Single-cell and spatial transcriptomics reveal 5-methylcytosine RNA methylation regulators immunologically reprograms tumor microenvironment characterizations, immunotherapy response and precision treatment of clear cell renal cell carcinoma
•We first revealed the relationship between the estimation of stromal, immune cells score and 5-methylcytosine (m5C) regulators at the pan-cancer level (33 types of cancer), and then depicted the association between m5C regulators and tumor-infiltrating immune cells in a meta-cohort of more than 100...
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Published in | Translational oncology Vol. 35; p. 101726 |
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Main Authors | , , , , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
01.09.2023
Neoplasia Press Elsevier |
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Abstract | •We first revealed the relationship between the estimation of stromal, immune cells score and 5-methylcytosine (m5C) regulators at the pan-cancer level (33 types of cancer), and then depicted the association between m5C regulators and tumor-infiltrating immune cells in a meta-cohort of more than 1000 patients with RCC.•Next, we established a novel 5-methylcytosine RNA modification related gene index (M5CRMRGI).•Additionally, we studied the effect of m5C on tumor microenvironment (TME) distribution, using single-cell sequencing data for in-depth analysis, and finally verified it using spatial sequencing data.•Notably, we predicted the efficacy of m5C on adjuvant therapy, which was verified in real-world immunological and targeted therapy cohorts.
Clear cell Renal Cell Carcinoma (ccRCC) is a highly heterogeneous disease, making it challenging to predict prognosis and therapy efficacy. In this study, we aimed to explore the role of 5-methylcytosine (m5C) RNA modification in ccRCC and its potential as a predictor for therapy response and overall survival (OS). We established a novel 5-methylcytosine RNA modification-related gene index (M5CRMRGI) and studied its effect on the tumor microenvironment (TME) using single-cell sequencing data for in-depth analysis, and verified it using spatial sequencing data. Our results showed that M5CRMRGI is an independent predictor of OS in multiple datasets and exhibited outstanding performance in predicting the OS of ccRCC. Distinct mutation profiles, hallmark pathways, and infiltration of immune cells in TME were observed between high- and low-M5CRMRGI groups. Single-cell/spatial transcriptomics revealed that M5CRMRGI could reprogram the distribution of tumor-infiltrating immune cells. Moreover, significant differences in tumor immunogenicity and tumor immune dysfunction and exclusion (TIDE) were observed between the two risk groups, suggesting a better response to immune checkpoint blockade therapy of the high-risk group. We also predicted six potential drugs binding to the core target of the M5CRMRGI signature via molecular docking. Real-world treatment cohort data proved once again that high-risk patients were appropriate for immune checkpoint blockade therapy, while low-risk patients were appropriate for Everolimus. Our study shows that the m5C modification landscape plays a role in TME distribution. The proposed M5CRMRGI-guided strategy for predicting survival and immunotherapy efficacy, we reported here, might also be applied to more cancers other than ccRCC. |
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AbstractList | Clear cell Renal Cell Carcinoma (ccRCC) is a highly heterogeneous disease, making it challenging to predict prognosis and therapy efficacy. In this study, we aimed to explore the role of 5-methylcytosine (m5C) RNA modification in ccRCC and its potential as a predictor for therapy response and overall survival (OS). We established a novel 5-methylcytosine RNA modification-related gene index (M5CRMRGI) and studied its effect on the tumor microenvironment (TME) using single-cell sequencing data for in-depth analysis, and verified it using spatial sequencing data. Our results showed that M5CRMRGI is an independent predictor of OS in multiple datasets and exhibited outstanding performance in predicting the OS of ccRCC. Distinct mutation profiles, hallmark pathways, and infiltration of immune cells in TME were observed between high- and low-M5CRMRGI groups. Single-cell/spatial transcriptomics revealed that M5CRMRGI could reprogram the distribution of tumor-infiltrating immune cells. Moreover, significant differences in tumor immunogenicity and tumor immune dysfunction and exclusion (TIDE) were observed between the two risk groups, suggesting a better response to immune checkpoint blockade therapy of the high-risk group. We also predicted six potential drugs binding to the core target of the M5CRMRGI signature via molecular docking. Real-world treatment cohort data proved once again that high-risk patients were appropriate for immune checkpoint blockade therapy, while low-risk patients were appropriate for Everolimus. Our study shows that the m5C modification landscape plays a role in TME distribution. The proposed M5CRMRGI-guided strategy for predicting survival and immunotherapy efficacy, we reported here, might also be applied to more cancers other than ccRCC. • We first revealed the relationship between the estimation of stromal, immune cells score and 5-methylcytosine (m5C) regulators at the pan-cancer level (33 types of cancer), and then depicted the association between m5C regulators and tumor-infiltrating immune cells in a meta-cohort of more than 1000 patients with RCC. • Next, we established a novel 5-methylcytosine RNA modification related gene index (M5CRMRGI). • Additionally, we studied the effect of m5C on tumor microenvironment (TME) distribution, using single-cell sequencing data for in-depth analysis, and finally verified it using spatial sequencing data. • Notably, we predicted the efficacy of m5C on adjuvant therapy, which was verified in real-world immunological and targeted therapy cohorts. Clear cell Renal Cell Carcinoma (ccRCC) is a highly heterogeneous disease, making it challenging to predict prognosis and therapy efficacy. In this study, we aimed to explore the role of 5-methylcytosine (m5C) RNA modification in ccRCC and its potential as a predictor for therapy response and overall survival (OS). We established a novel 5-methylcytosine RNA modification-related gene index (M5CRMRGI) and studied its effect on the tumor microenvironment (TME) using single-cell sequencing data for in-depth analysis, and verified it using spatial sequencing data. Our results showed that M5CRMRGI is an independent predictor of OS in multiple datasets and exhibited outstanding performance in predicting the OS of ccRCC. Distinct mutation profiles, hallmark pathways, and infiltration of immune cells in TME were observed between high- and low-M5CRMRGI groups. Single-cell/spatial transcriptomics revealed that M5CRMRGI could reprogram the distribution of tumor-infiltrating immune cells. Moreover, significant differences in tumor immunogenicity and tumor immune dysfunction and exclusion (TIDE) were observed between the two risk groups, suggesting a better response to immune checkpoint blockade therapy of the high-risk group. We also predicted six potential drugs binding to the core target of the M5CRMRGI signature via molecular docking. Real-world treatment cohort data proved once again that high-risk patients were appropriate for immune checkpoint blockade therapy, while low-risk patients were appropriate for Everolimus. Our study shows that the m5C modification landscape plays a role in TME distribution. The proposed M5CRMRGI-guided strategy for predicting survival and immunotherapy efficacy, we reported here, might also be applied to more cancers other than ccRCC. •We first revealed the relationship between the estimation of stromal, immune cells score and 5-methylcytosine (m5C) regulators at the pan-cancer level (33 types of cancer), and then depicted the association between m5C regulators and tumor-infiltrating immune cells in a meta-cohort of more than 1000 patients with RCC.•Next, we established a novel 5-methylcytosine RNA modification related gene index (M5CRMRGI).•Additionally, we studied the effect of m5C on tumor microenvironment (TME) distribution, using single-cell sequencing data for in-depth analysis, and finally verified it using spatial sequencing data.•Notably, we predicted the efficacy of m5C on adjuvant therapy, which was verified in real-world immunological and targeted therapy cohorts. Clear cell Renal Cell Carcinoma (ccRCC) is a highly heterogeneous disease, making it challenging to predict prognosis and therapy efficacy. In this study, we aimed to explore the role of 5-methylcytosine (m5C) RNA modification in ccRCC and its potential as a predictor for therapy response and overall survival (OS). We established a novel 5-methylcytosine RNA modification-related gene index (M5CRMRGI) and studied its effect on the tumor microenvironment (TME) using single-cell sequencing data for in-depth analysis, and verified it using spatial sequencing data. Our results showed that M5CRMRGI is an independent predictor of OS in multiple datasets and exhibited outstanding performance in predicting the OS of ccRCC. Distinct mutation profiles, hallmark pathways, and infiltration of immune cells in TME were observed between high- and low-M5CRMRGI groups. Single-cell/spatial transcriptomics revealed that M5CRMRGI could reprogram the distribution of tumor-infiltrating immune cells. Moreover, significant differences in tumor immunogenicity and tumor immune dysfunction and exclusion (TIDE) were observed between the two risk groups, suggesting a better response to immune checkpoint blockade therapy of the high-risk group. We also predicted six potential drugs binding to the core target of the M5CRMRGI signature via molecular docking. Real-world treatment cohort data proved once again that high-risk patients were appropriate for immune checkpoint blockade therapy, while low-risk patients were appropriate for Everolimus. Our study shows that the m5C modification landscape plays a role in TME distribution. The proposed M5CRMRGI-guided strategy for predicting survival and immunotherapy efficacy, we reported here, might also be applied to more cancers other than ccRCC. |
ArticleNumber | 101726 |
Author | Gui, Cheng-Peng Shu, Guan-Nan Wu, Rong-Pei Tang, Yi-Ming Wei, Jin-Huan Luo, Jun-Hang Zhang, Chi |
Author_xml | – sequence: 1 givenname: Cheng-Peng orcidid: 0000-0003-1067-0377 surname: Gui fullname: Gui, Cheng-Peng email: Chengpeng.Gui@utoronto.ca organization: Department of Urology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, PR China – sequence: 2 givenname: Jin-Huan surname: Wei fullname: Wei, Jin-Huan organization: Department of Urology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, PR China – sequence: 3 givenname: Chi surname: Zhang fullname: Zhang, Chi organization: Department of Urology, Third Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, PR China – sequence: 4 givenname: Yi-Ming surname: Tang fullname: Tang, Yi-Ming organization: Department of Urology, Second Affiliated Hospital, Guangzhou Medical University, Guangzhou, Guangdong, PR China – sequence: 5 givenname: Guan-Nan surname: Shu fullname: Shu, Guan-Nan organization: Department of Urology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, PR China – sequence: 6 givenname: Rong-Pei surname: Wu fullname: Wu, Rong-Pei email: wurp@mail.sysu.edu.cn organization: Department of Urology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, PR China – sequence: 7 givenname: Jun-Hang surname: Luo fullname: Luo, Jun-Hang email: luojunh@mail.sysu.edu.cn organization: Department of Urology, First Affiliated Hospital, Sun Yat-sen University, Guangzhou, Guangdong, PR China |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37379773$$D View this record in MEDLINE/PubMed |
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Keywords | Single-cell transcriptomics m5C RNA modification Clear cell renal cell carcinoma Tumor microenvironment Spatial transcriptomics |
Language | English |
License | This is an open access article under the CC BY-NC-ND license. Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
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Snippet | •We first revealed the relationship between the estimation of stromal, immune cells score and 5-methylcytosine (m5C) regulators at the pan-cancer level (33... Clear cell Renal Cell Carcinoma (ccRCC) is a highly heterogeneous disease, making it challenging to predict prognosis and therapy efficacy. In this study, we... • We first revealed the relationship between the estimation of stromal, immune cells score and 5-methylcytosine (m5C) regulators at the pan-cancer level (33... |
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SourceType | Open Website Open Access Repository Aggregation Database Index Database Publisher |
StartPage | 101726 |
SubjectTerms | Clear cell renal cell carcinoma m5C RNA modification Original Research Single-cell transcriptomics Spatial transcriptomics Tumor microenvironment |
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Title | Single-cell and spatial transcriptomics reveal 5-methylcytosine RNA methylation regulators immunologically reprograms tumor microenvironment characterizations, immunotherapy response and precision treatment of clear cell renal cell carcinoma |
URI | https://dx.doi.org/10.1016/j.tranon.2023.101726 https://www.ncbi.nlm.nih.gov/pubmed/37379773 https://search.proquest.com/docview/2831295763 https://pubmed.ncbi.nlm.nih.gov/PMC10316128 https://doaj.org/article/696e429bb2f545a5b0cb3b9bf8c9419d |
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