The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells

Cell

Volumn 111, Issue 2, 2002, Pages 241-250

  Van de Wetering, Marc ^a   Sancho, Elena ^a   Verweij, Cornelis ^b   De Lau, Wim ^a   Oving, Irma ^a   Hurlstone, Adam ^a   Van der Horn, Karin ^a   Batlle, Eduard ^a   Coudreuse, Damien ^a   Haramis, Anna Pavlina ^a   Tjon Pon Fong, Menno ^a   Moerer, Petra ^a   Van den Born, Maaike ^a   Soete, Gwen ^a   Pals, Steven ^c   Eilers, Martin ^d   Medema, Rene ^e   Clevers, Hans ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

^d PHILIPPS UNIVERSITY MARBURG   (Germany)

^e NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; RAN PROTEIN; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL CYCLE G1 PHASE; CELL DIFFERENTIATION; CELL PROLIFERATION; COLORECTAL CANCER; CONTROLLED STUDY; CRYPT CELL; GENE REPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; INTESTINE EPITHELIUM CELL; MITOSIS INHIBITION; NONHUMAN; ONCOGENE C MYC; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TRANSACTIVATION;

ANIMALIA;

EID: 18644373146     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(02)01014-0     Document Type: Article

References (51)

1. 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. 154:1999;29-35.
2. Batlle E., Henderson J.T., Beghtel H., van den Born M.M.W., Sancho E., Huls G., Meeldijk J., Roberston J., van de Wetering M., Pawson T., Clevers H. β-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell. 111:2002;251-263. this issue,
3. Bienz M., Clevers H. Linking colorectal cancer to Wnt signaling. Cell. 103:2000;311-320.
4. Castrop J., van Wichen D., Koomans Bitter M., van de Wetering M., de Weger R., van Dongen J., Clevers H. The human TCF-1 gene encodes a nuclear DNA-binding protein uniquely expressed in normal and neoplastic T-lineage lymphocytes. Blood. 86:1995;3050-3059.
5. Ciclitira P.J., Macartney J.C., Evan G. Expression of c-myc in non-malignant and pre-malignant gastrointestinal disorders. J. Pathol. 151:1987;293-296.
6. Deschenes C., Vezina A., Beaulieu J.F., Rivard N. Role of p27(Kip1) in human intestinal cell differentiation. Gastroenterology. 120:2001;423-438.
7. el Deiry W.S., Tokino T., Waldman T., Oliner J.D., Velculescu V.E., Burrell M., Hill D.E., Healy E., Rees J.L., Hamilton S.R.et al. Topological control of p21WAF1/CIP1 expression in normal and neoplastic tissues. Cancer Res. 55:1995;2910-2919.
8. Erisman M.D., Rothberg P.G., Diehl R.E., Morse C.C., Spandorfer J.M., Astrin S.M. Deregulation of c-myc gene expression in human colon carcinoma is not accompanied by amplification or rearrangement of the gene. Mol. Cell. Biol. 5:1985;1969-1976.
9. Evers B.M., Ko T.C., Li J., Thompson E.A. Cell cycle protein suppression and p21 induction in differentiating Caco-2 cells. Am. J. Physiol. 271:1996;G722-G727.
10. Fero M.L., Rivkin M., Tasch M., Porter P., Carow C.E., Firpo E., Polyak K., Tsai L.H., Broudy V., Perlmutter R.M.et al. A syndrome of multiorgan hyperplasia with features of gigantism, tumorigenesis, and female sterility in p27(Kip1)-deficient mice. Cell. 85:1996;733-744.
11. Fujita M., Furukawa Y., Tsunoda T., Tanaka T., Ogawa M., Nakamura Y. Up-regulation of the ectodermal-neural cortex 1 (ENC1) gene, a downstream target of the beta-catenin/T-cell factor complex, in colorectal carcinomas. Cancer Res. 61:2001;7722-7726.
12. Grandori C., Cowley S.M., James L.P., Eisenman R.N. The Myc/Max/Mad network and the transcriptional control of cell behaviour. Annu. Rev. Cell Dev. Biol. 16:2000;653-699.
13. Harper J.W., Adami G.R., Wei N., Keyomarsi K., Elledge S.J. The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell. 75:1993;805-816.
14. He T.C., Sparks A.B., Rago C., Hermeking H., Zawel L., da Costa L.T., Morin P.J., Vogelstein B., Kinzler K.W. Identification of c-MYC as a target of the APC pathway. Science. 281:1998;1509-1512.
15. Herold S., Wanzel M., Beuger V., Frohme C., Beul D., Hillukkala T., Syvaoja J., Saluz H.-P., Haenel F., Eilers M. Negative regulation of the mammalian UV response by Myc through association with Miz-1. Mol. Cell. 10:2002;509-521.
16. Kim J.S., Crooks H., Dracheva T., Nishanian T.G., Singh B., Jen J., Waldman T. Oncogenic beta-catenin is required for bone morphogenetic protein 4 expression in human cancer cells. Cancer Res. 62:2002;2744-2748.
17. Kinzler K.W., Vogelstein B. Lessons from hereditary colorectal cancer. Cell. 87:1996;159-170.
18. Kitahara O., Furukawa Y., Tanaka T., Kihara C., Ono K., Yanagawa R., Nita M.E., Takagi T., Nakamura Y., Tsunoda T. Alterations of gene expression during colorectal carcinogenesis revealed by cDNA microarrays after laser-capture microdissection of tumor tissues and normal epithelia. Cancer Res. 61:2001;3544-3549.
19. Kiyokawa H., Kineman R.D., Manova-Todorova K.O., Soares V.C., Hoffman E.S., Ono M., Khanam D., Hayday A.C., Frohman L.A., Koff A. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell. 85:1996;721-732.
20. Korinek V., Barker N., Morin P.J., van Wichen D., de Weger R., Kinzler K.W., Vogelstein B., Clevers H. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science. 275:1997;1784-1787.
21. Korinek V., Barker N., Moerer P., van Donselaar E., Huls G., Peters P.J., Clevers H. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat. Genet. 19:1998;379-383.
22. Korswagen H.C., Herman M.A., Clevers H.C. Distinct beta-catenins mediate adhesion and signalling functions in C. elegans. Nature. 406:2000;527-532.
23. Liu W., Dong X., Mai M., Seelan R.S., Taniguchi K., Krishnadath K.K., Halling K.C., Cunningham J.M., Qian C., Christensen E.et al. Mutations in AXIN2 cause colorectal cancer with defective mismatch repair by activating beta-catenin/TCF signalling. Nat. Genet. 26:2000;146-147.
24. Mariadason J.M., Bordonaro M., Aslam F., Shi L., Kuraguchi M., Velcich A., Augenlicht L.H. Down-regulation of beta-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Res. 61:2001;3465-3471.
25. Matthews J.B., Hassan I., Meng S., Archer S.Y., Hrnjez B.J., Hodin R.A. Na-K-2Cl cotransporter gene expression and function during enterocyte differentiation. Modulation of Cl-secretory capacity by butyrate. J. Clin. Invest. 101:1998;2072-2079.
26. Melhem M.F., Meisler A.I., Finley G.G., Bryce W.H., Jones M.O., Tribby I.I., Pipas J.M., Koski R.A. Distribution of cells expressing myc proteins in human colorectal epithelium, polyps, and malignant tumors. Cancer Res. 52:1992;5853-5864.
27. Miwa N., Furuse M., Tsukita S., Niikawa N., Nakamura Y., Furukawa Y. Involvement of claudin-1 in the beta-catenin/Tcf signaling pathway and its frequent upregulation in human colorectal cancers. Oncol. Res. 12:2001;469-476.
28. Molenaar M., van de Wetering M., Oosterwegel M., Peterson-Maduro J., Godsave S., Korinek V., Roose J., Destree O., Clevers H. XTcf-3 transcription factor mediates beta-catenin-induced axis formation in Xenopus embryos. Cell. 86:1996;391-399.
29. Morin P.J., Sparks A.B., Korinek V., Barker N., Clevers H., Vogelstein B., Kinzler K.W. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science. 275:1997;1787-1790.
30. Nakayama K., Ishida N., Shirane M., Inomata A., Inoue T., Shishido N., Horii I., Loh D.Y., Nakayama K. Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell. 85:1996;707-720.
31. Oba S.M., Wang Y.J., Song J.P., Li Z.Y., Kobayashi K., Tsugane S., Hamada G.S., Tanaka M., Sugimura H. Genomic structure and loss of heterozygosity of EPHB2 in colorectal cancer. Cancer Lett. 164:2001;97-104.
32. Philipp-Staheli J., Kim K.H., Payne S.R., Gurley K.E., Liggitt D., Longton G., Kemp C.J. Pathway-specific tumor suppression. Reduction of p27 accelerates gastrointestinal tumorigenesis in Apc mutant mice, but not in Smad3 mutant mice. Cancer Cell. 1:2002;355-368.
33. Potten C.S., Loeffler M. Stem cells. attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt Development. 110:1990;1001-1020.
34. Powell S.M., Zilz N., Beazer-Barclay Y., Bryan T.M., Hamilton S.R., Thibodeau S.N., Vogelstein B., Kinzler K.W. APC mutations occur early during colorectal tumorigenesis. Nature. 359:1992;235-237.
35. Quaroni A., Tian J.Q., Seth P., Ap R.C. p27(Kip1) is an inducer of intestinal epithelial cell differentiation. Am. J. Physiol. Cell Physiol. 279:2000;C1045-C1057.
36. Ramsay R.G., Thompson M.A., Hayman J.A., Reid G., Gonda T.J., Whitehead R.H. Myb expression is higher in malignant human colonic carcinoma and premalignant adenomatous polyps than in normal mucosa. Cell Growth Differ. 3:1992;723-730.
37. Roose J., Huls G., van Beest M., Moerer P., van der Horn K., Goldschmeding R., Logtenberg T., Clevers H. Synergy between tumor suppressor APC and the beta-catenin-Tcf4 target Tcf1. Science. 285:1999;1923-1926.
38. Rubinfeld B., Robbins P., El Gamil M., Albert I., Porfiri E., Polakis P. Stabilization of beta-catenin by genetic defects in melanoma cell lines. Science. 275:1997;1790-1792.
39. Satoh S., Daigo Y., Furukawa Y., Kato T., Miwa N., Nishiwaki T., Kawasoe T., Ishiguro H., Fujita M., Tokino T.et al. AXIN1 mutations in hepatocellular carcinomas, and growth suppression in cancer cells by virus-mediated transfer of AXIN1. Nat. Genet. 24:2000;245-250.
40. Seoane J., Pouponnot C., Staller P., Schader M., Eilers M., Massague J. TGFbeta influences Myc, Miz-1 and Smad to control the CDK inhibitor p15INK4b. Nat. Cell Biol. 3:2001;400-408.
41. Sherr C.J., Roberts J.M. CDK inhibitors. positive and negative regulators of G1-phase progression Genes Dev. 13:1999;1501-1512.
42. Shtutman M., Zhurinsky J., Simcha I., Albanese C., D'Amico M., Pestell R., Ben Ze'ev A. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. USA. 96:1999;5522-5527.
43. Staller P., Peukert K., Kiermaier A., Seoane J., Lukas J., Karsunky H., Moroy T., Bartek J., Massague J., Hanel F., Eilers M. Repression of p15INK4b expression by Myc through association with Miz-1. Nat. Cell Biol. 3:2001;392-399.
44. Tetsu O., McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 398:1999;422-426.
45. van de Wetering M., Cavallo R., Dooijes D., van Beest M., van Es J., Loureiro J., Ypma A., Hursh D., Jones T., Bejsovec A.et al. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell. 88:1997;789-799.
46. van Noort M., Meeldijk J., van der Zee R., Destree O., Clevers H. Wnt signaling controls the phosphorylation status of beta-catenin. J. Biol. Chem. 277:2002;17901-17905.
47. Wielenga V.J., Smits R., Korinek V., Smit L., Kielman M., Fodde R., Clevers H., Pals S.T. Expression of CD44 in Apc and Tcf mutant mice implies regulation by the WNT pathway. Am. J. Pathol. 154:1999;515-523.
48. Yang W., Velcich A., Mariadason J., Nicholas C., Corner G., Houston M., Edelmann W., Kucherlapati R., Holt P.R., Augenlicht L.H. p21(WAF1/cip1) is an important determinant of intestinal cell response to sulindac in vitro and in vivo. Cancer Res. 61:2001;6297-6302. a.
49. Yang W.C., Mathew J., Velcich A., Edelmann W., Kucherlapati R., Lipkin M., Yang K., Augenlicht L.H. Targeted inactivation of the p21(WAF1/cip1) gene enhances Apc-initiated tumor formation and the tumor-promoting activity of a Western-style high-risk diet by altering cell maturation in the intestinal mucosal. Cancer Res. 61:2001;565-569. b.
50. Zhang P., Wong C., Liu D., Finegold M., Harper J.W., Elledge S.J. P21(CIP1) and p57(KIP2) control muscle differentiation at the myogenion step. Genes Dev. 13:1999;213-224.
51. Zhu L., Skoultchi A.I. Coordinating cell proliferation and differentiation. Curr. Opin. Genet. Dev. 11:2001;91-97.