Acute WNT signalling activation perturbs differentiation within the adult stomach and rapidly leads to tumour formation

Oncogene

Volumn 32, Issue 16, 2013, Pages 2048-2057

  Radulescu, S ^a   Ridgway, R A ^a   Cordero, J ^a   Athineos, D ^a   Salgueiro, P ^a,b   Poulsom, R ^c   Neumann, J ^d   Jung, A ^d   Patel, S ^e   Woodgett, J ^e   Barker, N ^b   Pritchard, D M ^f   Oien, K ^g   Sansom, O J ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b INSTITUTE OF MEDICAL BIOLOGY   (Singapore)

^c Histopathology Laboratory and ISH Service   (United Kingdom)

^d UNIVERSITY OF MUNICH   (Germany)

^e MOUNT SINAI HOSPITAL   (Canada)

^f UNIVERSITY OF LIVERPOOL   (United Kingdom)

^g UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

catenin; APC; gastric cancer; GSK3

Indexed keywords

APC PROTEIN; BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3; PROTON PUMP; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER GENETICS; CANCER PROGNOSIS; CELL DIFFERENTIATION; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE LOCUS; GENE MUTATION; HOMEOSTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STOMACH CARCINOGENESIS; STOMACH GLAND POLYP; STOMACH POLYP;

ADENOMATOUS POLYPOSIS COLI; ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION; STOMACH NEOPLASMS; TRANSGENES; WNT PROTEINS;

MURINAE;

EID: 84876688065     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.224     Document Type: Article

References (75)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005; 55: 74-108.
2. Gatta G, Ciccolallo L, Kunkler I, Capocaccia R, Berrino F, Coleman MP et al. Survival from rare cancer in adults: a population-based study. Lancet Oncol 2006; 7: 132-140.
3. Smith MG, Hold GL, Tahara E, El-Omar EM. Cellular and molecular aspects of gastric cancer. World J Gastroenterol 2006; 12: 2979-2990.
4. Correa P, Shiao YH. Phenotypic and genotypic events in gastric carcinogenesis. Cancer Res 1994; 54: 1941s-1943s.
5. Lauren P. The Two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand 1965; 64: 31-49.
6. Milne AN, Carneiro F, O'Morain C, Offerhaus GJ. Nature meets nurture: molecular genetics of gastric cancer. Hum Genet 2009; 126: 615-628.
7. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M et al. Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 2001; 345: 784-789.
8. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process-First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 1992; 52: 6735-6740.
9. de Vries AC, van Grieken NC, Looman CW, Casparie MK, de Vries E, Meijer GA et al. Gastric cancer risk in patients with premalignant gastric lesions: a nationwide cohort study in the Netherlands. Gastroenterology 2008; 134: 945-952.
10. Parsonnet J, Friedman GD, Orentreich N, Vogelman H. Risk for gastric cancer in people with CagA positive or CagA negative Helicobacter pylori infection. Gut 1997; 40: 297-301.
11. Becker KF, Hofler H. Frequent somatic allelic inactivation of the E-cadherin gene in gastric carcinomas. J Natl Cancer Inst 1995; 87: 1082-1084.
12. Oda T, Kanai Y, Oyama T, Yoshiura K, Shimoyama Y, Birchmeier W et al. E-cadherin gene mutations in human gastric carcinoma cell lines. Proc Natl Acad Sci USA 1994; 91: 1858-1862.
13. Guilford PJ, Hopkins JB, Grady WM, Markowitz SD, Willis J, Lynch H et al. E-cadherin germline mutations define an inherited cancer syndrome dominated by diffuse gastric cancer. Hum Mutat 1999; 14: 249-255.
14. Chan EF, Gat U, McNiff JM, Fuchs E. A common human skin tumour is caused by activating mutations in beta-catenin. Nat Genet 1999; 21: 410-413.
15. Tycko B, Li CM, Buttyan R. The Wnt/beta-catenin pathway in Wilms tumors and prostate cancers. Curr Mol Med 2007; 7: 479-489.
16. Guillen-Ahlers H. Wnt signaling in renal cancer. Curr Drug Targets 2008; 9: 591-600.
17. Cavard C, Colnot S, Audard V, Benhamouche S, Finzi L, Torre C et al. Wnt/beta-catenin pathway in hepatocellular carcinoma pathogenesis and liver physiology. Future Oncol 2008; 4: 647-660.
18. Segditsas S, Tomlinson I. Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene 2006; 25: 7531-7537.
19. Miyoshi Y, Nagase H, Ando H, Horii A, Ichii S, Nakatsuru S et al. Somatic mutations of the APC gene in colorectal tumors: mutation cluster region in the APC gene. Hum Mol Genet 1992; 1: 229-233.
20. Nagase H, Miyoshi Y, Horii A, Aoki T, Petersen GM, Vogelstein B et al. Screening for germ-line mutations in familial adenomatous polyposis patients: 61 new patients and a summary of 150 unrelated patients. Hum Mutat 1992; 1: 467-473.
21. Kinzler KW, Nilbert MC, Su LK, Vogelstein B, Bryan TM, Levy DB et al. Identification of FAP locus genes from chromosome 5q21. Science 1991; 253: 661-665.
22. Half E, Bercovich D, Rozen P. Familial adenomatous polyposis. Orphanet J Rare Dis 2009; 4: 22.
23. Iida M, Yao T, Itoh H, Watanabe H, Kohrogi N, Shigematsu A et al. Natural history of fundic gland polyposis in patients with familial adenomatosis coli/Gardner's syndrome. Gastroenterology 1985; 89: 1021-1025.
24. Barker N. The canonical Wnt/beta-catenin signalling pathway. Methods Mol Biol 2008; 468: 5-15.
25. Shitashige M, Hirohashi S, Yamada T. Wnt signaling inside the nucleus. Cancer Sci 2008; 99: 631-637.
26. Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999; 398: 422-426.
27. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT et al. Identification of c-MYC as a target of the APC pathway. Science 1998; 281: 1509-1512.
28. Blache P, van de Wetering M, Duluc I, Domon C, Berta P, Freund JN et al. SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes. J Cell Biol 2004; 166: 37-47.
29. Barker N, Ridgway RA, van Es JH, van de Wetering M, Begthel H, van den Born M et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009; 457: 608-611.
30. Watanabe H, Enjoji M, Yao T, Ohsato K. Gastric lesions in familial adenomatosis coli: their incidence and histologic analysis. Hum Pathol 1978; 9: 269-283.
31. Bianchi LK, Burke CA, Bennett AE, Lopez R, Hasson H, Church JM. Fundic gland polyp dysplasia is common in familial adenomatous polyposis. Clin Gastroenterol Hepatol 2008; 6: 180-185.
32. Garrean S, Hering J, Saied A, Jani J, Espat NJ. Gastric adenocarcinoma arising from fundic gland polyps in a patient with familial adenomatous polyposis syndrome. Am Surg 2008; 74: 79-83.
33. Abraham SC, Nobukawa B, Giardiello FM, Hamilton SR, Wu TT. Fundic gland polyps in familial adenomatous polyposis: neoplasms with frequent somatic adenomatous polyposis coli gene alterations. Am J Pathol 2000; 157: 747-754.
34. Torbenson M, Lee JH, Cruz-Correa M, Ravich W, Rastgar K, Abraham SC et al. Sporadic fundic gland polyposis: a clinical, histological, and molecular analysis. Mod Pathol 2002; 15: 718-723.
35. Sekine S, Shibata T, Yamauchi Y, Nakanishi Y, Shimoda T, Sakamoto M et al. Beta-catenin mutations in sporadic fundic gland polyps. Virchows Arch 2002; 440: 381-386.
36. Abraham SC, Nobukawa B, Giardiello FM, Hamilton SR, Wu TT. Sporadic fundic gland polyps: common gastric polyps arising through activating mutations in the beta-catenin gene. Am J Pathol 2001; 158: 1005-1010.
37. Crabtree M, Sieber OM, Lipton L, Hodgson SV, Lamlum H, Thomas HJ et al. Refining the relation between 'first hits' and 'second hits' at the APC locus: the 'loose fit' model and evidence for differences in somatic mutation spectra among patients. Oncogene 2003; 22: 4257-4265.
38. Kim B, Byun SJ, Kim YA, Kim JE, Lee BL, Kim WH et al. Cell cycle regulators, APC/beta-catenin, NF-kappaB and Epstein-Barr virus in gastric carcinomas. Pathology 2010; 42: 58-65.
39. Tahara E. Molecular biology of gastric cancer. World J Surg 1995; 19: 484-488; discussion 489-90.
40. Horii A, Nakatsuru S, Miyoshi Y, Ichii S, Nagase H, Kato Y et al. The APC gene, responsible for familial adenomatous polyposis, is mutated in human gastric cancer. Cancer Res 1992; 52: 3231-3233.
41. Nakatsuru S, Yanagisawa A, Furukawa Y, Ichii S, Kato Y, Nakamura Y et al. Somatic mutations of the APC gene in precancerous lesion of the stomach. Hum Mol Genet 1993; 2: 1463-1465.
42. Clements WM, Wang J, Sarnaik A, Kim OJ, MacDonald J, Fenoglio-Preiser C et al. beta-Catenin mutation is a frequent cause of Wnt pathway activation in gastric cancer. Cancer Res 2002; 62: 3503-3506.
43. Park WS, Oh RR, Park JY, Lee SH, Shin MS, Kim YS et al. Frequent somatic mutations of the beta-catenin gene in intestinal-type gastric cancer. Cancer Res 1999; 59: 4257-4260.
44. Ebert MP, Fei G, Kahmann S, Muller O, Yu J, Sung JJ et al. Increased beta-catenin mRNA levels and mutational alterations of the APC and beta-catenin gene are present in intestinal-type gastric cancer. Carcinogenesis 2002; 23: 87-91.
45. Miyazawa K, Iwaya K, Kuroda M, Harada M, Serizawa H, Koyanagi Y et al. Nuclear accumulation of beta-catenin in intestinal-type gastric carcinoma: correlation with early tumor invasion. Virchows Arch 2000; 437: 508-513.
46. Kemp R, Ireland H, Clayton E, Houghton C, Howard L, Winton DJ. Elimination of background recombination: somatic induction of Cre by combined transcriptional regulation and hormone binding affinity. Nucleic Acids Res 2004; 32: e92.
47. Novak A, Guo C, Yang W, Nagy A, Lobe CG. Z/EG, a double reporter mouse line that expresses enhanced green fluorescent protein upon Cre-mediated excision. Genesis 2000; 28: 147-155.
48. Harada N, Tamai Y, Ishikawa T, Sauer B, Takaku K, Oshima M et al. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J 1999; 18: 5931-5942.
49. Sansom OJ, Reed KR, Hayes AJ, Ireland H, Brinkmann H, Newton IP et al. Loss of Apc in vivo immediately perturbs Wnt signaling, differentiation, and migration. Genes Dev 2004; 18: 1385-1390.
50. Forte JG, Forte TM, Black JA, Okamoto C, Wolosin JM. Correlation of parietal cell structure and function. J Clin Gastroenterol 1983; 5: 17-27.
51. Park do Y, Lauwers GY. Gastric polyps: classification and management. Arch Pathol Lab Med 2008; 132: 633-640.
52. Freeman HJ. Proton pump inhibitors and an emerging epidemic of gastric fundic gland polyposis. World J Gastroenterol 2008; 14: 1318-1320.
53. Spicer Z, Miller ML, Andringa A, Riddle TM, Duffy JJ, Doetschman T et al. Stomachs of mice lacking the gastric H, K-ATPase alpha-subunit have achlorhydria, abnormal parietal cells, and ciliated metaplasia. J Biol Chem 2000; 275: 21555-21565.
54. Zhao Z, Hou N, Sun Y, Teng Y, Yang X. Atp4b promoter directs the expression of Cre recombinase in gastric parietal cells of transgenic mice. J Genet Genomics 2010; 37: 647-652.
55. Barker N, van Es JH, Kuipers J, Kujala P, van den Born M, Cozijnsen M et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007; 449: 1003-1007.
56. Barker N, Huch M, Kujala P, van de Wetering M, Snippert HJ, van Es JH et al. Lgr5(+ve) stem cells drive self-renewal in the stomach and build long-lived gastric units in vitro. Cell Stem Cell 2010; 6: 25-36.
57. Shibata H, Toyama K, Shioya H, Ito M, Hirota M, Hasegawa S et al. Rapid colorectal adenoma formation initiated by conditional targeting of the Apc gene. Science 1997; 278: 120-123.
58. Franco AT, Israel DA, Washington MK, Krishna U, Fox JG, Rogers AB et al. Activation of beta-catenin by carcinogenic Helicobacter pylori. Proc Natl Acad Sci USA 2005; 102: 10646-10651.
59. Suzuki M, Mimuro H, Suzuki T, Park M, Yamamoto T, Sasakawa C. Interaction of CagA with Crk plays an important role in Helicobacter pylori-induced loss of gastric epithelial cell adhesion. J Exp Med 2005; 202: 1235-1247.
60. Sokolova O, Bozko PM, Naumann M. Helicobacter pylori suppresses glycogen synthase kinase 3beta to promote beta-catenin activity. J Biol Chem 2008; 283: 29367-29374.
61. Murata-Kamiya N, Kurashima Y, Teishikata Y, Yamahashi Y, Saito Y, Higashi H et al. Helicobacter pylori CagA interacts with E-cadherin and deregulates the beta-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells. Oncogene 2007; 26: 4617-4626.
62. Nakayama M, Hisatsune J, Yamasaki E, Isomoto H, Kurazono H, Hatakeyama M et al. Helicobacter pylori VacA-induced inhibition of GSK3 through the PI3K/Akt signaling pathway. J Biol Chem 2009; 284: 1612-1619.
63. Ng SS, Mahmoudi T, Danenberg E, Bejaoui I, de Lau W, Korswagen HC et al. Phosphatidylinositol 3-kinase signaling does not activate the wnt cascade. J Biol Chem 2009; 284: 35308-35313.
64. He XC, Yin T, Grindley JC, Tian Q, Sato T, Tao WA et al. PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat Genet 2007; 39: 189-198.
65. Gnad T, Feoktistova M, Leverkus M, Lendeckel U, Naumann M. Helicobacter pylori-induced activation of beta-catenin involves low density lipoprotein receptor-related protein 6 and Dishevelled. Mol Cancer 2010; 9: 31.
66. Suzuki M, Mimuro H, Kiga K, Fukumatsu M, Ishijima N, Morikawa H et al. Helicobacter pylori CagA phosphorylation-independent function in epithelial proliferation and inflammation. Cell Host Microbe 2009; 5: 23-34.
67. Zheng HC, Xu XY, Xia P, Yu M, Takahashi H, Takano Y. Involvement of inactive GSK3beta overexpression in tumorigenesis and progression of gastric carcinomas. Hum Pathol 2010; 41: 1255-1264.
68. Zhang H, Xue Y. Wnt pathway is involved in advanced gastric carcinoma. Hepa-togastroenterology 2008; 55: 1126-1130.
69. Oshima H, Matsunaga A, Fujimura T, Tsukamoto T, Taketo MM, Oshima M. Carcinogenesis in mouse stomach by simultaneous activation of the Wnt signaling and prostaglandin E2 pathway. Gastroenterology 2006; 131: 1086-1095.
70. Patel S, Doble BW, MacAulay K, Sinclair EM, Drucker DJ, Woodgett JR. Tissue-specific role of glycogen synthase kinase 3beta in glucose homeostasis and insulin action. Mol Cell Biol 2008; 28: 6314-6328.
71. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat Genet 1999; 21: 70-71.
72. Luche H, Weber O, Nageswara Rao T, Blum C, Fehling HJ. Faithful activation of an extra-bright red fluorescent protein in 'knock-in' Cre-reporter mice ideally suited for lineage tracing studies. Eur J Immunol 2007; 37: 43-53.
73. Przemeck SM, Duckworth CA, Pritchard DM. Radiation-induced gastric epithelial apoptosis occurs in the proliferative zone and is regulated by p53, bak, bax, and bcl-2. Am J Physiol Gastrointest Liver Physiol 2007; 292: G620-G627.
74. Ireland H, Kemp R, Houghton C, Howard L, Clarke AR, Sansom OJ et al. Inducible Cre-mediated control of gene expression in the murine gastrointestinal tract: effect of loss of beta-catenin. Gastroenterology 2004; 126: 1236-1246.
75. Gregorieff A, Pinto D, Begthel H, Destree O, Kielman M, Clevers H. Expression pattern of Wnt signaling components in the adult intestine. Gastroenterology 2005; 129: 626-638.