Site-dependent E-cadherin cleavage and nuclear translocation in a metastatic colorectal cancer model

American Journal of Pathology

Volumn 177, Issue 4, 2010, Pages 2067-2079

  Céspedes, María Virtudes ^a   Larriba, María Jesús ^c   Pavón, Miguel Angel ^a   Álamo, Patricia ^a   Casanova, Isolda ^a   Parreño, Matilde ^a   Feliu, Anna ^b   Sancho, Francesc Josep ^b   Muñoz, Alberto ^c   Mangues, Ramón ^a  

^a BIOMATERIALES Y NANOMEDICINA CIBER BBN   (Spain)

^b HOSPITAL DE LA SANTA CREU I SANT PAU   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; PRESENILIN 1; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER MODEL; COLORECTAL CANCER; CONTROLLED STUDY; HUMAN; HUMAN CELL; LYMPH NODE METASTASIS; METASTASIS; MOUSE; NONHUMAN; PERITONEUM METASTASIS; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SIGNET RING CARCINOMA; SURVIVAL; TUMOR GROWTH;

EID: 77957351492     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.100079     Document Type: Article

References (48)

1. DeVita VT Jr, Lawrence TS, Rosenberg SA: Cancer: Principles & Practice of Oncology. Eighth edition. Philadelphia, PA, Lippincott Williams & Wilkins, 2008, pp 1144-1197
2. Guyot F, Faivre J, Manfredi S, Meny B, Bonithon-Kopp C, Bouvier AM: Time trends in the treatment and survival of recurrences from colorectal cancer. Ann Oncol 2005, 16:756-761
3. Nelson WJ, Nusse R: Convergence of Wnt, beta-catenin, and cadherin pathways. Science 2004, 303:1483-1487
4. Perl AK, Wilgenbus P, Dahl U Semb H, Christofori G: A causal role for E-cadherin in the transition from adenoma to carcinoma. Nature 1998, 392:190-193
5. Becker KF, Atkinson MJ, Reich U, Becker I, Nekarda H, Siewert JR, Höfler H: E-cadherin gene mutations provide clues to diffuse type gastric carcinomas. Cancer Res 1994, 54:3845-3852
6. Bringuier PP, Umbas R, Schaafsma HE, Schaafsma HE, Karthaus HF, Debruyne FM, Schalken JA: Decreased E-cadherin immunoreactivity correlates with poor survival in patients with bladder tumors. Cancer Res 1993, 53:3241-3245
7. Dorudi S, Sheffield JP, Poulsom R, Northover JM, Hart IR: E-cadherin expression in colorectal cancer. An immunocytochemical and in situ hybridization study. Am J Pathol 1993, 142:981-986
8. Elzagheid A, Algars A, Bendardaf R, Lamlum H, Ristamaki R, Collan Y, Syrjanen K, Pyrhonen S: E-cadherin expression pattern in primary colorectal carcinomas and their metastases reflects disease outcome. World J Gastroenterol 2006, 12:4304-4309
9. Batistatou A, Charalabopoulos AK, Scopa CD, Nakanishi Y, Kappas A, Hirohashi S, Agnantis NJ, Charalabopoulos K: Expression patterns of dysadherin and E-cadherin in lymph node metastases of colorectal carcinoma. Virchows Arch 2006, 448:763-767
10. Ikeguchi M, Makino M, Kaibara N: Clinical significance of E-cadherin-catenin complex expression in metastatic foci of colorectal carcinoma. J Surg Oncol 2001, 77:201-207
11. Cano A, Pérez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA: The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2000, 2:76-83
12. Vega S, Morales AV, Ocaña OH, Valdés F, Fabregat I, Nieto MA: Snail blocks the cell cycle and confers resistance to cell death. Genes Dev 2004, 18:1131-1143
13. Blanco MJ, Moreno-Bueno G, Sarrió D, Locascio A, Cano A, Palacios J, Nieto MA: Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 2002, 21:3241-3246
14. Elloul S, Elstrand MB, Nesland JM, Tropé CG, Kvalheim G, Goldberg I, Reich R, Davidson B: Snail. Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma Cancer 2005, 103:1631-1643
15. Peinado H, Olmeda D, Cano A: Snail. Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Rev Cancer 2007, 7:415-428
16. Peña C, García JM, Silva J, García V, Rodríguez R, Alonso I, Millán I, Salas C, García de Herreros A, Muñoz A, Bonilla F: E-cadherin and vitamin D receptor regulation by SNAIL and ZEB1 in colon cancer: clinicopathological correlations. Hum Mol Genet 2005, 14:3361-3370
17. Roy HK, Smyrk TC, Koetsier J, Victor TA, Wali RK: The transcriptional repressor SNAIL is overexpressed in human colon cancer. Dig Dis Sci 2005, 50:42-46
18. Francí C, Gallén M, Alameda F, Baró T, Iglesias M, Virtanen I, García de Herreros A: Snail1 protein in the stroma as a new putative prognosis marker for colon tumours. PLoS One 2009, 4:e5595
19. Céspedes MV, Espina C, García-Cabezas MA, Trias M, Boluda A, Gómez del Pulgar MT, Sancho FJ, Nistal M, Lacal JC, Mangues R: Orthotopic microinjection of human colon cancer cells in nude mice induces tumor foci in all clinically relevant metastatic sites. Am J Pathol 2007, 170:1077-1085
20. Espina C, Céspedes MV, García-Cabezas MA, del Pulgar MT, Boluda A, Oroz LG, Cejas P, Nistal M, Mangues R, Lacal JC: A critical role for Rac1 in tumor progression of human colorectal adenocarcinoma cells. Am J Pathol 2008, 172:156-166
21. Pálmer HG, González-Sancho JM, Espada J, Berciano MT, Puig I, Baulida J, Quintanilla M, Cano A, García de Herreros A, Lafarga M, Muñoz A: Vitamin D3 promotes the differentiation of colon carcinoma cells by the induction of E-cadherin and the inhibition of beta-catenin signaling. J Cell Biol 2001, 154:369-387
22. Pálmer HG, Larriba MJ, García JM, Ordóñez- Morán P, Peña C, Peiró S, Puig I, Rodríguez R, de la Fuente R, Bernad A, Pollán M, Bonilla F, Gamallo C, García de Herreros A, Muñoz A: The transcription factor SNAIL represses vitamin D receptor expression and responsiveness in human colon cancer. Nat Med 2004, 10:917-919
23. Gottardi CJ, Wong E, Gumbiner BM: E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J Cell Biol 2001, 153:1049-1060
24. Raurell I, Codina M, Casagolda D, Del Valle B, Baulida J, García de Herreros A, Duñach M: Gamma-secretase-dependent and -independent effects of presenillin1 on beta-catenin.Tcf-4 transcrriptional activity. PLoS One 2008, e4080, 3:1-12
25. Aguilera O, Peña C, García JM, Larriba MJ, Ordóñez-Morán P, Navarro D, Barbáchano A, López de Silanes I, Ballestar E, Fraga MF, Esteller M, Gamallo C, Bonilla F, González-Sancho JM, Muñoz A: The Wnt antagonist DICKKOPF-1 gene is induced by 1alpha,25-dihydroxyvitamin D3 associated to the differentiation of human colon cancer cells. Carcinogenesis 2007, 28:1877-1884
26. Cespedes MV, Sancho FJ, Guerrero S, Parreno M, Casanova I, Pavon MA, Marcuello E, Trias M, Cascante M, Capella G, Mangues R: K-ras Asp12 mutant neither interacts with Raf, nor signals through Erk and is less tumorigenic than K-ras Val12. Carcinogenesis 2006, 27:2190-2200
27. Pavón MA, Parreño M, León X, Sancho FJ, Céspedes MV, Casanova I, Lopez-Pousa A, Mangues MA, Quer M, Barnadas A, Mangues R: Ku70 predicts response and primary tumor recurrence after therapy in locally advanced head and neck cancer. Int J Cancer 2008, 123:1068-1079
28. Ferber EC, Kajita M, Wadlow A, Tobiansky L, Niessen C, Ariga H, Daniel J, Fujita Y: A role for the cleaved cytoplasmic domain of E-cadherin in the nucleus. J Biol Chem 2008, 283:12691-12700
29. Mariadason JM, Bordonaro M, Aslam F, Shi L, Kuraguchi M, Velcich A, Augenlicht LH: Down-regulation of beta-catenin TCF signaling is linked to colonic epithelial cell differentiation. Cancer Res 2001, 61:3465-3471
30. Imai T, Horiuchi A, Shiozawa T, Osada R, Kikuchi N, Ohira S, Oka K, Konishi I: Elevated expression of E-cadherin and alpha-, beta-, and gamma-catenins in metastatic lesions compared with primary epithelial ovarian carcinomas. Hum Pathol 2004, 35:1469-1476
31. Salahshor S, Naidoo R, Serra S, Shih W, Tsao MS, Chetty R, Woodgett JR: Frequent accumulation of nuclear E-cadherin and alterations in the Wnt signaling pathway in esophageal squamous cell carcinomas. Mod Pathol 2008, 21:271-281
32. Han AC, Soler AP, Tang CK, Knudsen KA, Salazar H: Nuclear localization of E-cadherin expression in Merkel cell carcinoma. Arch Pathol Lab Med 2000, 124:1147-1151
33. Chetty R, Serra S: 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 2008, 52:325-330
34. Natalwala A, Spychal R, Tselepis C: Epithelial-mesenchymal transition mediated tumourigenesis in the gastrointestianl tract. World J Gastroenterol 2008, 14:3792-3797
35. Orsulic S, Huber O, Aberle H, Arnold S, Kemler R: E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1-mediated transactivation. J Cell Sci 1999, 112:1237-1245
36. Sadot E, Simcha I, Shtutman M, Ben-Ze'ev A, Geiger B: Inhibition of beta-catenin-mediated transactivation by cadherin derivatives. Proc Natl Acad Sci USA 1998, 95:15339-15344
37. Shitashige M, Satow R, Honda K, Ono M, Hirohashi S, Yamada T: Regulation of Wnt signaling by the nuclear pore complex. Gastroenterology 2008, 134:1961-1971
38. Corn PG, El-Deiry WS: Derangement of growth and differentiation control in oncogenesis. Bioessays 2002, 24:83-90
39. Marambaud P, Shioi J, Serban G, Georgakopoulos A, Sarner S, Nagy V, Baki L, Wen P, Efthimiopoulos S, Shao Z, Wisniewski T, Robakis NK: A presenilin-1/gamma-secretase cleavage releases the E-cadherin intracellular domain and regulates disassembly of adherens junctions. EMBO J 2002, 21:1948-1956
40. Brown MS, Ye J, Rawson RB, Goldstein JL: Regulated intramembrane proteolysis: a control mechanism conserved from bacteria to humans. Cell 2000, 100:391-398
41. Maetzel D, Denzel S, Mack B, Canis M, Went P, Benk M, Kieu C, Papior P, Baeuerle PA, Munz M, Gires O: Nuclear signalling by tumour-associated antigen EpCAM. Nat Cell Biol 2009, 11:162-171
42. Munz M, Baeuerle PA, Gires O: The emerging role of EpCAM in cancer and stem cell signaling. Cancer Res 2009, 69:5627-5629
43. Nuttall RK, Sampieri CL, Pennington CJ, Gill SE, Schultz GA, Edwards DR: Expression analysis of the entire MMP and TIMP gene families during mouse tissue development. FEBS Lett 2004, 563:129-134
44. Munshi HG, Stack MS: Reciprocal interactions between adhesion receptor signaling and MMP regulation. Cancer Metastasis Rev 2006, 25:45-56
45. Makino T, Tsujinaka T, Mishima H, Ikenaga M, Sawamura T, Nakamori S, Fujitani K, Hirao M, Kashiwazaki M, Masuda N, Takeda M, Mano M: Primary signet-ring cell carcinoma of the colon and rectum: report of eight cases and review of 154 Japanese cases. Hepatogastroenterology 2006, 53:845-849
46. Fu XY, Besterman JM, Monosov A, Hoffman RM: Models of human metastatic colon cancer in nude mice orthotopically constructed by using histologically intact patient specimens. Proc Natl Acad Sci USA 1991, 88:9345-9349
47. Jayne D: Molecular biology of peritoneal carcinomatosis. Cancer Treat Res 2007, 134:21-33
48. Bodenstine TM, Welch DR: Metastasis suppressors and the tumor microenvironment. Cancer Microenviron 2008, 1:1-11