E-cadherin can limit the transforming properties of activating β-catenin mutations

EMBO Journal

Volumn 34, Issue 18, 2015, Pages 2321-2333

  Huels, David J ^a   Ridgway, Rachel A ^a   Radulescu, Sorina ^a   Leushacke, Marc ^b   Campbell, Andrew D ^a   Biswas, Sujata ^c,d   Leedham, Simon ^c,d   Serra, Stefano ^e   Chetty, Runjan ^e   Moreaux, Guenievre ^a   Parry, Lee ^f   Matthews, James ^f   Song, Fei ^g   Hedley, Ann ^a   Kalna, Gabriela ^a   Ceteci, Fatih ^a   Reed, Karen R ^f   Meniel, Valerie S ^f   Maguire, Aoife ^h   Doyle, Brendan ^a,h   Söderberg, Ola ⁱ   Barker, Nick ^b   Watson, Alastair ^j   Larue, Lionel ^k   Clarke, Alan R ^f   Sansom, Owen J ^a   more..

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^e UNIVERSITY HEALTH NETWORK   (Canada)

^f CARDIFF UNIVERSITY   (United Kingdom)

^g JUSTUS LIEBIG UNIVERSITY   (Germany)

^h ST JAMES S HOSPITAL   (Ireland)

ⁱ UPPSALA UNIVERSITY   (Sweden)

^j UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^k Centre National de la Recherche Scientifique   (France)

more..

Author keywords

APC; colorectal cancer; E cadherin; catenin

Indexed keywords

WNT PROTEIN; BETA CATENIN; CADHERIN; CTNNB1 PROTEIN, MOUSE; TUMOR PROTEIN;

ADENOMATOUS POLYPOSIS COLI GENE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BETA CATENIN GENE; CONTROLLED STUDY; CRYPT CELL; CRYPT PROGENITOR CELL; E CADHERIN GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE LOSS; GENE MUTATION; GENETIC TRANSFORMATION; GLYCOGEN SYNTHASE KINASE 3 GENE; HUMAN; HUMAN TISSUE; IN VIVO STUDY; INTESTINAL STEM CELL; MOUSE; MUTATOR GENE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SMALL INTESTINE; WNT SIGNALING PATHWAY; ANIMAL; CELL TRANSFORMATION; COLON TUMOR; GENETICS; METABOLISM; MUTATION; PATHOLOGY; TRANSGENIC MOUSE;

ANIMALS; BETA CATENIN; CADHERINS; CELL TRANSFORMATION, NEOPLASTIC; COLONIC NEOPLASMS; MICE; MICE, TRANSGENIC; MUTATION; NEOPLASM PROTEINS; WNT SIGNALING PATHWAY;

EID: 84941745091     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201591739     Document Type: Article

References (40)

1. Ahn SM, Jang SJ, Shim JH, Kim D, Hong SM, Sung CO, Baek D, Haq F, Ansari AA, Lee SY, Chun SM, Choi S, Choi HJ, Kim J, Kim S, Hwang S, Lee YJ, Lee JE, Jung WR, Jang HY, et al., (2014) Genomic portrait of resectable hepatocellular carcinomas: implications of RB1 and FGF19 aberrations for patient stratification. Hepatology 60: 1972-1982
2. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M, Danenberg E, Clarke AR, Sansom OJ, Clevers H, (2009) Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 457: 608-611
3. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M, Haegebarth A, Korving J, Begthel H, Peters PJ, Clevers H, (2007) Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449: 1003-1007
4. Benhamouche S, Decaens T, Godard C, Chambrey R, Rickman DS, Moinard C, Vasseur-Cognet M, Kuo CJ, Kahn A, Perret C, Colnot S, (2006) Apc tumor suppressor gene is the "zonation-keeper" of mouse liver. Dev Cell 10: 759-770
5. Boussadia O, Kutsch S, Hierholzer A, Delmas V, Kemler R, (2002) E-cadherin is a survival factor for the lactating mouse mammary gland. Mech Dev 115: 53-62
6. Buchert M, Athineos D, Abud HE, Burke ZD, Faux MC, Samuel MS, Jarnicki AG, Winbanks CE, Newton IP, Meniel VS, Suzuki H, Stacker SA, Nathke IS, Tosh D, Huelsken J, Clarke AR, Heath JK, Sansom OJ, Ernst M, (2010) Genetic dissection of differential signaling threshold requirements for the Wnt/beta-catenin pathway in vivo. PLoS Genet 6: e1000816
7. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, Antipin Y, Reva B, Goldberg AP, Sander C, Schultz N, (2012) The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2: 401-404
8. Chetty R, Serra S, (2008) Membrane loss and aberrant nuclear localization of E-cadherin are consistent features of solid pseudopapillary tumour of the pancreas. An immunohistochemical study using two antibodies recognizing different domains of the E-cadherin molecule. Histopathology 52: 325-330
9. Clevers H, (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480
10. Cui J, Zhou X, Liu Y, Tang Z, Romeih M, (2003) Wnt signaling in hepatocellular carcinoma: analysis of mutation and expression of beta-catenin, T-cell factor-4 and glycogen synthase kinase 3-beta genes. J Gastroenterol Hepatol 18: 280-287
11. Doble BW, Patel S, Wood GA, Kockeritz LK, Woodgett JR, (2007) Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines. Dev Cell 12: 957-971
12. Edamoto Y, Hara A, Biernat W, Terracciano L, Cathomas G, Riehle HM, Matsuda M, Fujii H, Scoazec JY, Ohgaki H, (2003) Alterations of RB1, p53 and Wnt pathways in hepatocellular carcinomas associated with hepatitis C, hepatitis B and alcoholic liver cirrhosis. Int J Cancer 106: 334-341
13. Fischer JM, Miller AJ, Shibata D, Liskay RM, (2012) Different phenotypic consequences of simultaneous versus stepwise Apc loss. Oncogene 31: 2028-2038
14. Fodde R, Brabletz T, (2007) Wnt/beta-catenin signaling in cancer stemness and malignant behavior. Curr Opin Cell Biol 19: 150-158
15. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B, Sumer SO, Sun Y, Jacobsen A, Sinha R, Larsson E, Cerami E, Sander C, Schultz N, (2013) Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 6: pl1
16. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, Oshima M, Taketo MM, (1999) Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 18: 5931-5942
17. Hinoi T, Akyol A, Theisen BK, Ferguson DO, Greenson JK, Williams BO, Cho KR, Fearon ER, (2007) Mouse model of colonic adenoma-carcinoma progression based on somatic Apc inactivation. Cancer Res 67: 9721-9730
18. Ireland H, Kemp R, Houghton C, Howard L, Clarke AR, Sansom OJ, Winton DJ, (2004) Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: effect of loss of beta-catenin. Gastroenterology 126: 1236-1246
19. Kemp R, Ireland H, Clayton E, Houghton C, Howard L, Winton DJ, (2004) Elimination of background recombination: somatic induction of Cre by combined transcriptional regulation and hormone binding affinity. Nucleic Acids Res 32: e92
20. Kinzler KW, Vogelstein B, (1996) Lessons from hereditary colorectal cancer. Cell 87: 159-170
21. Korinek V, Barker N, Moerer P, van Donselaar E, Huls G, Peters PJ, Clevers H, (1998) Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat Genet 19: 379-383
22. Larue L, Ohsugi M, Hirchenhain J, Kemler R, (1994) E-cadherin null mutant embryos fail to form a trophectoderm epithelium. Proc Natl Acad Sci USA 91: 8263-8267
23. Leedham SJ, Rodenas-Cuadrado P, Howarth K, Lewis A, Mallappa S, Segditsas S, Davis H, Jeffery R, Rodriguez-Justo M, Keshav S, Travis SP, Graham TA, East J, Clark S, Tomlinson IP, (2013) A basal gradient of Wnt and stem-cell number influences regional tumour distribution in human and mouse intestinal tracts. Gut 62: 83-93
24. el Marjou F, Janssen KP, Chang BH, Li M, Hindie V, Chan L, Louvard D, Chambon P, Metzger D, Robine S, (2004) Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 39: 186-193
25. Myant KB, Cammareri P, McGhee EJ, Ridgway RA, Huels DJ, Cordero JB, Schwitalla S, Kalna G, Ogg EL, Athineos D, Timpson P, Vidal M, Murray GI, Greten FR, Anderson KI, Sansom OJ, (2013) ROS production and NF-kappaB activation triggered by RAC1 facilitate WNT-driven intestinal stem cell proliferation and colorectal cancer initiation. Cell Stem Cell 12: 761-773
26. Nathke IS, (2004) The adenomatous polyposis coli protein: the Achilles heel of the gut epithelium. Annu Rev Cell Dev Biol 20: 337-366
27. Patel S, Doble BW, MacAulay K, Sinclair EM, Drucker DJ, Woodgett JR, (2008) Tissue-specific role of glycogen synthase kinase 3beta in glucose homeostasis and insulin action. Mol Cell Biol 28: 6314-6328
28. Phelps RA, Chidester S, Dehghanizadeh S, Phelps J, Sandoval IT, Rai K, Broadbent T, Sarkar S, Burt RW, Jones DA, (2009) A two-step model for colon adenoma initiation and progression caused by APC loss. Cell 137: 623-634
29. Radulescu S, Ridgway RA, Appleton P, Kroboth K, Patel S, Woodgett J, Taylor S, Nathke IS, Sansom OJ, (2010) Defining the role of APC in the mitotic spindle checkpoint in vivo: APC-deficient cells are resistant to Taxol. Oncogene 29: 6418-6427
30. Riethmacher D, Brinkmann V, Birchmeier C, (1995) A targeted mutation in the mouse E-cadherin gene results in defective preimplantation development. Proc Natl Acad Sci USA 92: 855-859
31. Sansom OJ, Meniel VS, Muncan V, Phesse TJ, Wilkins JA, Reed KR, Vass JK, Athineos D, Clevers H, Clarke AR, (2007) Myc deletion rescues Apc deficiency in the small intestine. Nature 446: 676-679
32. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP, Batlle E, Simon-Assmann P, Clevers H, Nathke IS, Clarke AR, Winton DJ, (2004) Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 18: 1385-1390
33. Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, van Es JH, Abo A, Kujala P, Peters PJ, Clevers H, (2009) Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature 459: 262-265
34. Serra S, Salahshor S, Fagih M, Niakosari F, Radhi JM, Chetty R, (2007) Nuclear expression of E-cadherin in solid pseudopapillary tumors of the pancreas. JOP 8: 296-303
35. Shibata H, Toyama K, Shioya H, Ito M, Hirota M, Hasegawa S, Matsumoto H, Takano H, Akiyama T, Toyoshima K, Kanamaru R, Kanegae Y, Saito I, Nakamura Y, Shiba K, Noda T, (1997) Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 278: 120-123
36. Smits R, Ruiz P, Diaz-Cano S, Luz A, Jagmohan-Changur S, Breukel C, Birchmeier C, Birchmeier W, Fodde R, (2000) E-cadherin and adenomatous polyposis coli mutations are synergistic in intestinal tumor initiation in mice. Gastroenterology 119: 1045-1053
37. Sparks AB, Morin PJ, Vogelstein B, Kinzler KW, (1998) Mutational analysis of the APC/beta-catenin/Tcf pathway in colorectal cancer. Cancer Res 58: 1130-1134
38. TCGA (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487: 330-337
39. Tomasetti C, Vogelstein B, (2015) Cancer etiology. Variation in cancer risk among tissues can be explained by the number of stem cell divisions. Science 347: 78-81
40. Vermeulen L, Morrissey E, van der Heijden M, Nicholson AM, Sottoriva A, Buczacki S, Kemp R, Tavare S, Winton DJ, (2013) Defining stem cell dynamics in models of intestinal tumor initiation. Science 342: 995-998