A dynamic exchange of TCF3 and TCF4 transcription factors controls MYC expression in colorectal cancer cells

References

• Siegel R, Desantis C, Jemal A. Colorectal cancer statistics, 2014. CA Cancer J Clin 2014; 64:104-17; PMID:24639052; http://dx.doi.org/10.3322/caac.21220
   PubMed Web of Science ®Google Scholar
• Fearon ER. Molecular genetics of colorectal cancer. Annu Rev Pathol 2011; 6:479-507; PMID:21090969; http://dx.doi.org/10.1146/annurev-pathol-011110-130235
   PubMed Web of Science ®Google Scholar
• Clevers H, Nusse R. Wnt/beta-catenin signaling and disease. Cell 2012; 149:1192-205; PMID:22682243; http://dx.doi.org/10.1016/j.cell.2012.05.012
   PubMed Web of Science ®Google Scholar
• MacDonald BT, Tamai K, He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev Cell 2009; 17:9-26; PMID:19619488; http://dx.doi.org/10.1016/j.devcel.2009.06.016
   PubMed Web of Science ®Google Scholar
• Cadigan KM. TCFs and Wnt/beta-catenin signaling: more than one way to throw the switch. Curr Top Dev Biol 2012; 98:1-34; PMID:22305157; http://dx.doi.org/10.1016/B978-0-12-386499-4.00001-X
   PubMed Web of Science ®Google Scholar
• Mosimann C, Hausmann G, Basler K. Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol Cell Biol 2009; 10:276-86; PMID:19305417; http://dx.doi.org/10.1038/nrm2654
   PubMed Web of Science ®Google Scholar
• Cadigan KM, Waterman ML. TCF/LEFs and Wnt signaling in the nucleus. Cold Spring Harb Perspect Biol 2012; 4; PMID:23024173
   PubMed Web of Science ®Google Scholar
• Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B, Clevers H. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC−/− colon carcinoma. Science 1997; 275:1784-7; PMID:9065401; http://dx.doi.org/10.1126/science.275.5307.1784
   PubMed Web of Science ®Google Scholar
• 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 1998; 19:379-83; PMID:9697701; http://dx.doi.org/10.1038/1270
   PubMed Web of Science ®Google Scholar
• Barker N, Huls G, Korinek V, Clevers H. Restricted high level expression of Tcf-4 protein in intestinal and mammary gland epithelium. Am J Pathol 1999; 154:29-35; PMID:9916915; http://dx.doi.org/10.1016/S0002-9440(10)65247-9
   PubMed Web of Science ®Google Scholar
• van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, van der Horn K, Batlle E, Coudreuse D, Haramis AP, et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 2002; 111:241-50; PMID:12408868; http://dx.doi.org/10.1016/S0092-8674(02)01014-0
   PubMed Web of Science ®Google Scholar
• Angus-Hill ML, Elbert KM, Hidalgo J, Capecchi MR. T-cell factor 4 functions as a tumor suppressor whose disruption modulates colon cell proliferation and tumorigenesis. Proc Natl Acad Sci U S A 2011; 108:4914-9; PMID:21383188; http://dx.doi.org/10.1073/pnas.1102300108
   PubMed Web of Science ®Google Scholar
• Tang W, Dodge M, Gundapaneni D, Michnoff C, Roth M, Lum L. A genome-wide RNAi screen for Wnt/beta-catenin pathway components identifies unexpected roles for TCF transcription factors in cancer. Proc Natl Acad Sci U S A 2008; 105:9697-702; PMID:18621708; http://dx.doi.org/10.1073/pnas.0804709105
   PubMed Web of Science ®Google Scholar
• Merrill BJ. Wnt pathway regulation of embryonic stem cell self-renewal. Cold Spring Harb Perspect Biol 2012; 4:a007971; PMID:22952393; http://dx.doi.org/10.1101/cshperspect.a007971
   PubMed Web of Science ®Google Scholar
• Lien WH, Fuchs E. Wnt some lose some: transcriptional governance of stem cells by Wnt/beta-catenin signaling. Genes Dev 2014; 28:1517-32; PMID:25030692; http://dx.doi.org/10.1101/gad.244772.114
   PubMed Web of Science ®Google Scholar
• van Es JH, Haegebarth A, Kujala P, Itzkovitz S, Koo BK, Boj SF, Korving J, van den Born M, van Oudenaarden A, Robine S, et al. A critical role for the Wnt effector Tcf4 in adult intestinal homeostatic self-renewal. Mol Cell Biol 2012; 32:1918-27; PMID:22393260; http://dx.doi.org/10.1128/MCB.06288-11
   PubMed Web of Science ®Google Scholar
• Chiaro C, Lazarova DL, Bordonaro M. Tcf3 and cell cycle factors contribute to butyrate resistance in colorectal cancer cells. Biochem Biophys Res Commun 2012; 428:121-6; PMID:23063976; http://dx.doi.org/10.1016/j.bbrc.2012.10.018
   PubMed Web of Science ®Google Scholar
• Athineos D, Sansom OJ. Myc heterozygosity attenuates the phenotypes of APC deficiency in the small intestine. Oncogene 2010; 29:2585-90; PMID:20140021; http://dx.doi.org/10.1038/onc.2010.5
   PubMed Web of Science ®Google Scholar
• Ignatenko NA, Holubec H, Besselsen DG, Blohm-Mangone KA, Padilla-Torres JL, Nagle RB, de Alboránç IM, Guillen-R JM, Gerner EW. Role of c-Myc in intestinal tumorigenesis of the ApcMin/+ mouse. Cancer Biol Ther 2006; 5:1658-64; PMID:17106247; http://dx.doi.org/10.4161/cbt.5.12.3376
   PubMed Web of Science ®Google Scholar
• Sansom OJ, Meniel VS, Muncan V, Phesse TJ, Wilkins JA, Reed KR, Vass JK, Athineos D, Clevers H, Clarke AR. Myc deletion rescues Apc deficiency in the small intestine. Nature 2007; 446:676-9; PMID:17377531; http://dx.doi.org/10.1038/nature05674
   PubMed Web of Science ®Google Scholar
• Wilkins JA, Sansom OJ. C-Myc is a critical mediator of the phenotypes of Apc loss in the intestine. Cancer Res 2008; 68:4963-6; PMID:18593890; http://dx.doi.org/10.1158/0008-5472.CAN-07-5558
   PubMed Web of Science ®Google Scholar
• Yekkala K, Baudino TA. Inhibition of intestinal polyposis with reduced angiogenesis in ApcMin/+ mice due to decreases in c-Myc expression. Mol Cancer Res 2007; 5:1296-303; PMID:18171987; http://dx.doi.org/10.1158/1541-7786.MCR-07-0232
   PubMed Web of Science ®Google Scholar
• Konsavage WM, Jr., Yochum GS. The myc 3' wnt-responsive element suppresses colonic tumorigenesis. Mol Cell Biol 2014; 34:1659-69; PMID:24567369; http://dx.doi.org/10.1128/MCB.00969-13
   PubMed Web of Science ®Google Scholar
• Konsavage WM, Jr., Jin G, Yochum GS. The Myc 3' Wnt-responsive element regulates homeostasis and regeneration in the mouse intestinal tract. Mol Cell Biol 2012; 32:3891-902; PMID:22826434; http://dx.doi.org/10.1128/MCB.00548-12
   PubMed Web of Science ®Google Scholar
• Sur IK, Hallikas O, Vaharautio A, Yan J, Turunen M, Enge M, Taipale M, Karhu A, Aaltonen LA, Taipale J. Mice lacking a Myc enhancer that includes human SNP rs6983267 are resistant to intestinal tumors. Science 2012; 338:1360-3; PMID:23118011; http://dx.doi.org/10.1126/science.1228606
   PubMed Web of Science ®Google Scholar
• Bottomly D, Kyler SL, McWeeney SK, Yochum GS. Identification of {beta}-catenin binding regions in colon cancer cells using ChIP-Seq. Nucleic Acids Res 2010; 38:5735-45; PMID:20460455; http://dx.doi.org/10.1093/nar/gkq363
   PubMed Web of Science ®Google Scholar
• Yochum GS, McWeeney S, Rajaraman V, Cleland R, Peters S, Goodman RH. Serial analysis of chromatin occupancy identifies beta-catenin target genes in colorectal carcinoma cells. Proc Natl Acad Sci U S A 2007; 104:3324-9; PMID:17360646; http://dx.doi.org/10.1073/pnas.0611576104
   PubMed Web of Science ®Google Scholar
• Yochum GS, Cleland R, Goodman RH. A genome-wide screen for beta-catenin binding sites identifies a downstream enhancer element that controls c-Myc gene expression. Mol Cell Biol 2008; 28:7368-79; PMID:18852287; http://dx.doi.org/10.1128/MCB.00744-08
   PubMed Web of Science ®Google Scholar
• Mautner J, Joos S, Werner T, Eick D, Bornkamm GW, Polack A. Identification of two enhancer elements downstream of the human c-myc gene. Nucleic Acids Res 1995; 23:72-80; PMID:7870592; http://dx.doi.org/10.1093/nar/23.1.72
   PubMed Web of Science ®Google Scholar
• Yochum GS, Sherrick CM, Macpartlin M, Goodman RH. A beta-catenin/TCF-coordinated chromatin loop at MYC integrates 5′ and 3′ Wnt responsive enhancers. Proc Natl Acad Sci U S A 2010; 107:145-50; PMID:19966299; http://dx.doi.org/10.1073/pnas.0912294107
   PubMed Web of Science ®Google Scholar
• Mao CD, Byers SW. Cell-context dependent TCF/LEF expression and function: alternative tales of repression, de-repression and activation potentials. Crit Rev Eukaryot Gene Expr 2011; 21:207-36; PMID:22111711; http://dx.doi.org/10.1615/CritRevEukarGeneExpr.v21.i3.10
   PubMed Web of Science ®Google Scholar
• Konsavage WM, Jr., Kyler SL, Rennoll SA, Jin G, Yochum GS. Wnt/beta-catenin signaling regulates Yes-associated protein (YAP) gene expression in colorectal carcinoma cells. J Biol Chem 2012; 287:11730-9; PMID:22337891; http://dx.doi.org/10.1074/jbc.M111.327767
   PubMed Web of Science ®Google Scholar
• Yochum GS, Cleland R, McWeeney S, Goodman RH. An antisense transcript induced by Wnt/beta-catenin signaling decreases E2F4. J Biol Chem 2007; 282:871-8; PMID:17121828; http://dx.doi.org/10.1074/jbc.M609391200
   PubMed Web of Science ®Google Scholar
• Ilyas M, Tomlinson IP, Rowan A, Pignatelli M, Bodmer WF. Beta-catenin mutations in cell lines established from human colorectal cancers. Proc Natl Acad Sci U S A 1997; 94:10330-4; PMID:9294210; http://dx.doi.org/10.1073/pnas.94.19.10330
   PubMed Web of Science ®Google Scholar
• Deevi R, Fatehullah A, Jagan I, Nagaraju M, Bingham V, Campbell FC. PTEN regulates colorectal epithelial apoptosis through Cdc42 signalling. Br J Cancer 2011; 105:1313-21; PMID:21952626; http://dx.doi.org/10.1038/bjc.2011.384
   PubMed Web of Science ®Google Scholar
• Kang DW, Min do S. Positive feedback regulation between phospholipase D and Wnt signaling promotes Wnt-driven anchorage-independent growth of colorectal cancer cells. PLoS One 2010; 5:e12109; PMID:20711340; http://dx.doi.org/10.1371/journal.pone.0012109
   PubMed Web of Science ®Google Scholar
• Owens RB, Smith HS, Nelson-Rees WA, Springer EL. Epithelial cell cultures from normal and cancerous human tissues. J Natl Cancer Inst 1976; 56:843-9; PMID:176412
   PubMed Web of Science ®Google Scholar
• Wierstra I, Alves J. The c-myc promoter: still MysterY and challenge. Adv Cancer Res 2008; 99:113-333; PMID:18037408; http://dx.doi.org/10.1016/S0065-230X(07)99004-1
   PubMed Web of Science ®Google Scholar
• Toualbi K, Guller MC, Mauriz JL, Labalette C, Buendia MA, Mauviel A, Bernuau D. Physical and functional cooperation between AP-1 and beta-catenin for the regulation of TCF-dependent genes. Oncogene 2007; 26:3492-502; PMID:17146436; http://dx.doi.org/10.1038/sj.onc.1210133
   PubMed Web of Science ®Google Scholar
• Nesbit CE, Tersak JM, Prochownik EV. MYC oncogenes and human neoplastic disease. Oncogene 1999; 18:3004-16; PMID:10378696; http://dx.doi.org/10.1038/sj.onc.1202746
   PubMed Web of Science ®Google Scholar
• Yochum GS. Multiple Wnt/beta-catenin responsive enhancers align with the MYC promoter through long-range chromatin loops. PLoS One 2011; 6:e18966; PMID:21533051; http://dx.doi.org/10.1371/journal.pone.0018966
   PubMed Web of Science ®Google Scholar
• Tuupanen S, Turunen M, Lehtonen R, Hallikas O, Vanharanta S, Kivioja T, Björklund M, Wei G, Yan J, Niittymäki I, Mecklin JP, et al. The common colorectal cancer predisposition SNP rs6983267 at chromosome 8q24 confers potential to enhanced Wnt signaling. Nat Genet 2009; 41:885-90; PMID:19561604; http://dx.doi.org/10.1038/ng.406
   PubMed Web of Science ®Google Scholar
• Wright JB, Brown SJ, Cole MD. Upregulation of c-MYC in cis through a large chromatin loop linked to a cancer risk-associated single-nucleotide polymorphism in colorectal cancer cells. Mol Cell Biol 2010; 30:1411-20; PMID:20065031; http://dx.doi.org/10.1128/MCB.01384-09
   PubMed Web of Science ®Google Scholar
• Pomerantz MM, Ahmadiyeh N, Jia L, Herman P, Verzi MP, Doddapaneni H, Beckwith CA, Chan JA, Hills A, Davis M, et al. The 8q24 cancer risk variant rs6983267 shows long-range interaction with MYC in colorectal cancer. Nat Genet 2009; 41:882-4; PMID:19561607; http://dx.doi.org/10.1038/ng.403
   PubMed Web of Science ®Google Scholar
• Soucek L, Evan GI. The ups and downs of Myc biology. Curr Opin Genet Dev 2010; 20:91-5; PMID:19962879; http://dx.doi.org/10.1016/j.gde.2009.11.001
   PubMed Web of Science ®Google Scholar
• He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science 1998; 281:1509-12; PMID:9727977; http://dx.doi.org/10.1126/science.281.5382.1509
   PubMed Web of Science ®Google Scholar
• Arce L, Yokoyama NN, Waterman ML. Diversity of LEF/TCF action in development and disease. Oncogene 2006; 25:7492-504; PMID:17143293; http://dx.doi.org/10.1038/sj.onc.1210056
   PubMed Web of Science ®Google Scholar
• Shy BR, Wu CI, Khramtsova GF, Zhang JY, Olopade OI, Goss KH, Merrill BJ. Regulation of Tcf7l1 DNA binding and protein stability as principal mechanisms of Wnt/beta-catenin signaling. Cell Rep 2013; 4:1-9; PMID:23810553; http://dx.doi.org/10.1016/j.celrep.2013.06.001
   PubMed Web of Science ®Google Scholar
• Hikasa H, Sokol SY. Phosphorylation of TCF proteins by homeodomain-interacting protein kinase 2. J Biol Chem 2011; 286:12093-100; PMID:21285352; http://dx.doi.org/10.1074/jbc.M110.185280
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar