Ha-ras and β-catenin oncoproteins orchestrate metabolic programs in mouse liver tumors

International Journal of Cancer

Volumn 135, Issue 7, 2014, Pages 1574-1585

  Unterberger, Elif B ^a   Eichner, Johannes ^a   Wrzodek, Clemens ^a   Lempiäinen, Harri ^b   Luisier, Raphaëlle ^b   Terranova, Rémi ^b   Metzger, Ute ^a   Plummer, Simon ^c,e   Knorpp, Thomas ^a   Braeuning, Albert ^a   Moggs, Jonathan ^b   Templin, Markus F ^a   Honndorf, Valerie ^a   Piotto, Martial ^d   Zell, Andreas ^a   Schwarz, Michael ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b NOVARTIS PHARMA AG   (Switzerland)

^c CXR Biosciences Ltd   (United Kingdom)

^d Bruker Corporation   (United States)

^e MicroMatrices Assoc Ltd Scotland   (United Kingdom)

Author keywords

Ha ras; microarray; mouse hepatoma; tumor metabolism; Catenin

Indexed keywords

7 DEHYDROCHOLESTEROL; ACYL COENZYME A DESATURASE 1; ALPHA FETOPROTEIN; B RAF KINASE; BETA CATENIN; CHOLESTEROL 7ALPHA MONOOXYGENASE; DIETHYLNITROSAMINE; HA RAS PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; LANOSTEROL SYNTHASE; MESSENGER RNA; ONCOPROTEIN; PHENOBARBITAL; PHOSPHOPROTEIN; SIRTUIN 1; SMAD1 PROTEIN; TRANSCRIPTION FACTOR FKHR; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ARTICLE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; CTNNB1 GENE; DOWN REGULATION; ENERGY METABOLISM; GENE MUTATION; GENOTYPE; GLUCONEOGENESIS; IMMUNOHISTOCHEMISTRY; LIVER CARCINOGENESIS; LIVER TUMOR; MOUSE; MUTATIONAL ANALYSIS; NITROGEN METABOLISM; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTON NUCLEAR MAGNETIC RESONANCE; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSLATION INITIATION; TUMOR GENE; UPREGULATION; WESTERN BLOTTING; XENOBIOTIC METABOLISM;

HA-RAS; MICROARRAY; MOUSE HEPATOMA; TUMOR METABOLISM; Β-CATENIN;

ANIMALS; BETA CATENIN; BLOTTING, WESTERN; GENE EXPRESSION PROFILING; GENES, RAS; LIVER NEOPLASMS, EXPERIMENTAL; METABOLIC NETWORKS AND PATHWAYS; METABOLOMICS; MICE; MICRORNAS; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR MARKERS, BIOLOGICAL;

EID: 84904460849     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.28798     Document Type: Article

References (45)

1. Stahl S, Ittrich C, Marx-Stoelting P, et al. Genotype-phenotype relationships in hepatocellular tumors from mice and man. Hepatology 2005; 42: 353-61.
2. Aydinlik H, Nguyen TD, Moennikes O, et al. Selective pressure during tumor promotion by phenobarbital leads to clonal outgrowth of β-catenin-mutated mouse liver tumors. Oncogene 2001; 20: 7812-16.
3. Behrens J, Kries JPv, Kühl M, et al. Functional interaction of β-catenin with the transcription factor LEF-1. Nature 1996; 382: 638-41.
4. Jaworski M, Buchmann A, Bauer P, et al. B-raf and Ha-ras mutations in chemically induced mouse liver tumors. Oncogene 2005; 24: 1290-5.
5. Dhillon AS, Hagan S, Rath O, et al. MAP kinase signalling pathways in cancer. Oncogene 2007; 26: 3279-90.
6. Schulze A, Harris AL,. How cancer metabolism is tuned for proliferation and vulnerable to disruption. Nature 2012; 491: 364-73.
7. Ward PS, Thompson CB,. Metabolic reprogramming: a cancer hallmark even warburg did not anticipate. Cancer Cell 2012; 21: 297-308.
8. Rignall B, Ittrich C, Krause E, et al. Comparative transcriptome and proteome analysis of Ha-ras and B-raf mutated mouse liver tumors. J Proteome Res 2009; 8: 3987-94.
9. Jaworski M, Ittrich C, Hailfinger S, et al. Global gene expression in Ha-ras and B-raf mutated mouse liver tumors. Int J Cancer 2007; 121: 1382-5.
10. Strathmann J, Paal K, Ittrich C, et al. Proteome analysis of chemically induced mouse liver tumors with different genotype. Proteomics 2007; 7: 3318-31.
11. Wrzodek C, Eichner J, Zell A,. Pathway-based visualization of cross-platform microarray datasets. Bioinformatics 2012; 28: 3021-6.
12. Kristensen VN, Vaske CJ, Ursini-Siegel J, et al. Integrated molecular profiles of invasive breast tumors and ductal carcinoma in situ (DCIS) reveal differential vascular and interleukin signaling. Proc Natl Acad Sci USA 2012; 109: 2802-7.
13. Martín-Subero JI, Kreuz M, Bibikova M, et al. New insights into the biology and origin of mature aggressive B-cell lymphomas by combined epigenomic, genomic, and transcriptional profiling. Blood 2009; 113: 2488-97.
14. Shen L, Toyota M, Kondo Y, et al. Integrated genetic and epigenetic analysis identifies three different subclasses of colon cancer. Proc Natl Acad Sci 2007; 104: 18654-9.
15. Loeppen S, Koehle C, Buchmann A, et al. A β-catenin-dependent pathway regulates expression of cytochrome P450 isoforms in mouse liver tumors. Carcinogenesis 2005; 26: 239-48.
16. Hailfinger S, Jaworski M, Braeuning A, et al. Zonal gene expression in murine liver: lessons from tumors. Hepatology 2006; 43: 407-14.
17. Buchmann A, Karcier Z, Schmid B, et al. Differential selection for B-raf and Ha-ras mutated liver tumors in mice with high and low susceptibility to hepatocarcinogenesis. Mutat Res 2008; 638: 66-74.
18. Lempiainen H, Muller A, Brasa S, et al. Phenobarbital mediates an epigenetic switch at the constitutive androstane receptor (CAR) target gene Cyp2b10 in the liver of B6C3F1 mice. PLoS One 2011; 6: e18216.
19. Braeuning A, Heubach Y, Knorpp T, et al. Gender-specific interplay of signaling through beta-catenin and CAR in the regulation of xenobiotic-induced hepatocyte proliferation. Toxicol Sci 2011; 123: 113-22.
20. Benahmed MA, Santelmo N, Elbayed K, et al. The assessment of the quality of the graft in an animal model for lung transplantation using the metabolomics 1H high-resolution magic angle spinning NMR spectroscopy. Magn Reson Med 2012; 68: 1026-38.
21. Castejon D, Villa P, Calvo MM, et al. 1H-HRMAS NMR study of smoked Atlantic salmon (Salmo salar). Magn Reson Chem 2010; 48: 693-703.
22. Rooney OM, Troke J, Nicholson JK, et al. High-resolution diffusion and relaxation-edited magic angle spinning 1H NMR spectroscopy of intact liver tissue. Magn Reson Med 2003; 50: 925-30.
23. Kauffmann A, Gentleman R, Huber W,. arrayQualityMetrics-a bioconductor package for quality assessment of microarray data. Bioinformatics 2009; 25: 415-16.
24. Smyth GK,. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3: Article3.
25. Lopez-Romero P,. Pre-processing and differential expression analysis of Agilent microRNA arrays using the AgiMicroRna Bioconductor library. BMC Genomics 2011; 12: 64.
26. Rignall B, Braeuning A, Buchmann A, et al. Tumor formation in liver of conditional beta-catenin-deficient mice exposed to a diethylnitrosamine/ phenobarbital tumor promotion regimen. Carcinogenesis 2010; 32: 52-7.
27. Jaworski M, Hailfinger S, Buchmann A, et al. Human p53 knock-in (hupki) mice do not differ in liver tumor response from their counterparts with murine p53. Carcinogenesis 2005; 26: 1829-34.
28. Marx-Stoelting P, Mahr J, Knorpp T, et al. Tumor promotion in liver of mice with a conditional Cx26 knockout. Toxicol Sci 2008; 103: 260-7.
29. Gaidatzis D, van Nimwegen E, Hausser J, et al. Inference of miRNA targets using evolutionary conservation and pathway analysis. BMC Bioinformatics 2007; 8: 69.
30. Maragkakis M, Vergoulis T, Alexiou P, et al. DIANA-microT Web server upgrade supports Fly and Worm miRNA target prediction and bibliographic miRNA to disease association. Nucleic Acids Res 2011; 39: W145-W148.
31. Friedman RC, Farh KK, Burge CB, et al. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19: 92-105.
32. Kanehisa M, Goto S, Sato Y, et al. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 2012; 40: D109-D114.
33. Braeuning A, Ittrich C, Kohle C, et al. Zonal gene expression in mouse liver resembles expression patterns of Ha-ras and beta-catenin mutated hepatomas. Drug Metab Dispos 2007; 35: 503-7.
34. Braeuning A, Ittrich C, Kohle C, et al. Differential gene expression in periportal and perivenous mouse hepatocytes. FEBS J 2006; 273: 5051-61.
35. Benhamouche S, Decaens T, Godard C, et al. Apc tumor suppressor gene is the "zonation-keeper" of mouse liver. Dev Cell 2006; 10: 759-70.
36. Wang B, Hsu SH, Frankel W, et al. 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 2012; 56: 186-97.
37. Gokey NG, Lopez-Anido C, Gillian-Daniel AL, et al. Early growth response 1 (Egr1) regulates cholesterol biosynthetic gene expression. J Biol Chem 2011; 286: 29501-10.
38. Gougelet A, Torre C, Veber P, et al. T-cell factor 4 and beta-catenin chromatin occupansies pattern zonal liver metabolism. Hepatology 2013. Doi: 10.1002/hep.26924.
39. Anastasiou D, Poulogiannis G, Asara JM, et al. Inhibition of pyruvate kinase M2 by reactive oxygen species contributes to cellular antioxidant responses. Science 2011; 334: 1278-83.
40. Yuneva MO, Fan TW, Allen TD, et al. The metabolic profile of tumors depends on both the responsible genetic lesion and tissue type. Cell Metab 2012; 15: 157-70.
41. Gebhardt R,. Metabolic zonation of the liver: regulation and implications for liver function. Pharmacol Ther 1992; 53: 275-354.
42. Hall RK, Sladek FM, Granner DK,. The orphan receptors COUP-TF and HNF-4 serve as accessory factors required for induction of phosphoenolpyruvate carboxykinase gene transcription by glucocorticoids. Proc Natl Acad Sci USA 1995; 92: 412-16.
43. Clendening JW, Pandyra A, Boutros PC, et al. Dysregulation of the mevalonate pathway promotes transformation. Proc Natl Acad Sci USA 2010; 107: 15051-6.
44. Gregg J, Fraizer G,. Transcriptional regulation of EGR1 by EGF and the ERK signaling pathway in prostate cancer cells. Genes Cancer 2012; 2: 900-9.
45. Qureshi SA, Cao XM, Sukhatme VP, et al. v-Src activates mitogen-responsive transcription factor Egr-1 via serum response elements. J Biol Chem 1991; 266: 10802-6.