Cooperativity of E-cadherin and Smad4 loss to promote diffuse-type gastric adenocarcinoma and metastasis

Molecular Cancer Research

Volumn 12, Issue 8, 2014, Pages 1088-1099

  Park, Jun Won ^a,b   Jang, Seok Hoon ^a   Park, Dong Min ^a   Lim, Na Jung ^a   Deng, Chuxia ^c   Kim, Dae Yong ^b   Green, Jeffrey E ^d   Kim, Hark Kyun ^a  

^a National Cancer Center   (South Korea)

^b Seoul National University   (South Korea)

^c National Institute of Diabetes and Digestive and Kidney Diseases   (South Korea)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CRE RECOMBINASE; PROTEIN P53; SMAD4 PROTEIN; TRANSCRIPTION FACTOR PDX 1; UVOMORULIN; VILLIN; CADHERIN; SMAD4 PROTEIN, MOUSE;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST ADENOCARCINOMA; BREAST CANCER; CANCER GROWTH; CELL CYCLE PROGRESSION; CELL MIGRATION; CONTROLLED STUDY; DISTANT METASTASIS; DOWN REGULATION; FEMALE; GENOTYPE; HETEROZYGOSITY; HUMAN; HUMAN TISSUE; INTESTINE CANCER; LUNG METASTASIS; METASTASIS; MOUSE; MOUSE MAMMARY TUMOR ONCOVIRUS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STOMACH ADENOCARCINOMA; WILD TYPE; ADENOCARCINOMA; ANIMAL; GENETICS; PATHOLOGY; STOMACH TUMOR;

ADENOCARCINOMA; ANIMALS; BETA CATENIN; CADHERINS; MICE; NEOPLASM METASTASIS; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; STOMACH NEOPLASMS;

EID: 84905975877     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-14-0192-T     Document Type: Article

References (41)

1. Alberts S, Cervantes A, van de Velde C. Gastric cancer: epidemiology, pathology, and treatment. Ann Oncol 2003;14:31-6.
2. Maesawa C, Tamura G, Suzuki Y, Ogasawara S, Sakata K, Kashiwaba M, et al. The sequential accumulation of genetic alterations characteristic of the colorectal adenoma-carcinoma sequence does not occur between gastric adenoma and adenocarcinoma. J Pathol 1995;176:249-58.
3. Schmierer B, Hill CS. TGF beta-SMAD signal transduction: molecular specificity and functional flexibility. Nat Rev Mol Cell Biol 2007;8:970-82. (Pubitemid 350174642)
4. Wang LH, Kim SH, Lee JH, Choi YL, Kim YC, Park TS, et al. Inactivation of SMAD4 tumor suppressor gene during gastric carcinoma progression. Clin Cancer Res 2007;13:102-10. (Pubitemid 46121858)
5. Becker KF, Atkinson MJ, Reich U, Becker I, Nekarda H, Siewert JR, et al. E-cadherin gene mutations provide clues to diffuse type gastric carcinomas. Cancer Res 1994;54:3845-52. (Pubitemid 24241205)
6. Machado JC, Oliveira C, Carvalho R, Soares P, Berx G, Caldas C, et al. E-cadherin gene (CDH1) promoter methylation as the second hit in sporadic diffuse gastric carcinoma. Oncogene 2001;20:1525-8. (Pubitemid 32291203)
7. Rosivatz E, Becker I, Specht K, Fricke E, Luber B, Busch R, et al. Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am J Pathol 2002;161:1881-91. (Pubitemid 35265545)
8. Sirard C, de la Pompa JL, Elia A, Itie A, Mirtsos C, Cheung A, et al. The tumor suppressor gene Smad4/Dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev 1998;12:107-19. (Pubitemid 28083662)
9. Xu X, Brodie SG, Yang X, Im YH, Parks WT, Chen L, et al. Haploid loss of the tumor suppressor Smad4/Dpc4 initiates gastric polyposis and cancer in mice. Oncogene 2000;19:1868-74. (Pubitemid 30219029)
10. Shimada S, Mimata A, Sekine M, Mogushi K, Akiyama Y, Fukamachi H, et al. Synergistic tumour suppressor activity of E-cadherin and p53 in a conditional mouse model for metastatic diffuse type gastric cancer. Gut 2012;61:344-53.
11. Hingorani SR, Petricoin EF, Maitra A, Rajapakse V, King C, Jacobetz MA, et al. Preinvasive and invasive ductal pancreatic cancer and its early detection in the mouse. Cancer Cell 2003;4:437-50. (Pubitemid 38050041)
12. Jonkers J, Meuwissen R, van der Gulden H, Peterse H, van der Valk M, Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditionalmousemodel for breast cancer. Nat Genet 2001;29:418-25. (Pubitemid 34326692)
13. Boussadia O, Kutsch S, Hierholzer A, Delmas V, Kemler R. E-cadherin is a survival factor for the lactating mouse mammary gland. Mech Dev 2002;115:53- 62.
14. Yang X, Li C, Herrera PL, Deng CX. Generation of Smad4/Dpc4 conditional knockout mice. Genesis 2002;32:80-1. (Pubitemid 34211702)
15. Larsson LI, Madsen OD, Serup P, Jonsson J, Edlund H. Pancreatic-duodenal homeobox 1-role in gastric endocrine patterning. Mech Dev 1996;60:175-84. (Pubitemid 27067071)
16. el Marjou F, Janssen KP, Chang BH, Li M, Hindie V, Chan L, et al. Tissue-specific and inducible Cre-mediated recombination in the gut epithelium. Genesis 2004;39:186-93. (Pubitemid 39079517)
17. Qiao XT, Ziel JW, McKimpson W, Madison BB, Todisco A, Merchant JL, et al. Prospective identification of a multi-lineage progenitor in murine stomach epithelium. Gastroenterology 2007;133:1989-98.
18. Andrechek ER, Hardy WR, Siegel PM, Rudnicki MA, Cardiff RD, Muller WJ. Amplification of the neu/erbB-2 oncogene in a mouse model of mammary tumorigenesis. Proc Natl Acad Sci U S A 2000;97:3444-9. (Pubitemid 30183322)
19. Leung KM, Elashoff RM, Afifi AA. Censoring issues in survival analysis. Annu Rev Public Health 1997;18:83-104. (Pubitemid 27194065)
20. Allard MA, Bachet JB, Beauchet A, Julie C, Malafosse R, Penna C, et al. Linear quantification of lymphoid infiltration of the tumor margin: a reproducible method, developed with colorectal cancer tissues, for assessing a highly variable prognostic factor. Diagn Pathol 2012;7:156.
21. Ho SB, Takamura K, Anway R, Shekels LL, Toribara NW, Ota H. The adherent gastric mucous layer is composed of alternating layers of MUC5AC and MUC6 mucin proteins. Dig Dis Sci 2004;49:1598-606. (Pubitemid 39335542)
22. Derksen PW, Liu X, Saridin F, van der Gulden H, Zevenhoven J, Evers B, et al. Somatic inactivation of E-cadherin and p53 in mice leads to metastatic lobular mammary carcinoma through induction of anoikis resistance and angiogenesis. Cancer Cell 2006;10:437-49. (Pubitemid 44693469)
23. Oliveira C, Bordin MC, Grehan N, Huntsman D, Suriano G, Machado JC, et al. Screening E-cadherin in gastric cancer families reveals germline mutations only in hereditary diffuse gastric cancer kindred. Hum Mutat 2002;19:510-7. (Pubitemid 34461624)
24. Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, et al. Variable β-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci U S A 2001;98:10356-61. (Pubitemid 32803024)
25. Shirai YT, Ehata S, Yashiro M, Yanagihara K, Hirakawa K, Miyazono K. Bone morphogenetic protein-2 and -4 play tumor suppressive roles in human diffuse-type gastric carcinoma. Am J Pathol 2011;179:2920-30.
26. Wen XZ, Miyake S, Akiyama Y, Yuasa Y. BMP-2 modulates the proliferation and differentiation of normal and cancerous gastric cells. Biochem Biophys Res Commun 2004;316:100-6. (Pubitemid 38299134)
27. Itoh K, Kataoka H, Sasaki M, Tanida S, Oshima T, Ogasawara N, et al. Bone morphogenetic protein 2 induced differentiation toward superficial epithelial cells in the gastric mucosa. J Gastroenterol 2006;41:1064-75. (Pubitemid 44896721)
28. Wang TC, Dangler CA, Chen D, Goldenring JR, Koh T, Raychowdhury R, et al. Synergistic interaction between hypergastrinemia and Helicobacter infection in a mouse model of gastric cancer. Gastroenterology 2000;118:36-47. (Pubitemid 30020371)
29. Lefebvre O, Chenard MP, Masson R, Linares J, Dierich A, LeMeur M, et al. Gastric mucosa abnormalities and tumorigenesis in mice lacking the pS2 trefoil protein. Science 1996;274:259-62. (Pubitemid 26353205)
30. Judd LM, Alderman BM, Howlett M, Shulkes A, Dow C, Moverley J, et al. Gastric cancer development in mice lacking the SHP2 binding site on the IL-6 family co-receptor gp130. Gastroenterology 2004;126:196-207. (Pubitemid 38040736)
31. Takaku K, Oshima M, Miyoshi H, Matsui M, Seldin MF, Taketo MM. Intestinal tumorigenesis in compound mutant mice of both Dpc4 (Smad4) and Apc genes. Cell 1998;92:645-56. (Pubitemid 28141513)
32. Humar B, Blair V, Charlton A, More H, Martin I, Guilford P. E-cadherin deficiency initiates gastric signet-ring cell carcinoma in mice and man. Cancer Res 2009;69:2050-6.
33. Pharoah PD, Guilford P, Caldas C. Incidence of gastric cancer and breast cancer in CDH1 (E-cadherin) mutation carriers from hereditary diffuse gastric cancer families. Gastroenterology 2001;121:1348-53. (Pubitemid 33140452)
34. 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;131:1086-95. (Pubitemid 44498691)
35. Gilles C, Polette M, Mestdagt M, Nawrocki-Raby B, Ruggeri P, Birembaut P, et al. Transactivation of vimentin by beta-catenin in human breast cancer cells. Cancer Res 2003;63:2658-64. (Pubitemid 36605210)
36. Brabletz T, Jung A, Dag S, Hlubek F, Kirchner T. beta-catenin regulates the expression of the matrix metalloproteinase-7 in human colorectal cancer. Am J Pathol 1999;155:1033-8. (Pubitemid 29488909)
37. Gradl D, Kühl M, Wedlich D. The Wnt/Wg signal transducer betacatenin controls fibronectin expression. Mol Cell Biol 1999;19:5576-87. (Pubitemid 29339915)
38. Mann B, Gelos M, Siedow A, Hanski ML, Gratchev A, Ilyas M, et al. Target genes of beta-catenin-T cell-factor/lymphoid-enhancer-factor signaling in human colorectal carcinomas. Proc Natl Acad Sci U S A 1999;96:1603-8. (Pubitemid 29098498)
39. Zhang B, Halder SK, Kashikar ND, Cho YJ, Datta A, Gorden DL, et al. Antimetastatic role of Smad4 signaling in colorectal cancer. Gastroenterology 2010;138:969-80.
40. Ding Z, Wu CJ, Chu GC, Xiao Y, Ho D, Zhang J, et al. SMAD4-dependent barrier constrains prostate cancer growth and metastatic progression. Nature 2011;470:269-73.
41. Freeman TJ, Smith JJ, Chen X, Washington MK, Roland JT, Means AL, et al. Smad4-mediated signaling inhibits intestinal neoplasia by inhibiting expression of β-catenin. Gastroenterology 2012;142:562-71.