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pmid:31195368
B7-CD28 gene family expression is associated with prognostic and immunological characteristics of diffuse large B-cell lymphoma.
Gangjian Wang · Xiaorui Fu · Yu Chang · Xin Li · Xiaolong Wu · Ling Li · Lei Zhang · Zhenchang Sun · Xudong Zhang · Mingzhi Zhang
Aging · 2019 doi:10.18632/aging.102025
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Experiment
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Data
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Analysis
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Execution
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Complete file
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Here, we explored associations between clinical and immune features and B7-CD28 gene family expression in Gene Expression Omnibus (GEO) datasets representing 1812 diffuse large B-cell lymphoma (DLBCL) patients. This included 414 in the GSE10846 training cohort and 470 and 928 patients in the GSE31312 and GSE117556 validation cohorts, respectively. Four survival-associated genes identified in the GSE10846 cohort by univariate Cox analysis were incorporated into a multivariate analysis, ultimately establishing a three-gene risk signature. Risk scores assigned based on expression of these genes were validated by Kaplan–Meier and multivariable Cox analyses in the remaining datasets and in important clinical subsets. High-risk patients had shorter overall survival and, in some cases, progression-free survival than low-risk patients. Additionally, expression of programmed cell death 1 (PD-1) and programmed death ligand 1 (PD-L1), as well as several other important immune checkpoint genes, differed between high-risk and low-risk patients, as did the proportions of various immune-infiltrating cells. Finally, further analysis confirmed that these B7-CD28 genes play important roles in immune responses altered in DLBCL.", "claims": [{"id": "claim-method", "statement": "The survival-related genes then were incorporated into a Cox proportional hazard regression model to establish a risk score equation. 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"application/vnd.ncbi.geo-series+json", "uri": "https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE31312", "sha256": null, "bytes": null, "access": "open", "state": "resolved", "reader": null, "reader_status": "reader_required", "identifier": "GSE31312", "version": null, "note": "Publicly available DLBCL patient clinical and gene expression data from the GSE10846 and GSE31312 datasets, which used the GPL570 platform, and the GSE117556 dataset, which used the GPL14951 platform, were obtained from the GEO database. After excluding patients for whom clinical data were not available, data from 1812 DLBCL patients were used in this study. 414 patients from the GSE10846 dataset were used as a training cohort, and 470 and 928 patients from the GSE31312 and GSE117556 datasets, respectively, were used as validation cohorts.", "structure": {"repository": "GEO", "access_route": "GEO accession URL", "access_statement_verbatim": "Publicly available DLBCL patient clinical and gene expression data from the GSE10846 and GSE31312 datasets, which used the GPL570 platform, and the GSE117556 dataset, which used the GPL14951 platform, were obtained from the GEO database. After excluding patients for whom clinical data were not available, data from 1812 DLBCL patients were used in this study. 414 patients from the GSE10846 dataset were used as a training cohort, and 470 and 928 patients from the GSE31312 and GSE117556 datasets, respectively, were used as validation cohorts.", "access_statement_kind": "repository_route_statement", "sample_accessions": ["GSM775979", "GSM775980", "GSM775981", "GSM775982", "GSM775983", "GSM775984", "GSM775985", "GSM775986", "GSM775987", "GSM775988", "GSM775989", "GSM775990", "GSM775991", "GSM775992", "GSM775993", "GSM775994", "GSM775995", "GSM775996", "GSM775997", "GSM775998", "GSM775999", "GSM776000", "GSM776001", "GSM776002", "GSM776003", "GSM776004", "GSM776005", "GSM776006", "GSM776007", "GSM776008", "GSM776009", "GSM776010", "GSM776011", "GSM776012", "GSM776013", "GSM776014", "GSM776015", "GSM776016", "GSM776017", "GSM776018", "GSM776019", "GSM776020", "GSM776021", "GSM776022", "GSM776023", "GSM776024", "GSM776025", 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application of a new immunophenotypic algorithm for molecular subtype classification of Diffuse Large B-Cell Lymphoma (DLBCL): Report from an International DLBCL Rituximab-CHOP Consortium Program Study", "resolution_checked_at": "2026-11-01T15:39:54Z", "resolution_check": "identifier_resolution_only_no_download_no_licence_read", "downloaded": false, "licence_read": false}}, {"id": "asset:table:pmid:31195368:1", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:ebdef74e4f1855b5278f0d45a4bcb89cf35875b73ea700a9436d7adee052efa8", "bytes": 1596, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[3]/table-wrap[1]#t1", "version": null, "note": "Clinical characteristics of the patients in GSE10846 and GSE31312.", "structure": {"pmcid": "PMC6629000", "section_index": 3, "section_title": "Three B7-CD28 family genes predict overall survival in DLBCL", "row_count": 40, "column_count": 4}, "table": {"label": "Table 1", "caption": "Clinical characteristics of the patients in GSE10846 and GSE31312.", "rows": [["Characteristics", "GSE10846 (n=414)(%)", "GSE31312 (n=470) (%)", "GSE117556 (n=928) (%)"], ["Age, No.(%)", "", "", ""], ["<=60", "188(45.4)", "200(42.6)", "332(35.8)"], [">60", "226(54.6)", "270(57.4)", "596(64.2)"], ["Subtype, No.(%)", "", "", ""], ["GCB", "183(44.2)", "227(48.3)", "475(51.2)"], ["ABC", "167(40.3)", "199(42.3)", "274(26.3)"], ["Na", "64(15.5)", "44(9.4)", "209(22.5)"], ["Stage, No.(%)", "", "", ""], ["I~II", "189(45.7)", "220(46.8)", "268(30.8)"], ["III~IV", "217(52.4)", "229(48.7)", "638(68.8)"], ["Na", "8(1.9)", "21(4.5)", "4(0.4)"], ["ECOG, No.(%)", "", "", ""], ["<=1", "296(71.5)", "374(79.6)", "823(88.7)"], [">1", "93(22.5)", "96(20.4)", "105(11.3)"], ["NA", "25(6)", "", ""], ["LDH", "", "", ""], ["Normal", "173(41.8)", "148(31.5)", ""], ["Elevated", "178(43.0)", "278(59.1)", ""], ["Na", "63(15.2)", "44(9.4)", ""], ["Extranodal site, No.(%)", "", "", ""], ["No", "238(57.5)", "194(41.3)", "407(43.9)"], ["Yes", "145(35)", "276(58.7)", "521(56.1)"], ["Na", "31(7.5)", "", ""], ["Treatment, No.(%)", "", "", ""], ["R-Chop", "233(56.3)", "", "469(50.5)"], ["Chop", "181(43.7)", "", ""], ["RB-Chop", "", "", "459(49.5)"], ["IPI,", "", "", ""], ["<=2", "", "274(58.3)", "482(51.9)"], [">2", "", "150(31.9)", "446(48.1)"], ["Na", "", "46(9.8)", ""], ["Tumor size, N0.(%)", "", "", ""], ["<=5", "", "268(57.0)", "354(381)"], [">5", "", "98(20.9)", "574(61.9)"], ["Na", "", "104(22.1)", ""], ["B sympyom, No(%)", "", "", ""], ["No", "", "276(58.7)", ""], ["Yes", "", "132(28.1)", ""], ["Na", "", "62(13.2)", ""]], "row_count": 40, "column_count": 4, "numeric_cells": 72, "header_rows": 0, "locator": "section[3]/table-wrap[1]#t1"}}, {"id": "asset:table:pmid:31195368:2", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:76c31d5002be04022b27bec9f17502a505ff1a6d7d800ba50e6b8f7a18b27d17", "bytes": 1049, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[3]/table-wrap[2]#t2", "version": null, "note": "B7-CD28 gene univariate Cox proportional hazards models in GSE10846.", "structure": {"pmcid": "PMC6629000", "section_index": 3, "section_title": "Three B7-CD28 family genes predict overall survival in DLBCL", "row_count": 16, "column_count": 5}, "table": {"label": "Table 2", "caption": "B7-CD28 gene univariate Cox proportional hazards models in GSE10846.", "rows": [["Official symbol", "Aliases", "Hazard ratio", "p-value", "Family"], ["HHLA2", "B7-H5, B7-H7", "1.046", "0.468", "B7 Family"], ["BTLA", "CD272", "1.127", "0.074", "CD28 Family"], ["CD28", "Tp44", "0.910", "0.121", "CD28 Family"], ["CD86", "B7-2, CD28LG2", "0.725", "0.001", "B7 Family"], ["CD80", "B7, CD28LG1", "0.772", "0.007", "B7 Family"], ["ICOS", "AILIM, CD278", "0.904", "0.003", "CD28 Family"], ["NCR3", "NKp30, CD337", "0.956", "0.349", "CD28 Family"], ["VSIR", "B7-H5, C10orf54", "0.903", "0.318", "B7 Family"], ["ICOSLG", "B7-H2, CD275", "0.944", "0.307", "B7 Family"], ["PDCD1", "PD1, CD279", "0.980", "0.743", "CD28 Family"], ["PDCD1LG2", "PD-L2, CD273", "0.926", "0.127", "B7 Family"], ["CD274", "B7-H1, PD-L1", "1.142", "0.102", "B7 Family"], ["CD276", "B7-H3", "1.011", "0.892", "B7 Family"], ["CTLA4", "CD152", "0.836", "0.025", "CD28 Family"], ["VTCN1", "B7-H4", "1.070", "0.212", "B7 Family"]], "row_count": 16, "column_count": 5, "numeric_cells": 52, "header_rows": 0, "locator": "section[3]/table-wrap[2]#t2"}}, {"id": "asset:table:pmid:31195368:3", "role": "table", "format": "jats-table", "media_type": "application/vnd.jats.table+json", "uri": null, "sha256": "sha256:fdd12de6549a6e1a7304858f64be7bd6116fc505a997172f25bb65d1038a0231", "bytes": 1747, "access": "open", "state": "verified", "reader": "read_table", "reader_status": "available", "identifier": "section[3]/table-wrap[3]#t3", "version": null, "note": "Multivariate Cox proportional hazards regression analysis of the B7-CD28 signature and clinical characteristics in GSE10846 and GSE 31312.", "structure": {"pmcid": "PMC6629000", "section_index": 3, "section_title": "Three B7-CD28 family genes predict overall survival in DLBCL", "row_count": 13, "column_count": 13}, "table": {"label": "Table 3", "caption": "Multivariate Cox proportional hazards regression analysis of the B7-CD28 signature and clinical characteristics in GSE10846 and GSE 31312.", "rows": [["Variable", "GSE10846 OS", "GSE31312 OS", "GSE31312 PFS", "GSE117556 OS"], ["HR", "95%CI", "p-value", "HR", "95%CI", "p-value", "HR", "95%CI", "p-value", "HR", "95%CI", "p-value"], ["Riskscore", "1.714", "1.08~2.72", "0.022", "1.090", "1.026~1.158", "0.005", "1.62", "1.106~2.372", "0.013", "5.47", "1.98~15.117", "0.001"], ["Age", "2.267", "1.502~3.42", "<0.001", "1.696", "1.07~2.689", "0.025", "1.107", "0.728~1.683", "0.634", "1.374", "0.87~2.169", "0.173"], ["Subtype", "2.238", "1.506~3.328", "<0.001", "1.434", "0.95~2.165", "0.086", "1.378", "0.925~2.052", "0.115", "1.47", "1.01~2.139", "0.44"], ["Stage", "1.170", "0.789~1.734", "0.436", "1.879", "1.083~3.259", "0.025", "2.017", "1.192~3.414", "0.009", "1.216", "0.134~-2.016", "0.447"], ["ECOG", "1.826", "1.202~2.773", "0.005", "1.515", "0.903~2.54", "0.115", "1.323", "0.804~2.176", "0.271", "2.021", "1.267~3.224", "0.003"], ["LDH", "1.970", "1.312~2.958", "0.001", "1.102", "0.674~1.802", "0.699", "1.17", "0.721~1.899", "0.526", "", "", ""], ["Extranodal site", "1.339", "0.842~2.127", "0.217", "1.139", "0.727~1.783", "0.570", "1.078", "0.709~1.641", "0.724", "0.795", "0.536~1.180", "0.255"], ["Treatment", "1.978", "1.251~3.127", "0.004", "", "", "", "", "", "", "0.864", "0.598~1.25", "0.439"], ["IPI", "", "", "", "1.812", "1.024~3.207", "0.041", "1.737", "0.995~3.034", "0.052", "2.117", "1.291~3.471", "0.003"], ["Tumor size", "", "", "", "1.402", "0.908~2.164", "0.127", "1.01", "0.652~1.564", "0.965", "1.230", "0.809~1.869", "0.333"], ["B symptoms", "", "", "", "0.978", "0.641~1.493", "0.919", "1.023", "0.684~1.529", "0.912", "", "", ""]], "row_count": 13, "column_count": 13, "numeric_cells": 119, "header_rows": 0, "locator": "section[3]/table-wrap[3]#t3"}}], "gaps": ["asset:data:geo:GSE10846 not downloaded", "asset:data:geo:GSE10846 licence not read", "asset:data:geo:GSE117556 not downloaded", "asset:data:geo:GSE117556 licence not read", "asset:data:geo:GSE31312 not downloaded", "asset:data:geo:GSE31312 licence not read"]}, "analysis": {"state": "partial", "methods": [{"id": "method-1", "family": "survival_analysis", "specific": "kaplan_meier", "label": "Survival analysis", "dsl_operations": ["survival_km"], "missing_operations": [], "expressible": true, "parameters": {}, "data_shapes": ["time_to_event_with_censoring"], "evidence": {"score": 0.8, "band": "high", "quote": "Kaplan-Meier"}}, {"id": "method-2", "family": "survival_analysis", "specific": "cox_proportional_hazards", "label": "Survival analysis", "dsl_operations": ["cox_ph"], "missing_operations": [], "expressible": true, "parameters": {}, "data_shapes": ["time_to_event_with_censoring"], "evidence": {"score": 0.8, "band": "high", "quote": "Cox proportional hazards"}}, {"id": "method-3", "family": "survival_analysis", "specific": "log_rank_test", "label": "Survival analysis", "dsl_operations": ["logrank_test"], "missing_operations": [], "expressible": true, "parameters": {}, "data_shapes": ["time_to_event_with_censoring"], "evidence": {"score": 0.8, "band": "high", "quote": "log-rank"}}, {"id": "method-4", "family": null, "specific": null, "label": "Cox proportional hazard regression", "dsl_operations": [], "missing_operations": [], "expressible": null, "parameters": {}, "data_shapes": [], "evidence": {"score": 1.0, "band": "reordered", "quote": "The survival-related genes then were incorporated into a Cox proportional hazard regression model to establish a risk score equation. Publicly available DLBCL patient clinical and gene expression data from the GSE10846 and GSE31312 datasets, which used the GPL570 platform, and the GSE117556 dataset, which used the GPL14951 platform, were obtained from the GEO database."}}], "targets": [], "gaps": ["method.reader_named_unmapped"]}, "capability": {"state": "complete", "requirements": [{"capability_id": "capability:computational_analysis", "label": "Computational analysis platform", "assay_families": ["meta_analysis", "machine_learning", "survival_analysis", "statistical_regression", "pca", "molecular_docking", "network_analysis", "differential_expression", "gwas"], "availability_state": "owned", "tier_unlocked": "R1", "candidate": "Automated Assays Laravel application and simulated adapters"}], "gaps": []}, "readiness": {"state": "complete", "tier": "R1", "blocking_axis": "none", "blocked_on": "nothing:replicable_now", "axes": {"method": {"tier": "R1", "expressible": true, "required_operations": ["survival_km"], "missing_operations": [], "basis": "The paper names the method it used and the corpus's method extractor maps it onto the DSL catalogue: kaplan_meier."}, "capability": {"tier": "R1", "capability_id": "capability:computational_analysis", "availability_state": "owned", "basis": "The computational analysis is owned. The physical bench the paper used is not, so a physical validation cannot be run here."}, "data": {"tier": "R1", "reachable": true, "accessions": ["GSE10846", "GSE31312", "GSE117556"], "resolved_accessions": ["GSE10846", "GSE31312", "GSE117556"], "statements": ["Publicly available DLBCL patient clinical and gene expression data from the GSE10846 and GSE31312 datasets, which used the GPL570 platform, and the GSE117556 dataset, which used the GPL14951 platform, were obtained from the GEO database. After excluding patients for whom clinical data were not available, data from 1812 DLBCL patients were used in this study. 414 patients from the GSE10846 dataset were used as a training cohort, and 470 and 928 patients from the GSE31312 and GSE117556 datasets, respectively, were used as validation cohorts."], "basis": "The paper names GSE10846, GSE31312, GSE117556 in Gene Expression Omnibus (GEO) and the accession resolves in the repository. No dataset was downloaded and no licence was read."}}, "can_run": {"dsl_operations": ["survival_km"], "assets": ["source:pmid:31195368", "data:geo:GSE10846", "asset:table:pmid:31195368:1", "asset:table:pmid:31195368:2", "asset:table:pmid:31195368:3"], "steps": ["run_analysis"]}, "must_build": {"dsl_operations": [], "converters": [], "readers": [], "capabilities": [], "data_gaps": ["data:geo:GSE10846"]}, "gaps": []}, "review": {"state": "partial", "machine_critique": {"kind": "extraction_review", "reader": {"model": "MiniMax-M3.1-Flash", "provider": "minimax", "provider_family": "minimax", "read_at": "2026-10-31T18:15:05Z", "independence": "single_reader"}, "evidence_check": {"method": "reordered", "availability": null}, "calls": 3, "usage": {"prompt_tokens": 26053, "completion_tokens": 3422, "cached_tokens": 784}}, "human_critique": null, "stages": [{"id": "extraction", "state": "complete", "reader": "MiniMax-M3.1-Flash", "provider": "minimax"}], "gaps": ["review.independent_reader", "review.machine_critique", "review.human_critique"]}, "execution": {"state": "absent", "status": "not_run", "mode": null, "runs": [], "gaps": ["execution.not_run"]}, "provenance": {"entities": [{"id": "pmid:31195368", "type": "paper", "label": "pmid:31195368"}, {"id": "source:pmid:31195368", "type": "manuscript", "label": "PMID 31195368 full text"}, {"id": "data:geo:GSE10846", "type": "dataset", "label": "GEO GSE10846"}], "activities": [{"id": "activity-reading-sci-2026-11-01", "type": "classification", "used": [{"id": "pmid:31195368", "type": "paper", "label": "pmid:31195368"}, {"id": "source:pmid:31195368", "type": "manuscript", "label": "PMID 31195368 full text"}, {"id": "data:geo:GSE10846", "type": "dataset", "label": "GEO GSE10846"}], "agent": "agent:corpus-assay-engine"}, {"id": "activity-read-31195368", "type": "extraction", "used": ["source:pmid:31195368"], "agent": "agent:minimax-reader"}, {"id": "activity-resolve-GSE10846", "type": "accession_resolution", "used": ["data:geo:GSE10846"], "agent": "agent:corpus-assay-engine"}], "agents": [{"id": "agent:corpus-assay-engine", "type": "software", "label": "Corpus assay engine"}, {"id": "agent:minimax-reader", "type": "software", "label": "MiniMax literature reader"}], "source_run_id": "reading-sci-2026-11-01", "dsl_catalogue_fingerprint": "343fb30756ba6ec3", "capability_table_fingerprint": "2cb3e42f047d2ecf", "snapshot_id": "ba34b49490d9bfaf"}, "lineage": {"parent_id": "pmid:31195368", "parent_hash": "sha256:cb6a8e284b8f618388611c881978a48152e24b6f08ca5cfe0748f8299005d375", "fork_of": null, "generation": 6}, "gaps": ["asset:data:geo:GSE10846 licence not read", "asset:data:geo:GSE10846 not downloaded", "asset:data:geo:GSE117556 licence not read", "asset:data:geo:GSE117556 not downloaded", "asset:data:geo:GSE31312 licence not read", "asset:data:geo:GSE31312 not downloaded", "execution.not_run", "method.reader_named_unmapped", "review.human_critique", "review.independent_reader", "review.machine_critique"], "assays": [{"role": "analysis", "definition_id": "survival_analysis", "definition_version": "f2132e96ae6c7a4e", "definition_digest": null, "required_operations": ["survival_km"], "support_state": "supported", "source_hashes": {"dsl_catalogue": "f2132e96ae6c7a4e"}, "confidence": 0.8, "evidence": ["Kaplan-Meier"], "order_basis": "analysis_only", "id": "assay:1"}]}