{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,27]],"date-time":"2026-04-27T23:28:27Z","timestamp":1777332507525,"version":"3.51.4"},"reference-count":81,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,8,1]],"date-time":"2025-08-01T00:00:00Z","timestamp":1754006400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>Stomach adenocarcinoma (STAD) exhibits high molecular heterogeneity and poor prognosis, necessitating robust biomarkers for risk stratification. While SUMOylation, a post-translational modification, regulates tumor progression, its prognostic and immunological roles in STAD remain underexplored.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>Prognostic SUMOylation-related genes (SRGs) were screened via univariate Cox regression, and patients were stratified into molecular subtypes using unsupervised consensus clustering. A SUMOylation Risk Score (SRS) model was developed using 69 machine learning models across 10 algorithms, with performance evaluated by C-index and AUC. Immune infiltration, pathway enrichment identified key SRGs, and <jats:italic>in vitro<\/jats:italic> functional assays were validated.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Two molecular subtypes (A\/B) with distinct SUMOylation patterns, survival outcomes (log-rank <jats:italic>p<\/jats:italic> &amp;lt; 0.001), and immune microenvironments were identified. The random survival forest (RSF)-based SRS model (AUC: 0.97) stratified patients into high-\/low-risk groups, where high-risk patients exhibited advanced tumor stages, immune suppression, and elevated TIDE scores (<jats:italic>p<\/jats:italic> &amp;lt; 0.001). Functional enrichment linked low-risk groups to genome stability pathways (DNA repair, cell cycle control). <jats:italic>In vitro<\/jats:italic> validation confirmed that L3MBTL2 and VHL knockdown promoted proliferation, migration, and invasion in AGS cells (<jats:italic>p<\/jats:italic> &amp;lt; 0.05).<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>This study establishes SRGs as independent prognostic indicators and defines SUMOylation-driven subtypes with distinct immune and molecular features. The SRS model and functional validation of L3MBTL2\/VHL provide actionable insights for personalized STAD management and immunotherapy targeting. (214 words)<\/jats:p><\/jats:sec>","DOI":"10.3389\/fimmu.2025.1527233","type":"journal-article","created":{"date-parts":[[2025,8,1]],"date-time":"2025-08-01T05:33:26Z","timestamp":1754026406000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":1,"title":["SUMOylation-related genes define prognostic subtypes in stomach adenocarcinoma: integrating single-cell analysis and machine learning analyses"],"prefix":"10.3389","volume":"16","author":[{"given":"Kaiping","family":"Luo","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Donghui","family":"Xing","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiang","family":"He","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yixin","family":"Zhai","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yanan","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hongjie","family":"Zhan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhigang","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2025,8,1]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1186\/s13045-023-01451-3","article-title":"Gastric cancer treatment: recent progress and future perspectives","volume":"16","author":"Guan","year":"2023","journal-title":"J Hematol OncolJ Hematol Oncol"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.3322\/caac.21660","article-title":"Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries","volume":"71","author":"Sung","year":"2021","journal-title":"CA Cancer J Clin"},{"key":"B3","doi-asserted-by":"publisher","first-page":"22","DOI":"10.1186\/s40880-019-0368-6","article-title":"Current cancer situation in China: good or bad news from the 2018 Global Cancer Statistics","volume":"39","author":"Feng","year":"2019","journal-title":"Cancer Commun"},{"key":"B4","doi-asserted-by":"publisher","DOI":"10.1053\/j.gastro.2017.04.022","article-title":"Global prevalence of helicobacter pylori infection: systematic review and meta-analysis","volume":"153","author":"Hooi","year":"2017","journal-title":"Gastroenterology"},{"key":"B5","doi-asserted-by":"publisher","first-page":"398","DOI":"10.1038\/35006081","article-title":"Interleukin-1 polymorphisms associated with increased risk of gastric cancer","volume":"404","author":"El-Omar","year":"2000","journal-title":"Nature"},{"key":"B6","doi-asserted-by":"publisher","first-page":"1153","DOI":"10.1053\/j.gastro.2015.05.059","article-title":"Genetics and molecular pathogenesis of gastric adenocarcinoma","volume":"149","author":"Tan","year":"2015","journal-title":"Gastroenterology"},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1146\/annurev-pathol-032520-024949","article-title":"The spectrum of helicobacter-mediated diseases","volume":"16","author":"Robinson","year":"2021","journal-title":"Annu Rev Pathol"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.3892\/ijo.2018.4280","article-title":"The post-translational modification, SUMOylation, and cancer (Review)","volume":"52","author":"Han","year":"2018","journal-title":"Int J Oncol"},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.1002\/emmm.201100707","article-title":"Ubiquitylation in immune disorders and cancer: from molecular mechanisms to therapeutic implications","volume":"4","author":"Fulda","year":"2012","journal-title":"EMBO Mol Med"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1038\/nrc.2016.143","article-title":"SUMO and the robustness of cancer","volume":"17","author":"Seeler","year":"2017","journal-title":"Nat Rev Cancer"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1016\/j.tibs.2015.09.006","article-title":"SUMOylation-mediated regulation of cell cycle progression and cancer","volume":"40","author":"Eifler","year":"2015","journal-title":"Trends Biochem Sci"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.3390\/ijms20163895","article-title":"The SUMO pathway in hematomalignancies and their response to therapies","volume":"20","author":"Boulanger","year":"2019","journal-title":"Int J Mol Sci"},{"key":"B13","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1186\/s11658-024-00624-3","article-title":"Crosstalk between SUMOylation and other post-translational modifications in breast cancer","volume":"29","author":"Wei","year":"2024","journal-title":"Cell Mol Biol Lett"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.3390\/ijms21093207","article-title":"Post-translational modifications of transcription factors harnessing the etiology and pathophysiology in colonic diseases","volume":"21","author":"Hsu","year":"2020","journal-title":"Int J Mol Sci"},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1038\/nmeth.1226","article-title":"Mapping and quantifying mammalian transcriptomes by RNA-Seq","volume":"5","author":"Mortazavi","year":"2008","journal-title":"Nat Methods"},{"key":"B16","doi-asserted-by":"publisher","first-page":"193","DOI":"10.1016\/j.ejca.2021.03.005","article-title":"Applications of single-cell and bulk RNA sequencing in onco-immunology","volume":"149","author":"Kuksin","year":"2021","journal-title":"Eur J Cancer Oxf Engl 1990"},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2022.898925","article-title":"Integration of bulk RNA sequencing and single-cell RNA sequencing to reveal uveal melanoma tumor heterogeneity and cells related to survival","volume":"13","author":"Gao","year":"2022","journal-title":"Front Immunol"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1038\/bjc.2017.220","article-title":"HYPE or HOPE: the prognostic value of infiltrating immune cells in cancer","volume":"117","author":"Barnes","year":"2017","journal-title":"Br J Cancer"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1016\/j.ccr.2013.03.018","article-title":"Relapse or eradication of cancer is predicted by peptide-major histocompatibility complex affinity","volume":"23","author":"Engels","year":"2013","journal-title":"Cancer Cell"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.656364","article-title":"Aspects of the tumor microenvironment involved in immune resistance and drug resistance","volume":"12","author":"Khalaf","year":"2021","journal-title":"Front Immunol"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2020.01280","article-title":"Cancer stem cells-origins and biomarkers: perspectives for targeted personalized therapies","volume":"11","author":"Walcher","year":"2020","journal-title":"Front Immunol"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1002\/cac2.12012","article-title":"Emerging role of deep learning-based artificial intelligence in tumor pathology","volume":"40","author":"Jiang","year":"2020","journal-title":"Cancer Commun Lond Engl"},{"key":"B23","doi-asserted-by":"publisher","DOI":"10.1038\/s41573-019-0024-5","article-title":"Applications of machine learning in drug discovery and development","volume":"18","author":"Vamathevan","year":"2019","journal-title":"Nat Rev Drug Discov"},{"key":"B24","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1186\/s12967-017-1285-6","article-title":"In silico prediction of novel therapeutic targets using gene\u2013disease association data","volume":"15","author":"Ferrero","year":"2017","journal-title":"J Transl Med"},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1093\/bib\/bbw113","article-title":"A review on machine learning principles for multi-view biological data integration","volume":"19","author":"Li","year":"2018","journal-title":"Brief Bioinform"},{"key":"B26","doi-asserted-by":"publisher","DOI":"10.1016\/j.artmed.2019.07.007","article-title":"Data-driven modeling and prediction of blood glucose dynamics: Machine learning applications in type 1 diabetes","volume":"98","author":"Woldaregay","year":"2019","journal-title":"Artif Intell Med"},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkaa1020","article-title":"TISCH: a comprehensive web resource enabling interactive single-cell transcriptome visualization of tumor microenvironment","volume":"49","author":"Sun","year":"2021","journal-title":"Nucleic Acids Res"},{"key":"B28","doi-asserted-by":"publisher","first-page":"3573","DOI":"10.1016\/j.cell.2021.04.048","article-title":"Integrated analysis of multimodal single-cell data","volume":"184","author":"Hao","year":"2021","journal-title":"Cell"},{"key":"B29","doi-asserted-by":"publisher","DOI":"10.1021\/acs.chemrestox.2c00245","article-title":"Navigating transcriptomic connectivity mapping workflows to link chemicals with bioactivities","volume":"35","author":"Shah","year":"2022","journal-title":"Chem Res Toxicol"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.3389\/fcell.2023.1094588","article-title":"SUMOylation patterns and signature characterize the tumor microenvironment and predict prognosis in lung adenocarcinoma","volume":"11","author":"Chen","year":"2023","journal-title":"Front Cell Dev Biol"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.1093\/nar\/gkv007","article-title":"limma powers differential expression analyses for RNA-sequencing and microarray studies","volume":"43","author":"Ritchie","year":"2015","journal-title":"Nucleic Acids Res"},{"key":"B32","doi-asserted-by":"publisher","DOI":"10.1038\/s41576-018-0088-9","article-title":"Challenges in unsupervised clustering of single-cell RNA-seq data","volume":"20","author":"Kiselev","year":"2019","journal-title":"Nat Rev Genet"},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2024.1460547","article-title":"Integrating multi-omics and machine learning survival frameworks to build a prognostic model based on immune function and cell death patterns in a lung adenocarcinoma cohort","volume":"15","author":"Xie","year":"2024","journal-title":"Front Immunol"},{"key":"B34","doi-asserted-by":"publisher","first-page":"393","DOI":"10.1186\/s12967-024-05158-y","article-title":"Comprehensive analysis of bulk and single-cell transcriptomic data reveals a novel signature associated with endoplasmic reticulum stress, lipid metabolism, and liver metastasis in pancreatic cancer","volume":"22","author":"Liu","year":"2024","journal-title":"J Transl Med"},{"key":"B35","doi-asserted-by":"publisher","first-page":"816","DOI":"10.1038\/s41467-022-28421-6","article-title":"Machine learning-based integration develops an immune-derived lncRNA signature for improving outcomes in colorectal cancer","volume":"13","author":"Liu","year":"2022","journal-title":"Nat Commun"},{"key":"B36","doi-asserted-by":"publisher","DOI":"10.1186\/s12964-021-00814-y","article-title":"Comprehensive analysis of a TNF family based-signature in diffuse gliomas with regard to prognosis and immune significance","volume":"20","author":"Wang","year":"2022","journal-title":"Cell Commun Signal CCS"},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1038\/s41591-018-0136-1","article-title":"Signatures of T cell dysfunction and exclusion predict cancer immunotherapy response","volume":"24","author":"Jiang","year":"2018","journal-title":"Nat Med"},{"key":"B38","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0107468","article-title":"pRRophetic: an R package for prediction of clinical chemotherapeutic response from tumor gene expression levels","volume":"9","author":"Geeleher","year":"2014","journal-title":"PloS One"},{"key":"B39","doi-asserted-by":"publisher","first-page":"1113","DOI":"10.1053\/j.gastro.2016.01.028","article-title":"Association between helicobacter pylori eradication and gastric cancer incidence: A systematic review and meta-analysis","volume":"150","author":"Lee","year":"2016","journal-title":"Gastroenterology"},{"key":"B40","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-0691.2009.03031.x","article-title":"Helicobacter pylori and gastric adenocarcinoma","volume":"15","author":"Herrera","year":"2009","journal-title":"Clin Microbiol Infect Off Publ Eur Soc Clin Microbiol Infect Dis"},{"key":"B41","doi-asserted-by":"publisher","first-page":"196","DOI":"10.1016\/j.canlet.2013.08.016","article-title":"Helicobacter pylori-induced gastric inflammation and gastric cancer","volume":"345","author":"Wang","year":"2014","journal-title":"Cancer Lett"},{"key":"B42","unstructured":"Insights in Post-Translational Modifications: Ubiquitin and SUMO"},{"key":"B43","doi-asserted-by":"publisher","DOI":"10.3390\/ijms23063281","article-title":"Insights in post-translational modifications: ubiquitin and SUMO","volume":"23","author":"Salas-Lloret","year":"2022","journal-title":"Int J Mol Sci"},{"key":"B44","doi-asserted-by":"publisher","first-page":"842","DOI":"10.1038\/s41419-021-04127-3","article-title":"NSUN2 modified by SUMO-2\/3 promotes gastric cancer progression and regulates mRNA m5C methylation","volume":"12","author":"Hu","year":"2021","journal-title":"Cell Death Dis"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms12326","article-title":"Role of SUMO activating enzyme in cancer stem cell maintenance and self-renewal","volume":"7","author":"Du","year":"2016","journal-title":"Nat Commun"},{"key":"B46","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.065565","article-title":"SUMOylation modulates the function of Aurora-B kinase","volume":"123","author":"Fern\u00e1ndez-Miranda","year":"2010","journal-title":"J Cell Sci"},{"key":"B47","doi-asserted-by":"publisher","DOI":"10.1016\/s0960-9822(00)00673-4","article-title":"INCENP binds the Aurora-related kinase AIRK2 and is required to target it to chromosomes, the central spindle and cleavage furrow","volume":"10","author":"Adams","year":"2000","journal-title":"Curr Biol CB"},{"key":"B48","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/djr326","article-title":"mRNA expression of BRCA1, PIAS1, and PIAS4 and survival after second-line docetaxel in advanced gastric cancer","volume":"103","author":"Wei","year":"2011","journal-title":"JNCI J Natl Cancer Inst"},{"key":"B49","doi-asserted-by":"publisher","first-page":"ra88","DOI":"10.1126\/scisignal.2003485","article-title":"RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage","volume":"5","author":"Guzzo","year":"2012","journal-title":"Sci Signal"},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0089506","article-title":"Sentrin\/SUMO specific proteases as novel tissue-selective modulators of vitamin D receptor-mediated signaling","volume":"9","author":"Lee","year":"2014","journal-title":"PloS One"},{"key":"B51","doi-asserted-by":"publisher","first-page":"38","DOI":"10.1186\/s13072-021-00412-9","article-title":"SUMOylated non-canonical polycomb PRC1.6 complex as a prerequisite for recruitment of transcription factor RBPJ","volume":"14","author":"Sotomska","year":"2021","journal-title":"Epigenet Chromatin"},{"key":"B52","doi-asserted-by":"publisher","DOI":"10.1016\/s0960-9822(98)70044-2","article-title":"Ubc9p and the conjugation of SUMO-1 to RanGAP1 and RanBP2","volume":"8","author":"Saitoh","year":"1998","journal-title":"Curr Biol CB"},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1128\/MCB.01603-09","article-title":"Phosphorylation-dependent interaction of SATB1 and PIAS1 directs SUMO-regulated caspase cleavage of SATB1","volume":"30","author":"Tan","year":"2010","journal-title":"Mol Cell Biol"},{"key":"B54","doi-asserted-by":"publisher","DOI":"10.1016\/j.jmb.2018.10.017","article-title":"Conformational flexibility of ubiquitin-modified and SUMO-modified PCNA shown by full-ensemble hybrid methods","volume":"430","author":"Powers","year":"2018","journal-title":"J Mol Biol"},{"key":"B55","doi-asserted-by":"publisher","DOI":"10.1016\/j.biopha.2006.07.082","article-title":"Post-translational modifications of steroid receptors","volume":"60","author":"Faus","year":"2006","journal-title":"BioMed Pharmacother"},{"key":"B56","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1016\/j.mce.2011.10.030","article-title":"The biology of progesterone receptor in the normal mammary gland and in breast cancer","volume":"357","author":"Obr","year":"2012","journal-title":"Mol Cell Endocrinol"},{"key":"B57","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1038\/ncb0204-89","article-title":"Modifying NEMO","volume":"6","author":"Hay","year":"2004","journal-title":"Nat Cell Biol"},{"key":"B58","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2021.784319","article-title":"In pursuit of distinctiveness: transmembrane nucleoporins and their disease associations","volume":"11","author":"Bindra","year":"2021","journal-title":"Front Oncol"},{"key":"B59","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.198390","article-title":"Localisation of Nup153 and SENP1 to nuclear pore complexes is required for 53BP1-mediated DNA double-strand break repair","volume":"130","author":"Duheron","year":"2017","journal-title":"J Cell Sci"},{"key":"B60","doi-asserted-by":"publisher","first-page":"268","DOI":"10.1186\/s12876-023-02850-z","article-title":"SMC1A facilitates gastric cancer cell proliferation, migration, and invasion via promoting SNAIL activated EMT","volume":"23","author":"Liu","year":"2023","journal-title":"BMC Gastroenterol"},{"key":"B61","doi-asserted-by":"publisher","DOI":"10.21037\/tcr-22-168","article-title":"In silico development and validation of a novel glucose and lipid metabolism-related gene signature in gastric cancer","volume":"11","author":"Yang","year":"2022","journal-title":"Transl Cancer Res"},{"key":"B62","doi-asserted-by":"publisher","DOI":"10.1007\/s11626-021-00627-w","article-title":"Nucleoporin 37 promotes the cell proliferation, migration, and invasion of gastric cancer through activating the PI3K\/AKT\/mTOR signaling pathway","volume":"57","author":"Zhang","year":"2021","journal-title":"In Vitro Cell Dev Biol Anim"},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.1155\/2023\/6079957","article-title":"Construction of a TTN mutation-based prognostic model for evaluating immune microenvironment, cancer stemness, and outcomes of colorectal cancer patients","volume":"2023","author":"Zhao","year":"2023","journal-title":"Stem Cells Int"},{"key":"B64","doi-asserted-by":"publisher","DOI":"10.1182\/blood.2021013164","article-title":"Genomic landscape of TCR\u03b1\u03b2 and TCR\u03b3\u03b4 T-large granular lymphocyte leukemia","volume":"139","author":"Cheon","year":"2022","journal-title":"Blood"},{"key":"B65","doi-asserted-by":"publisher","DOI":"10.1182\/blood.2021014472","article-title":"Molecular characterization of mutant TP53 acute myeloid leukemia and high-risk myelodysplastic syndrome","volume":"139","author":"Grob","year":"2022","journal-title":"Blood"},{"key":"B66","doi-asserted-by":"publisher","DOI":"10.3390\/cancers15030745","article-title":"DRP1 inhibition enhances venetoclax-induced mitochondrial apoptosis in TP53-mutated acute myeloid leukemia cells through BAX\/BAK activation","volume":"15","author":"Jang","year":"2023","journal-title":"Cancers"},{"key":"B67","doi-asserted-by":"publisher","first-page":"794","DOI":"10.3892\/ol.2021.13055","article-title":"A novel long non-coding RNA TTN-AS1\/microRNA-589-5p\/FOXP1 positive feedback loop increases the proliferation, migration and invasion of pancreatic cancer cell lines","volume":"22","author":"Zhao","year":"2021","journal-title":"Oncol Lett"},{"key":"B68","doi-asserted-by":"publisher","DOI":"10.1016\/j.critrevonc.2022.103841","article-title":"Characteristics of gastric cancer around the world","volume":"181","author":"L\u00f3pez","year":"2023","journal-title":"Crit Rev Oncol Hematol"},{"key":"B69","doi-asserted-by":"publisher","DOI":"10.1002\/cam4.6083","article-title":"Clinical characteristics and prognostic analysis of SMARCA4-deficient non-small cell lung cancer","volume":"12","author":"Liang","year":"2023","journal-title":"Cancer Med"},{"key":"B70","doi-asserted-by":"publisher","DOI":"10.1158\/1055-9965.EPI-09-0729","article-title":"ESR1\/SYNE1 polymorphism and invasive epithelial ovarian cancer risk: an Ovarian Cancer Association Consortium study","volume":"19","author":"Doherty","year":"2010","journal-title":"Cancer Epidemiol biomark Prev Publ Am Assoc Cancer Res Cosponsored Am Soc Prev Oncol"},{"key":"B71","doi-asserted-by":"publisher","DOI":"10.3390\/biomedicines9121819","article-title":"SYNE1 exonic variant rs9479297 contributes to concurrent hepatocellular and transitional cell carcinoma double primary cancer","volume":"9","author":"Chu","year":"2021","journal-title":"Biomedicines"},{"key":"B72","doi-asserted-by":"publisher","DOI":"10.1016\/j.bbcan.2021.188503","article-title":"Roles of CA125 in diagnosis, prediction, and oncogenesis of ovarian cancer","volume":"1875","author":"Zhang","year":"2021","journal-title":"Biochim Biophys Acta BBA - Rev Cancer"},{"key":"B73","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2024.1356913","article-title":"MUC1 and MUC16: critical for immune modulation in cancer therapeutics","volume":"15","author":"Chen","year":"2024","journal-title":"Front Immunol"},{"key":"B74","doi-asserted-by":"publisher","first-page":"181","DOI":"10.1186\/s13048-023-01207-0","article-title":"MUC16 stimulates neutrophils to an inflammatory and immunosuppressive phenotype in ovarian cancer","volume":"16","author":"Wu","year":"2023","journal-title":"J Ovarian Res"},{"key":"B75","doi-asserted-by":"publisher","DOI":"10.1016\/j.stem.2012.06.002","article-title":"The polycomb group protein L3mbtl2 assembles an atypical PRC1-family complex that is essential in pluripotent stem cells and early development","volume":"11","author":"Qin","year":"2012","journal-title":"Cell Stem Cell"},{"key":"B76","doi-asserted-by":"publisher","DOI":"10.1002\/advs.202307526","article-title":"Development of complementary photo-arginine\/lysine to promote discovery of Arg\/Lys hPTMs interactomes","volume":"11","author":"Zong","year":"2024","journal-title":"Adv Sci"},{"key":"B77","doi-asserted-by":"publisher","first-page":"R119","DOI":"10.1186\/gb-2013-14-10-r119","article-title":"A screen for hydroxymethylcytosine and formylcytosine binding proteins suggests functions in transcription and chromatin regulation","volume":"14","author":"Iurlaro","year":"2013","journal-title":"Genome Biol"},{"key":"B78","doi-asserted-by":"publisher","DOI":"10.1097\/CM9.0000000000000094","article-title":"Progress of small ubiquitin-related modifiers in kidney diseases","volume":"132","author":"Li","year":"2019","journal-title":"Chin Med J (Engl)"},{"key":"B79","doi-asserted-by":"publisher","DOI":"10.7150\/ijbs.73398","article-title":"A positive feedback loop between inactive VHL-triggered histone lactylation and PDGFR\u03b2 Signaling drives clear cell renal cell carcinoma progression","volume":"18","author":"Yang","year":"2022","journal-title":"Int J Biol Sci"},{"key":"B80","doi-asserted-by":"publisher","DOI":"10.1016\/s1055-3207(02)00002-9","article-title":"Epidemiologic trends in esophageal and gastric cancer in the United States","volume":"11","author":"Brown","year":"2002","journal-title":"Surg Oncol Clin N Am"},{"key":"B81","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1016\/j.gie.2016.02.028","article-title":"Screening and surveillance for gastric cancer in the United States: Is it needed","volume":"84","author":"Kim","year":"2016","journal-title":"Gastrointest Endosc"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2025.1527233\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,8,1]],"date-time":"2025-08-01T05:33:28Z","timestamp":1754026408000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2025.1527233\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,8,1]]},"references-count":81,"alternative-id":["10.3389\/fimmu.2025.1527233"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2025.1527233","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,8,1]]},"article-number":"1527233"}}