Integrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype-specific therapeutic strategies

Abstract Localized prostate cancer (PCa) is highly variable in their response to therapies. Although a fraction of this heterogeneity can be explained by clinical factors or genomic and transcriptomic profiling, the proteomic-based profiling of aggressive PCa remains poorly understood. Here, we prof...

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Main Authors: Wei Ou, Xin-Xin Zhang, Bin Li, Ying Tuo, Ren-Xuan Lin, Peng-Fei Liu, Jian-Ping Guo, Hio-Cheng Un, Ming-Hao Li, Jia-Hao Lei, Xiao-Jing Gao, Fu-Fu Zheng, Ling-Wu Chen, Ling-Li Long, Zong-Ren Wang
Format: Article
Language:English
Published: Nature Portfolio 2025-04-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-58569-w
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author Wei Ou
Xin-Xin Zhang
Bin Li
Ying Tuo
Ren-Xuan Lin
Peng-Fei Liu
Jian-Ping Guo
Hio-Cheng Un
Ming-Hao Li
Jia-Hao Lei
Xiao-Jing Gao
Fu-Fu Zheng
Ling-Wu Chen
Ling-Li Long
Zong-Ren Wang
author_facet Wei Ou
Xin-Xin Zhang
Bin Li
Ying Tuo
Ren-Xuan Lin
Peng-Fei Liu
Jian-Ping Guo
Hio-Cheng Un
Ming-Hao Li
Jia-Hao Lei
Xiao-Jing Gao
Fu-Fu Zheng
Ling-Wu Chen
Ling-Li Long
Zong-Ren Wang
author_sort Wei Ou
collection DOAJ
description Abstract Localized prostate cancer (PCa) is highly variable in their response to therapies. Although a fraction of this heterogeneity can be explained by clinical factors or genomic and transcriptomic profiling, the proteomic-based profiling of aggressive PCa remains poorly understood. Here, we profiled the genome, transcriptome, proteome and phosphoproteome of 145 cases of localized PCa in Chinese patients. Proteome-based stratification of localized PCa revealed three subtypes with distinct molecular features: immune subgroup, arachidonic acid metabolic subgroup and sialic acid metabolic subgroup with highest biochemical recurrence (BCR) rates. Further, we nominated NANS protein, a key enzyme in sialic acid synthesis as a potential prognostic biomarker for aggressive PCa and validated in two independent cohorts. Finally, taking advantage of cell-derived orthotopic transplanted mouse models, single-cell RNA sequencing (scRNA-seq) and immunofluorescence analysis, we revealed that targeting NANS can reverse the immunosuppressive microenvironment through restricting the sialoglycan-sialic acid-recognizing immunoglobulin superfamily lectin (Siglec) axis, thereby inhibiting tumor growth of PCa. In sum, we integrate multi-omic data to refine molecular subtyping of localized PCa, and identify NANS as a potential prognostic biomarker and therapeutic option for aggressive PCa.
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spelling doaj-art-9124bc2c6ea9414b8e44768053734a0c2025-08-20T03:07:43ZengNature PortfolioNature Communications2041-17232025-04-0116111710.1038/s41467-025-58569-wIntegrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype-specific therapeutic strategiesWei Ou0Xin-Xin Zhang1Bin Li2Ying Tuo3Ren-Xuan Lin4Peng-Fei Liu5Jian-Ping Guo6Hio-Cheng Un7Ming-Hao Li8Jia-Hao Lei9Xiao-Jing Gao10Fu-Fu Zheng11Ling-Wu Chen12Ling-Li Long13Zong-Ren Wang14Department of Urology, The First Affiliated Hospital, Sun Yat-sen UniversityDepartment of Urology, The First Affiliated Hospital, Sun Yat-sen UniversityClinical Trials Unit, The First Affiliated Hospital, Sun Yat-sen UniversityDepartment of Pathology, The First Affiliated Hospital, Sun Yat-sen UniversityDepartment of Urology, The First Affiliated Hospital, Sun Yat-sen UniversityShanghai Applied Protein Technology Co., LtdInstitute of Precision Medicine, the First Affiliated Hospital, Sun Yat-sen University, GuangzhouDepartment of Urology, The First Affiliated Hospital, Sun Yat-sen UniversityDepartment of Urology, The First Affiliated Hospital, Sun Yat-sen UniversityDepartment of Urology, The First Affiliated Hospital, Sun Yat-sen UniversityShanghai Applied Protein Technology Co., LtdDepartment of Urology, The First Affiliated Hospital, Sun Yat-sen UniversityDepartment of Urology, The First Affiliated Hospital, Sun Yat-sen UniversityClinical Trials Unit, The First Affiliated Hospital, Sun Yat-sen UniversityDepartment of Urology, The First Affiliated Hospital, Sun Yat-sen UniversityAbstract Localized prostate cancer (PCa) is highly variable in their response to therapies. Although a fraction of this heterogeneity can be explained by clinical factors or genomic and transcriptomic profiling, the proteomic-based profiling of aggressive PCa remains poorly understood. Here, we profiled the genome, transcriptome, proteome and phosphoproteome of 145 cases of localized PCa in Chinese patients. Proteome-based stratification of localized PCa revealed three subtypes with distinct molecular features: immune subgroup, arachidonic acid metabolic subgroup and sialic acid metabolic subgroup with highest biochemical recurrence (BCR) rates. Further, we nominated NANS protein, a key enzyme in sialic acid synthesis as a potential prognostic biomarker for aggressive PCa and validated in two independent cohorts. Finally, taking advantage of cell-derived orthotopic transplanted mouse models, single-cell RNA sequencing (scRNA-seq) and immunofluorescence analysis, we revealed that targeting NANS can reverse the immunosuppressive microenvironment through restricting the sialoglycan-sialic acid-recognizing immunoglobulin superfamily lectin (Siglec) axis, thereby inhibiting tumor growth of PCa. In sum, we integrate multi-omic data to refine molecular subtyping of localized PCa, and identify NANS as a potential prognostic biomarker and therapeutic option for aggressive PCa.https://doi.org/10.1038/s41467-025-58569-w
spellingShingle Wei Ou
Xin-Xin Zhang
Bin Li
Ying Tuo
Ren-Xuan Lin
Peng-Fei Liu
Jian-Ping Guo
Hio-Cheng Un
Ming-Hao Li
Jia-Hao Lei
Xiao-Jing Gao
Fu-Fu Zheng
Ling-Wu Chen
Ling-Li Long
Zong-Ren Wang
Integrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype-specific therapeutic strategies
Nature Communications
title Integrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype-specific therapeutic strategies
title_full Integrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype-specific therapeutic strategies
title_fullStr Integrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype-specific therapeutic strategies
title_full_unstemmed Integrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype-specific therapeutic strategies
title_short Integrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype-specific therapeutic strategies
title_sort integrated proteogenomic characterization of localized prostate cancer identifies biological insights and subtype specific therapeutic strategies
url https://doi.org/10.1038/s41467-025-58569-w
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