T-cell factor 4 and β-catenin chromatin occupancies pattern zonal liver metabolism in mice

Hepatology

Volumn 59, Issue 6, 2014, Pages 2344-2357

  Gougelet, Angélique ^a,b   Torre, Cyril ^a,b   Veber, Philippe ^a,b   Sartor, Chiara ^a,b   Bachelot, Laura ^a,b   Denechaud, Pierre Damien ^a,b   Godard, Cécile ^a,b   Moldes, Marthe ^a,b   Burnol, Anne Françoise ^a,b   Dubuquoy, Céline ^a,b   Terris, Benoit ^a,c   Guillonneau, François ^a,d   Ye, Tao ^e   Schwarz, Michael ^f   Braeuning, Albert ^f   Perret, Christine ^a,b   Colnot, Sabine ^a,b  

^a INSTITUT COCHIN   (France)

^b INSERM   (France)

^c Service d'Anatomie et Cytologie Pathologiques AP HP Hôpital Cochin Université Paris Descartes ^*  (France)

^d 3P5 proteomics facility ^*  (France)

^e UNIVERSITÉ DE STRASBOURG   (France)

^f Institute of Experimental and Clinical Pharmacology and Toxicology   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CELL NUCLEUS RECEPTOR; HEPATOCYTE NUCLEAR FACTOR 4; T CELL FACTOR 4; T CELL FACTOR PROTEIN; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA BINDING; GENE; IN VIVO STUDY; LIVER CELL; LIVER CELL CARCINOMA; LIVER METABOLISM; MALE; METABOLOME; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANIMALS; BETA CATENIN; CHROMATIN; GENE REGULATORY NETWORKS; HEPATOCYTE NUCLEAR FACTOR 4; HEPATOCYTES; HUMANS; LIPID METABOLISM; LIVER; LIVER NEOPLASMS; MALE; MICE; MICE, KNOCKOUT; RECEPTOR CROSS-TALK; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN;

EID: 84901605165     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.26924     Document Type: Article

References (39)

1. Jungermann K, Kietzmann T. Zonation of parenchymal and nonparenchymal metabolism in liver. Annu Rev Nutr 1996;16:179-203.
2. Torre C, Perret C, Colnot S. Molecular determinants of liver zonation. Prog Mol Biol Transl Sci 2010;97:127-150.
3. Benhamouche S, Decaens T, Godard C, Chambrey R, Rickman DS, Moinard C, et al. Apc tumor suppressor gene is the "zonation-keeper" of mouse liver. Dev Cell 2006;10:759-770.
4. Sekine S, Lan BY, Bedolli M, Feng S, Hebrok M. Liver-specific loss of beta-catenin blocks glutamine synthesis pathway activity and cytochrome p450 expression in mice. Hepatology 2006;43:817-825.
5. Cadigan KM, Waterman ML. TCF/LEFs and Wnt signaling in the nucleus. Cold Spring Harb Perspect Biol 2012;4:a007906.
6. Colnot S, Decaens T, Niwa-Kawakita M, Godard C, Hamard G, Kahn A, et al. Liver-targeted disruption of Apc in mice activates beta-catenin signaling and leads to hepatocellular carcinomas. Proc Natl Acad Sci U S A 2004;101:17216-17221.
7. Audard V, Grimber G, Elie C, Radenen B, Audebourg A, Letourneur F, et al. Cholestasis is a marker for hepatocellular carcinomas displaying beta-catenin mutations. J Pathol 2007;212:345-352.
8. Torre C, Benhamouche S, Mitchell C, Godard C, Veber P, Letourneur F, et al. The transforming growth factor-alpha and cyclin D1 genes are direct targets of beta-catenin signaling in hepatocyte proliferation. J Hepatol 2011;55:86-95.
9. Brault V, Moore R, Kutsch S, Ishibashi M, Rowitch DH, McMahon AP, et al. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 2001;128:1253-1264.
10. Tannour-Louet M, Porteu A, Vaulont S, Kahn A, Vasseur-Cognet M. A tamoxifen-inducible chimeric Cre recombinase specifically effective in the fetal and adult mouse liver. Hepatology 2002;35:1072-1081.
11. Nelson JD, Denisenko O, Bomsztyk K. Protocol for the fast chromatin immunoprecipitation (ChIP) method. Nat Protoc 2006;1:179-185.
12. Boj SF, van Es JH, Huch M, Li VS, José A, Hatzis P, et al. Diabetes risk gene and Wnt effector Tcf7l2/TCF4 controls hepatic response to perinatal and adult metabolic demand. Cell 2012;151:1595-1607.
13. Stamatoyannopoulos JA, Snyder M, Hardison R, Ren B, Gingeras T, Gilbert DM, et al. An encyclopedia of mouse DNA elements (Mouse ENCODE). Genome Biol 2012;13:418.
14. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 2010;107:21931-21936.
15. Decaens T, Godard C, de Reynies A, Rickman DS, Tronche F, Couty JP, et al. Stabilization of beta-catenin affects mouse embryonic liver growth and hepatoblast fate. Hepatology 2008;47:247-258.
16. Ye T, Krebs AR, Choukrallah MA, Keime C, Plewniak F, Davidson I, Tora L. seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res 2011;39:e35.
17. Anson M, Crain-Denoyelle AM, Baud V, Chereau F, Gougelet A, Terris B, et al. Oncogenic beta-catenin triggers an inflammatory response that determines the aggressiveness of hepatocellular carcinoma in mice. J Clin Invest 2012;122:586-599.
18. Braeuning A, Ittrich C, Kohle C, Hailfinger S, Bonin M, Buchmann A, Schwarz M. Differential gene expression in periportal and perivenous mouse hepatocytes. FEBS J 2006;273:5051-5061.
19. Holloway MG, Miles GD, Dombkowski AA, Waxman DJ. Liver-specific hepatocyte nuclear factor-4alpha deficiency: greater impact on gene expression in male than in female mouse liver. Mol Endocrinol 2008;22:1274-1286.
20. Schmidt D, Wilson MD, Ballester B, Schwalie PC, Brown GD, Marshall A, et al. Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science 2010;328:1036-1040.
21. Cattin AL, Le Beyec J, Barreau F, Saint-Just S, Houllier A, Gonzalez FJ, et al. Hepatocyte nuclear factor 4alpha, a key factor for homeostasis, cell architecture, and barrier function of the adult intestinal epithelium. Mol Cell Biol 2009;29:6294-6308.
22. Beilke LD, Aleksunes LM, Holland RD, Besselsen DG, Beger RD, Klaassen CD, Cherrington NJ. Constitutive androstane receptor-mediated changes in bile acid composition contributes to hepatoprotection from lithocholic acid-induced liver injury in mice. Drug Metab Dispos 2009;37:1035-1045.
23. Le Martelot G, Claudel T, Gatfield D, Schaad O, Kornmann B, Lo Sasso G, et al. REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis. PLoS Biol 2009;7:e1000181.
24. Mosimann C, Hausmann G, Basler K. Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol Cell Biol 2009;10:276-286.
25. Cole MF, Johnstone SE, Newman JJ, Kagey MH, Young RA. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev 2008;22:746-755.
26. Affolter M, Pyrowolakis G, Weiss A, Basler K. Signal-induced repression: the exception or the rule in developmental signaling? Dev Cell 2008;15:11-22.
27. Odom DT, Zizlsperger N, Gordon DB, Bell GW, Rinaldi NJ, Murray HL, et al. Control of pancreas and liver gene expression by HNF transcription factors. Science 2004;303:1378-1381.
28. Stanulovic VS, Kyrmizi I, Kruithof-de Julio M, Hoogenkamp M, Vermeulen JL, Ruijter JM, et al. Hepatic HNF4alpha deficiency induces periportal expression of glutamine synthetase and other pericentral enzymes. Hepatology 2007;45:433-444.
29. Colletti M, Cicchini C, Conigliaro A, Santangelo L, Alonzi T, Pasquini E, et al. Convergence of Wnt signaling on the HNF4alpha-driven transcription in controlling liver zonation. Gastroenterology 2009;137:660-672.
30. Kaestner KH. In the zone: how a hepatocyte knows where it is. Gastroenterology 2009;137:425-427.
31. Torre C, Perret C, Colnot S. Transcription dynamics in a physiological process: beta-catenin signaling directs liver metabolic zonation. Int J Biochem Cell Biol 2011;43:271-278.
32. Grant SF, Thorleifsson G, Reynisdottir I, Benediktsson R, Manolescu A, Sainz J, et al. Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat Genet 2006;38:320-323.
33. Yamagata K, Furuta H, Oda N, Kaisaki PJ, Menzel S, Cox NJ, et al. Mutations in the hepatocyte nuclear factor-4alpha gene in maturity-onset diabetes of the young (MODY1). Nature 1996;384:458-460.
34. Chafey P, Finzi L, Boisgard R, Cauzac M, Clary G, Broussard C, et al. Proteomic analysis of beta-catenin activation in mouse liver by DIGE analysis identifies glucose metabolism as a new target of the Wnt pathway. Proteomics 2009;9:3889-3900.
35. Liu H, Fergusson MM, Wu JJ, Rovira II, Liu J, Gavrilova O, et al. Wnt signaling regulates hepatic metabolism. Sci Signal 2011;4:ra6.
36. Behari J, Yeh TH, Krauland L, Otruba W, Cieply B, Hauth B, et al. Liver-specific beta-catenin knockout mice exhibit defective bile acid and cholesterol homeostasis and increased susceptibility to diet-induced steatohepatitis. Am J Pathol 2010;176:744-753.
37. Yeh TH, Krauland L, Singh V, Zou B, Devaraj P, Stolz DB, et al. Liver-specific beta-catenin knockout mice have bile canalicular abnormalities, bile secretory defect, and intrahepatic cholestasis. Hepatology 2010;52:1410-1419.
38. Ning BF, Ding J, Yin C, Zhong W, Wu K, Zeng X, et al. Hepatocyte nuclear factor 4 alpha suppresses the development of hepatocellular carcinoma. Cancer Res 2010;70:7640-7651.
39. Braeuning A, Schwarz M. beta-Catenin as a multilayer modulator of zonal cytochrome P450 expression in mouse liver. Biol Chem 2010;391:139-148.