Association of RNA-modification "writer" genes with prognosis and response to immunotherapy in patients with low-grade glioma
RNA modification is a key regulatory mechanism involved in tumorigenesis, tumor progression, and the immune response. However, the potential role of RNA modification "writer" genes in the immune microenvironment of gliomas and their effect on the response to immunotherapy remains unclear....
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| Veröffentlicht in: | PloS one 2023-01, Vol.18 (1), p.e0279119-e0279119 |
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| creator | Zhang, Lupeng Qu, Chiwen Shi, Chen Wu, Fan Tang, Yifan Li, Yue Li, Jinlong Feng, Huicong Zhong, Suye Yang, Jun Zeng, Xiaomin Peng, Xiaoning |
| description | RNA modification is a key regulatory mechanism involved in tumorigenesis, tumor progression, and the immune response. However, the potential role of RNA modification "writer" genes in the immune microenvironment of gliomas and their effect on the response to immunotherapy remains unclear. The purpose of this study was to evaluate the role of RNA modification "writer" gene in the prognosis and immunotherapy response of low-grade glioma (LGG). The consensus non-negative matrix factorization (CNMF) method was used to identify different RNA modification subtypes. We used a novel eigengene screening method, the variable neighborhood learning Harris Hawks optimizer (VNLHHO), to screen for eigengenes among the RNA modification subtypes. We constructed a principal components analysis score(PCA_score)-based prognostic prediction model and validated it using an independent cohort. We also analyzed the association between PCA_score and the immune and molecular features of LGG. The results suggested that LGG can be divided into two different RNA modification-based subtypes with distinct prognostic and molecular features. High PCA_score was significantly associated with a poor prognosis in LGG and was an independent prognostic factor. A nomogram containing PCA_score and clinical features was constructed, and it showed a significant predictive value. PCA_score was negatively correlated with tumor purity and the abundance of CD4+ T cells in LGG patients. LGG patients with high PCA_score had lower Tumor Immune Dysfunction and Exclusion scores and showed an immunotherapy response. In conclusion, we report a novel RNA modification-based prognostic model for LGG that lays the foundation for evaluating LGG prognosis and developing more effective therapeutic strategies for these tumors. |
| doi_str_mv | 10.1371/journal.pone.0279119 |
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However, the potential role of RNA modification "writer" genes in the immune microenvironment of gliomas and their effect on the response to immunotherapy remains unclear. The purpose of this study was to evaluate the role of RNA modification "writer" gene in the prognosis and immunotherapy response of low-grade glioma (LGG). The consensus non-negative matrix factorization (CNMF) method was used to identify different RNA modification subtypes. We used a novel eigengene screening method, the variable neighborhood learning Harris Hawks optimizer (VNLHHO), to screen for eigengenes among the RNA modification subtypes. We constructed a principal components analysis score(PCA_score)-based prognostic prediction model and validated it using an independent cohort. We also analyzed the association between PCA_score and the immune and molecular features of LGG. The results suggested that LGG can be divided into two different RNA modification-based subtypes with distinct prognostic and molecular features. High PCA_score was significantly associated with a poor prognosis in LGG and was an independent prognostic factor. A nomogram containing PCA_score and clinical features was constructed, and it showed a significant predictive value. PCA_score was negatively correlated with tumor purity and the abundance of CD4+ T cells in LGG patients. LGG patients with high PCA_score had lower Tumor Immune Dysfunction and Exclusion scores and showed an immunotherapy response. In conclusion, we report a novel RNA modification-based prognostic model for LGG that lays the foundation for evaluating LGG prognosis and developing more effective therapeutic strategies for these tumors.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0279119</identifier><identifier>PMID: 36649311</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Algorithms ; Biology and Life Sciences ; Brain tumors ; Care and treatment ; CD4 antigen ; Chemotherapy ; Datasets ; Drug resistance ; Enzymes ; Epigenetics ; Evaluation ; Gene expression ; Genes ; Genetic aspects ; Genomes ; Genomics ; Glioma ; Glioma - diagnosis ; Glioma - genetics ; Glioma - therapy ; Gliomas ; Health aspects ; Humans ; Immune response ; Immune system ; Immunotherapy ; Lymphocytes ; Lymphocytes T ; Medical prognosis ; Medicine and Health Sciences ; Microenvironments ; Mutation ; Nervous system ; Nomograms ; Nomographs ; Patient outcomes ; Prediction models ; Principal components analysis ; Prognosis ; Radiation therapy ; Regulatory mechanisms (biology) ; Research and analysis methods ; Ribonucleic acid ; RNA ; RNA modification ; RNA processing ; Software packages ; Survival analysis ; Tumor Microenvironment - genetics ; Tumorigenesis ; Tumors</subject><ispartof>PloS one, 2023-01, Vol.18 (1), p.e0279119-e0279119</ispartof><rights>Copyright: © 2023 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</rights><rights>COPYRIGHT 2023 Public Library of Science</rights><rights>2023 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2023 Zhang et al 2023 Zhang et al</rights><rights>2023 Zhang et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c641t-c940b1d1e058f8fbd5b053660aec59c2b10fc583c4f1e1dc11ea9ef2c7df53763</cites><orcidid>0000-0001-9383-7608</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9844866/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC9844866/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79343,79344</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36649311$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Lupeng</creatorcontrib><creatorcontrib>Qu, Chiwen</creatorcontrib><creatorcontrib>Shi, Chen</creatorcontrib><creatorcontrib>Wu, Fan</creatorcontrib><creatorcontrib>Tang, Yifan</creatorcontrib><creatorcontrib>Li, Yue</creatorcontrib><creatorcontrib>Li, Jinlong</creatorcontrib><creatorcontrib>Feng, Huicong</creatorcontrib><creatorcontrib>Zhong, Suye</creatorcontrib><creatorcontrib>Yang, Jun</creatorcontrib><creatorcontrib>Zeng, Xiaomin</creatorcontrib><creatorcontrib>Peng, Xiaoning</creatorcontrib><title>Association of RNA-modification "writer" genes with prognosis and response to immunotherapy in patients with low-grade glioma</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>RNA modification is a key regulatory mechanism involved in tumorigenesis, tumor progression, and the immune response. However, the potential role of RNA modification "writer" genes in the immune microenvironment of gliomas and their effect on the response to immunotherapy remains unclear. The purpose of this study was to evaluate the role of RNA modification "writer" gene in the prognosis and immunotherapy response of low-grade glioma (LGG). The consensus non-negative matrix factorization (CNMF) method was used to identify different RNA modification subtypes. We used a novel eigengene screening method, the variable neighborhood learning Harris Hawks optimizer (VNLHHO), to screen for eigengenes among the RNA modification subtypes. We constructed a principal components analysis score(PCA_score)-based prognostic prediction model and validated it using an independent cohort. We also analyzed the association between PCA_score and the immune and molecular features of LGG. The results suggested that LGG can be divided into two different RNA modification-based subtypes with distinct prognostic and molecular features. High PCA_score was significantly associated with a poor prognosis in LGG and was an independent prognostic factor. A nomogram containing PCA_score and clinical features was constructed, and it showed a significant predictive value. PCA_score was negatively correlated with tumor purity and the abundance of CD4+ T cells in LGG patients. LGG patients with high PCA_score had lower Tumor Immune Dysfunction and Exclusion scores and showed an immunotherapy response. In conclusion, we report a novel RNA modification-based prognostic model for LGG that lays the foundation for evaluating LGG prognosis and developing more effective therapeutic strategies for these tumors.</description><subject>Algorithms</subject><subject>Biology and Life Sciences</subject><subject>Brain tumors</subject><subject>Care and treatment</subject><subject>CD4 antigen</subject><subject>Chemotherapy</subject><subject>Datasets</subject><subject>Drug resistance</subject><subject>Enzymes</subject><subject>Epigenetics</subject><subject>Evaluation</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic aspects</subject><subject>Genomes</subject><subject>Genomics</subject><subject>Glioma</subject><subject>Glioma - diagnosis</subject><subject>Glioma - genetics</subject><subject>Glioma - therapy</subject><subject>Gliomas</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Immune response</subject><subject>Immune system</subject><subject>Immunotherapy</subject><subject>Lymphocytes</subject><subject>Lymphocytes T</subject><subject>Medical prognosis</subject><subject>Medicine and Health Sciences</subject><subject>Microenvironments</subject><subject>Mutation</subject><subject>Nervous system</subject><subject>Nomograms</subject><subject>Nomographs</subject><subject>Patient outcomes</subject><subject>Prediction models</subject><subject>Principal components analysis</subject><subject>Prognosis</subject><subject>Radiation therapy</subject><subject>Regulatory mechanisms (biology)</subject><subject>Research and analysis methods</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>RNA modification</subject><subject>RNA processing</subject><subject>Software packages</subject><subject>Survival analysis</subject><subject>Tumor Microenvironment - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Lupeng</au><au>Qu, Chiwen</au><au>Shi, Chen</au><au>Wu, Fan</au><au>Tang, Yifan</au><au>Li, Yue</au><au>Li, Jinlong</au><au>Feng, Huicong</au><au>Zhong, Suye</au><au>Yang, Jun</au><au>Zeng, Xiaomin</au><au>Peng, Xiaoning</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Association of RNA-modification "writer" genes with prognosis and response to immunotherapy in patients with low-grade glioma</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2023-01-17</date><risdate>2023</risdate><volume>18</volume><issue>1</issue><spage>e0279119</spage><epage>e0279119</epage><pages>e0279119-e0279119</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>RNA modification is a key regulatory mechanism involved in tumorigenesis, tumor progression, and the immune response. However, the potential role of RNA modification "writer" genes in the immune microenvironment of gliomas and their effect on the response to immunotherapy remains unclear. The purpose of this study was to evaluate the role of RNA modification "writer" gene in the prognosis and immunotherapy response of low-grade glioma (LGG). The consensus non-negative matrix factorization (CNMF) method was used to identify different RNA modification subtypes. We used a novel eigengene screening method, the variable neighborhood learning Harris Hawks optimizer (VNLHHO), to screen for eigengenes among the RNA modification subtypes. We constructed a principal components analysis score(PCA_score)-based prognostic prediction model and validated it using an independent cohort. We also analyzed the association between PCA_score and the immune and molecular features of LGG. The results suggested that LGG can be divided into two different RNA modification-based subtypes with distinct prognostic and molecular features. High PCA_score was significantly associated with a poor prognosis in LGG and was an independent prognostic factor. A nomogram containing PCA_score and clinical features was constructed, and it showed a significant predictive value. PCA_score was negatively correlated with tumor purity and the abundance of CD4+ T cells in LGG patients. LGG patients with high PCA_score had lower Tumor Immune Dysfunction and Exclusion scores and showed an immunotherapy response. In conclusion, we report a novel RNA modification-based prognostic model for LGG that lays the foundation for evaluating LGG prognosis and developing more effective therapeutic strategies for these tumors.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>36649311</pmid><doi>10.1371/journal.pone.0279119</doi><tpages>e0279119</tpages><orcidid>https://orcid.org/0000-0001-9383-7608</orcidid><oa>free_for_read</oa></addata></record> |
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| recordid | cdi_plos_journals_2766402628 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Algorithms Biology and Life Sciences Brain tumors Care and treatment CD4 antigen Chemotherapy Datasets Drug resistance Enzymes Epigenetics Evaluation Gene expression Genes Genetic aspects Genomes Genomics Glioma Glioma - diagnosis Glioma - genetics Glioma - therapy Gliomas Health aspects Humans Immune response Immune system Immunotherapy Lymphocytes Lymphocytes T Medical prognosis Medicine and Health Sciences Microenvironments Mutation Nervous system Nomograms Nomographs Patient outcomes Prediction models Principal components analysis Prognosis Radiation therapy Regulatory mechanisms (biology) Research and analysis methods Ribonucleic acid RNA RNA modification RNA processing Software packages Survival analysis Tumor Microenvironment - genetics Tumorigenesis Tumors |
| title | Association of RNA-modification "writer" genes with prognosis and response to immunotherapy in patients with low-grade glioma |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-02T09%3A26%3A35IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Association%20of%20RNA-modification%20%22writer%22%20genes%20with%20prognosis%20and%20response%20to%20immunotherapy%20in%20patients%20with%20low-grade%20glioma&rft.jtitle=PloS%20one&rft.au=Zhang,%20Lupeng&rft.date=2023-01-17&rft.volume=18&rft.issue=1&rft.spage=e0279119&rft.epage=e0279119&rft.pages=e0279119-e0279119&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0279119&rft_dat=%3Cgale_plos_%3EA733560409%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2766402628&rft_id=info:pmid/36649311&rft_galeid=A733560409&rft_doaj_id=oai_doaj_org_article_b0012f844cb54fe2b7e243d605e15e4f&rfr_iscdi=true |