IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38360-5.html
   My bibliography  Save this article

Spatially resolved multi-omics highlights cell-specific metabolic remodeling and interactions in gastric cancer

Author

Listed:
  • Chenglong Sun

    (Chinese Academy of Medical Sciences and Peking Union Medical College
    Qilu University of Technology (Shandong Academy of Sciences)
    Qilu University of Technology (Shandong Academy of Sciences))

  • Anqiang Wang

    (Peking University Cancer Hospital and Institute)

  • Yanhe Zhou

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Panpan Chen

    (Qilu University of Technology (Shandong Academy of Sciences)
    Qilu University of Technology (Shandong Academy of Sciences))

  • Xiangyi Wang

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Jianpeng Huang

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Jiamin Gao

    (Chinese Academy of Medical Sciences and Peking Union Medical College)

  • Xiao Wang

    (Qilu University of Technology (Shandong Academy of Sciences)
    Qilu University of Technology (Shandong Academy of Sciences))

  • Liebo Shu

    (Shanghai Luming Biological Technology co.Ltd)

  • Jiawei Lu

    (Shanghai Luming Biological Technology co.Ltd)

  • Wentao Dai

    (Fudan University
    Shanghai Jiao Tong University School of Medicine)

  • Zhaode Bu

    (Peking University Cancer Hospital and Institute)

  • Jiafu Ji

    (Peking University Cancer Hospital and Institute)

  • Jiuming He

    (Chinese Academy of Medical Sciences and Peking Union Medical College
    Chinese Academy of Medical Sciences and Peking Union Medical College)

Abstract

Mapping tumor metabolic remodeling and their spatial crosstalk with surrounding non-tumor cells can fundamentally improve our understanding of tumor biology, facilitates the designing of advanced therapeutic strategies. Here, we present an integration of mass spectrometry imaging-based spatial metabolomics and lipidomics with microarray-based spatial transcriptomics to hierarchically visualize the intratumor metabolic heterogeneity and cell metabolic interactions in same gastric cancer sample. Tumor-associated metabolic reprogramming is imaged at metabolic-transcriptional levels, and maker metabolites, lipids, genes are connected in metabolic pathways and colocalized in the heterogeneous cancer tissues. Integrated data from spatial multi-omics approaches coherently identify cell types and distributions within the complex tumor microenvironment, and an immune cell-dominated “tumor-normal interface” region where tumor cells contact adjacent tissues are characterized with distinct transcriptional signatures and significant immunometabolic alterations. Our approach for mapping tissue molecular architecture provides highly integrated picture of intratumor heterogeneity, and transform the understanding of cancer metabolism at systemic level.

Suggested Citation

  • Chenglong Sun & Anqiang Wang & Yanhe Zhou & Panpan Chen & Xiangyi Wang & Jianpeng Huang & Jiamin Gao & Xiao Wang & Liebo Shu & Jiawei Lu & Wentao Dai & Zhaode Bu & Jiafu Ji & Jiuming He, 2023. "Spatially resolved multi-omics highlights cell-specific metabolic remodeling and interactions in gastric cancer," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38360-5
    DOI: 10.1038/s41467-023-38360-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38360-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38360-5?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. Alma Andersson & Ludvig Larsson & Linnea Stenbeck & Fredrik Salmén & Anna Ehinger & Sunny Z. Wu & Ghamdan Al-Eryani & Daniel Roden & Alex Swarbrick & Åke Borg & Jonas Frisén & Camilla Engblom & Joakim, 2021. "Spatial deconvolution of HER2-positive breast cancer delineates tumor-associated cell type interactions," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. Bradley I. Reinfeld & Matthew Z. Madden & Melissa M. Wolf & Anna Chytil & Jackie E. Bader & Andrew R. Patterson & Ayaka Sugiura & Allison S. Cohen & Ahmed Ali & Brian T. Do & Alexander Muir & Caroline, 2021. "Cell-programmed nutrient partitioning in the tumour microenvironment," Nature, Nature, vol. 593(7858), pages 282-288, May.
    3. Miranda V. Hunter & Reuben Moncada & Joshua M. Weiss & Itai Yanai & Richard M. White, 2021. "Spatially resolved transcriptomics reveals the architecture of the tumor-microenvironment interface," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    4. Chia-Lin Chen & Sheng-Chieh Hsu & Tan-Ya Chung & Cheng-Ying Chu & Hung-Jung Wang & Pei-Wen Hsiao & Shauh-Der Yeh & David K. Ann & Yun Yen & Hsing-Jien Kung, 2021. "Arginine is an epigenetic regulator targeting TEAD4 to modulate OXPHOS in prostate cancer cells," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    5. Laura Poillet-Perez & Xiaoqi Xie & Le Zhan & Yang Yang & Daniel W. Sharp & Zhixian Sherrie Hu & Xiaoyang Su & Anurag Maganti & Cherry Jiang & Wenyun Lu & Haiyan Zheng & Marcus W. Bosenberg & Janice M., 2018. "Autophagy maintains tumour growth through circulating arginine," Nature, Nature, vol. 563(7732), pages 569-573, November.
    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. Aditi Sahu & Kivanc Kose & Lukas Kraehenbuehl & Candice Byers & Aliya Holland & Teguru Tembo & Anthony Santella & Anabel Alfonso & Madison Li & Miguel Cordova & Melissa Gill & Christi Fox & Salvador G, 2022. "In vivo tumor immune microenvironment phenotypes correlate with inflammation and vasculature to predict immunotherapy response," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Ping Yang & Hong Qin & Yiyu Li & Anhua Xiao & Enze Zheng & Han Zeng & Chunxiao Su & Xiaoqing Luo & Qiannan Lu & Meng Liao & Lei Zhao & Li Wei & Zac Varghese & John F. Moorhead & Yaxi Chen & Xiong Z. R, 2022. "CD36-mediated metabolic crosstalk between tumor cells and macrophages affects liver metastasis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Yanming Ren & Zongyao Huang & Lingling Zhou & Peng Xiao & Junwei Song & Ping He & Chuanxing Xie & Ran Zhou & Menghan Li & Xiangqun Dong & Qing Mao & Chao You & Jianguo Xu & Yanhui Liu & Zhigang Lan & , 2023. "Spatial transcriptomics reveals niche-specific enrichment and vulnerabilities of radial glial stem-like cells in malignant gliomas," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Syamantak Khan & June Ho Shin & Valentina Ferri & Ning Cheng & Julia E. Noel & Calvin Kuo & John B. Sunwoo & Guillem Pratx, 2021. "High-resolution positron emission microscopy of patient-derived tumor organoids," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    5. Reza Mirzazadeh & Zaneta Andrusivova & Ludvig Larsson & Phillip T. Newton & Leire Alonso Galicia & Xesús M. Abalo & Mahtab Avijgan & Linda Kvastad & Alexandre Denadai-Souza & Nathalie Stakenborg & Ale, 2023. "Spatially resolved transcriptomic profiling of degraded and challenging fresh frozen samples," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    6. 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.
    7. Arezou Rahimi & Luis A. Vale-Silva & Maria Fälth Savitski & Jovan Tanevski & Julio Saez-Rodriguez, 2024. "DOT: a flexible multi-objective optimization framework for transferring features across single-cell and spatial omics," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. Benjamin L. Walker & Qing Nie, 2023. "NeST: nested hierarchical structure identification in spatial transcriptomic data," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Yueli Yang & Wenqi Jia & Zhiwei Luo & Yunpan Li & Hao Liu & Lixin Fu & Jinxiu Li & Yu Jiang & Junjian Lai & Haiwei Li & Babangida Jabir Saeed & Yi Zou & Yuan Lv & Liang Wu & Ting Zhou & Yongli Shan & , 2024. "VGLL1 cooperates with TEAD4 to control human trophectoderm lineage specification," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    10. Zhiyuan Yuan & Yisi Li & Minglei Shi & Fan Yang & Juntao Gao & Jianhua Yao & Michael Q. Zhang, 2022. "SOTIP is a versatile method for microenvironment modeling with spatial omics data," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    11. Lulu Shang & Xiang Zhou, 2022. "Spatially aware dimension reduction for spatial transcriptomics," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    12. Honglei Ren & Benjamin L. Walker & Zixuan Cang & Qing Nie, 2022. "Identifying multicellular spatiotemporal organization of cells with SpaceFlow," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Guidantonio Malagoli Tagliazucchi & Anna J. Wiecek & Eloise Withnell & Maria Secrier, 2023. "Genomic and microenvironmental heterogeneity shaping epithelial-to-mesenchymal trajectories in cancer," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    14. Shijia Zhu & Naoto Kubota & Shidan Wang & Tao Wang & Guanghua Xiao & Yujin Hoshida, 2024. "STIE: Single-cell level deconvolution, convolution, and clustering in in situ capturing-based spatial transcriptomics," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Jingyang Qian & Jie Liao & Ziqi Liu & Ying Chi & Yin Fang & Yanrong Zheng & Xin Shao & Bingqi Liu & Yongjin Cui & Wenbo Guo & Yining Hu & Hudong Bao & Penghui Yang & Qian Chen & Mingxiao Li & Bing Zha, 2023. "Reconstruction of the cell pseudo-space from single-cell RNA sequencing data with scSpace," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    16. Yuefan Huang & Vakul Mohanty & Merve Dede & Kyle Tsai & May Daher & Li Li & Katayoun Rezvani & Ken Chen, 2023. "Characterizing cancer metabolism from bulk and single-cell RNA-seq data using METAFlux," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    17. Laura Yerly & Christine Pich-Bavastro & Jeremy Domizio & Tania Wyss & Stéphanie Tissot-Renaud & Michael Cangkrama & Michel Gilliet & Sabine Werner & François Kuonen, 2022. "Integrated multi-omics reveals cellular and molecular interactions governing the invasive niche of basal cell carcinoma," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    18. Qiang Feng & Zhida Liu & Xuexin Yu & Tongyi Huang & Jiahui Chen & Jian Wang & Jonathan Wilhelm & Suxin Li & Jiwon Song & Wei Li & Zhichen Sun & Baran D. Sumer & Bo Li & Yang-Xin Fu & Jinming Gao, 2022. "Lactate increases stemness of CD8 + T cells to augment anti-tumor immunity," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    19. Kai Cao & Qiyu Gong & Yiguang Hong & Lin Wan, 2022. "A unified computational framework for single-cell data integration with optimal transport," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    20. Matteo Villa & David E. Sanin & Petya Apostolova & Mauro Corrado & Agnieszka M. Kabat & Carmine Cristinzio & Annamaria Regina & Gustavo E. Carrizo & Nisha Rana & Michal A. Stanczak & Francesc Baixauli, 2024. "Prostaglandin E2 controls the metabolic adaptation of T cells to the intestinal microenvironment," Nature Communications, Nature, vol. 15(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_s41467-023-38360-5. 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.