The Wnt signaling pathway effector TCF7L2 is upregulated by insulin and represses hepatic gluconeogenesis

American Journal of Physiology - Endocrinology and Metabolism

Volumn 303, Issue 9, 2012, Pages

  Ip, Wilfred ^a,b   Shao, Weijuan ^b   Chiang, Yu ting Alex ^a,b   Jin, Tianru ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

catenin; Glucose production; Liver; Phosphoenolpyruvate carboxykinase; Transcription factor 7 like 2; Wnt 3a

Indexed keywords

BETA CATENIN; INSULIN; LITHIUM; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR 7 LIKE 2; WNT PROTEIN; WNT3A PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FEEDING; GENE EXPRESSION; GENE REPRESSION; GENE SILENCING; GLUCONEOGENESIS; HUMAN; HUMAN CELL; LIVER CELL; MOUSE; NONHUMAN; NUTRIENT AVAILABILITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; UPREGULATION;

ANIMALS; CELL LINE, TUMOR; CELLS, CULTURED; DOWN-REGULATION; GENE SILENCING; GLUCONEOGENESIS; HEPATOCYTES; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHOSPHORYLATION; POSTPRANDIAL PERIOD; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA, MESSENGER; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN; UP-REGULATION; WNT SIGNALING PATHWAY;

EID: 84868331392     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00249.2012     Document Type: Article

References (42)

1. Ahlzen M, Johansson LE, Cervin C, Tornqvist H, Groop L, Ridderstrale M. Expression of the transcription factor 7-like 2 gene (TCF7L2) in human adipocytes is down regulated by insulin. Biochem Biophys Res Commun 370: 49-52, 2008.
2. Columbus J, Chiang Y, Shao W, Zhang N, Wang D, Gaisano HY, Wang Q, Irwin DM, Jin T. Insulin treatment and high-fat diet feeding reduces the expression of three Tcf genes in rodent pancreas. J Endocrinol 207: 77-86, 2010.
3. da Silva Xavier G, Loder MK, McDonald A, Tarasov AI, Carzaniga R, Kronenberger K, Barg S, Rutter GA. TCF7L2 regulates late events in insulin secretion from pancreatic islet beta-cells. Diabetes 58: 894-905, 2009.
4. DasGupta R, Fuchs E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126: 4557-4568, 1999.
5. Desbois-Mouthon C, Cadoret A, Blivet-Van Eggelpoël MJ, Bertrand F, Cherqui G, Perret C, Capeau J. Insulin and IGF-1 stimulate the beta-catenin pathway through two signalling cascades involving GSK-3beta inhibition and Ras activation. Oncogene 20: 252-259, 2001.
6. Ding VW, Chen RH, McCormick F. Differential regulation of glycogen synthase kinase 3beta by insulin and Wnt signaling. J Biol Chem 275: 32475-32481, 2000.
7. Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, Korswagen HC. Functional interaction between beta-catenin and FOXO in oxidative stress signaling. Science 308: 1181-1184, 2005.
8. Gebhardt R, Hovhannisyan A. Organ patterning in the adult stage: the role of Wnt/beta-catenin signaling in liver zonation and beyond. Dev Dyn 239: 45-55, 2010.
9. Grant SF, Hakonarson H, Schwartz S. Can the genetics of type 1 and type 2 diabetes shed light on the genetics of latent autoimmune diabetes in adults? Endocr Rev 31: 183-193, 2010.
10. Grant SF, Thorleifsson G, Reynisdottir I, Benediktsson R, Manolescu A, Sainz J, Helgason A, Stefansson H, Emilsson V, Helgadottir A, Styrkarsdottir U, Magnusson KP, Walters GB, Palsdottir E, Jonsdottir T, Gudmundsdottir T, Gylfason A, Saemundsdottir J, Wilensky RL, Reilly MP, Rader DJ, Bagger Y, Christiansen C, Gudnason V, Sigurdsson G, Thorsteinsdottir U, Gulcher JR, Kong A, Stefansson K. Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat Genet 38: 320-323, 2006.
11. Hay DC, Fletcher J, Payne C, Terrace JD, Gallagher RC, Snoeys J, Black JR, Wojtacha D, Samuel K, Hannoun Z, Pryde A, Filippi C, Currie IS, Forbes SJ, Ross JA, Newsome PN, Iredale JP. Highly efficient differentiation of hESCs to functional hepatic endoderm requires ActivinA and Wnt3a signaling. Proc Natl Acad Sci USA 105: 12301-12306, 2008.
12. Hino S, Tanji C, Nakayama KI, Kikuchi A. Phosphorylation of betacatenin by cyclic AMP-dependent protein kinase stabilizes beta-catenin through inhibition of its ubiquitination. Mol Cell Biol 25: 9063-9072, 2005.
13. Hu M, Kurobe M, Jeong YJ, Fuerer C, Ghole S, Nusse R, Sylvester KG. Wnt/beta-catenin signaling in murine hepatic transit amplifying progenitor cells. Gastroenterology 133: 1579-1591, 2007.
14. Jin T, George Fantus I, Sun J. Wnt and beyond Wnt: multiple mechanisms control the transcriptional property of beta-catenin. Cell Signal 20: 1697-1704, 2008.
15. Jin T, Liu L. The Wnt signaling pathway effector TCF7L2 and type 2 diabetes mellitus. Mol Endocrinol 22: 2383-2392, 2008.
16. Jungermann K, Katz N. Functional specialization of different hepatocyte populations. Physiol Rev 69: 708-764, 1989.
17. Kahn CR, Lauris V, Koch S, Crettaz M, Granner DK. Acute and chronic regulation of phosphoenolpyruvate carboxykinase mRNA by insulin and glucose. Mol Endocrinol 3: 840-845, 1989.
18. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19: 379-383, 1998.
19. Krutzfeldt J, Stoffel M. Regulation of wingless-type MMTV integration site family (WNT) signalling in pancreatic islets from wild-type and obese mice. Diabetologia 53: 123-127, 2010.
20. Liu H, Fergusson MM, Wu JJ, Rovira II, Liu J, Gavrilova O, Lu T, Bao J, Han D, Sack MN, Finkel T. Wnt signaling regulates hepatic metabolism. Sci Signal 4: ra6, 2011.
21. Locke JM, Da Silva Xavier G, Rutter GA, Harries LW. An alternative polyadenylation signal in TCF7L2 generates isoforms that inhibit T cell factor/lymphoid-enhancer factor (TCF/LEF)-dependent target genes. Diabetologia 54: 3078-3082, 2011.
22. Lyssenko V, Lupi R, Marchetti P, Del Guerra S, Orho-Melander M, Almgren P, Sjögren M, Ling C, Eriksson KF, Lethagen AL, Mancarella R, Berglund G, Tuomi T, Nilsson P, Del Prato S, Groop L. Mechanisms by which common variants in the TCF7L2 gene increase risk of type 2 diabetes. J Clin Invest 117: 2155-2163, 2007.
23. Matsumoto M, Pocai A, Rossetti L, Depinho RA, Accili D. Impaired regulation of hepatic glucose production in mice lacking the forkhead transcription factor Foxo1 in liver. Cell Metab 6: 208-216, 2007.
24. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 275: 1787-1790, 1997.
25. Ni Z, Anini Y, Fang X, Mills G, Brubaker PL, Jin T. Transcriptional activation of the proglucagon gene by lithium and beta-catenin in intestinal endocrine L cells. J Biol Chem 278: 1380-1387, 2003.
26. Norton L, Fourcaudot M, Abdul-Ghani MA, Winnier D, Mehta FF, Jenkinson CP, Defronzo RA. Chromatin occupancy of transcription factor 7-like 2 (TCF7L2) and its role in hepatic glucose metabolism. Diabetologia 54: 3132-3142, 2011.
27. Philippe J. Insulin regulation of the glucagon gene is mediated by an insulin-responsive DNA element. Proc Natl Acad Sci USA 88: 7224-7227, 1991.
28. Pilgaard K, Jensen CB, Schou JH, Lyssenko V, Wegner L, Brons C, Vilsboll T, Hansen T, Madsbad S, Holst JJ, Volund A, Poulsen P, Groop L, Pedersen O, Vaag AA. The T allele of rs7903146 TCF7L2 is associated with impaired insulinotropic action of incretin hormones, reduced 24 h profiles of plasma insulin and glucagon, and increased hepatic glucose production in young healthy men. Diabetologia 52: 1298-1307, 2009.
29. Ross SE, Hemati N, Longo KA, Bennett CN, Lucas PC, Erickson RL, MacDougald OA. Inhibition of adipogenesis by Wnt signaling. Science 289: 950-953, 2000.
30. Savic D, Ye H, Aneas I, Park SY, Bell GI, Nobrega MA. Alterations in TCF7L2 expression define its role as a key regulator of glucose metabolism. Genome Res 21: 1417-1425, 2011.
31. Schäfer SA, Tschritter O, Machicao F, Thamer C, Stefan N, Gallwitz B, Holst JJ, Dekker JM, 't Hart LM, Nijpels G, van Haeften TW, Häring HU, Fritsche A. Impaired glucagon-like peptide-1-induced insulin secretion in carriers of transcription factor 7-like 2 (TCF7L2) gene polymorphisms. Diabetologia 50: 2443-2450, 2007.
32. Schinner S. Wnt-signalling and the metabolic syndrome. Horm Metab Res 41: 159-163, 2009.
33. Shu L, Matveyenko AV, Kerr-Conte J, Cho JH, McIntosh CH, Maedler K. Decreased TCF7L2 protein levels in type 2 diabetes mellitus correlate with downregulation of GIP-and GLP-1 receptors and impaired beta-cell function. Hum Mol Genet 18: 2388-2399, 2009.
34. Shu L, Sauter NS, Schulthess FT, Matveyenko AV, Oberholzer J, Maedler K. Transcription factor 7-like 2 regulates beta-cell survival and function in human pancreatic islets. Diabetes 57: 645-653, 2008.
35. Stambolic V, Ruel L, Woodgett JR. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr Biol 6: 1664-1668, 1996.
36. Sugden PH, Fuller SJ, Weiss SC, Clerk A. Glycogen synthase kinase 3 (GSK3) in the heart: a point of integration in hypertrophic signalling and a therapeutic target? A critical analysis. Br J Pharmacol 153, Suppl 1: S137-S153, 2008.
37. Sun J, Khalid S, Rozakis-Adcock M, Fantus IG, Jin T. P-21-activated protein kinase-1 functions as a linker between insulin and Wnt signaling pathways in the intestine. Oncogene 28: 3132-3144, 2009.
38. Sun J, Wang D, Jin T. Insulin alters the expression of components of the Wnt signaling pathway including TCF-4 in the intestinal cells. Biochim Biophys Acta 1800: 344-351, 2010.
39. Wegner L, Hussain MS, Pilgaard K, Hansen T, Pedersen O, Vaag A, Poulsen P. Impact of TCF7L2 rs7903146 on insulin secretion and action in young and elderly Danish twins. J Clin Endocrinol Metab 93: 4013-4019, 2008.
40. Xi L, Xiao C, Bandsma RH, Naples M, Adeli K, Lewis GF. C-reactive protein impairs hepatic insulin sensitivity and insulin signaling in rats: role of mitogen-activated protein kinases. Hepatology 53: 127-135, 2011.
41. Yi F, Brubaker PL, Jin T. TCF-4 mediates cell type-specific regulation of proglucagon gene expression by beta-catenin and glycogen synthase kinase-3beta. J Biol Chem 280: 1457-1464, 2005.
42. Yi F, Sun J, Lim GE, Fantus IG, Brubaker PL, Jin T. Cross talk between the insulin and Wnt signaling pathways: evidence from intestinal endocrine L cells. Endocrinology 149: 2341-2351, 2008.