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1. Fat Induces Glucose Metabolism in Nontransformed Liver Cells and Promotes Liver Tumorigenesis.

Author

Broadfield LA, Duarte JAG, Schmieder R, Broekaert D, Veys K, Planque M, Vriens K, Karasawa Y, Napolitano F, Fujita S, Fujii M, Eto M, Holvoet B, Vangoitsenhoven R, Fernandez-Garcia J, Van Elsen J, Dehairs J, Zeng J, Dooley J, Rubio RA, van Pelt J, Grünewald TGP, Liston A, Mathieu C, Deroose CM, Swinnen JV, Lambrechts D, di Bernardo D, Kuroda S, De Bock K, and Fendt SM

Subjects
Animals, Carcinoma, Hepatocellular metabolism, Cell Transformation, Neoplastic, Citric Acid Cycle physiology, Fatty Acids metabolism, Glucose Tolerance Test, Humans, Lactic Acid biosynthesis, Lipid Metabolism, Liver Neoplasms metabolism, Mice, Mice, Inbred C57BL, Obesity complications, Palmitates pharmacology, Peroxisomes metabolism, Proteomics, Pyruvate Carboxylase metabolism, Random Allocation, Reactive Oxygen Species metabolism, Serine metabolism, Transcriptional Activation, Carcinoma, Hepatocellular etiology, Diet, High-Fat, Dietary Fats metabolism, Glucose metabolism, Hepatocytes metabolism, Liver Neoplasms etiology
Abstract

Hepatic fat accumulation is associated with diabetes and hepatocellular carcinoma (HCC). Here, we characterize the metabolic response that high-fat availability elicits in livers before disease development. After a short term on a high-fat diet (HFD), otherwise healthy mice showed elevated hepatic glucose uptake and increased glucose contribution to serine and pyruvate carboxylase activity compared with control diet (CD) mice. This glucose phenotype occurred independently from transcriptional or proteomic programming, which identifies increased peroxisomal and lipid metabolism pathways. HFD-fed mice exhibited increased lactate production when challenged with glucose. Consistently, administration of an oral glucose bolus to healthy individuals revealed a correlation between waist circumference and lactate secretion in a human cohort. In vitro , palmitate exposure stimulated production of reactive oxygen species and subsequent glucose uptake and lactate secretion in hepatocytes and liver cancer cells. Furthermore, HFD enhanced the formation of HCC compared with CD in mice exposed to a hepatic carcinogen. Regardless of the dietary background, all murine tumors showed similar alterations in glucose metabolism to those identified in fat exposed nontransformed mouse livers, however, particular lipid species were elevated in HFD tumor and nontumor-bearing HFD liver tissue. These findings suggest that fat can induce glucose-mediated metabolic changes in nontransformed liver cells similar to those found in HCC. SIGNIFICANCE: With obesity-induced hepatocellular carcinoma on a rising trend, this study shows in normal, nontransformed livers that fat induces glucose metabolism similar to an oncogenic transformation., (©2021 American Association for Cancer Research.)

Published
2021
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2. Fat Induces Glucose Metabolism in Nontransformed Liver Cells and Promotes Liver Tumorigenesis

Author

Rebeca Alba Rubio, Shinya Kuroda, Chantal Mathieu, Yasuaki Karasawa, Jos van Pelt, Jia Zeng, Roberta Schmieder, Thomas G. P. Grunewald, Johannes V. Swinnen, Bryan Holvoet, Jonas Dehairs, Masashi Fujii, Roman Vangoitsenhoven, Francesco Napolitano, Diego di Bernardo, James Dooley, Koen Veys, Adrian Liston, Dorien Broekaert, Lindsay A. Broadfield, Juan Fernández-García, Sarah-Maria Fendt, Kim Vriens, Miki Eto, Diether Lambrechts, Joao A.G. Duarte, Katrien De Bock, Suguru Fujita, Christophe Deroose, Mélanie Planque, Joke Van Elsen, Broadfield, L. A., Duarte, J. A. G., Schmieder, R., Broekaert, D., Veys, K., Planque, M., Vriens, K., Karasawa, Y., Napolitano, F., Fujita, S., Fujii, M., Eto, M., Holvoet, B., Vangoitsenhoven, R., Fernandez-Garcia, J., Van Elsen, J., Dehairs, J., Zeng, J., Dooley, J., Rubio, R. A., Van Pelt, J., Grunewald, T. G. P., Liston, A., Mathieu, C., Deroose, C. M., Swinnen, J. V., Lambrechts, D., Di Bernardo, D., Kuroda, S., De Bock, K., and Fendt, S. -M.

Subjects
0301 basic medicine, Proteomics, Cancer Research, Glucose uptake, Palmitates, Palmitate, Mice, Random Allocation, 0302 clinical medicine, Serine, Hepatocyte, Dietary Fat, chemistry.chemical_classification, Chemistry, Fatty Acids, Liver Neoplasms, 3. Good health, Cell Transformation, Neoplastic, Oncology, Liver Neoplasm, 030220 oncology & carcinogenesis, Pyruvate carboxylase activity, Liver cancer, Reactive Oxygen Specie, Human, Transcriptional Activation, medicine.medical_specialty, Carcinoma, Hepatocellular, Citric Acid Cycle, Carbohydrate metabolism, Peroxisome, Diet, High-Fat, Article, 03 medical and health sciences, Internal medicine, Diabetes mellitus, medicine, Peroxisomes, Animals, Humans, Lactic Acid, Obesity, Carcinogen, Pyruvate Carboxylase, Reactive oxygen species, Animal, Proteomic, Lipid metabolism, Glucose Tolerance Test, medicine.disease, Lipid Metabolism, Dietary Fats, Mice, Inbred C57BL, 030104 developmental biology, Endocrinology, Glucose, Hepatocytes, Reactive Oxygen Species, Fatty Acid
Abstract

Hepatic fat accumulation is associated with diabetes and hepatocellular carcinoma (HCC). Here, we characterize the metabolic response that high-fat availability elicits in livers before disease development. After a short term on a high-fat diet (HFD), otherwise healthy mice showed elevated hepatic glucose uptake and increased glucose contribution to serine and pyruvate carboxylase activity compared with control diet (CD) mice. This glucose phenotype occurred independently from transcriptional or proteomic programming, which identifies increased peroxisomal and lipid metabolism pathways. HFD-fed mice exhibited increased lactate production when challenged with glucose. Consistently, administration of an oral glucose bolus to healthy individuals revealed a correlation between waist circumference and lactate secretion in a human cohort. In vitro, palmitate exposure stimulated production of reactive oxygen species and subsequent glucose uptake and lactate secretion in hepatocytes and liver cancer cells. Furthermore, HFD enhanced the formation of HCC compared with CD in mice exposed to a hepatic carcinogen. Regardless of the dietary background, all murine tumors showed similar alterations in glucose metabolism to those identified in fat exposed nontransformed mouse livers, however, particular lipid species were elevated in HFD tumor and nontumor-bearing HFD liver tissue. These findings suggest that fat can induce glucose-mediated metabolic changes in nontransformed liver cells similar to those found in HCC. Significance: With obesity-induced hepatocellular carcinoma on a rising trend, this study shows in normal, nontransformed livers that fat induces glucose metabolism similar to an oncogenic transformation.

Published
2021

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