", "67 (73.63%)"], ["Yes", "24 (26.37%)"], ["History of targeted molecular therapy"], ["No", "29 (31.87%)"], ["Yes", "62 (68.13%)"], ["Tobacco smoking history"], ["Lifelong non-smoker", "34 (37.36%)"], ["Current smoker", "16 (17.58%)"], ["Current reformed smoker for >15 years", "21 (23.08%)"], ["Current reformed smoker for ≤15 years", "15 (16.48%)"], ["Current reformed smoker, duration not specified", "5 (5.49%)"], ["Alcohol drinking history"], ["No", "25 (27.47%)"], ["Yes", "66 (72.53%)"], ["History of chronic pancreatitis"], ["No", "80 (87.91%)"], ["Yes", "11 (12.09%)"], ["History of diabetes"], ["No", "67 (73.63%)"], ["Yes", "24 (26.37%)"], ["History of prior malignancy"], ["No", "82 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"1"], ["Middle", "30 (32.97%)", "1.56 (0.79, 3.08) 0.1991"], ["High", "31 (34.07%)", "2.17 (1.12, 4.19) 0.0218"], ["Age", "63.59 ± 11.31", "1.02 (1.00, 1.05) 0.0663"], ["Age tertile", "", ""], ["Low", "30 (32.97%)", "1"], ["Middle", "29 (31.87%)", "1.07 (0.53, 2.16) 0.8510"], ["High", "32 (35.16%)", "1.68 (0.88, 3.22) 0.1155"], ["Sex", "", ""], ["Male", "52 (57.14%)", "1"], ["Female", "39 (42.86%)", "1.06 (0.62, 1.79) 0.8367"], ["Size(cm)", "3.77 ± 1.44", "1.24 (1.03, 1.49) 0.0235"], ["Size(cm) tertile", "", ""], ["Low", "26 (28.57%)", "1"], ["Middle", "25 (27.47%)", "0.91 (0.43, 1.92) 0.7992"], ["High", "40 (43.96%)", "1.33 (0.72, 2.46) 0.3660"], ["Site", "", ""], ["Head of pancreas", "74 (81.32%)", "1"], ["Body and tail of pancreas and others", "17 (18.68%)", "0.37 (0.16, 0.87) 0.0225"], ["Subtype", "", ""], ["Pancreas-adenocarcinoma ductal type", "79 (86.81%)", "1"], ["Pancreas-adenocarcinoma- other subtype", "12 (13.19%)", "0.30 (0.11, 0.84) 0.0215"], ["Grade", "", ""], ["G1 and 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(1.73, 12.96) 0.0025", "4.74 (1.73, 12.96) 0.0025", "3.58 (1.50, 8.51) 0.0040"], ["Age", "1.02 (1.00, 1.05) 0.0663", "1.02 (1.00, 1.05) 0.0872", "1.03 (1.00, 1.05) 0.0536", "NA"], ["Sex"], ["Male", "1", "1", "1", "NA"], ["Female", "1.06 (0.62, 1.79) 0.8367", "0.88 (0.51, 1.52) 0.6477", "0.86 (0.50, 1.48) 0.5961", "NA"], ["Size(cm)", "1.24 (1.03, 1.49) 0.0235", "1.19 (0.96, 1.47) 0.1219", "1.19 (0.96, 1.47) 0.1167", "1.30 (1.00, 1.68) 0.0463"], ["Site"], ["Head of pancreas", "1", "1", "1", "1"], ["Body and tail of pancreas and others", "0.37 (0.16, 0.87) 0.0225", "0.51 (0.21, 1.23) 0.1351", "0.49 (0.20, 1.19) 0.1143", "0.44 (0.16, 1.15) 0.0944"], ["Subtype"], ["Pancreas-adenocarcinoma ductal type", "1", "1", "1", "1"], ["Pancreas-adenocarcinoma-other subtype", "0.30 (0.11, 0.84) 0.0215", "0.53 (0.18, 1.58) 0.2524", "0.78 (0.26, 2.29) 0.6462", "0.49 (0.16, 1.47) 0.2005"], ["Grade"], ["G1 and G2", "1", "1", "1", "NA"], ["G3 and G4", "1.57 (0.92, 2.68) 0.0975", "1.39 (0.80, 2.42) 0.2490", "1.22 (0.70, 2.14) 0.4853", "NA"], ["T"], ["T1 and T2", "1", "1", "1", "1"], ["T3 and T4", "3.24 (1.28, 8.20) 0.0129", "4.00 (0.53, 29.92) 0.1770", "4.33 (0.58, 32.56) 0.1543", "4.50 (0.60, 33.92) 0.1439"], ["N"], ["N0", "1", "1", "1", "1"], ["N1", "2.69 (1.35, 5.36) 0.0049", "0.89 (0.08, 10.23) 0.9268", "0.48 (0.04, 5.72) 0.5603", "0.21 (0.01,3.20) 0.2603"], ["M"], ["M0", "1", "1", "1", "NA"], ["M1", "2.10 (0.28, 15.54) 0.4681", "0.44 (0.04, 5.46) 0.5261", "0.53 (0.04, 6.58) 0.6213", "NA"], ["Mx", "0.79 (0.46, 1.36) 0.4016", "0.74 (0.42, 1.30) 0.2906", "0.81 (0.46, 1.43) 0.4621", "NA"], ["AJCC stage"], ["I", "1", "1", "1", "1"], ["IIA", "1.33 (0.35, 4.99) 0.6770", "1.25 (0.33, 4.77) 0.7401", "0.96 (0.26, 3.64) 0.9571", "0.22 (0.02, 2.63) 0.2340"], ["IIB", "3.34 (1.19, 9.41) 0.0224", "3.13 (1.11, 8.83) 0.0315", "2.11 (0.75, 5.92) 0.1553", "2.00 (0.06, 64.49) 0.6957"], ["III and IV", "7.42 (1.59, 34.63) 0.0108", "8.61 (1.81, 40.88) 0.0068", "4.07 (0.85, 19.52) 0.0796", "1.60 (0.07, 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0.0729", "0.54 (0.27, 1.09) 0.0866", "0.83 (0.38, 1.83) 0.6512"], ["History of targeted molecular therapy"], ["No", "1", "1", "1", "1"], ["Yes", "0.30 (0.17, 0.51) <0.0001", "0.17 (0.09, 0.31) <0.0001", "0.16 (0.08, 0.31) <0.0001", "0.17 (0.06, 0.48) 0.0009"], ["Tobacco smoking history"], ["Lifelong non-smoker", "1", "1", "1", "NA"], ["Current or former smoker", "0.77 (0.45, 1.32) 0.3397", "0.76 (0.44, 1.31) 0.3207", "0.78 (0.45, 1.34) 0.3657", "NA"], ["Alcohol drinking history"], ["No", "1", "1", "1", "NA"], ["Yes", "1.27 (0.70, 2.30) 0.4252", "1.34 (0.70, 2.57) 0.3778", "1.10 (0.58, 2.08) 0.7676", "NA"], ["History of chronic pancreatitis"], ["No", "1", "1", "1", "NA"], ["Yes", "0.81 (0.37, 1.79) 0.6029", "1.09 (0.47, 2.52) 0.8359", "0.84 (0.36, 1.97) 0.6950", "NA"], ["History of diabetes"], ["No", "1", "1", "1", "NA"], ["Yes", "0.94 (0.50, 1.75) 0.8422", "0.92 (0.49, 1.75) 0.8053", "0.85 (0.45, 1.59) 0.6058", "NA"], ["History of Prior Malignancy"], ["No", "1", "1", "1", "NA"], 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