Citation: Yanhua Chen, Xian Ding, Jun Zhou, Zhaoying Wang, Yunhai Bo, Ying Hu, Qingce Zang, Jing Xu, Ruiping Zhang, Jiuming He, Fen Yang, Zeper Abliz. Plasma metabolomics combined with mass spectrometry imaging reveals crosstalk between tumor and plasma in gastric cancer genesis and metastasis[J]. Chinese Chemical Letters, ;2025, 36(1): 110351. doi: 10.1016/j.cclet.2024.110351 shu

Plasma metabolomics combined with mass spectrometry imaging reveals crosstalk between tumor and plasma in gastric cancer genesis and metastasis

Yanhua Chen ^{a, e, f, 1} ,
Xian Ding ^{b, h, 1} ,
Jun Zhou ^{c, 1} ,
Zhaoying Wang ^{a, e} ,
Yunhai Bo ^d ,
Ying Hu ^g ,
Qingce Zang ^b ,
Jing Xu ^b ,
Ruiping Zhang ^b ,
Jiuming He ^b ,
Fen Yang ^{d, *,} ,
Zeper Abliz ^{b, *,}

a.
Key Laboratory of Mass Spectrometry Imaging and Metabolomics (State Ethnic Affairs Commission), Center for Imaging and Systems Biology, College of Life and Environmental Sciences, Minzu University of China, Beijing 100081, China
b.
State Key Laboratory of Bioactive Substance and Function of Natural Medicines, Institute of Materia Medica, Chinese Academy of Medical Sciences, Peking Union Medical College, Beijing 100050, China
c.
Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Gastrointestinal Oncology, Peking University Cancer Hospital & Institute, Beijing 100142, China
d.
Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Center of Drug Clinical Trial, Peking University Cancer Hospital and Institute, Beijing 100142, China
e.
Beijing Engineering Research Center of Food Environment and Public Health, Minzu University of China, Beijing 100081, China
f.
Key laboratory of Ethnomedicine of Ministry of Education, School of Pharmacy, Minzu University of China, Beijing 100081, China
g.
Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Department of BioBank, Peking University Cancer Hospital and Institute, Beijing 100142, China
h.
Pharmacy Department of Beijing Chao–Yang Hospital, Capital Medical University, Beijing 100020, China

Received Date: 22 April 2024
Revised Date: 19 July 2024
Accepted Date: 20 August 2024
Available Online: 20 August 2024

Figures(4)

Gastric Carcinoma (GC) is a highly fatal malignant tumor with a poor prognosis. Its elevated mortality rates are primarily due to its proclivity for late-stage metastasis. Exploring the metabolic interactions between tumor microenvironment and the systemic bloodstream could help to clearly understand the mechanisms and identify precise biomarkers of tumor growth, proliferation, and metastasis. In this study, an integrative approach that combines plasma metabolomics with mass spectrometry imaging of tumor tissue was developed to investigate the global metabolic landscape of GC tumorigenesis and metastasis. The results showed that the oxidized glutathione to glutathione ratio (GSSH/GSH) became increased in non-distal metastatic GC (M0), which means an accumulation of oxidative stress in tumor tissues. Furthermore, it was found that the peroxidation of polyunsaturated fatty acids, such as 9,10-EpOMe, 9-HOTrE, etc., were accelerated in both plasma and tumor tissues of distal metastatic GC (M1). These changes were further confirmed the potential effect of CYP2E1 and GGT1 in metastatic potential of GC by mass spectrometry imaging (MSI) and immunohistochemistry (IHC). Collectively, our findings reveal the integrated multidimensional metabolomics approach is a clinical useful method to unravel the blood-tumor metabolic crosstalk, illuminate reprogrammed metabolic networks, and provide reliable circulating biomarkers.
- Metabolomics,
- Spatial-resolved metabolomics,
- Gastric cancer,
- Blood-tumor metabolic crosstalk,
- Lipid peroxidation
1. [1]
  H. Sung, J. Ferlay, R.L. Siegel, et al., CA Cancer J. Clin. 71 (2021) 209–249. doi: 10.3322/caac.21660
2. [2]
  E. Morgan, M. Arnold, M.C. Camargo, et al., eClinicalMedicine 47 (2022) 101404. doi: 10.1016/j.eclinm.2022.101404
3. [3]
  E.C. Smyth, M. Moehler, Ther. Adv. Med. Oncol. 11 (2019), doi: 10.1177/1758835919867522. doi: 10.1177/1758835919867522
4. [4]
  M.Z. Qiu, S.M. Shi, Z.H. Chen, et al., Cancer Med. 7 (2018) 3662–3672. doi: 10.1002/cam4.1661
5. [5]
  W. Yasui, N Oue, P.P. Aung, et al., Gastric Cancer 8 (2005) 86–94. doi: 10.1007/s10120-005-0320-0
6. [6]
  K. Ganesh, J. Massague, Nat. Med. 27 (2021) 34–44. doi: 10.1038/s41591-020-01195-4
7. [7]
  P. Bu, K.Y. Chen, K. Xiang, et al., Cell Metab. 27 (2018) 1249–1262 e4. doi: 10.1016/j.cmet.2018.04.003
8. [8]
  A.P. Gomes, D. Ilter, V. Low, et al., Nature 585 (2020) 283–287. doi: 10.1038/s41586-020-2630-0
9. [9]
  Y.Z. Chen, B.H. Wang, Y.Z. Zhao, et al., Nat. Commun. 15 (2024) 1657. doi: 10.1038/s41467-024-46043-y
10. [10]
  X.X. Wang, B.L. Wang, F.F. Ji, et al., Chin. Chem. Lett. 35 (2024) 109653. doi: 10.1016/j.cclet.2024.109653
11. [11]
  B. Faubert, A. Solmonson, R.J. DeBerardinis, Science 368 (2020) eaaw5473. doi: 10.1126/science.aaw5473
12. [12]
  U.E. Martinez-Outschoorn, M. Peiris-Pages, R.G. Pestell, et al., Nat. Rev. Clin. Oncol. 14 (2017) 11–31. doi: 10.1038/nrclinonc.2016.60
13. [13]
  A. Tasdogan, B. Faubert, V. Ramesh, et al., Nature 577 (2020) 115–120. doi: 10.1038/s41586-019-1847-2
14. [14]
  C.L. Sun, T.G. Li, X.W. Song, et al., Proc. Natl. Acad. Sci. U. S. A. 116 (2019) 52–57. doi: 10.1073/pnas.1808950116
15. [15]
  J.P. Huang, S.S. Gao, K. Wang, et al., Chin. Chem. Lett. 34 (2023) 107865. doi: 10.1016/j.cclet.2022.107865
16. [16]
  X. Ding, F. Yang, Y.H. Chen, et al., Anal. Chem. 94 (2022) 7500–7509. doi: 10.1021/acs.analchem.1c05502
17. [17]
  C.L. Sun, A.Q. Wang, Zhou Y.H, et al., Nat. Commun. 14 (2023) 2692. doi: 10.1038/s41467-023-38360-5
18. [18]
  L. Kumar, M.E. Futschik, Bioinformation 2 (2007) 5–7. doi: 10.6026/97320630002005
19. [19]
  G. Barrera, ISRN Oncol. 2012 (2012) 137289.
20. [20]
  P. Liu, W. Zhu, C. Chen, et al., Life Sci. 247 (2020) 117443. doi: 10.1016/j.lfs.2020.117443
21. [21]
  K. Ohshima, E. Morii, Metabolites 11 (2021) 28. doi: 10.3390/metabo11010028
22. [22]
  V. Chiurchiu, A. Leuti, M. Maccarrone, Front Immunol. 9 (2018) 38. doi: 10.3389/fimmu.2018.00038
23. [23]
  S. Enya, K. Kawakami, Y. Suzuki, et al., Dis. Model Mech. 11 (2018) dmm032383.
24. [24]
  K. Strassburg, A.M.L. Huijbrechts, K.A. Kortekaas, et al., Anal. Bioanal. Chem. 404 (2012) 1413–1426. doi: 10.1007/s00216-012-6226-x
25. [25]
  H. Bayir, T.S. Anthonymuthu, Y.Y. Tyurina, et al., Cell Chem. Biol. 27 (2020) 387–408. doi: 10.1016/j.chembiol.2020.03.014
26. [26]
  S. Doll, M. Conrad, IUBMB Life 69 (2017) 423–434. doi: 10.1002/iub.1616
1. [1]
  Xiaoxiao Wang , Bolun Wang , Fenfen Ji , Jie Yan , Jiacheng Fang , Doudou Zhang , Ji Xu , Jing Ji , Xinran Hao , Hemi Luan , Yanjun Hong , Shulan Qiu , Min Li , Zhu Yang , Wenlan Liu , Xiaodong Cai , Zongwei Cai . Discovery of plasma biomarkers for Parkinson’s disease diagnoses based on metabolomics and lipidomics. Chinese Chemical Letters, 2024, 35(11): 109653-. doi: 10.1016/j.cclet.2024.109653
2. [2]
  Quan Lu , Lulu Zhang , Zihan Chen , Jiajia Lv , Jie Gao , Xinmin Li , Hongyu Li , Wen Shi , Xiaohua Li , Huimin Ma , Zeli Yuan . A lipid droplet-targeting fluorescence probe for monitoring of lipid peroxidation in ferroptosis and non-alcoholic fatty liver disease. Chinese Chemical Letters, 2025, 36(8): 110620-. doi: 10.1016/j.cclet.2024.110620
3. [3]
  Qiongqiong Wan , Zhourui Zhang , Mengmeng Zhao , Xianqin Ruan , Yanhong Hao , Jiajun Deng , Yunlang She , Minglei Yang , Yongxiang Song , Feng Jin , Ailin Wei , Sheng Zhong , Jie Zheng , Dong Xie , Suming Chen . Efficient diagnosis of benign and malignant pulmonary nodules based on Nano-zero-valent iron enhanced serum metabolic fingerprinting. Chinese Chemical Letters, 2025, 36(10): 110794-. doi: 10.1016/j.cclet.2024.110794
4. [4]
  Xuyang Chai , Hiu-Lok Ngan , Yuanyuan Song , Zenghua Qi , Lifang Zhao , Wenqi Chen , Shanshan Chen , Zhenhua Yang , Ruijin Li , Chuan Dong , Zhu Yang , Zongwei Cai . Real-world PM_2.5 exposure induces prostaglandin disruption and low-density lipoprotein oxidation, exacerbating atherogenesis in ApoE^−/− mice. Chinese Chemical Letters, 2025, 36(9): 110671-. doi: 10.1016/j.cclet.2024.110671
5. [5]
  Yue Xu , Lingzhi Wang , Liu Yang , Renliang Xue , Haowen Zhu , Qifeng Liu , Xueqi Lv , Ruiping Zhang , Jun Tu , Qingce Zang , Yinghong Wang . Spatial metabolomics combined with transcriptomics to reveal heterogeneous metabolism and drug response in the heart of rats with heart failure. Chinese Chemical Letters, 2025, 36(7): 110958-. doi: 10.1016/j.cclet.2025.110958
6. [6]
  Aolei Tan , Xiaoxiao Ma . Exploring the functional roles of small-molecule metabolites in disease research: Recent advancements in metabolomics. Chinese Chemical Letters, 2024, 35(8): 109276-. doi: 10.1016/j.cclet.2023.109276
7. [7]
  Yao-Hua Gu , Yu Chen , Qing Li , Neng-Bin Xie , Xue Xing , Jun Xiong , Min Hu , Tian-Zhou Li , Ke-Yu Yuan , Yu Liu , Tang Tang , Fan He , Bi-Feng Yuan . Metabolome profiling by widely-targeted metabolomics and biomarker panel selection using machine-learning for patients in different stages of chronic kidney disease. Chinese Chemical Letters, 2024, 35(11): 109627-. doi: 10.1016/j.cclet.2024.109627
8. [8]
  Qian Wu , Yuanxia Lv , Zixuan Guo , Zhihao Zhao , Zhimin Zhang , Hongmei Lu . A Case Study and Practice of Research-Oriented Comprehensive Instrumental Analysis Laboratory Courses. University Chemistry, 2025, 40(10): 194-202. doi: 10.12461/PKU.DXHX202411063
9. [9]
  Gaojian Yang , Zhiyang Li , Rabia Usman , Zhu Chen , Yuan Liu , Song Li , Hui Chen , Yan Deng , Yile Fang , Nongyue He . DNA walker induced "signal on" fluorescence aptasensor strategy for rapid and sensitive detection of extracellular vesicles in gastric cancer. Chinese Chemical Letters, 2025, 36(2): 109930-. doi: 10.1016/j.cclet.2024.109930
10. [10]
  Huamei Zhang , Jingjing Liu , Mingyue Li , Shida Ma , Xucong Zhou , Aixia Meng , Weina Han , Jin Zhou . Imaging polarity changes in pneumonia and lung cancer using a lipid droplet-targeted near-infrared fluorescent probe. Chinese Chemical Letters, 2024, 35(12): 110020-. doi: 10.1016/j.cclet.2024.110020
11. [11]
  Chao Zhao , Chenyu Gao , Zhiyi Yang , Tianyou Cao , Qian Luo , Zhijun Zhang . Whole brain lipid dyshomeostasis in depressive-like behavior young adult rats: Mapping by mass spectrometry imaging-based spatial omics. Chinese Chemical Letters, 2025, 36(10): 111089-. doi: 10.1016/j.cclet.2025.111089
12. [12]
  Jiayin Zhou , Depeng Liu , Longqiang Li , Min Qi , Guangqiang Yin , Tao Chen . Responsive organic room-temperature phosphorescence materials for spatial-time-resolved anti-counterfeiting. Chinese Chemical Letters, 2024, 35(11): 109929-. doi: 10.1016/j.cclet.2024.109929
13. [13]
  Keqiang Shi , Xiujuan Hong , Dongyan Xu , Tao Pan , Huiwen Wang , Hongru Feng , Cheng Guo , Yuanjiang Pan . Analysis of RNA modifications in peripheral white blood cells from breast cancer patients by mass spectrometry. Chinese Chemical Letters, 2025, 36(3): 110079-. doi: 10.1016/j.cclet.2024.110079
14. [14]
  Yunjie Dang , Yanru Feng , Xiao Chen , Chaoxing He , Shujie Wei , Dingyang Liu , Jinlong Qi , Huaxing Zhang , Shaokun Yang , Zhiyun Niu , Bai Xiang . Development of a multi-level pH-responsive lipid nanoplatform for efficient co-delivery of siRNA and small-molecule drugs in tumor treatment. Chinese Chemical Letters, 2024, 35(12): 109660-. doi: 10.1016/j.cclet.2024.109660
15. [15]
  Yuanzheng Wang , Chen Zhang , Shuyan Han , Xiaoli Kong , Changyun Quan , Jun Wu , Wei Zhang . Cancer cell membrane camouflaged biomimetic gelatin-based nanogel for tumor inhibition. Chinese Chemical Letters, 2024, 35(11): 109578-. doi: 10.1016/j.cclet.2024.109578
16. [16]
  Yanfei Liu , Yaqin Hu , Yifu Tan , Qiwen Chen , Zhenbao Liu . Tumor acidic microenvironment activatable DNA nanostructure for precise cancer cell targeting and inhibition. Chinese Chemical Letters, 2025, 36(1): 110289-. doi: 10.1016/j.cclet.2024.110289
17. [17]
  Shuang Liang , Jianjun Yao , Dan Liu , Mengli Zhou , Yong Cui , Zhaohui Wang . Tumor-responsive covalent organic polymeric nanoparticles enhancing STING activation for cancer immunotherapy. Chinese Chemical Letters, 2025, 36(3): 109856-. doi: 10.1016/j.cclet.2024.109856
18. [18]
  Honghao Sun , Huimin Zhao , Ronghui Yin , Chenxi Zhou , Ming Wu , Yueyang Deng , Zhanwei Zhou , Minjie Sun . Injectable hydrogel-based tumor vaccine with fibrotic tumor immune microenvironment remodeling to prevent breast cancer postoperative recurrence and metastases. Chinese Chemical Letters, 2025, 36(5): 110067-. doi: 10.1016/j.cclet.2024.110067
19. [19]
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20. [20]
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