Gene network analysis of glucose linked signaling pathways and their role in human hepatocellular carcinoma cell growth and survival in HuH7 and HepG2 cell Lines

BioMed Research International

Volumn 2015, Issue , 2015, Pages

  Berger, Emmanuelle ^a   Vega, Nathalie ^a   Weiss Gayet, Michèle ^b   Géloën, Alain ^a  

^a UNIVERSITÉ DE LYON   (France)

^b CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2; APOLIPOPROTEIN C3; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYCLOOXYGENASE 2; EARLY GROWTH RESPONSE FACTOR 1; GLUCOSE; GLUCOSE OXIDASE; GLYCOSYLPHOSPHATIDYLINOSITOL PHOSPHOLIPASE D; HEPATOCYTE NUCLEAR FACTOR 3; INTERFERON REGULATORY FACTOR 1; INTERLEUKIN 6 RECEPTOR; LIVER X RECEPTOR; METFORMIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; PROTEIN KINASE LKB1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSCRIPTION FACTOR CARBOHYDRATE RESPONSIVE ELEMENT BINDING PROTEIN; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR HES 1; TUMOR MARKER; UNCLASSIFIED DRUG; UPSTREAM STIMULATORY FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PPARGC1A PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; STK11 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; BIOINFORMATICS; CANCER SURVIVAL; CELL ADHESION; CELL COUNT; CELL DEATH; CELL DENSITY; CELL GROWTH; CELL PROLIFERATION; CELL SIZE; CELL STIMULATION; CELL STRESS; CELL SURFACE; CELL SURVIVAL; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME SYNTHESIS; GENE CONTROL; GENE IDENTIFICATION; GENE MUTATION; GENE TARGETING; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; GLYCOLYSIS; HEPATOCELLULAR CARCINOMA CELL LINE; HEPG2 CELL LINE; HUH7 CELL LINE; HUMAN; HUMAN CELL; IC50; INTRACELLULAR SIGNALING; LIVER FUNCTION; NONHUMAN; ONCOGENE MYC; RAT; SIGNAL TRANSDUCTION; UNINDEXED SEQUENCE; UPREGULATION; BIOSYNTHESIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; HEP-G2 CELL LINE; LIVER CELL CARCINOMA; LIVER TUMOR; METABOLISM; PATHOLOGY;

CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE REGULATORY NETWORKS; GLUCOSE; GLYCOLYSIS; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; METFORMIN; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; PPAR ALPHA; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84941052252     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2015/821761     Document Type: Article

References (71)

1. A. Dey and K. Swaminathan, "Hyperglycemia-induced mitochondrial alterations in liver, " Life Sciences, vol. 87, no. 7-8, pp. 197-214, 2010.
2. F. Giacco and M. Brownlee, "Oxidative stress and diabetic complications, " Circulation Research, vol. 107, no. 9, pp. 1058-1070, 2010.
3. R. Dentin, S. Hedrick, J. Xie, J. Yates III, and M. Montminy, "Hepatic glucose sensing via the CREB coactivator CRTC2, " Science, vol. 319, no. 5868, pp. 1402-1405, 2008.
4. J. F. Decaux, O.Marcillat, A. L. Pichard, J. Henry, andA. Kahn, "Glucose-dependent and-independent effect of insulin on gene expression, " The Journal of Biological Chemistry, vol. 266, no. 6, pp. 3432-3438, 1991.
5. D. van Deursen, H. Jansen, and A. J. M. Verhoeven, "Glucose increases hepatic lipase expression in HepG2 liver cells through upregulation of upstream stimulatory factors 1 and 2, " Diabetologia, vol. 51, no. 11, pp. 2078-2087, 2008.
6. A.-Y. Tu and J. J. Albers, "Glucose regulates the transcription of human genes relevant toHDLmetabolism: responsive elements for peroxisome proliferator-activated receptor are involved in the regulation of phospholipid transfer protein, " Diabetes, vol. 50, no. 8, pp. 1851-1856, 2001.
7. Y. Iwasaki, M. Kambayashi, M. Asai, M. Yoshida, T. Nigawara, and K. Hashimoto, "High glucose alone, as well as in combination with proinflammatory cytokines, stimulates nuclear factor kappa-B-mediated transcription in hepatocytes in vitro, " Journal of Diabetes and Its Complications, vol. 21, no. 1, pp. 56-62, 2007.
8. R. Sugimoto, M. Enjoji, M. Kohjima et al., "High glucose stimulates hepatic stellate cells to proliferate and to produce collagen through free radical production and activation of mitogen-activated protein kinase, " Liver International, vol. 25, no. 5, pp. 1018-1026, 2005.
9. M. A. Patil, M.-S. Chua, K.-H. Pan et al., "An integrated data analysis approach to characterize genes highly expressed in hepatocellular carcinoma, " Oncogene, vol. 24, no. 23, pp. 3737-3747, 2005.
10. Y. Midorikawa, M. Makuuchi, W. Tang, and H. Aburatani, "Microarray-based analysis for hepatocellular carcinoma: from gene expression profiling to new challenges, " World Journal of Gastroenterology, vol. 13, no. 10, pp. 1487-1492, 2007.
11. A. Teufel, A. Weinmann, M. Krupp, M. Budinger, and P. R. Galle, "Genome-wide analysis of factors regulating gene expression in liver, " Gene, vol. 389, no. 2, pp. 114-121, 2007.
12. E. Berger, N. Vega, H. Vidal, and A. Gelöen, "Gene network analysis leads to functional validation of pathways linked to cancer cell growth and survival, " Biotechnology Journal, vol. 7, no. 11, pp. 1395-1404, 2012.
13. L. Xu, L. Hui, S. Wang et al., "Expression profiling suggested a regulatory role of liver-enriched transcription factors in human hepatocellular carcinoma, " Cancer Research, vol. 61, no. 7, pp. 3176-3181, 2001.
14. C. M. Wong and I.O. L.Ng, "Molecular pathogenesis of hepatocellular carcinoma, " Liver International, vol. 28, no. 2, pp. 160-174, 2008.
15. H. Huynh, T. T. T. Nguyen, K.-H. P. Chow, P. H. Tan, K. C. Soo, and E. Tran, "Over-expression of the mitogen-activated protein kinase (MAPK) kinase (MEK)-MAPK in hepatocellular carcinoma: its role in tumor progression and apoptosis, " BMC Gastroenterology, vol. 3, article 19, 2003.
16. K. Iyoda, Y. Sasaki, M. Horimoto et al., "Involvement of the p38 mitogen-activated protein kinase cascade in hepatocellular carcinoma, " Cancer, vol. 97, no. 12, pp. 3017-3026, 2003.
17. D. Nishimura, H. Ishikawa, K. Matsumoto et al., "DHMEQ, a novel NF-κB inhibitor, induces apoptosis and cell-cycle arrest in human hepatoma cells, " International Journal of Oncology, vol. 29, no. 3, pp. 713-719, 2006.
18. P. Poma, M. Notarbartolo, M. Labbozzetta et al., "Antitumor effects of the novel NF-kappaB inhibitor dehydroxymethylepoxyquinomicin on human hepatic cancer cells: Analysis of synergy with cisplatin and of possible correlation with inhibition of pro-survival genes and IL-6 production, " International Journal of Oncology, vol. 28, no. 4, pp. 923-930, 2006.
19. M. You, M. Matsumoto, C. M. Pacold, W. K. Cho, and D. W. Crabb, "The role of AMP-activated protein kinase in the action of ethanol in the liver, "Gastroenterology, vol. 127, no.6, pp. 1798-1808, 2004.
20. M. Adachi and D. A. Brenner, "High molecular weight adiponectin inhibits proliferation of hepatic stellate cells via activation of adenosine monophosphate-activated protein kinase, " Hepatology, vol. 47, no. 2, pp. 677-685, 2008.
21. C. M. Palmeira, A. P. Rolo, J. Berthiaume, J. A. Bjork, and K. B. Wallace, "Hyperglycemia decreases mitochondrial function: the regulatory role ofmitochondrial biogenesis, " Toxicology and Applied Pharmacology, vol. 225, no. 2, pp. 214-220, 2007.
22. L. Qiao, O. A. MacDougald, and J. Shao, "CCAAT/enhancerbinding protein α mediates induction of hepatic phosphoenolpyruvate carboxykinase by p38 mitogen-activated protein kinase, "The Journal of Biological Chemistry, vol. 281, no. 34, pp. 24390-24397, 2006.
23. T. Nishikawa, D. Edelstein, X. L. Du et al., "Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage, " Nature, vol. 404, no. 6779, pp. 787-790, 2000.
24. J. Díaz-Delfín, M. Morales, and C. Caelles, "Hypoglycemic action of thiazolidinediones/peroxisome proliferator-activated receptor γ by inhibition of the c-Jun NH2-terminal kinase pathway, " Diabetes, vol. 56, no. 7, pp. 1865-1871, 2007.
25. E. Berger, S. Rome, N. Vega, C. Ciancia, and H. Vidal, "Transcriptome profiling in response to adiponectin in human cancer-derived cells, " Physiological Genomics, vol. 42, no. 1, pp. 61-70, 2010.
26. Y. Benjamini and Y. Hochberg, "Controlling the false discovery rate: a practical and powerful approach to in multiple testing under depenancy, " Journal of the Royal Statistical Society B, vol. 57, pp. 289-300, 1995.
27. Y.-S. Jeong, D. Kim, Y. S.Lee et al., "Integratedexpressionprofiling and Genome-Wide analysis of ChREBP targets reveals the dual role for ChREBP in Glucose-Regulated gene expression, " PLoS ONE, vol. 6, no. 7, Article ID e22544, 2011.
28. Y. Ruike, A. Ichimura, S. Tsuchiya et al., "Global correlation analysis for micro-RNA and mRNA expression profiles in human cell lines, " Journal of Human Genetics, vol. 53, no. 6, pp. 515-523, 2008.
29. E. T. Sawey, M. Chanrion, C. Cai et al., "Identification of a therapeutic strategy targeting amplified FGF19 in liver cancer by oncogenomic screening, " Cancer Cell, vol. 19, no. 3, pp. 347-358, 2011.
30. A. Dey and K. Chandrasekaran, "Hyperglycemia induced changes in liver: in vivo and in vitro studies, " Current Diabetes Reviews, vol. 5, no. 2, pp. 67-78, 2009.
31. T. Chiba, O. Yokosuka, M. Arai et al., "Identification of genes up-regulated by histone deacetylase inhibition with cDNA microarray and exploration of epigenetic alterations on hepatoma cells, " Journal of Hepatology, vol. 41, no. 3, pp. 436-445, 2004.
32. L. Sivertsson, M. Ek, M. Darnell, I. Edebert, M. Ingelman-Sundberg, and E. P. A. Neve, "CYP3A4 catalytic activity is induced in confluent Huh7 hepatoma cells, " Drug Metabolism and Disposition, vol. 38, no. 6, pp. 995-1002, 2010.
33. M. Cervello, D. Bachvarov, A. Cusimano et al., "COX-2-dependent and COX-2-independent mode of action of celecoxib in human liver cancer cells, " OMICS, vol. 15, no. 6, pp. 383-392, 2011.
34. D. Foderà, N. D'Alessandro, A. Cusimano et al., "Induction of apoptosis and inhibition of cell growth in human hepatocellular carcinoma cells by COX-2 inhibitors, " Annals of the New York Academy of Sciences, vol. 1028, pp. 440-449, 2004.
35. S. Wilkening, F. Stahl, and A. Bader, "Comparison of primary human hepatocytes and hepatoma cell line Hepg2 with regard to their biotransformation properties, " Drug Metabolism and Disposition, vol. 31, no. 8, pp. 1035-1042, 2003.
36. S. N. Hart, Y. Li, K. Nakamoto, E.-A. Subileau, D. Steen, and X.-B. Zhong, "A comparison of whole genome gene expression profiles of HepaRG cells and HepG2 cells to primary human hepatocytes and human liver tissues, " Drug Metabolism & Disposition, vol. 38, no. 6, pp. 988-994, 2010.
37. L. Guo, S. Dial, L. Shi et al., "Similarities and differences in the expression of drug-metabolizing enzymes between human hepatic cell lines and primary human hepatocytes, " Drug Metabolism & Disposition, vol. 39, no. 3, pp. 528-538, 2011.
38. U. Klingmüller, A. Bauer, S. Bohl et al., "Primary mouse hepatocytes for systems biology approaches: a standardized in vitro systemformodelling of signal transduction pathways, " IEE Proceedings: Systems Biology, vol. 153, no. 6, pp. 433-447, 2006.
39. B. Wang, S.-H. Hsu, W. Frankel, K. Ghoshal, and S. T. Jacob, "Stat3-mediated activation of microRNA-23a suppresses gluconeogenesis in hepatocellular carcinoma by down-regulating glucose-6-phosphatase and peroxisome proliferator-activated receptor gamma, coactivator 1 alpha, " Hepatology, vol. 56, no. 1, pp. 186-197, 2012.
40. D. M. Moran, M. A. Mattocks, P. A. Cahill, L. G. Koniaris, and I. H. McKillop, "Interleukin-6 mediates G0/G1 growth arrest in hepatocellular carcinoma through a STAT 3-dependent pathway, " Journal of Surgical Research, vol. 147, no. 1, pp. 23-33, 2008.
41. H. Kim and H. Baumann, "Dual signaling role of the protein tyrosine phosphatase SHP-2 in regulating expression of acutephase plasma proteins by interleukin-6 cytokine receptors in hepatic cells, " Molecular and Cellular Biology, vol. 19, no. 8, pp. 5326-5338, 1999.
42. M. Hatziapostolou, C. Polytarchou, E. Aggelidou et al., "An HNF4α-miRNA inflammatory feedback circuit regulates hepatocellular oncogenesis, " Cell, vol. 147, no. 6, pp. 1233-1247, 2011.
43. H. Sun, M. S. Chua, D. Yang, A. Tsalenko, B. J. Peter, and S. So, "Antibody arrays identify potential diagnostic markers of hepatocellular carcinoma, " Biomarker Insights, vol. 3, pp. 1-18, 2008.
44. T. Miyazaki, J. D. Bub, M. Uzuki, and Y. Iwamoto, "Adiponectin activates c-Jun NH2-terminal kinase and inhibits signal transducer and activator of transcription 3, " Biochemical and Biophysical Research Communications, vol. 333, no. 1, pp. 79-87, 2005.
45. R. J. Shaw, K. A. Lamia, D. Vasquez et al., "The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin, " Science, vol. 310, no. 5754, pp. 1642-1646, 2005.
46. L. Ma, L. N. Robinson, and H. C. Towle, "ChREBP?Mlx is the principal mediator of glucose-induced gene expression in the liver, " The Journal of Biological Chemistry, vol. 281, no. 39, pp. 28721-28730, 2006.
47. P. Sancho and I. Fabregat, "The NADPH oxidase inhibitor VAS2870 impairs cell growth and enhances TGF-beta-induced apoptosis of liver tumor cells, " Biochemical Pharmacology, vol. 81, no. 7, pp. 917-924, 2011.
48. M. Marí, A. Morales, A. Colell, C. García-Ruiz, and J. C. Fernández-Checa, "Mitochondrial glutathione, a key survival antioxidant, " Antioxidants and Redox Signaling, vol. 11, no. 11, pp. 2685-2700, 2009.
49. J. Pajaud, S. Kumar, C. Rauch, F. Morel, and C. Aninat, "Regulation of signal transduction by glutathione transferases, " International Journal ofHepatology, vol. 2012, Article ID137676, 11 pages, 2012.
50. K. T. Morgan, H. Ni, H. R. Brown et al., "Application of cDNA microarray technology to in vitro toxicology and the selection of genes for a real-time RT-PCR-based screen for oxidative stress in Hep-G2 cells, " Toxicologic Pathology, vol. 30, no. 4, pp. 435-451, 2002.
51. D. Loiseau, D. Morvan, A. Chevrollier et al., "Mitochondrial bioenergetic background confers a survival advantage to HepG2 cells in response to chemotherapy, " Molecular Carcinogenesis, vol. 48, no. 8, pp. 733-741, 2009.
52. I. Leclerc, A. Kahn, and B. Doiron, "The 5'-AMP-activated protein kinase inhibits the transcriptional stimulation by glucose in liver cells, acting through the glucose response complex, " FEBS Letters, vol. 431, no. 2, pp. 180-184, 1998.
53. J. T. Rodgers, C. Lerin, W. Haas, S. P. Gygi, B. M. Spiegelman, and P. Puigserver, "Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1, " Nature, vol. 434, no. 7029, pp. 113-118, 2005.
54. S. Fogarty and D. G. Hardie, "Development of protein kinase activators: AMPKas a target in metabolic disorders and cancer, " Biochimica et Biophysica Acta, vol. 1804, no. 3, pp. 581-591, 2010.
55. L. E. Nelson, R. J. Valentine, J. M. Cacicedo, M.-S. Gauthier, Y. Ido, and N. B. Ruderman, "A novel inverse relationship between metformin-triggered AMPK-SIRT1 signaling and p53 protein abundance in high glucose-exposedHepG2 cells, "TheAmerican Journal of Physiology-Cell Physiology, vol. 303, no. 1, pp. C4-C13, 2012.
56. J. Kah, A. Wüstenberg, A. D. Keller et al., "Selective induction of apoptosis by HMG-CoA reductase inhibitors in hepatoma cells and dependence on p53 expression, " Oncology Reports, vol. 28, no. 3, pp. 1077-1083, 2012.
57. S. Nemoto, M. M. Fergusson, and T. Finkel, "SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1α, " The Journal of Biological Chemistry, vol. 280, no. 16, pp. 16456-16460, 2005.
58. B. Lu, A. H. Moser, J. K. Shigenaga, K. R. Feingold, and C. Grunfeld, "Type II nuclear hormone receptors, coactivator, and target gene repression in adipose tissue in the acute-phase response, " Journal of Lipid Research, vol. 47, no. 10, pp. 2179-2190, 2006.
59. P. de Candia, R. Blekhman, A. E. Chabot, A. Oshlack, and Y. Gilad, "A combination of genomic approaches reveals the role of FOXO1a in regulating an oxidative stress response pathway, " PLoS ONE, vol. 3, no. 2, Article ID e1670, 2008.
60. I. Leclerc, C. Lenzner, L. Gourdon, S. Vaulont, A. Kahn, and B. Viollet, "Hepatocyte nuclear factor-4alpha involved in type 1maturity-onset diabetes of the young is a novel target of AMPactivated protein kinase, " Diabetes, vol. 50, no. 7, pp. 1515-1521, 2001.
61. T. Naiki, M. Nagaki, Y. Shidoji et al., "Analysis of gene expression profile induced by hepatocyte nuclear factor 4alpha in hepatoma cells using an oligonucleotide microarray, " The Journal of Biological Chemistry, vol. 277, no. 16, pp. 14011-14019, 2002.
62. Y.H.Hong, U. S. Varanasi, W.Yang, andT. Leff, "AMP-activated protein kinase regulates HNF4α transcriptional activity by inhibiting dimer formation and decreasing protein stability, " The Journal of Biological Chemistry, vol. 278, no. 30, pp. 27495-27501, 2003.
63. K. Tachibana, Y. Kobayashi, T. Tanaka et al., "Gene expression profiling of potential peroxisome proliferator-activated receptor (PPAR) target genes in human hepatoblastoma cell lines inducibly expressing different PPAR isoforms, " Nuclear Receptor, vol. 3, article 3, 2005.
64. Y. Ba, C.-N. Zhang, Y. Zhang, and C.-Y. Zhang, "Downregulation of PGC-1alpha expression in human hepatocellular carcinoma, " Chinese Journal of Oncology, vol. 30, no. 8, pp. 593-597, 2008.
65. C. P. Martínez-Jiménez, M. J. Gómez-Lechón, J. V. Castell, and R. Jover, "Underexpressed coactivators PGC1α and SRC1 impair hepatocyte nuclear factor 4α function and promote dedifferentiation in human hepatoma cells, " The Journal of Biological Chemistry, vol. 281, no. 40, pp. 29840-29849, 2006.
66. S. Vougier, S. H. Cheung, L. Li, G. Hodgson, and P. E. Shaw, "Anomalous behaviour of the STAT3 binding site in the human c-myc P2 promoter, " Biochemical and Biophysical Research Communications, vol. 364, no. 3, pp. 627-632, 2007.
67. waf1 transcription by STAT3 proteins, " The Journal of Biological Chemistry, vol. 278, no. 5, pp. 2990-2996, 2003.
68. P. Briata, C. Laurino, and R. Gherzi, "c-myc gene expression in human cells is controlled by glucose, " Biochemical and Biophysical Research Communications, vol. 165, no. 3, pp. 1123-1129, 1989.
69. V. V. Iyer, H. Yang, M. G. Ierapetritou, and C. M. Roth, "Effects of glucose and insulin onHepG2-C3A cellmetabolism, " Biotechnology and Bioengineering, vol. 107, no. 2, pp. 347-356, 2010.
70. M. Polanski and N. L. Anderson, "A list of candidate cancer biomarkers for targeted proteomics, " Biomarker Insights, vol. 1, pp. 7-48, 2007.
71. L. Pirola, A. Balcerczyk, R. W. Tothill et al., "Genome-wide analysis distinguishes hyperglycemia regulated epigenetic signatures of primary vascular cells, " Genome Research, vol. 21, no. 10, pp. 1601-1615, 2011.