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Metabonomic Studies of Human Hepatocellular Carcinoma Using High-Resolution Magic-Angle Spinning 1H NMR Spectroscopy in Conjunction with Multivariate Data Analysis

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State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, Wuhan Centre for Magnetic Resonance, Wuhan Institute of Physics and Mathematics, the Chinese Academy of Sciences, Wuhan 430071, P. R. China, Graduate University of the Chinese Academy of Sciences, Beijing 100049, P.R. China, Department of General Surgery, Union Hospital, Huazhong University of Science and Technology, Wuhan 430022, P. R. China, Department of General Surgery, Wuxi No.2 People's Hospital, Jiangsu 214002, P. R. China, and Department of Pathology, Union Hospital, Huazhong University of Science and Technology, Wuhan 430022, P.R. China
Cite this: J. Proteome Res. 2007, 6, 7, 2605–2614
Publication Date (Web):June 12, 2007
Copyright © 2007 American Chemical Society

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    High-resolution magic-angle spinning (MAS) 1H nuclear magnetic resonance spectroscopy has been employed to characterize the metabolite composition (i.e., metabonome) of the human hepatocellular carcinoma (HCC) tumor in combination with principal component analysis (PCA). The results showed that (a) the metabonomes of both low-grade HCC and high-grade HCC tumors differ markedly from that of the adjacent non-involved tissues; and (b) low-grade HCC tumors have clear differences in metabonome from that of the high-grade HCC tumors. Compared with the non-involved adjacent liver tissues, HCC tumors had elevated levels of lactate, glutamate, glutamine, glycine, leucine, alanine, choline metabolites, and phosphorylethanolamine (PE), but declined levels of triglycerides, glucose, and glycogen. The levels of lactate, amino acids including glutamate, glutamine, glycine, leucine and alanine, choline and phosphorylethanolamine (PE) were higher but the levels of PC, GPC, triglycerides, glucose, and glycogen were lower in high-grade HCC than in low-grade HCC tumors. Compared with non-cirrhotic, low-grade HCC tumors, the cirrhotic, low-grade HCC tumors showed statistically significant increases in lactate, phosphocholine (PC), and glycerophosphocholine (GPC). The necrosis in HCC tumors resulted in a drastic increase in the levels of observable triglycerides, signals of which dominated their 1H NMR spectra. These results indicated that HRMAS combined with PCA offers a useful tool for understanding the tumor biochemistry and classification of liver tumor tissues; such tool may also have some potential for liver tumor diagnosis and prognosis even when some other disease processes are present.

    Keywords: Magic-angle spinning NMR • Hepatocellular carcinoma • Pattern recognition • metabonomics

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     Wuhan Institute of Physics and Mathematics, the Chinese Academy of Sciences.

     Graduate University of the Chinese Academy of Sciences.

     Department of General Surgery, Union Hospital, Huazhong University of Science and Technology.


     Wuxi No.2 People's Hospital.

     Department of Pathology, Union Hospital, Huazhong University of Science and Technology.


      To whom correspondence should be addressed. E-mails:  huiru.tang@ (H. R.Tang); [email protected] (F. Deng).

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    Spectra of non-involved liver tissues and low- and high-grade HCC tumors. This material is available free of charge via the Internet at

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    52. Minakshi Prasad, Somesh Banerjee, Suman, Rajesh Kumar, Lukumoni Buragohain, Mayukh Ghosh. Proteomics and Metabolomics in Cancer Diagnosis and Therapy. 2022, 3649-3677.
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    61. Rui Hu, Tao Li, Yunhuang Yang, Yuan Tian, Limin Zhang. NMR-Based Metabolomics in Cancer Research. 2021, 201-218.
    62. Minakshi Prasad, Somesh Banerjee, Suman, Rajesh Kumar, Lukumoni Buragohain, Mayukh Ghosh. Proteomics and Metabolomics in Cancer Diagnosis and Therapy. 2021, 1-31.
    63. Benjamin Buchard, Camille Teilhet, Natali Abeywickrama Samarakoon, Sylvie Massoulier, Juliette Joubert-Zakeyh, Corinne Blouin, Christelle Reynes, Robert Sabatier, Anne-Sophie Biesse-Martin, Marie-Paule Vasson, Armando Abergel, Aicha Demidem. Two Metabolomics Phenotypes of Human Hepatocellular Carcinoma in Non-Alcoholic Fatty Liver Disease According to Fibrosis Severity. Metabolites 2021, 11 (1) , 54.
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    65. Marina Serra, Amedeo Columbano, Andrea Perra, Marta Anna Kowalik. Animal Models: A Useful Tool to Unveil Metabolic Changes in Hepatocellular Carcinoma. Cancers 2020, 12 (11) , 3318.
    66. Jia Zhou, Shuangming Yue, Quanhui Peng, Lizhi Wang, Zhisheng Wang, Bai Xue. Metabonomic Responses of Grazing Yak to Different Concentrate Supplementations in Cold Season. Animals 2020, 10 (9) , 1595.
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    72. Aurélien Amiel, Marie Tremblay-Franco, Roselyne Gautier, Simon Ducheix, Alexandra Montagner, Arnaud Polizzi, Laurent Debrauwer, Hervé Guillou, Justine Bertrand-Michel, Cécile Canlet. Proton NMR Enables the Absolute Quantification of Aqueous Metabolites and Lipid Classes in Unique Mouse Liver Samples. Metabolites 2020, 10 (1) , 9.
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    74. Elaine Holmes, Ian D. Wilson, John C. Lindon. An Overview of Metabolic Phenotyping and Its Role in Systems Biology. 2019, 1-51.
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    79. Jingyu Yan, Guoxiang Xie, Chungeng Liang, Yiyang Hu, Aihua Zhao, Fengjie Huang, Ping Hu, Ping Liu, Wei Jia, Xiaoning Wang. Herbal medicine Yinchenhaotang protects against α-naphthylisothiocyanate-induced cholestasis in rats. Scientific Reports 2017, 7 (1)
    80. Camille Teilhet, Daniel Morvan, Juliette Joubert-Zakeyh, Anne-Sophie Biesse, Bruno Pereira, Sylvie Massoulier, Pierre Dechelotte, Denis Pezet, Emmanuel Buc, Géraldine Lamblin, Michel Peoc’h, Jack Porcheron, Marie-Paule Vasson, Armando Abergel, Aicha Demidem. Specificities of Human Hepatocellular Carcinoma Developed on Non-Alcoholic Fatty Liver Disease in Absence of Cirrhosis Revealed by Tissue Extracts 1H-NMR Spectroscopy. Metabolites 2017, 7 (4) , 49.
    81. Christopher Dietz, Felix Ehret, Francesco Palmas, Lindsey A. Vandergrift, Yanni Jiang, Vanessa Schmitt, Vera Dufner, Piet Habbel, Johannes Nowak, Leo L. Cheng. Applications of high‐resolution magic angle spinning MRS in biomedical studies II—Human diseases. NMR in Biomedicine 2017, 30 (11)
    82. Wenxue Chen, Shaohua Lu, Guifang Wang, Fener Chen, Chunxue Bai. Staging research of human lung cancer tissues by high‐resolution magic angle spinning proton nuclear magnetic resonance spectroscopy (HRMAS 1 H NMR) and multivariate data analysis. Asia-Pacific Journal of Clinical Oncology 2017, 13 (5)
    83. Hsi-Wen Yeh, Szu-Shuo Lee, Chieh-Yu Chang, Chun-Mei Hu, Yuh-Shan Jou. Pyrimidine metabolic rate limiting enzymes in poorly-differentiated hepatocellular carcinoma are signature genes of cancer stemness and associated with poor prognosis. Oncotarget 2017, 8 (44) , 77734-77751.
    84. Ding Cao, Can Cai, Mingxin Ye, Junhua Gong, Menghao Wang, Jinzheng Li, Jianping Gong. Differential metabonomic profiles of primary hepatocellular carcinoma tumors from alcoholic liver disease, HBV-infected, and HCV-infected cirrhotic patients. Oncotarget 2017, 8 (32) , 53313-53325.
    85. Diaa Osman, Omnia Ali, Manar Obada, Hatem El‐Mezayen, Hala El‐Said. Chromatographic determination of some biomarkers of liver cirrhosis and hepatocellular carcinoma in Egyptian patients. Biomedical Chromatography 2017, 31 (6)
    86. Laurence Le Moyec, Mohamed N. Triba, Pierre Nahon, Nadia Bouchemal, Edith Hantz, Corentine Goossens, Roland Amathieu, Philippe Savarin. Nuclear magnetic resonance metabolomics and human liver diseases: The principles and evidence associated with protein and carbohydrate metabolism. Biomedical Reports 2017, 6 (4) , 387-395.
    87. Isaie Sibomana, Nicholas J. DelRaso, David Mattie, Michael L. Raymer, Nicholas V. Reo. Furosemide enhances the sensitivity of urinary metabolomics for assessment of kidney function. Metabolomics 2017, 13 (3)
    88. Ting Li, Pengchi Deng. Nuclear Magnetic Resonance technique in tumor metabolism. Genes & Diseases 2017, 4 (1) , 28-36.
    89. Daniela Rodrigues, Márcia Monteiro, Carmen Jerónimo, Rui Henrique, Luís Belo, Maria de Lourdes Bastos, Paula Guedes de Pinho, Márcia Carvalho. Renal cell carcinoma: a critical analysis of metabolomic biomarkers emerging from current model systems. Translational Research 2017, 180 , 1-11.
    90. L. F. Wang, S. D. Jia, G. Q. Yang, R. Y. Liu, G. Y. Yang, M. Li, H. S. Zhu, Y. Y. Wang, L. Q. Han. The effects of acute lipopolysaccharide challenge on dairy goat liver metabolism assessed with 1 HNMR metabonomics. Journal of Animal Physiology and Animal Nutrition 2017, 101 (1) , 180-189.
    91. Fengmin Yang, Jie Du, Hong Zhang, Guorui Ruan, Junfeng Xiang, Lixia Wang, Hongxia Sun, Aijiao Guan, Gang Shen, Yan Liu, Xiaomeng Guo, Qian Li, Yalin Tang, . Serum Metabolomics of Burkitt Lymphoma Mouse Models. PLOS ONE 2017, 12 (1) , e0170896.
    92. Asem I Fitian, Roniel Cabrera. Disease monitoring of hepatocellular carcinoma through metabolomics. World Journal of Hepatology 2017, 9 (1) , 1.
    93. Limin Zhang, Emmanuel Hatzakis, Andrew D. Patterson. NMR-Based Metabolomics and Its Application in Drug Metabolism and Cancer Research. Current Pharmacology Reports 2016, 2 (5) , 231-240.
    94. Shan Xu, Yuan Tian, Yili Hu, Nijia Zhang, Sheng Hu, Dandan Song, Zhengshun Wu, Yulan Wang, Yanfang Cui, Huiru Tang. Tumor growth affects the metabonomic phenotypes of multiple mouse non-involved organs in an A549 lung cancer xenograft model. Scientific Reports 2016, 6 (1)
    95. Yuan Tian, Tangpeng Xu, Jia Huang, Limin Zhang, Shan Xu, Bin Xiong, Yulan Wang, Huiru Tang. Tissue Metabonomic Phenotyping for Diagnosis and Prognosis of Human Colorectal Cancer. Scientific Reports 2016, 6 (1)
    96. Xingchen Shang, Xia Zhong, Xingsong Tian. Metabolomics of papillary thyroid carcinoma tissues: potential biomarkers for diagnosis and promising targets for therapy. Tumor Biology 2016, 37 (8) , 11163-11175.
    97. Vignesh Ramesh, Kumaresan Ganesan. Integrative functional genomic analysis unveils the differing dysregulated metabolic processes across hepatocellular carcinoma stages. Gene 2016, 588 (1) , 19-29.
    98. Yang Chen, Jianyin Zhou, Jinquan Li, Jianghua Feng, Zhong Chen, Xiaomin Wang. Plasma metabolomic analysis of human hepatocellular carcinoma: Diagnostic and therapeutic study. Oncotarget 2016, 7 (30) , 47332-47342.
    99. Yan Lin, Changchun Ma, Chengkang Liu, Zhening Wang, Jurong Yang, Xinmu Liu, Zhiwei Shen, Renhua Wu. NMR-based fecal metabolomics fingerprinting as predictors of earlier diagnosis in patients with colorectal cancer. Oncotarget 2016, 7 (20) , 29454-29464.
    100. Dan Yue, Yuwei Zhang, Liuliu Cheng, Jinhu Ma, Yufeng Xi, Liping Yang, Chao Su, Bin Shao, Anliang Huang, Rong Xiang, Ping Cheng. Hepatitis B virus X protein (HBx)-induced abnormalities of nucleic acid metabolism revealed by 1H-NMR-based metabonomics. Scientific Reports 2016, 6 (1)
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