IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37221-5.html
   My bibliography  Save this article

Comprehensive proteogenomic characterization of early duodenal cancer reveals the carcinogenesis tracks of different subtypes

Author

Listed:
  • Lingling Li

    (Fudan University)

  • Dongxian Jiang

    (Fudan University)

  • Hui Liu

    (Henan Normal University)

  • Chunmei Guo

    (Fudan University)

  • Rui Zhao

    (Xinhua HospitalShanghai Jiao Tong University School of Medicine)

  • Qiao Zhang

    (Fudan University)

  • Chen Xu

    (Fudan University)

  • Zhaoyu Qin

    (Fudan University)

  • Jinwen Feng

    (Fudan University)

  • Yang Liu

    (Fudan University)

  • Haixing Wang

    (Fudan University)

  • Weijie Chen

    (Fudan University)

  • Xue Zhang

    (Fudan University)

  • Bin Li

    (Fudan University)

  • Lin Bai

    (Fudan University)

  • Sha Tian

    (Fudan University)

  • Subei Tan

    (Fudan University)

  • Zixiang Yu

    (Fudan University)

  • Lingli Chen

    (Fudan University)

  • Jie Huang

    (Fudan University)

  • Jian-Yuan Zhao

    (Xinhua HospitalShanghai Jiao Tong University School of Medicine
    Zhengzhou University)

  • Yingyong Hou

    (Fudan University)

  • Chen Ding

    (Fudan University)

Abstract

The subtypes of duodenal cancer (DC) are complicated and the carcinogenesis process is not well characterized. We present comprehensive characterization of 438 samples from 156 DC patients, covering 2 major and 5 rare subtypes. Proteogenomics reveals LYN amplification at the chromosome 8q gain functioned in the transmit from intraepithelial neoplasia phase to infiltration tumor phase via MAPK signaling, and illustrates the DST mutation improves mTOR signaling in the duodenal adenocarcinoma stage. Proteome-based analysis elucidates stage-specific molecular characterizations and carcinogenesis tracks, and defines the cancer-driving waves of the adenocarcinoma and Brunner’s gland subtypes. The drug-targetable alanyl-tRNA synthetase (AARS1) in the high tumor mutation burden/immune infiltration is significantly enhanced in DC progression, and catalyzes the lysine-alanylation of poly-ADP-ribose polymerases (PARP1), which decreases the apoptosis of cancer cells, eventually promoting cell proliferation and tumorigenesis. We assess the proteogenomic landscape of early DC, and provide insights into the molecular features corresponding therapeutic targets.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37221-5
    DOI: 10.1038/s41467-023-37221-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37221-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-37221-5?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. Daniel D. Lee & H. Sebastian Seung, 1999. "Learning the parts of objects by non-negative matrix factorization," Nature, Nature, vol. 401(6755), pages 788-791, October.
    3. Marcin J. Suskiewicz & Florian Zobel & Tom E. H. Ogden & Pietro Fontana & Antonio Ariza & Ji-Chun Yang & Kang Zhu & Lily Bracken & William J. Hawthorne & Dragana Ahel & David Neuhaus & Ivan Ahel, 2020. "HPF1 completes the PARP active site for DNA damage-induced ADP-ribosylation," Nature, Nature, vol. 579(7800), pages 598-602, March.
    4. 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.
    5. Philipp Mertins & D. R. Mani & Kelly V. Ruggles & Michael A. Gillette & Karl R. Clauser & Pei Wang & Xianlong Wang & Jana W. Qiao & Song Cao & Francesca Petralia & Emily Kawaler & Filip Mundt & Karste, 2016. "Proteogenomics connects somatic mutations to signalling in breast cancer," Nature, Nature, vol. 534(7605), pages 55-62, June.
    6. Björn Schwanhäusser & Dorothea Busse & Na Li & Gunnar Dittmar & Johannes Schuchhardt & Jana Wolf & Wei Chen & Matthias Selbach, 2011. "Global quantification of mammalian gene expression control," Nature, Nature, vol. 473(7347), pages 337-342, May.
    7. 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.
    8. Xiaotian Ni & Zhaoli Tan & Chen Ding & Chunchao Zhang & Lan Song & Shuai Yang & Mingwei Liu & Ru Jia & Chuanhua Zhao & Lei Song & Wanlin Liu & Quan Zhou & Tongqing Gong & Xianju Li & Yanhong Tai & Wei, 2019. "A region-resolved mucosa proteome of the human stomach," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    9. Mark A. Eckert & Fabian Coscia & Agnieszka Chryplewicz & Jae Won Chang & Kyle M. Hernandez & Shawn Pan & Samantha M. Tienda & Dominik A. Nahotko & Gang Li & Ivana Blaženović & Ricardo R. Lastra & Mari, 2019. "Proteomics reveals NNMT as a master metabolic regulator of cancer-associated fibroblasts," Nature, Nature, vol. 569(7758), pages 723-728, May.
    10. Ludmil B. Alexandrov & Jaegil Kim & Nicholas J. Haradhvala & Mi Ni Huang & Alvin Wei Tian Ng & Yang Wu & Arnoud Boot & Kyle R. Covington & Dmitry A. Gordenin & Erik N. Bergstrom & S. M. Ashiqul Islam , 2020. "The repertoire of mutational signatures in human cancer," Nature, Nature, vol. 578(7793), pages 94-101, February.
    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. 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.
    2. 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.
    3. 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.
    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. 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.
    6. 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.
    7. 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.
    8. Yangzi Chen & Bohong Wang & Yizi Zhao & Xinxin Shao & Mingshuo Wang & Fuhai Ma & Laishou Yang & Meng Nie & Peng Jin & Ke Yao & Haibin Song & Shenghan Lou & Hang Wang & Tianshu Yang & Yantao Tian & Pen, 2024. "Metabolomic machine learning predictor for diagnosis and prognosis of gastric cancer," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Jonathan J. Swietlik & Stefanie Bärthel & Chiara Falcomatà & Diana Fink & Ankit Sinha & Jingyuan Cheng & Stefan Ebner & Peter Landgraf & Daniela C. Dieterich & Henrik Daub & Dieter Saur & Felix Meissn, 2023. "Cell-selective proteomics segregates pancreatic cancer subtypes by extracellular proteins in tumors and circulation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Qingli Guo & Eszter Lakatos & Ibrahim Al Bakir & Kit Curtius & Trevor A. Graham & Ville Mustonen, 2022. "The mutational signatures of formalin fixation on the human genome," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    11. Yunzhi Wang & Rongkui Luo & Xuan Zhang & Hang Xiang & Bing Yang & Jinwen Feng & Mengjie Deng & Peng Ran & Akesu Sujie & Fan Zhang & Jiajun Zhu & Subei Tan & Tao Xie & Pin Chen & Zixiang Yu & Yan Li & , 2023. "Proteogenomics of diffuse gliomas reveal molecular subtypes associated with specific therapeutic targets and immune-evasion mechanisms," Nature Communications, Nature, vol. 14(1), pages 1-32, December.
    12. Ji Min Lee & Henrik M. Hammarén & Mikhail M. Savitski & Sung Hee Baek, 2023. "Control of protein stability by post-translational modifications," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Del Corso, Gianna M. & Romani, Francesco, 2019. "Adaptive nonnegative matrix factorization and measure comparisons for recommender systems," Applied Mathematics and Computation, Elsevier, vol. 354(C), pages 164-179.
    14. P Fogel & C Geissler & P Cotte & G Luta, 2022. "Applying separative non-negative matrix factorization to extra-financial data," Working Papers hal-03689774, HAL.
    15. Xiao-Bai Li & Jialun Qin, 2017. "Anonymizing and Sharing Medical Text Records," Information Systems Research, INFORMS, vol. 28(2), pages 332-352, June.
    16. Mohammad Soltani & Cesar A Vargas-Garcia & Duarte Antunes & Abhyudai Singh, 2016. "Intercellular Variability in Protein Levels from Stochastic Expression and Noisy Cell Cycle Processes," PLOS Computational Biology, Public Library of Science, vol. 12(8), pages 1-23, August.
    17. Naiyang Guan & Lei Wei & Zhigang Luo & Dacheng Tao, 2013. "Limited-Memory Fast Gradient Descent Method for Graph Regularized Nonnegative Matrix Factorization," PLOS ONE, Public Library of Science, vol. 8(10), pages 1-10, October.
    18. Spelta, A. & Pecora, N. & Rovira Kaltwasser, P., 2019. "Identifying Systemically Important Banks: A temporal approach for macroprudential policies," Journal of Policy Modeling, Elsevier, vol. 41(1), pages 197-218.
    19. M. Moghadam & K. Aminian & M. Asghari & M. Parnianpour, 2013. "How well do the muscular synergies extracted via non-negative matrix factorisation explain the variation of torque at shoulder joint?," Computer Methods in Biomechanics and Biomedical Engineering, Taylor & Francis Journals, vol. 16(3), pages 291-301.
    20. Yasuhiko Haga & Yoshitaka Sakamoto & Keiko Kajiya & Hitomi Kawai & Miho Oka & Noriko Motoi & Masayuki Shirasawa & Masaya Yotsukura & Shun-Ichi Watanabe & Miyuki Arai & Junko Zenkoh & Kouya Shiraishi &, 2023. "Whole-genome sequencing reveals the molecular implications of the stepwise progression of lung adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-19, 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_s41467-023-37221-5. 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.