Intestinal adenomagenesis involves core molecular signatures of the epithelial-mesenchymal transition

Journal of Molecular Histology

Volumn 39, Issue 3, 2008, Pages 283-294

  Chen, Xiaodi ^a   Halberg, Richard B ^a   Burch, Ryan P ^a   Dove, William F ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Apc Min; E cadherin; Epithelial mesenchymal transition; Intestinal adenoma; Vimentin

Indexed keywords

BIOLOGICAL MARKER; RAS PROTEIN; RNA; SMAD3 PROTEIN; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA; UVOMORULIN; VIMENTIN; WNT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER INVASION; CARCINOGENESIS; CELL PROLIFERATION; COLON ADENOCARCINOMA; COLON ADENOMA; COLON MUCOSA; CONTROLLED STUDY; EPITHELIUM; HUMAN; HUMAN TISSUE; INTESTINE; MAMMAL; MESENCHYME; MOLECULAR BIOLOGY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TUMOR CELL;

ADENOMA; ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; AZOXYMETHANE; CADHERINS; CELL PROLIFERATION; EPITHELIUM; FIBRONECTINS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; IMMUNOHISTOCHEMISTRY; INTESTINAL NEOPLASMS; INTESTINAL POLYPS; MESODERM; MICE; MUTATION; NEOPLASM INVASIVENESS; PHENOTYPE; RAS PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; VIMENTIN; WNT PROTEINS;

GASTROPODA; MAMMALIA; MURINAE; MUS;

EID: 42549137908     PISSN: 15672379     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10735-008-9164-3     Document Type: Article

References (57)

1. American Cancer Society (2007) Cancer facts & figures 2007
2. Amos-Landgraf JM, Kwong LN, Kendziorski CM, Reichelderfer M, Torrealba J, Weichert J, Haag JD, Chen KS, Waller JL, Gould MN, Dove WF (2007) A target-selected Apc-mutant rat kindred enhances the modeling of familial human colon cancer. Proc Natl Acad Sci USA 104:4036-4041
3. Bachman KE, Park BH (2005) Duel nature of TGF-β signaling: tumor suppressor vs. tumor promoter. Curr Opin Oncol 17:49-54
4. Bates RC, Mercurio AM (2005) The epithelial-mesenchymal transition (EMT) and colorectal cancer progression. Cancer Biol Ther 4:365-370
5. Bates RC, Bellovin DI, Brown C, Maynard E, Wu B, Kawakatsu H, Sheppard D, Oettgen P, Mercurio AM (2005) Transcriptional activation of integrin β6 during the epithelial-mesenchymal transition defines a novel prognostic indicator of aggressive colon carcinoma. J Clin Invest 115:339-347
6. Batlle E, Bacani J, Begthel H, Jonkeer S, Gregorieff A, van de BM, Malats N, Sancho E, Boon E, Pawson T, Gallinger S, Pals S, Clevers H (2005) EphB receptor activity suppresses colorectal cancer progression. Nature 435:1126-1130
7. Behrens J, Jerchow BA, Wurtele M, Grimm J, Asbrand C, Wirtz R, Kuhl M, Wedlich D, Birchmeier W (1998) Functional interaction of an axin homolog, conductin, with β-catenin, APC, and GSK3β. Science 280:596-599
8. Bond JH (2000) Polyp guideline: diagnosis, treatment, and surveillance for patients with colorectal polyps. Practice parameters committee of the American College of Gastroenterology. Am J Gastroenterol 95:3053-3063
9. Boudreau F, Lussier CR, Mongrain S, Darsigny M, Drouin JL, Doyon G, Suh ER, Beaulieu JF, Rivard N, Perreault N (2007) Loss of cathepsin L activity promotes claudin-1 overexpression and intestinal neoplasia. FASEB J 21:3853-3865
10. Brabletz T, Jung A, Reu S, Porzner M, Hlubek F, Kunz-Schughart LA, Knuechel R, Kirchner T (2001) Variable β-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc Natl Acad Sci USA 98:10356-10361
11. Brabletz T, Hlubek F, Spaderna S, Schmalhofer O, Hiendlmeyer E, Jung A, Kirchner T (2005) Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal-epithelial transition, stem cells and β-catenin. Cells Tissues Organs 179:56-65
12. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F, Nieto MA (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2:76-83
13. Chen X, Halberg RB, Ehrhardt WM, Torrealba J, Dove WF (2003) Clusterin as a biomarker in murine and human intestinal neoplasia. Proc Natl Acad Sci USA 100:9530-9535
14. Chen WD, Han ZJ, Skoletsky J, Olson J, Sah J, Myeroff L, Platzer P, Lu S, Dawson D, Willis J, Pretlow TP, Lutterbaugh J, Kasturi L, Willson JK, Rao JS, Shuber A, Markowitz SD (2005) Detection in fecal DNA of colon cancer-specific methylation of the nonexpressed vimentin gene. J Natl Cancer Inst 97:1124-1132
15. Christiansen JJ, Rajasekaran AK (2006) Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 66:8319-8326
16. Comijn J, Berx G, Vermassen P, Verschueren K, van Grunsven L, Bruyneel E, Mareel M, Huylebroeck D, van Roy F (2001) The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol Cell 7:1267-1278
17. Eger A, Stockinger A, Schaffhauser B, Beug H, Foisner R (2000) Epithelial mesenchymal transition by c-Fos estrogen receptor activation involves nuclear translocation of β-catenin and upregulation of β-catenin/lymphoid enhancer binding factor-1 transcriptional activity. J Cell Biol 148:173-188
18. Fodde R, Edelmann W, Yang K, van Leeuwen C, Carlson C, Renault B, Breukel C, Alt E, Lipkin M, Khan PM, Kucherlapati R (1994) A targeted chain-termination mutation in the mouse Apc gene results in multiple intestinal tumors. Proc Natl Acad Sci USA 91:8969-8973
19. Franci C, Takkunen M, Dave N, Alameda F, Gomez S, Rodriguez R, Escriva M, Montserrat-Sentis B, Baro T, Garrido M, Bonilla F, Virtanen I, Garcia dH (2006) Expression of Snail protein in tumor-stroma interface. Oncogene 25:5134-5144
20. Gilles C, Polette M, Mestdagt M, Nawrocki-Raby B, Ruggeri P, Birembaut P, Foidart JM (2003) Transactivation of vimentin by beta-catenin in human breast cancer cells. Cancer Res 63:2658-2664
21. Gotzmann J, Mikula M, Eger A, Schulte-Hermann R, Foisner R, Beug H, Mikulits W (2004) Molecular aspects of epithelial cell plasticity: implications for local tumor invasion and metastasis. Mutat Res 566:9-20
22. Greenburg G, Hay ED (1982) Epithelia suspended in collagen gels can lose polarity and express characteristics of migrating mesenchymal cells. J Cell Biol 95:333-339
23. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100:57-70
24. Heldin CH, Miyazono K, ten Dijke P (1997) TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390:465-471
25. Herzig M, Christofori G (2002) Recent advances in cancer research: mouse models of tumorigenesis. Biochim Biophys Acta 1602:97-113
26. Hunter K (2005) The intersection of inheritance and metastasis: the role and implications of germline polymorphism in tumor dissemination. Cell Cycle 4:1719-1721
27. Janda E, Lehmann K, Killisch I, Jechlinger M, Herzig M, Downward J, Beug H, Grunert S (2002) Ras and TGFβ cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J Cell Biol 156:299-313
28. Kaiser S, Park YK, Franklin JL, Halberg RB, Yu M, Jessen WJ, Freudenberg J, Chen X, Haigis K, Jegga AG, Kong S, Sakthivel B, Xu H, Reichling T, Azhar M, Boivin GP, Roberts RB, Bissahoyo AC, Gonzales F, Bloom GC, Eschrich S, Carter SL, Aronow JE, Kleimeyer J, Kleimeyer M, Ramaswamy V, Settle SH, Boone B, Levy S, Graff JM, Doetschman T, Groden J, Dove WF, Threadgill DW, Yeatman TJ, Coffey RJ Jr, Aronow BJ (2007) Transcriptional recapitulation and subversion of embryonic colon development by mouse colon tumor models and human colon cancer. Genome Biol 8:R131
29. Kaklamani VG, Pasche B (2004) Role of TGF-β in cancer and the potential for therapy and prevention. Expert Rev Anticancer Ther 4:649-661
30. Kang Y, Massague J (2004) Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118:277-279
31. Kemler R, Hierholzer A, Kanzler B, Kuppig S, Hansen K, Taketo MM, de Vries WN, Knowles BB, Solter D (2004) Stabilization of β-catenin in the mouse zygote leads to premature epithelial-mesenchymal transition in the epiblast. Development 131:5817-5824
32. Min/+ on mouse Chromosome 18. Genetics 176:1237-1244
33. Li Y, Yang J, Dai C, Wu C, Liu Y (2003) Role for integrin-linked kinase in mediating tubular epithelial to mesenchymal transition and renal interstitial fibrogenesis. J Clin Invest 112:503-516
34. Limper AH, Roman J (1992) Fibronectin. A versatile matrix protein with roles in thoracic development, repair and infection. Chest 101:1663-1673
35. Marais R, Marshall CJ (1996) Control of the ERK MAP kinase cascade by Ras and Raf. Cancer Surv 27:101-125
36. Maschler S, Wirl G, Spring H, Bredow DV, Sordat I, Beug H, Reichmann E (2005) Tumor cell invasiveness correlates with changes in integrin expression and localization. Oncogene 24:2032-2041
37. Menke A, Philippi C, Vogelmann R, Seidel B, Lutz MP, Adler G, Wedlich D (2001) Down-regulation of E-cadherin gene expression by collagen type I and type III in pancreatic cancer cell lines. Cancer Res 61:3508-3517
38. Moser AR, Pitot HC, Dove WF (1990) A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 247:322-324
39. Ngai J, Capetanaki YG, Lazarides E (1985) Expression of the genes coding for the intermediate filament proteins vimentin and desmin. Ann NY Acad Sci 455:144-157
40. Nieto MA, Sargent MG, Wilkinson DG, Cooke J (1994) Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 264:835-839
41. Park BJ, Park JI, Byun DS, Park JH, Chi SG (2000) Mitogenic conversion of transforming growth factor-β1 effect by oncogenic Ha-Ras-induced activation of the mitogen-activated protein kinase signaling pathway in human prostate cancer. Cancer Res 60:3031-3038
42. Reeves R, Edberg DD, Li Y (2001) Architectural transcription factor HMGI(Y) promotes tumor progression and mesenchymal transition of human epithelial cells. Mol Cell Biol 21:575-594
43. Roberts AB, Russo A, Felici A, Flanders KC (2003) Smad3: a key player in pathogenetic mechanisms dependent on TGF-β. Ann NY Acad Sci 995:1-10
44. Savagner P (2001) Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 23:912-923
45. Smith RA, von Eschenbach AC, Wender R, Levin B, Byers T, Rothenberger D, Brooks D, Creasman W, Cohen C, Runowicz C, Saslow D, Cokkinides V, Eyre H (2001) American Cancer Society guidelines for the early detection of cancer: update of early detection guidelines for prostate, colorectal, and endometrial cancers. Also: update 2001-testing for early lung cancer detection. CA Cancer J Clin 51:38-75
46. Sporn MB (1996) The war on cancer. Lancet 347:1377-1381
47. Su LK, Kinzler KW, Vogelstein B, Preisinger AC, Moser AR, Luongo C, Gould KA, Dove WF (1992) Multiple intestinal neoplasia caused by a mutation in the murine homolog of the APC gene. Science 256:668-670
48. Takahashi M, Wakabayashi K (2004) Gene mutations and altered gene expression in azoxymethane-induced colon carcinogenesis in rodents. Cancer Sci 95:475-480
49. Taki M, Kamata N, Yokoyama K, Fujimoto R, Tsutsumi S, Nagayama M (2003) Down-regulation of Wnt-4 and up-regulation of Wnt-5a expression by epithelial-mesenchymal transition in human squamous carcinoma cells. Cancer Sci 94:593-597
50. Tarin D, Thompson EW, Newgreen DF (2005) The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 65:5996-6000
51. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ, Parrish M, Atsma D, Witteveen A, Glas A, Delahaye L, van d V, Bartelink H, Rodenhuis S, Rutgers ET, Friend SH, Bernards R (2002) A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 347:1999-2009
52. Wierzbicka-Patynowski I, Schwarzbauer JE (2003) The ins and outs of fibronectin matrix assembly. J Cell Sci 116:3269-3276
53. Wilson CL, Heppner KJ, Labosky PA, Hogan BLM, Matrisian LM (1997) Intestinal tumorigenesis is suppressed in mice lacking the metalloproteinase matrilysin. Proc Natl Acad Sci USA 94:1402-1407
54. Wood LD, Parsons DW, Jones S, Lin J, Sjoblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, Silliman N, Szabo S, Dezso Z, Ustyanksky V, Nikolskaya T, Nikolsky Y, Karchin R, Wilson PA, Kaminker JS, Zhang Z, Croshaw R, Willis J, Dawson D, Shipitsin M, Willson JK, Sukumar S, Polyak K, Park BH, Pethiyagoda CL, Pant PV, Ballinger DG, Sparks AB, Hartigan J, Smith DR, Suh E, Papadopoulos N, Buckhaults P, Markowitz SD, Parmigiani G, Kinzler KW, Velculescu VE, Vogelstein B (2007) The genomic landscapes of human breast and colorectal cancers. Science 318:1108-1113
55. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:927-939
56. Zavadil J, Bottinger EP (2005) TGF-β and epithelial-to-mesenchymal transitions. Oncogene 24:5764-5774
57. Zhu Y, Richardson JA, Parada LF, Graff JM (1998) Smad3 mutant mice develop metastatic colorectal cancer. Cell 94:703-714