IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-41139-3.html
   My bibliography  Save this article

Proteogenomics of different urothelial bladder cancer stages reveals distinct molecular features for papillary cancer and carcinoma in situ

Author

Listed:
  • Zhenmei Yao

    (Fudan University)

  • Ning Xu

    (Fudan University)

  • Guoguo Shang

    (Fudan University)

  • Haixing Wang

    (Fudan University)

  • Hui Tao

    (Anhui Medical University)

  • Yunzhi Wang

    (Fudan University)

  • Zhaoyu Qin

    (Fudan University)

  • Subei Tan

    (Fudan University)

  • Jinwen Feng

    (Fudan University)

  • Jiajun Zhu

    (Fudan University)

  • Fahan Ma

    (Fudan University)

  • Sha Tian

    (Fudan University)

  • Qiao Zhang

    (Fudan University)

  • Yuanyuan Qu

    (Fudan University, Shanghai Genitourinary Cancer Institute)

  • Jun Hou

    (Fudan University)

  • Jianming Guo

    (Fudan University)

  • Jianyuan Zhao

    (Shanghai Jiao Tong University School of Medicine
    Zhengzhou University)

  • Yingyong Hou

    (Fudan University)

  • Chen Ding

    (Fudan University)

Abstract

The progression of urothelial bladder cancer (UC) is a complicated multi-step process. We perform a comprehensive multi-omics analysis of 448 samples from 190 UC patients, covering the whole spectrum of disease stages and grades. Proteogenomic integration analysis indicates the mutations of HRAS regulated mTOR signaling to form urothelial papilloma rather than papillary urothelial cancer (PUC). DNA damage is a key signaling pathway in the progression of carcinoma in situ (CIS) and related to APOBEC signature. Glucolipid metabolism increase and lower immune cell infiltration are associated with PUC compared to CIS. Proteomic analysis distinguishes the origins of invasive tumors (PUC-derived and CIS-derived), related to distinct clinical prognosis and molecular features. Additionally, loss of RBPMS, associated with CIS-derived tumors, is validated to increase the activity of AP-1 and promote metastasis. This study reveals the characteristics of two distinct branches (PUC and CIS) of UC progression and may eventually benefit clinical practice.

Suggested Citation

  • Zhenmei Yao & Ning Xu & Guoguo Shang & Haixing Wang & Hui Tao & Yunzhi Wang & Zhaoyu Qin & Subei Tan & Jinwen Feng & Jiajun Zhu & Fahan Ma & Sha Tian & Qiao Zhang & Yuanyuan Qu & Jun Hou & Jianming Gu, 2023. "Proteogenomics of different urothelial bladder cancer stages reveals distinct molecular features for papillary cancer and carcinoma in situ," Nature Communications, Nature, vol. 14(1), pages 1-25, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41139-3
    DOI: 10.1038/s41467-023-41139-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-41139-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-41139-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Sai Ge & Xia Xia & Chen Ding & Bei Zhen & Quan Zhou & Jinwen Feng & Jiajia Yuan & Rui Chen & Yumei Li & Zhongqi Ge & Jiafu Ji & Lianhai Zhang & Jiayuan Wang & Zhongwu Li & Yumei Lai & Ying Hu & Yanyan, 2018. "A proteomic landscape of diffuse-type gastric cancer," Nature Communications, Nature, vol. 9(1), pages 1-16, December.
    2. Yi Liu & Renaud Dentin & Danica Chen & Susan Hedrick & Kim Ravnskjaer & Simon Schenk & Jill Milne & David J. Meyers & Phil Cole & John Yates III & Jerrold Olefsky & Leonard Guarente & Marc Montminy, 2008. "A fasting inducible switch modulates gluconeogenesis via activator/coactivator exchange," Nature, Nature, vol. 456(7219), pages 269-273, November.
    3. Ying Jiang & Aihua Sun & Yang Zhao & Wantao Ying & Huichuan Sun & Xinrong Yang & Baocai Xing & Wei Sun & Liangliang Ren & Bo Hu & Chaoying Li & Li Zhang & Guangrong Qin & Menghuan Zhang & Ning Chen & , 2019. "Proteomics identifies new therapeutic targets of early-stage hepatocellular carcinoma," Nature, Nature, vol. 567(7747), pages 257-261, March.
    4. David A. Barbie & Pablo Tamayo & Jesse S. Boehm & So Young Kim & Susan E. Moody & Ian F. Dunn & Anna C. Schinzel & Peter Sandy & Etienne Meylan & Claudia Scholl & Stefan Fröhling & Edmond M. Chan & Ma, 2009. "Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1," Nature, Nature, vol. 462(7269), pages 108-112, November.
    5. Xiao-Hui Wang & Sha Xu & Xiang-Yu Zhou & Rui Zhao & Yan Lin & Jing Cao & Wei-Dong Zang & Hui Tao & Wei Xu & Ming-Qing Li & Shi-Min Zhao & Li-Ping Jin & Jian-Yuan Zhao, 2021. "Low chorionic villous succinate accumulation associates with recurrent spontaneous abortion risk," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    6. Kosuke Yoshihara & Maria Shahmoradgoli & Emmanuel Martínez & Rahulsimham Vegesna & Hoon Kim & Wandaliz Torres-Garcia & Victor Treviño & Hui Shen & Peter W. Laird & Douglas A. Levine & Scott L. Carter , 2013. "Inferring tumour purity and stromal and immune cell admixture from expression data," Nature Communications, Nature, vol. 4(1), pages 1-11, December.
    7. Sai Ge & Xia Xia & Chen Ding & Bei Zhen & Quan Zhou & Jinwen Feng & Jiajia Yuan & Rui Chen & Yumei Li & Zhongqi Ge & Jiafu Ji & Lianhai Zhang & Jiayuan Wang & Zhongwu Li & Yumei Lai & Ying Hu & Yanyan, 2018. "Author Correction: A proteomic landscape of diffuse-type gastric cancer," Nature Communications, Nature, vol. 9(1), pages 1-1, December.
    8. Eva Hernando & Zaher Nahlé & Gloria Juan & Elena Diaz-Rodriguez & Miguel Alaminos & Michael Hemann & Loren Michel & Vivek Mittal & William Gerald & Robert Benezra & Scott W. Lowe & Carlos Cordon-Cardo, 2004. "Rb inactivation promotes genomic instability by uncoupling cell cycle progression from mitotic control," Nature, Nature, vol. 430(7001), pages 797-802, August.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Yan Li & Chen Xu & Bing Wang & Fujiang Xu & Fahan Ma & Yuanyuan Qu & Dongxian Jiang & Kai Li & Jinwen Feng & Sha Tian & Xiaohui Wu & Yunzhi Wang & Yang Liu & Zhaoyu Qin & Yalan Liu & Jing Qin & Qi Son, 2022. "Proteomic characterization of gastric cancer response to chemotherapy and targeted therapy reveals potential therapeutic strategies," Nature Communications, Nature, vol. 13(1), pages 1-26, December.
    2. Yan Li & Bing Wang & Wentao Yang & Fahan Ma & Jianling Zou & Kai Li & Subei Tan & Jinwen Feng & Yunzhi Wang & Zhaoyu Qin & Zhiyu Chen & Chen Ding, 2024. "Longitudinal plasma proteome profiling reveals the diversity of biomarkers for diagnosis and cetuximab therapy response of colorectal cancer," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    3. Lingling Li & Dongxian Jiang & Hui Liu & Chunmei Guo & Rui Zhao & Qiao Zhang & Chen Xu & Zhaoyu Qin & Jinwen Feng & Yang Liu & Haixing Wang & Weijie Chen & Xue Zhang & Bin Li & Lin Bai & Sha Tian & Su, 2023. "Comprehensive proteogenomic characterization of early duodenal cancer reveals the carcinogenesis tracks of different subtypes," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    4. Wenhao Shi & Yushen Wang & Chen Xu & Yan Li & Sai Ge & Bin Bai & Kecheng Zhang & Yunzhi Wang & Nairen Zheng & Juan Wang & Shiqi Wang & Gang Ji & Jipeng Li & Yongzhan Nie & Wenquan Liang & Xiaosong Wu , 2023. "Multilevel proteomic analyses reveal molecular diversity between diffuse-type and intestinal-type gastric cancer," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    5. Yuanyuan Qu & Jinwen Feng & Xiaohui Wu & Lin Bai & Wenhao Xu & Lingli Zhu & Yang Liu & Fujiang Xu & Xuan Zhang & Guojian Yang & Jiacheng Lv & Xiuping Chen & Guo-Hai Shi & Hong-Kai Wang & Da-Long Cao &, 2022. "A proteogenomic analysis of clear cell renal cell carcinoma in a Chinese population," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    6. Lingling Li & Dongxian Jiang & Qiao Zhang & Hui Liu & Fujiang Xu & Chunmei Guo & Zhaoyu Qin & Haixing Wang & Jinwen Feng & Yang Liu & Weijie Chen & Xue Zhang & Lin Bai & Sha Tian & Subei Tan & Chen Xu, 2023. "Integrative proteogenomic characterization of early esophageal cancer," Nature Communications, Nature, vol. 14(1), pages 1-28, December.
    7. Wanzun Lin & Li Chen & Haojiong Zhang & Xianxin Qiu & Qingting Huang & Fangzhu Wan & Ziyu Le & Shikai Geng & Anlan Zhang & Sufang Qiu & Long Chen & Lin Kong & Jiade J. Lu, 2023. "Tumor-intrinsic YTHDF1 drives immune evasion and resistance to immune checkpoint inhibitors via promoting MHC-I degradation," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    8. Shengli Li & Li Yuan & Zhi-Yuan Xu & Jing-Li Xu & Gui-Ping Chen & Xiaoqing Guan & Guang-Zhao Pan & Can Hu & Jinyun Dong & Yi-An Du & Li-Tao Yang & Mao-Wei Ni & Rui-Bin Jiang & Xiu Zhu & Hang Lv & Han-, 2023. "Integrative proteomic characterization of adenocarcinoma of esophagogastric junction," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    9. Yuanyuan Qu & Xiaohui Wu & Aihetaimujiang Anwaier & Jinwen Feng & Wenhao Xu & Xiaoru Pei & Yu Zhu & Yang Liu & Lin Bai & Guojian Yang & Xi Tian & Jiaqi Su & Guo-Hai Shi & Da-Long Cao & Fujiang Xu & Yu, 2022. "Proteogenomic characterization of MiT family translocation renal cell carcinoma," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    10. Yin Li & Manling Jiang & Ling Aye & Li Luo & Yong Zhang & Fengkai Xu & Yongqi Wei & Dan Peng & Xiang He & Jie Gu & Xiaofang Yu & Guoping Li & Di Ge & Chunlai Lu, 2024. "UPP1 promotes lung adenocarcinoma progression through the induction of an immunosuppressive microenvironment," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    11. Xiaoping Su & Xiaofan Lu & Sehrish Khan Bazai & Linda Dainese & Arnauld Verschuur & Benoit Dumont & Roger Mouawad & Li Xu & Wenxuan Cheng & Fangrong Yan & Sabine Irtan & Véronique Lindner & Catherine , 2023. "Delineating the interplay between oncogenic pathways and immunity in anaplastic Wilms tumors," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    12. Kang Wang & Ioannis Zerdes & Henrik J. Johansson & Dhifaf Sarhan & Yizhe Sun & Dimitris C. Kanellis & Emmanouil G. Sifakis & Artur Mezheyeuski & Xingrong Liu & Niklas Loman & Ingrid Hedenfalk & Jonas , 2024. "Longitudinal molecular profiling elucidates immunometabolism dynamics in breast cancer," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    13. Brian D. Lehmann & Antonio Colaprico & Tiago C. Silva & Jianjiao Chen & Hanbing An & Yuguang Ban & Hanchen Huang & Lily Wang & Jamaal L. James & Justin M. Balko & Paula I. Gonzalez-Ericsson & Melinda , 2021. "Multi-omics analysis identifies therapeutic vulnerabilities in triple-negative breast cancer subtypes," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    14. Khoa A. Tran & Venkateswar Addala & Rebecca L. Johnston & David Lovell & Andrew Bradley & Lambros T. Koufariotis & Scott Wood & Sunny Z. Wu & Daniel Roden & Ghamdan Al-Eryani & Alexander Swarbrick & E, 2023. "Performance of tumour microenvironment deconvolution methods in breast cancer using single-cell simulated bulk mixtures," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    15. Qi Song & Ye Yang & Dongxian Jiang & Zhaoyu Qin & Chen Xu & Haixing Wang & Jie Huang & Lingli Chen & Rongkui Luo & Xiaolei Zhang & Yufeng Huang & Lei Xu & Zixiang Yu & Subei Tan & Minying Deng & Ruqun, 2022. "Proteomic analysis reveals key differences between squamous cell carcinomas and adenocarcinomas across multiple tissues," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    16. Hailiang Zhang & Lin Bai & Xin-Qiang Wu & Xi Tian & Jinwen Feng & Xiaohui Wu & Guo-Hai Shi & Xiaoru Pei & Jiacheng Lyu & Guojian Yang & Yang Liu & Wenhao Xu & Aihetaimujiang Anwaier & Yu Zhu & Da-Long, 2023. "Proteogenomics of clear cell renal cell carcinoma response to tyrosine kinase inhibitor," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    17. Shaoshuai Tang & Yunzhi Wang & Rongkui Luo & Rundong Fang & Yufeng Liu & Hang Xiang & Peng Ran & Yexin Tong & Mingjun Sun & Subei Tan & Wen Huang & Jie Huang & Jiacheng Lv & Ning Xu & Zhenmei Yao & Qi, 2024. "Proteomic characterization identifies clinically relevant subgroups of soft tissue sarcoma," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    18. Qingnan Liang & Yuefan Huang & Shan He & Ken Chen, 2023. "Pathway centric analysis for single-cell RNA-seq and spatial transcriptomics data with GSDensity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    19. Cecilia Pessoa Rodrigues & Aindrila Chatterjee & Meike Wiese & Thomas Stehle & Witold Szymanski & Maria Shvedunova & Asifa Akhtar, 2021. "Histone H4 lysine 16 acetylation controls central carbon metabolism and diet-induced obesity in mice," Nature Communications, Nature, vol. 12(1), pages 1-21, December.
    20. Lucia Taraborrelli & Yasin Şenbabaoğlu & Lifen Wang & Junghyun Lim & Kerrigan Blake & Noelyn Kljavin & Sarah Gierke & Alexis Scherl & James Ziai & Erin McNamara & Mark Owyong & Shilpa Rao & Aslihan Ka, 2023. "Tumor-intrinsic expression of the autophagy gene Atg16l1 suppresses anti-tumor immunity in colorectal cancer," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-41139-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.