Tissue-specific alternative splicing of TCF7L2

Human Molecular Genetics

Volumn 18, Issue 20, 2009, Pages 3795-3804

  Prokunina Olsson, Ludmila ^a,b   Welch, Cullan ^c   Hansson, Ola ^d   Adhikari, Neeta ^e   Scott, Laura J ^e   Usher, Nicolle ^c   Tong, Maurine ^a   Sprau, Andrew ^a   Swift, Amy ^a   Bonnycastle, Lori L ^a   Erdos, Michael R ^a   He, Zhi ^e   Saxena, Richa ^f   Harmon, Brennan ^g   Kotova, Olga ^d   Hoffman, Eric P ^g   Altshuler, David ^f   Groop, Leif ^d   Boehnke, Michael ^e   Collins, Francis S ^a   Hall, Jennifer L ^c   more..

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d LUND UNIVERSITY DIABETES CENTRE   (Sweden)

^e UNIVERSITY OF MICHIGAN   (United States)

^f BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^g CHILDREN'S NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; MESSENGER RNA; PROINSULIN; TRANSCRIPTION FACTOR 7 LIKE 2;

ALLELE; ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; COLON; CONTROLLED STUDY; EMBRYO; FEMALE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC DIFFERENCE; GENETIC RISK; GENETIC VARIABILITY; GENOTYPE; HUMAN; HUMAN CELL; HUMAN TISSUE; INTRON; LIVER; LYMPHOBLASTOID CELL LINE; MONOCYTE; NON INSULIN DEPENDENT DIABETES MELLITUS; NUCLEOTIDE SEQUENCE; PANCREAS; PANCREAS ISLET; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SKELETAL MUSCLE; SUBCUTANEOUS FAT; TISSUE SPECIFICITY;

ADOLESCENT; ADULT; ALTERNATIVE SPLICING; CELL LINE; COLON; DIABETES MELLITUS, TYPE 2; FEMALE; GENE EXPRESSION; HUMANS; ISLETS OF LANGERHANS; LIVER; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; ORGAN SPECIFICITY; PANCREAS; PROTEIN ISOFORMS; TCF TRANSCRIPTION FACTORS; YOUNG ADULT;

EID: 70349569023     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp321     Document Type: Article

References (59)

1. Grant, S.F., Thorleifsson, G., Reynisdottir, I., Benediktsson, R., Manolescu, A., Sainz, J., Helgason, A., Stefansson, H., Emilsson, V., Helgadottir, A. et al. (2006) Variant of transcription factor 7-like 2 (TCF7L2) gene confers risk of type 2 diabetes. Nat. Genet. 38, 320-323.
2. Scott, L.J., Mohlke, K.L., Bonnycastle, L.L., Willer, C.J., Li, Y., Duren, W.L., Erdos, M.R., Stringham, H.M., Chines, P.S., Jackson, A.U. et al. (2007) A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science, 316 1341-1345.
3. Saxena, R., Voight, B.F., Lyssenko, V., Burtt, N.P., de Bakker, P.I., Chen, H., Roix, J.J., Kathiresan, S., Hirschhorn, J.N., Daly, M.J. et al. (2007) Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science, 316, 1331-1336.
4. Zeggini, E., Weedon, M.N., Lindgren, C.M., Frayling, T.M., Elliott, K.S., Lango, H., Timpson, N.J., Perry, J.R., Rayner, N.W., Freathy, R.M. et al. (2007) Replication of genome-wide association signals in UK samples reveals risk loci for type 2 diabetes. Science, 316, 1336-1341.
5. Zhang, C., Qi, L., Hunter, D.J., Meigs, J.B., Manson, J.E., van Dam, R.M. and Hu, F.B. (2006) Variant of transcription factor 7-like 2 (TCF7L2) gene and the risk of type 2 diabetes in large cohorts of U.S. women and men. Diabetes, 55, 2645-2648.
6. van Vliet-Ostaptchouk, J.V., Shiri-Sverdlov, R., Zhernakova, A., Strengman, E., van Haeften, T.W., Hofker, M.H. and Wijmenga, C. (2007) Association of variants of transcription factor 7-like 2 (TCF7L2) with susceptibility to type 2 diabetes in the Dutch Breda cohort. Diabetologia, 50, 59-62.
7. Scott, L.J., Bonnycastle, L.L., Willer, C.J., Sprau, A.G., Jackson, A.U., Narisu, N., Duren, W.L., Chines, P.S., Stringham, H.M., Erdos, M.R. et al. (2006) Association of transcription factor 7-like 2 (TCF7L2) variants with type 2 diabetes in a Finnish sample. Diabetes 55, 26490-2653.
8. Saxena, R., Gianniny, L., Burtt, N.P., Lyssenko, V., Giuducci, C., Sjogren, M., Florez, J.C., Almgren, P., Isomaa, B., Orho-Melander, M. et al. (2006) Common single nucleotide polymorphisms in TCF7L2 are reproducibly associated with type 2 diabetes and reduce the insulin response to glucose in nondiabetic individuals. Diabetes, 55 2890-2895.
9. Mayans, S., Lackovic, K., Lindgren, P., Ruikka, K., Agren, A., Eliasson, M. and Holmberg, D. (2007) TCF7L2 polymorphisms are associated with type 2 diabetes in northern Sweden. Eur. J. Hum. Genet., 15, 342-346.
10. Marzi, C., Huth, C., Kolz, M., Grallert, H., Meisinger, C., Wichmann, H.E., Rathmann, W., Herder, C. and Illig, T. (2007) Variants of the transcription factor 7-like 2 gene (TCF7L2) are strongly associated with type 2 diabetes but not with the metabolic syndrome in the MONICA/KORA surveys. Horm. Metab. Res., 39, 46-52.
11. Humphries, S.E., Gable, D., Cooper, J.A., Ireland, H., Stephens, J.W., Hurel, S.J., Li, K.W., Palmen, J., Miller, M.A., Cappuccio, F.P. et al. (2006) Common variants in the TCF7L2 gene and predisposition to type 2 diabetes in UK European Whites, Indian Asians and Afro-Caribbean men and women. J. Mol. Med., 84, 1-10.
12. Helgason, A., Palsson, S., Thorleifsson, G., Grant, S.F., Emilsson, V., Gunnarsdottir, S., Adeyemo, A., Chen, Y., Chen, G., Reynisdottir, I. et al. (2007) Refining the impact of TCF7L2 gene variants on type 2 diabetes and adaptive evolution. Nat. Genet., 39, 218-225.
13. Groves, C.J., Zeggini, E., Minton, J., Frayling, T.M., Weedon, M.N., Rayner, N.W., Hitman, G.A., Walker, M., Wiltshire, S., Hattersley, A.T. et al. (2006) Association analysis of 6,736 U.K. subjects provides replication and confirms TCF7L2 as a type 2 diabetes susceptibility gene with a substantial effect on individual risk. Diabetes, 55, 2640-2644.
14. Damcott, C.M., Pollin, T.I., Reinhart, L.J., Ott, S.H., Shen, H., Silver, K.D., Mitchell, B.D. and Shuldiner, A.R. (2006) Polymorphisms in the transcription factor 7-like 2 (TCF7L2) gene are associated with type 2 diabetes in the Amish: Replication and evidence for a role in both insulin secretion and insulin resistance. Diabetes, 55, 2654-2659.
15. Chandak, G.R., Janipalli, C.S., Bhaskar, S., Kulkarni, S.R., Mohankrishna, P., Hattersley, A.T., Frayling, T.M. and Yajnik, C.S. (2007) Common variants in the TCF7L2 gene are strongly associated with type 2 diabetes mellitus in the Indian population. Diabetologia, 50, 63-67.
16. Schafer, S.A., Tschritter, O., Machicao, F., Thamer, C., Stefan, N., Gallwitz, B., Holst, J.J., Dekker, J.M., t'Hart, L.M., Nijpels, G. et al. (2007) Impaired glucagon-like peptide-1-induced insulin secretion in carriers of transcription factor 7-like 2 (TCF7L2) gene polymorphisms. Diabetologia, 50, 2443-2450.
17. Raitakari, O.T., Ronnemaa, T., Huupponen, R., Viikari, L., Fan, M., Marniemi, J., Hutri-Kahonen, N., Viikari, J.S. and Lehtimaki, T. (2007) Variation of the transcription factor 7-like 2 (TCF7L2) gene predicts impaired fasting glucose in healthy young adults: The Cardiovascular Risk in Young Finns Study. Diabetes Care, 30, 2299-2301.
18. Palmer, N.D., Lehtinen, A.B., Langefeld, C.D., Campbell, J.K., Haffner, S.M., Norris, J.M., Bergman, R.N., Goodarzi, M.O., Rotter, J.I. and Bowden, D.W. (2008) Association of TCF7L2 gene polymorphisms with reduced acute insulin response in Hispanic Americans. J. Clin. Endocrinol. Metab., 93, 304-309.
19. Munoz, J., Lok, K.H., Gower, B.A., Fernandez, J.R., Hunter, G.R., Lara-Castro, C., De Luca, M. and Garvey, W.T. (2006) Polymorphism in the transcription factor 7-like 2 (TCF7L2) gene is associated with reduced insulin secretion in nondiabetic women. Diabetes, 55, 3630-3634.
20. Watanabe, R.M., Allayee, H., Xiang, A.H., Trigo, E., Hartiala, J., Lawrence, J.M. and Buchanan, T.A. (2007) Transcription factor 7-like 2 (TCF7L2) is associated with gestational diabetes mellitus and interacts with adiposity to alter insulin secretion in Mexican Americans. Diabetes, 56, 1481-1485.
21. Wang, J., Kuusisto, J., Vanttinen, M., Kuulasmaa, T., Lindstrom, J., Tuomilehto, J., Uusitupa, M. and Laakso, M. (2007) Variants of transcription factor 7-like 2 (TCF7L2) gene predict conversion to type 2 diabetes in the Finnish Diabetes Prevention Study and are associated with impaired glucose regulation and impaired insulin secretion. Diabetologia, 50, 1192-1200.
22. Stolerman, E.S., Manning, A.K., McAteer, J.B., Fox, C.S., Dupuis, J., Meigs, J.B. and Florez, J.C. (2009) TCF7L2 variants are associated with increased proinsulin/insulin ratios but not obesity traits in the Framingham Heart Study. Diabetologia, 52, 614-620.
23. Stancakova, A., Kuulasmaa, T., Paananen, J., Jackson, A.U., Bonnycastle, L.L., Collins, F.S., Boehnke, M., Kuusisto, J. and Laakso, M. (2009) Association of 18 confirmed susceptibility loci for type 2 diabetes with indices of insulin release, proinsulin conversion, and insulin sensitivity in 5 327 non-diabetic Finnish men. Diabetes (Epub ahead of print).
24. Clevers, H. and van de Wetering, M. (1997) TCF/LEF factor earn their wings. Trends Genet., 13, 485-489.
25. Brantjes, H., Barker, N., van Es, J. and Clevers, H. (2002) TCF: Lady Justice casting the final verdict on the outcome of Wnt signalling. Biol. Chem., 383, 255-261.
26. Korinek, V., Barker, N., Moerer, P., van Donselaar, E., Huls, G., Peters, P.J. and Clevers, H. (1998) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat. Genet., 19, 379-383.
27. Yi, F., Brubaker, P.L. and Jin, T. (2005) 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.
28. Lyssenko, V., Lupi, R., Marchetti, P., Del Guerra, S., Orho-Melander, M., Almgren, P., Sjogren, M., Ling, C., Eriksson, K.F., Lethagen, A.L. et al. (2007) Mechanisms by which common variants in the TCF7L2 gene increase risk of type 2 diabetes. J. Clin. Invest., 117 2155-2163.
29. Pilgaard, K., Jensen, C.B., Schou, J.H., Lyssenko, V., Wegner, L., Brons, C., Vilsboll, T., Hansen, T., Madsbad, S., Holst, J.J. et al. (2009) 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.
30. Zhang, W., Duan, S., Bleibel, W.K., Wisel, S.A., Huang, R.S., Wu, X., He, L., Clark, T.A., Chen, T.X., Schweitzer, A.C. et al. (2008) Identification of common genetic variants that account for transcript isoform variation between human populations. Hum. Genet., 125 81-93.
31. Graham, R.R., Kozyrev, S.V., Baechler, E.C., Reddy, M.V., Plenge, R.M., Bauer, J.W., Ortmann, W.A., Koeuth, T., Gonzalez Escribano, M.F., Pons-Estel, B. et al. (2006) A common haplotype of interferon regulatory factor 5 (IRF5) regulates splicing and expression and is associated with increased risk of systemic lupus erythematosus. Nat. Genet., 38, 550-555.
32. Ahlzen, M., Johansson, L.E., Cervin, C., Tornqvist, H., Groop, L. and Ridderstrale, M. (2008) 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.
33. Wegner, L., Hussain, M.S., Pilgaard, K., Hansen, T., Pedersen, O., Vaag, A. and Poulsen, P. (2008) Impact of TCF7L2 rs7903146 on Insulin Secretion and Action in Young and Elderly Danish Twins. J. Clin. Endocrinol. Metab., 93, 4013-4019.
34. Elbein, S.C., Chu, W.S., Das, S.K., Yao-Borengasser, A., Hasstedt, S.J., Wang, H., Rasouli, N. and Kern, P.A. (2007) Transcription factor 7-like 2 polymorphisms and type 2 diabetes, glucose homeostasis traits and gene expression in US participants of European and African descent. Diabetologia, 50, 1621-1630.
35. Cauchi, S., Meyre, D., Dina, C., Choquet, H., Samson, C., Gallina, S., Balkau, B., Charpentier, G., Pattou, F., Stetsyuk, V. et al. (2006) Transcription factor TCF7L2 genetic study in the French population: Expression in human beta-cells and adipose tissue and strong association with type 2 diabetes. Diabetes, 55, 2903-2908.
36. Huertas-Vazquez, A., Plaisier, C., Weissglas-Volkov, D., Sinsheimer, J., Canizales-Quinteros, S., Cruz-Bautista, I., Nikkola, E., Herrera-Hernandez, M., Davila-Cervantes, A., Tusie-Luna, T. et al. (2008) TCF7L2 is associated with high serum triacylglycerol and differentially expressed in adipose tissue in families with familial combined hyperlipidaemia. Diabetologia, 51, 62-69.
37. Hindle, A.K., Brody, F., Tevar, R., Kluk, B., Hill, S., McCaffrey, T. and Fu, S. (2008) TCF7L2 expression in diabetic patients undergoing bariatric surgery. Surg. Endosc., 23, 1292-1297.
38. Osmark, P., Hansson, O., Jonsson, A., Ronn, T., Groop, L. and Renstrom, E. (2009) Unique splicing pattern of the TCF7L2 gene in human pancreatic islets. Diabetologia, 52, 850-854.
39. Duval, A., Busson-Leconiat, M., Berger, R. and Hamelin, R. (2000) Assignment of the TCF-4 gene (TCF7L2) to human chromosome band 10q25.3. Cytogenet. Cell Genet., 88, 264-265.
40. Howng, S.L., Huang, F.H., Hwang, S.L., Lieu, A.S., Sy, W.D., Wang, C. and Hong, Y.R. (2004) Differential expression and splicing isoform analysis of human Tcf-4 transcription factor in brain tumors. Int. J. Oncol., 25, 1685-1692.
41. Shiina, H., Igawa, M., Breault, J., Ribeiro-Filho, L., Pookot, D., Urakami, S., Terashima, M., Deguchi, M., Yamanaka, M., Shirai, M. et al. (2003) The human T-cell factor-4 gene splicing isoforms, Wnt signal pathway, and apoptosis in renal cell carcinoma. Clin. Cancer Res., 9, 2121-2132.
42. Van de Wetering, M., Castrop, J., Korinek, V. and Clevers, H. (1996) Extensive alternative splicing and dual promoter usage generate Tcf-1 protein isoforms with differential transcription control properties. Mol. Cell Biol., 16, 745-752.
43. Hovanes, K., Li, T.W. and Waterman, M.L. (2000) The human LEF-1 gene contains a promoter preferentially active in lymphocytes and encodes multiple isoforms derived from alternative splicing. Nucleic Acids Res., 28, 1994-2003.
44. Hovanes, K., Li, T.W., Munguia, J.E., Truong, T., Milovanovic, T., Lawrence Marsh, J., Holcombe, R.F. and Waterman, M.L. (2001) Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat. Genet., 28, 53-57.
45. Kozak, M. (1987) An analysis of 5′-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res., 15, 8125-8148.
46. Reynisdottir, I., Thorleifsson, G., Benediktsson, R., Sigurdsson, G., Emilsson, V., Einarsdottir, A.S., Hjorleifsdottir, E.E., Orlygsdottir, G.T., Bjornsdottir, G.T., Saemundsdottir, J. et al. (2003) Localization of a susceptibility gene for type 2 diabetes to chromosome 5q34-q35.2. Am. J. Hum. Genet., 73, 323-335.
47. Duggirala, R., Blangero, J., Almasy, L., Dyer, T.D., Williams, K.L., Leach, R.J., O'Connell, P. and Stern, M.P. (1999) Linkage of type 2 diabetes mellitus and of age at onset to a genetic location on chromosome 10q in Mexican Americans. Am. J. Hum. Genet., 64, 1127-1140.
48. Li, T.W., Ting, J.H., Yokoyama, N.N., Bernstein, A., van de Wetering, M. and Waterman, M.L. (2006) Wnt activation and alternative promoter repression of LEF1 in colon cancer. Mol. Cell Biol., 26, 5284-5299.
49. Benassayag, C., Montero, L., Colombie, N., Gallant, P., Cribbs, D. and Morello, D. (2005) Human c-Myc isoforms differentially regulate cell growth and apoptosis in Drosophila melanogaster. Mol. Cell Biol., 25, 9897-9909.
50. Zaika, A.I., Slade, N., Erster, S.H., Sansome, C., Joseph, T.W., Pearl, M., Chalas, E. and Moll, U.M. (2002) DeltaNp73, a dominant-negative inhibitor of wild-type p53 and TAp73, is up-regulated in human tumors. J. Exp. Med., 196, 765-780.
51. Korinek, V., Barker, N., Morin, P.J., van Wichen, D., de Weger, R., Kinzler, K.W., Vogelstein, B. and Clevers, H. (1997) Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science, 275, 1784-1787.
52. Brantjes, H., Roose, J., van De Wetering, M. and Clevers, H. (2001) All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Res., 29, 1410-1419.
53. Fang, M., Li, J., Blauwkamp, T., Bhambhani, C., Campbell, N. and Cadigan, K.M. (2006) C-terminal-binding protein directly activates and represses Wnt transcriptional targets in Drosophila. EMBO J., 25, 2735-2745.
54. Atcha, F.A., Syed, A., Wu, B., Hoverter, N.P., Yokoyama, N.N., Ting, J.H., Munguia, J.E., Mangalam, H.J., Marsh, J.L. and Waterman, M.L. (2007) A unique DNA binding domain converts T-cell factors into strong Wnt effectors. Mol. Cell Biol., 27, 8352-8363.
55. Tang, W., Dodge, M., Gundapaneni, D., Michnoff, C., Roth, M. and Lum, L. (2008) A genome-wide RNAi screen for Wnt/beta-catenin pathway components identifies unexpected roles for TCF transcription factors in cancer. Proc. Natl. Acad Sci. USA, 105, 9697-9702.
56. Shu, L., Sauter, N.S., Schulthess, F.T., Matveyenko, A.V., Oberholzer, J. and Maedler, K. (2008) Transcription factor 7-like 2 regulates beta-cell survival and function in human pancreatic islets. Diabetes 57, 645-653.
57. Atcha, F.A., Munguia, J.E., Li, T.W., Hovanes, K. and Waterman, M.L. (2003) A new beta-catenin-dependent activation domain in T cell factor. J. Biol. Chem., 278, 16169-16175.
58. Listerman, I., Sapra, A.K. and Neugebauer, K.M. (2006) Cotranscriptional coupling of splicing factor recruitment and precursor messenger RNA splicing in mammalian cells. Nat. Struct. Mol. Biol., 13, 815-822.
59. Kornblihtt, A.R., de la Mata, M., Fededa, J.P., Munoz, M.J. and Nogues, G. (2004) Multiple links between transcription and splicing. RNA, 10, 1489-1498.