{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,9]],"date-time":"2026-09-09T19:52:00Z","timestamp":1788983520950,"version":"build-2803163510"},"reference-count":32,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,3,6]],"date-time":"2025-03-06T00:00:00Z","timestamp":1741219200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Immunol."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>The tumor microenvironment plays a crucial role in the progression of both glioma and glioma-induced autoimmune encephalitis. However, there remains a significant lack of effective therapeutic targets for these diseases.<\/jats:p><\/jats:sec><jats:sec><jats:title>Method<\/jats:title><jats:p>We collected 54 CT images of glioma patients and 54 glioma-induced autoimmune encephalitis patients, respectively. Radiomics features were extracted from tumors and encephalitis regions using Python, followed by dimensionality reduction via random forest and lasso regression, and construction of radiomics-based risk scores. Genomic data matched with clinical information were analyzed to identify key prognostic genes significantly associated with risk scores. Gene expression was validated by immunohistochemistry using our clinical samples. Immune infiltration was evaluated using five algorithms (MCP-counter, EPIC, TIMER, QUANT and IPS). The association between hub genes and immune checkpoint markers as well as immunoregulation-related genes was also analyzed using Spearman correlation.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>We identified 980 radiomics features both in glioma and encephalitis patient images and selected four key features through lasso regression to build a radiomics-based risk score. COL22A1 was strongly correlated with the risk score and identified as the hub prognostic gene. COL22A1 expression was higher in glioblastoma tissues and cell lines, and correlated with clinical factors such as higher age, WHO grade, and IDH mutation status. Immune infiltration analysis indicated associations with diverse immune and stromal cell populations, including CD8<jats:sup>+<\/jats:sup>T cells, macrophages, and CAFs. COL22A1 was also positively correlated with immune checkpoints and immune-regulated genes.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>Our study highlights the critical role of COL22A1 in gliomas and glioma-Induced Autoimmune Encephalitis, demonstrating its strong association with poor prognosis and its significant involvement in tumor immune regulation.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fimmu.2025.1562070","type":"journal-article","created":{"date-parts":[[2025,3,6]],"date-time":"2025-03-06T05:10:57Z","timestamp":1741237857000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":11,"title":["Artificial intelligence-based radiogenomics reveals the potential immunoregulatory role of COL22A1 in glioma and its induced autoimmune encephalitis"],"prefix":"10.3389","volume":"16","author":[{"given":"Bingchao","family":"Yan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qian","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dacheng","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leili","family":"Ding","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jingfeng","family":"Qu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Renfei","family":"Du","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenjie","family":"Shi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ulf D.","family":"Kahlert","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhengquan","family":"Yu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2025,3,6]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"v1","DOI":"10.1093\/neuonc\/noac202","article-title":"CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2015\u20132019","volume":"24","author":"Ostrom","year":"2022","journal-title":"Neuro-oncology"},{"key":"B2","doi-asserted-by":"publisher","DOI":"10.1007\/s40336-022-00489-6","article-title":"Epidemiology, risk factors, and prognostic factors of gliomas","volume":"10","author":"Pellerino","year":"2022","journal-title":"Clin Trans Imaging"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1002\/cac2.v42.11","article-title":"An update on the molecular biology of glioblastoma, with clinical implications and progress in its treatment","volume":"42","author":"Verdugo","year":"2022","journal-title":"Cancer Commun"},{"key":"B4","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1186\/s13046-022-02349-7","article-title":"Emerging therapies for glioblastoma: current state and future directions","volume":"41","author":"Rong","year":"2022","journal-title":"J Exp Clin Cancer Res"},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1093\/neuonc\/noab106","article-title":"The 2021 WHO classification of tumors of the central nervous system: a summary","volume":"23","author":"Louis","year":"2021","journal-title":"Neuro-oncology"},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa043330","article-title":"Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma","volume":"352","author":"Stupp","year":"2005","journal-title":"N Engl J Med"},{"key":"B7","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1016\/B978-0-12-802997-8.00004-9","article-title":"Surgical approaches for the gliomas","volume":"134","author":"Watts","year":"2016","journal-title":"Handb Clin neurology"},{"key":"B8","doi-asserted-by":"publisher","DOI":"10.1038\/nm.2721","article-title":"A brain tumor molecular imaging strategy using a new triple-modality MRI-photoacoustic-Raman nanoparticle","volume":"18","author":"Kircher","year":"2012","journal-title":"Nat Med"},{"key":"B9","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1158\/0008-5472.CAN-18-1733","article-title":"Temozolomide induces senescence and repression of DNA repair pathways in glioblastoma cells via activation of ATR\u2013CHK1, p21, and NF-\u03baB","volume":"79","author":"Aasland","year":"2019","journal-title":"Cancer Res"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.2174\/156652409788167087","article-title":"Hypoxia and radiation therapy: past history, ongoing research, and future promise","volume":"9","author":"Rockwell","year":"2009","journal-title":"Curr Mol Med"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1016\/j.cpan.2024.12.001","article-title":"Emerging trends and hot topics in the application of multi-omics in drug discovery: A bibliometric and visualized study","volume":"21","author":"Wang","year":"2024","journal-title":"Curr Pharm Anal"},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.1200\/jco.2015.33.15_suppl.2009","article-title":"ReACT: Overall survival from a randomized phase II study of rindopepimut (CDX-110) plus bevacizumab in relapsed glioblastoma","volume":"62","author":"Reardon","year":"2015","journal-title":"Am Soc Clin Oncol"},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.1126\/scitranslmed.aan4220","article-title":"Cancer immunotherapy with recombinant poliovirus induces IFN-dominant activation of dendritic cells and tumor antigen\u2013specific CTLs","volume":"9","author":"Brown","year":"2017","journal-title":"Sci Trans Med"},{"key":"B14","doi-asserted-by":"publisher","first-page":"3721","DOI":"10.3390\/cancers13153721","article-title":"Immunotherapy in glioblastoma: a clinical perspective","volume":"13","author":"Desbaillets","year":"2021","journal-title":"Cancers"},{"key":"B15","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1186\/s13045-024-01634-6","article-title":"Harnessing the tumor microenvironment: targeted cancer therapies through modulation of epithelial-mesenchymal transition","volume":"18","author":"Glaviano","year":"2025","journal-title":"J Hematol Oncol"},{"key":"B16","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1186\/s12943-023-01722-0","article-title":"Gamma delta T-cell-based immune checkpoint therapy: attractive candidate for antitumor treatment","volume":"22","author":"Gao","year":"2023","journal-title":"Mol Cancer"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/s12967-018-1507-6","article-title":"First results on survival from a large Phase 3 clinical trial of an autologous dendritic cell vaccine in newly diagnosed glioblastoma","volume":"16","author":"Liau","year":"2018","journal-title":"J Trans Med"},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.1136\/practneurol-2020-002567","article-title":"Autoimmune encephalitis: clinical spectrum and management","volume":"21","author":"Uy","year":"2021","journal-title":"Pract neurology"},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.3389\/fonc.2023.1254674","article-title":"Case Report: Brain tumor\u2019s pitfalls: two cases of high-grade brain tumors mimicking autoimmune encephalitis with positive onconeuronal antibodies","volume":"13","author":"Consoli","year":"2023","journal-title":"Front Oncol"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.2174\/0118761429273223231124072223","article-title":"Molecular insight into the apoptotic mechanism of cancer cells: an explicative review","volume":"17","author":"Karati","year":"2024","journal-title":"Curr Mol Pharmacol"},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1007\/s00330-022-09066-x","article-title":"Image-based deep learning identifies glioblastoma risk groups with genomic and transcriptomic heterogeneity: a multi-center study","volume":"33","author":"Yan","year":"2023","journal-title":"Eur Radiology"},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.1038\/s41591-019-0349-y","article-title":"Immune and genomic correlates of response to anti-PD-1 immunotherapy in glioblastoma","volume":"25","author":"Zhao","year":"2019","journal-title":"Nat Med"},{"key":"B23","doi-asserted-by":"crossref","DOI":"10.1016\/B978-0-12-809847-9.00022-2","article-title":"Type XXII collagen","volume-title":"Biochemistry of Collagens, Laminins and Elastin","author":"Kehlet","year":"2016"},{"key":"B24","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1158\/2159-8290.CD-18-0193","article-title":"Remodeling of the collagen matrix in aging skin promotes melanoma metastasis and affects immune cell motility","volume":"9","author":"Kaur","year":"2019","journal-title":"Cancer discovery"},{"key":"B25","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s10048-024-00763-x","article-title":"Identification of established and novel extracellular matrix components in glioblastoma as targets for angiogenesis and prognosis","author":"Barbosa","year":"2024","journal-title":"Neurogenetics"},{"key":"B26","doi-asserted-by":"publisher","first-page":"9842","DOI":"10.18632\/aging.205054","article-title":"Prognosis and immunoinfiltration analysis of angiogene-related genes in grade 4 diffuse gliomas","volume":"15","author":"Liu","year":"2023","journal-title":"Aging (Albany NY)"},{"key":"B27","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1186\/s12943-024-01972-6","article-title":"CTLs heterogeneity and plasticity: implications for cancer immunotherapy","volume":"23","author":"Peng","year":"2024","journal-title":"Mol Cancer"},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1002\/imt2.v2.3","article-title":"HPVTIMER: A shiny web application for tumor immune estimation in human papillomavirus-associated cancers","volume":"2","author":"Liu","year":"2023","journal-title":"Imeta"},{"key":"B29","doi-asserted-by":"publisher","first-page":"91779","DOI":"10.18632\/oncotarget.21586","article-title":"Recurrent glioma clinical trial, CheckMate-143: the game is not over yet","volume":"8","author":"Filley","year":"2017","journal-title":"Oncotarget"},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.2174\/1874467217666230908111754","article-title":"At the crossroads of TNF \u03b1 Signaling and cancer","volume":"17","author":"Manohar","year":"2024","journal-title":"Curr Mol Pharmacol"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.2147\/IJGM.S463649","article-title":"Unveiling collagen\u2019s role in breast cancer: insights into expression patterns, functions and clinical implications","volume":"17","author":"Li","year":"2024","journal-title":"Int J Gen Med"},{"key":"B32","doi-asserted-by":"publisher","first-page":"PS18","DOI":"10.1158\/1538-7445.SABCS20-PS18-41","article-title":"Abstract PS18-41: Somatic mutational landscapes of invasive ductal and lobular carcinomas in the GENIE consortium cohort: Real-world gene actionability assessment of 8,756 breast cancer patients","volume":"81","author":"Leal","year":"2021","journal-title":"Cancer Res"}],"container-title":["Frontiers in Immunology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2025.1562070\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,3,6]],"date-time":"2025-03-06T05:11:00Z","timestamp":1741237860000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fimmu.2025.1562070\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,3,6]]},"references-count":32,"alternative-id":["10.3389\/fimmu.2025.1562070"],"URL":"https:\/\/doi.org\/10.3389\/fimmu.2025.1562070","relation":{},"ISSN":["1664-3224"],"issn-type":[{"value":"1664-3224","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,3,6]]},"article-number":"1562070"}}