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Volume 11
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Article

Two Metabolomics Phenotypes of Human Hepatocellular Carcinoma in Non-Alcoholic Fatty Liver Disease According to Fibrosis Severity

by
Benjamin Buchard
1,2,
Camille Teilhet
1,2,
Natali Abeywickrama Samarakoon
2,
Sylvie Massoulier
1,
Juliette Joubert-Zakeyh
3,
Corinne Blouin
3,
Christelle Reynes
4,
Robert Sabatier
4,
Anne-Sophie Biesse-Martin
5,
Marie-Paule Vasson
2,
Armando Abergel
1,6 and
Aicha Demidem
2,*
1
Department of Digestive and Hepatobiliary Medecine, CHU Clermont-Ferrand, F-63000 Clermont-Ferrand, France
2
INRA, Human Nutrition Unit, Clermont Auvergne University, F-63000 Clermont-Ferrand, France
3
Department of Anatomo-pathology, CHU Clermont Ferrand, F-63000 Clermont-Ferrand, France
4
Laboratory of Biostatistics, Computer Science and Pharmaceutical Physics, UMR 5203, Faculty of Pharmacy, F-34 093 Montpellier, France
5
Team RMN-START, Clermont Auvergne University, F-63000 Clermont-Ferrand, France
6
UMR CNRS 6284, Clermont Auvergne University, F-63000 Clermont-Ferrand, France
*
Author to whom correspondence should be addressed.
Metabolites 2021, 11(1), 54; https://doi.org/10.3390/metabo11010054
Submission received: 2 November 2020 / Revised: 29 December 2020 / Accepted: 12 January 2021 / Published: 14 January 2021
(This article belongs to the Section Endocrinology and Clinical Metabolic Research)
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Abstract

Non-Alcoholic Fatty Liver Disease (NAFLD) is considered as the forthcoming predominant cause for hepatocellular carcinoma (HCC). NAFLD-HCC may rise in non-cirrhotic livers in 40 to 50% of patients. The aim of this study was to identify different metabolic pathways of HCC according to fibrosis level (F0F1 vs. F3F4). A non-targeted metabolomics strategy was applied. We analyzed 52 pairs of human HCC and adjacent non-tumoral tissues which included 26 HCC developed in severe fibrosis or cirrhosis (F3F4) and 26 in no or mild fibrosis (F0F1). Tissue extracts were analyzed using 1H-Nuclear Magnetic Resonance spectroscopy. An optimization evolutionary method based on genetic algorithm was used to identify discriminant metabolites. We identified 34 metabolites differentiating the two groups of NAFLD-HCC according to fibrosis level, allowing us to propose two metabolomics phenotypes of NAFLD-HCC. We showed that HCC-F0F1 mainly overexpressed choline derivatives and glutamine, whereas HCC-F3F4 were characterized by a decreased content of monounsaturated fatty acids (FA), an increase of saturated FA and an accumulation of branched amino acids. Comparing HCC-F0F1 and HCC-F3F4, differential expression levels of glucose, choline derivatives and phosphoethanolamine, monounsaturated FA, triacylglycerides were identified as specific signatures. Our metabolomics analysis of HCC tissues revealed for the first time two phenotypes of HCC developed in NAFLD according to fibrosis level. This study highlighted the impact of the underlying liver disease on metabolic reprogramming of the tumor.
Keywords: hepatocarcinoma; fibrosis; non-alcoholic fatty liver disease; nuclear magnetic resonance; metabolomics hepatocarcinoma; fibrosis; non-alcoholic fatty liver disease; nuclear magnetic resonance; metabolomics

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MDPI and ACS Style

Buchard, B.; Teilhet, C.; Abeywickrama Samarakoon, N.; Massoulier, S.; Joubert-Zakeyh, J.; Blouin, C.; Reynes, C.; Sabatier, R.; Biesse-Martin, A.-S.; Vasson, M.-P.; et al. Two Metabolomics Phenotypes of Human Hepatocellular Carcinoma in Non-Alcoholic Fatty Liver Disease According to Fibrosis Severity. Metabolites 2021, 11, 54. https://doi.org/10.3390/metabo11010054

AMA Style

Buchard B, Teilhet C, Abeywickrama Samarakoon N, Massoulier S, Joubert-Zakeyh J, Blouin C, Reynes C, Sabatier R, Biesse-Martin A-S, Vasson M-P, et al. Two Metabolomics Phenotypes of Human Hepatocellular Carcinoma in Non-Alcoholic Fatty Liver Disease According to Fibrosis Severity. Metabolites. 2021; 11(1):54. https://doi.org/10.3390/metabo11010054

Chicago/Turabian Style

Buchard, Benjamin, Camille Teilhet, Natali Abeywickrama Samarakoon, Sylvie Massoulier, Juliette Joubert-Zakeyh, Corinne Blouin, Christelle Reynes, Robert Sabatier, Anne-Sophie Biesse-Martin, Marie-Paule Vasson, and et al. 2021. "Two Metabolomics Phenotypes of Human Hepatocellular Carcinoma in Non-Alcoholic Fatty Liver Disease According to Fibrosis Severity" Metabolites 11, no. 1: 54. https://doi.org/10.3390/metabo11010054

APA Style

Buchard, B., Teilhet, C., Abeywickrama Samarakoon, N., Massoulier, S., Joubert-Zakeyh, J., Blouin, C., Reynes, C., Sabatier, R., Biesse-Martin, A.-S., Vasson, M.-P., Abergel, A., & Demidem, A. (2021). Two Metabolomics Phenotypes of Human Hepatocellular Carcinoma in Non-Alcoholic Fatty Liver Disease According to Fibrosis Severity. Metabolites, 11(1), 54. https://doi.org/10.3390/metabo11010054

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