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pmid:33767996

Prognostic Signature of Immune Genes and Immune-Related LncRNAs in Neuroblastoma: A Study Based on GEO and TARGET Datasets.

Xiaodan Zhong · Ying Tao · Jian Chang · Yutong Zhang · Hao Zhang · Linyu Wang · Yuanning Liu

Frontiers in oncology · 2021 doi:10.3389/fonc.2021.631546

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2026-11-01T15:41:30Z
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title
Prognostic Signature of Immune Genes and Immune-Related LncRNAs in Neuroblastoma: A Study Based on GEO and TARGET Datasets.
doi
10.3389/fonc.2021.631546
pmid
33767996
authors array · 7 items
[0]
Xiaodan Zhong
[1]
Ying Tao
[2]
Jian Chang
[3]
Yutong Zhang
[4]
Hao Zhang
[5]
Linyu Wang
[6]
Yuanning Liu
journal
Frontiers in oncology
year
2021
abstract
BACKGROUND: The prognostic value of immune-related genes and lncRNAs in neuroblastoma has not been elucidated, especially in subgroups with different outcomes. This study aimed to explore immune-related prognostic signatures. MATERIALS AND METHODS: Immune-related prognostic genes and lncRNAs were identified by univariate Cox regression analysis in the training set. The top 20 C-index genes and 17 immune-related lncRNAs were included in prognostic model construction, and random forest and the Least Absolute Shrinkage and Selection Operator (LASSO) regression algorithms were employed to select features. The risk score model was constructed and assessed using the Kaplan-Meier plot and the receiver operating characteristic curve. Functional enrichment analysis of the immune-related lncRNAs was conducted using the STRING database. RESULTS: In GSE49710, five immune genes (CDK4, PIK3R1, THRA, MAP2K2, and ULBP2) were included in the risk score five genes (RS5_G) signature, and eleven immune-related lncRNAs (LINC00260, FAM13A1OS, AGPAT4-IT1, DUBR, MIAT, TSC22D1-AS1, DANCR, MIR137HG, ERC2-IT1, LINC01184, LINC00667) were brought into risk score LncRNAs (RS_Lnc) signature. Patients were divided into high/low-risk score groups by the median. Overall survival and event/progression-free survival time were shortened in patients with high scores, both in training and validation cohorts. The same results were found in subgroups. In grouping ability assessment, the area under the curves (AUCs) in distinguishing different groups ranged from 0.737 to 0.94, better in discriminating MYCN status and high risk in training cohort (higher than 0.9). Multivariate Cox analysis demonstrated that RS5_G and RS_Lnc were the independent risk factors for overall and event/progression-free survival (all p-values <0.001). Correlation analysis showed that RS5_G and RS_Lnc were negatively associated with aDC, CD8+ T cells, but positively correlated with Th2 cells. Functional enrichment analyzes demonstrated that immune-related lncRNAs are mainly enriched in cancer-related pathways and immune-related pathways. CONCLUSION: We identified the immune-related prognostic signature RS5_G and RS_Lnc. The predicting and grouping ability is close to being even better than those reported in other studies, especially in subgroups. This study provided prognostic signatures that may help clinicians to choose optimal treatment strategies and showed a new insight for NB treatment. These results need further biological experiments and clinical validation.
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Univariate Cox proportional model survival analysis (22) was performed in GSE49710.
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sections[4] "Identification of Survival-Related Immune Genes" paragraph 2
quote
Univariate Cox proportional model survival analysis (22) was performed in GSE49710.
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Publicly available datasets were analyzed in this study. This data can be found here: The expression data of training cohort GSE49710 (n=498, GPL16876) was downloaded from GEO database (https://www.ncbi.nlm.nih.gov/gds/?term=), survival information and validation datasets were downloaded from R2 database (https://hgserver1.amc.nl/cgi-bin/r2/main.cgi), including Neuroblastoma public—Versteeg—88 (GSE16476, GPL570), TARGET—Asgharzadeh—249, and Neuroblastoma Primary—NRC—283 (GSE85047, GPL5175).
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sections[19] "Data Availability Statement" paragraph 2
quote
Publicly available datasets were analyzed in this study. This data can be found here: The expression data of training cohort GSE49710 (n=498, GPL16876) was downloaded from GEO database (https://www.ncbi.nlm.nih.gov/gds/?term=), survival information and validation datasets were downloaded from R2 database (https://hgserver1.amc.nl/cgi-bin/r2/main.cgi), including Neuroblastoma public—Versteeg—88 (GSE16476, GPL570), TARGET—Asgharzadeh—249, and Neuroblastoma Primary—NRC—283 (GSE85047, GPL5175).
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Top 20 prognostic immune-related genes in GSE49710.
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Identification of Survival-Related Immune Genes
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Top 20 prognostic immune-related genes in GSE49710.
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HR
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Identification of Survival-Related Immune Genes
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Table 1
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Top 20 prognostic immune-related genes in GSE49710.
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0.63
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1.837
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0.756
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[2] array · 10 items
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0.785
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0.527
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PPP3CB
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0.753
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15
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MIA
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0.614
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0.748
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[8] array · 10 items
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0.559
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0.765
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6
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MAP2K2
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3.80
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1.7E-15
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0.746
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Univariate Cox regression analysis in GSE49710.
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PMC7985261
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13
section_title
Prognostic Model RS5_G Had Good Performance in Predicting Neuroblastoma Outcomes
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table object · 8 fields
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Table 2
caption
Univariate Cox regression analysis in GSE49710.
rows array · 8 items
[0] array · 3 items
[0]
Features
[1]
Overall Survival
[2]
Event-free Survival
[1] array · 8 items
[0]
HR
[1]
95% CI
[2]
p-value
[3]
C-index
[4]
HR
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95% CI
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p-value
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RS5_G
[1]
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2.348-3.167
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1.893
[6]
1.708-2.097
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3.339
[6]
2.462-4.529
[7]
9.06E-15
[8]
0.628
[4] array · 9 items
[0]
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[1]
20.84
[2]
11.6-37.43
[3]
<2E-16
[4]
0.806
[5]
5.302
[6]
3.875-7.254
[7]
<2E-16
[8]
0.679
[5] array · 9 items
[0]
Mycn status
[1]
7.651
[2]
5.167-11.33
[3]
<2E-16
[4]
0.705
[5]
3.231
[6]
2.36-4.425
[7]
2.58E-13
[8]
0.598
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[0]
INSS_h1
[1]
14.35
[2]
7.238-28.45
[3]
2.38E-14
[4]
0.742
[5]
4.68
[6]
3.297-6.642
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<2E-16
[8]
0.663
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[0]
RS_Lnc
[1]
2.718
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2.331-3.17
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<2E-16
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0.851
[5]
1.85
[6]
1.658-2.065
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Multivariate Cox regression analysis in GSE49710.
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Prognostic Model RS5_G Had Good Performance in Predicting Neuroblastoma Outcomes
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Table 3
caption
Multivariate Cox regression analysis in GSE49710.
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Overall Survival
[2]
Event-free Survival
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[0]
HR
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95% CI
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C-index
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RS5_G
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1.874
[2]
1.504-2.335
[3]
2.15E-08
[4]
0.881
[5]
1.626
[6]
1.385-1.98
[7]
2.65E-09
[8]
0.751
[3] array · 7 items
[0]
Age group
[1]
1.134
[2]
0.592-2.171
[3]
0.704
[4]
0.95
[5]
0.602-1.499
[6]
0.826
[4] array · 7 items
[0]
High risk
[1]
3.804
[2]
1.604-9.024
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0.002
[4]
1.82
[5]
1.026-3.23
[6]
0.041
[5] array · 7 items
[0]
Mycn status
[1]
1.102
[2]
0.679-1.789
[3]
0.695
[4]
0.712
[5]
0.468-1.082
[6]
0.11
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2.302
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0.99-5.352
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0.05
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null
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Univariate Cox proportional model survival analysis
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Univariate Cox proportional model survival analysis (22) was performed in GSE49710.
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method.group_comparison_mann_whitney
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The paper names the method it used and the corpus's method extractor maps it onto the DSL catalogue: mann_whitney.
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Publicly available datasets were analyzed in this study. This data can be found here: The expression data of training cohort GSE49710 (n=498, GPL16876) was downloaded from GEO database (https://www.ncbi.nlm.nih.gov/gds/?term=), survival information and validation datasets were downloaded from R2 database (https://hgserver1.amc.nl/cgi-bin/r2/main.cgi), including Neuroblastoma public—Versteeg—88 (GSE16476, GPL570), TARGET—Asgharzadeh—249, and Neuroblastoma Primary—NRC—283 (GSE85047, GPL5175).
basis
The paper names GSE49710 (n=498, Neuroblastoma public—Versteeg—88 (GSE16476, Neuroblastoma Primary—NRC—283 (GSE85047, but the accession does not resolve in the repository (no reason recorded, no reason recorded, no reason recorded), so the data cannot be reached from here. No dataset was downloaded and no licence was read.
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Complete file 
{"sci_version": "1.2", "schema": "https://corpus.bntrg.co.uk/sci/1.0/sci.schema.json", "id": "pmid:33767996", "kind": "science-record", "revision": 7, "content_hash": "sha256:d22b3c40ec5b9cdb1ee2490554c9c551bdb57324ce383e0a92584fa6be875c12", "created_at": "2026-11-01T15:41:30Z", "updated_at": "2026-11-01T22:03:25Z", "generator": {"name": "corpus-assay-engine", "run_id": "reading-sci-2026-11-01"}, "paper": {"state": "complete", "title": "Prognostic Signature of Immune Genes and Immune-Related LncRNAs in Neuroblastoma: A Study Based on GEO and TARGET Datasets.", "doi": "10.3389/fonc.2021.631546", "pmid": "33767996", "authors": ["Xiaodan Zhong", "Ying Tao", "Jian Chang", "Yutong Zhang", "Hao Zhang", "Linyu Wang", "Yuanning Liu"], "journal": "Frontiers in oncology", "year": 2021, "abstract": "BACKGROUND: The prognostic value of immune-related genes and lncRNAs in neuroblastoma has not been elucidated, especially in subgroups with different outcomes. This study aimed to explore immune-related prognostic signatures.\nMATERIALS AND METHODS: Immune-related prognostic genes and lncRNAs were identified by univariate Cox regression analysis in the training set. The top 20 C-index genes and 17 immune-related lncRNAs were included in prognostic model construction, and random forest and the Least Absolute Shrinkage and Selection Operator (LASSO) regression algorithms were employed to select features. The risk score model was constructed and assessed using the Kaplan-Meier plot and the receiver operating characteristic curve. Functional enrichment analysis of the immune-related lncRNAs was conducted using the STRING database.\nRESULTS: In GSE49710, five immune genes (CDK4, PIK3R1, THRA, MAP2K2, and ULBP2) were included in the risk score five genes (RS5_G) signature, and eleven immune-related lncRNAs (LINC00260, FAM13A1OS, AGPAT4-IT1, DUBR, MIAT, TSC22D1-AS1, DANCR, MIR137HG, ERC2-IT1, LINC01184, LINC00667) were brought into risk score LncRNAs (RS_Lnc) signature. Patients were divided into high/low-risk score groups by the median. Overall survival and event/progression-free survival time were shortened in patients with high scores, both in training and validation cohorts. The same results were found in subgroups. In grouping ability assessment, the area under the curves (AUCs) in distinguishing different groups ranged from 0.737 to 0.94, better in discriminating MYCN status and high risk in training cohort (higher than 0.9). Multivariate Cox analysis demonstrated that RS5_G and RS_Lnc were the independent risk factors for overall and event/progression-free survival (all p-values <0.001). Correlation analysis showed that RS5_G and RS_Lnc were negatively associated with aDC, CD8+ T cells, but positively correlated with Th2 cells. Functional enrichment analyzes demonstrated that immune-related lncRNAs are mainly enriched in cancer-related pathways and immune-related pathways.\nCONCLUSION: We identified the immune-related prognostic signature RS5_G and RS_Lnc. The predicting and grouping ability is close to being even better than those reported in other studies, especially in subgroups. This study provided prognostic signatures that may help clinicians to choose optimal treatment strategies and showed a new insight for NB treatment. These results need further biological experiments and clinical validation.", "claims": [{"id": "claim-method", "statement": "Univariate Cox proportional model survival analysis (22) was performed in GSE49710.", "kind": "methodological", "target": null, "evidence": [{"asset": "source:pmid:33767996", "locator": "sections[4] \"Identification of Survival-Related Immune Genes\" paragraph 2", "quote": "Univariate Cox proportional model survival analysis (22) was performed in GSE49710."}], "state": "complete"}, {"id": "claim-data-access", "statement": "Publicly available datasets were analyzed in this study. This data can be found here: The expression data of training cohort GSE49710 (n=498, GPL16876) was downloaded from GEO database (https://www.ncbi.nlm.nih.gov/gds/?term=), survival information and validation datasets were downloaded from R2 database (https://hgserver1.amc.nl/cgi-bin/r2/main.cgi), including Neuroblastoma public—Versteeg—88 (GSE16476, GPL570), TARGET—Asgharzadeh—249, and Neuroblastoma Primary—NRC—283 (GSE85047, GPL5175).", "kind": "methodological", "target": null, "evidence": [{"asset": "source:pmid:33767996", "locator": "sections[19] \"Data Availability Statement\" paragraph 2", "quote": "Publicly available datasets were analyzed in this study. This data can be found here: The expression data of training cohort GSE49710 (n=498, GPL16876) was downloaded from GEO database (https://www.ncbi.nlm.nih.gov/gds/?term=), survival information and validation datasets were downloaded from R2 database (https://hgserver1.amc.nl/cgi-bin/r2/main.cgi), including Neuroblastoma public—Versteeg—88 (GSE16476, GPL570), TARGET—Asgharzadeh—249, and Neuroblastoma Primary—NRC—283 (GSE85047, GPL5175)."}], "state": "complete"}], "gaps": []}, "experiment": {"state": "partial", "objective": null, "steps": [{"id": "read_published_estimate", "order": 1, "name": "Read the published estimate from the source", "kind": "other", "state": "complete", "blocked_on": null, "description": "The claim, method and evidence span published with the source article.", "duration_hours": null, "parameters": {}, "inputs": ["source:pmid:33767996"], "outputs": ["the published estimate and its evidence"], "instruments": [], "reagents": []}, {"id": "obtain_source_data", "order": 2, "name": "Obtain the source data from the named repository", "kind": "data-preparation", "state": "blocked", "blocked_on": "data:accession_absent", "description": "The GEO series accession resolves and its sample accessions are listed. This lane did not download the dataset or read its licence.", "duration_hours": null, "parameters": {}, "inputs": [], "outputs": ["the source data with its repository provenance"], "instruments": [], "reagents": []}, {"id": "run_analysis", "order": 3, "name": "Run the published analysis", "kind": "analysis", "state": "blocked", "blocked_on": "method:group_comparison_mann_whitney", "description": "Apply the paper's statistical method to the resolved series and compare the result with the published target.", "duration_hours": null, "parameters": {}, "inputs": [], "outputs": ["the replicated result and its comparison"], "instruments": [], "reagents": []}], "materials": [], "instruments": [], "reagents": [], "conditions": {}, "gaps": ["step:run_analysis blocked on method:group_comparison_mann_whitney", "step:obtain_source_data blocked on data:accession_absent"]}, "data": {"state": "partial", "assets": [{"id": "source:pmid:33767996", "role": "manuscript", "format": "xml", "media_type": 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The physical bench the paper used is not, so a physical validation cannot be run here."}, "data": {"tier": "R4", "reachable": false, "accessions": ["GSE49710 (n=498", "Neuroblastoma public—Versteeg—88 (GSE16476", "Neuroblastoma Primary—NRC—283 (GSE85047"], "resolved_accessions": [], "statements": ["Publicly available datasets were analyzed in this study. This data can be found here: The expression data of training cohort GSE49710 (n=498, GPL16876) was downloaded from GEO database (https://www.ncbi.nlm.nih.gov/gds/?term=), survival information and validation datasets were downloaded from R2 database (https://hgserver1.amc.nl/cgi-bin/r2/main.cgi), including Neuroblastoma public—Versteeg—88 (GSE16476, GPL570), TARGET—Asgharzadeh—249, and Neuroblastoma Primary—NRC—283 (GSE85047, GPL5175)."], "basis": "The paper names GSE49710 (n=498, Neuroblastoma public—Versteeg—88 (GSE16476, Neuroblastoma Primary—NRC—283 (GSE85047, but the accession does not resolve in the repository (no reason recorded, no reason recorded, no reason recorded), so the data cannot be reached from here. No dataset was downloaded and no licence was read."}}, "can_run": {"dsl_operations": [], "assets": ["source:pmid:33767996", "asset:table:pmid:33767996:1", "asset:table:pmid:33767996:2", "asset:table:pmid:33767996:3", "asset:table:pmid:33767996:4"], "steps": []}, "must_build": {"dsl_operations": [{"operation": "group_comparison_mann_whitney", "unlocks_papers": null, "priority": null}], "converters": [], "readers": [], "capabilities": [], "data_gaps": ["data:geo:None"]}, "gaps": ["data:accession_absent"]}, "review": {"state": "partial", "machine_critique": {"kind": "extraction_review", "reader": {"model": "MiniMax-M3.1-Flash", "provider": "minimax", "provider_family": "minimax", "read_at": "2026-10-31T18:28:38Z", "independence": "single_reader"}, "evidence_check": {"method": "verbatim", "availability": "verbatim"}, "calls": 3, "usage": {"prompt_tokens": 44622, "completion_tokens": 2701, "cached_tokens": 785}}, "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:33767996", "type": "paper", "label": "pmid:33767996"}, {"id": "source:pmid:33767996", "type": "manuscript", "label": "PMID 33767996 full text"}, {"id": "data:geo:None", "type": "dataset", "label": "GEO None"}], "activities": [{"id": "activity-reading-sci-2026-11-01", "type": "classification", "used": [{"id": "pmid:33767996", "type": "paper", "label": "pmid:33767996"}, {"id": "source:pmid:33767996", "type": "manuscript", "label": "PMID 33767996 full text"}, {"id": "data:geo:None", "type": "dataset", "label": "GEO None"}], "agent": "agent:corpus-assay-engine"}, {"id": "activity-read-33767996", "type": "extraction", "used": ["source:pmid:33767996"], "agent": "agent:minimax-reader"}, {"id": "activity-resolve-None", "type": "accession_resolution", "used": ["data:geo:None"], "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:33767996", "parent_hash": "sha256:93d48bcc360d1537eb060e3f4a41f180c4cf95d87f0e794fbbe521e5498e2f91", "fork_of": null, "generation": 6}, "gaps": ["execution.not_run", "method.group_comparison_mann_whitney", "method.reader_named_unmapped", "review.human_critique", "review.independent_reader", "review.machine_critique", "step:obtain_source_data blocked on data:accession_absent", "step:run_analysis blocked on method:group_comparison_mann_whitney"], "assays": [{"role": "analysis", "definition_id": "group_comparison", "definition_version": "f2132e96ae6c7a4e", "definition_digest": null, "required_operations": [], "support_state": "partial", "source_hashes": {"dsl_catalogue": "f2132e96ae6c7a4e"}, "confidence": 0.8, "evidence": ["Mann-Whitney"], "order_basis": "analysis_only", "id": "assay:1"}]}