SMAD4 mediates mesenchymal-epithelial reversion in SW480 colon carcinoma cells

Anticancer Research

Volumn 30, Issue 7, 2010, Pages 2603-2613

  Pohl, Michael ^a   Radacz, Yvonne ^a   Pawlik, Nicole ^a   Schoeneck, Anna ^a   Baldus, Stephan E ^b   Munding, Johanna ^c   Schmiegel, Wolff ^a,c,d   Schwarte Waldhoff, Irmgard ^a   Reinacher Schick, Anke ^a,d  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

E cadherin; Epithelial phenotype; Invasion and metastasis; Mesenchymal epithelial reversion; SMAD4

Indexed keywords

CYTOKINE; MOLECULAR MARKER; SMAD PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; CANCER CELL CULTURE; CARCINOMA CELL; CELL ADHESION; CELL ASSAY; CELL DIFFERENTIATION; CELL INVASION; CELL MIGRATION; COLON CARCINOGENESIS; COLON CARCINOMA; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; ENZYME RECONSTITUTION; EPITHELIAL MESENCHYMAL TRANSITION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INTESTINE CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE; WESTERN BLOTTING; WOUND HEALING;

ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; COLONIC NEOPLASMS; EPITHELIAL CELLS; HUMANS; MESODERM; MICE; NEOPLASM INVASIVENESS; SIGNAL TRANSDUCTION; SMAD4 PROTEIN; TRANSFECTION; TRANSFORMING GROWTH FACTOR BETA; TRANSPLANTATION, HETEROLOGOUS; WOUND HEALING;

EID: 77955785880     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (43)

1. De Wever O, Pauwels P, De Craene B, Sabbah M, Emami S, Redeuilh G, Gespach C, Bracke M and Berx G: Molecular and pathological signatures of epithelial-mesenchymal transitions at the cancer invasion front. Histochem Cell Biol 130: 481-494, 2008.
2. Thiery JP: Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454, 2002.
3. Simon-Assmann P, Lefebvre O, Bellissent-Waydelich A, Olsen J, Orian-Rousseau V and De Arcangelis A: The laminins: role in intestinal morphogenesis and differentiation. Ann NY Acad Sci 859: 46-64, 1998. (Pubitemid 29021006)
4. Brabletz T, Hlubek F, Spaderna S, Schmalhofer O, Hiendlmeyer E, Jung A and Kirchner T: Invasion and metastasis in colorectal cancer: epithelial-mesenchymal transition, mesenchymal-epithelial transition, stem cells and β-catenin. Cells Tissues Organs 179: 56-65, 2005. (Pubitemid 40976289)
5. Thiery JP and Sleeman JP: Complex networks orchestrate epithelial-mesenchymal transitions. Nat Rev Mol Cell Biol 7: 131-142, 2006.
6. Gruenert S, Jechlinger M and Beug H: Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat Rev Mol Cell Biol 4: 657-665, 2003. (Pubitemid 36934968)
7. Kalluri R and Neilson EG: Epithelial-mesenchymal transition and its implications for fibrosis. J Clin Invest 112: 1776-1784, 2003. (Pubitemid 38063698)
8. Gofuku J, Shiozaki H, Tsujinaka T, Inoue M, Tamura S, Doki Y, Matsui S, Tsukita S, Kikkawa N and Monden M: Expression of E-cadherin and alpha-catenin in patients with colorectal carcinoma. Correlation with cancer invasion and metastasis. Am J Clin Pathol 111: 29-37, 1999. (Pubitemid 29024963)
9. Lowy AM, Knight J and Groden J: Restoration of E-cadherin/beta-catenin expression in pancreatic cancer cells inhibits growth by induction of apoptosis. Surgery 132: 141-148, 2002. (Pubitemid 35024754)
10. Rashid MG, Sanda MG, Vallorosi CJ, Rios-Doria J, Rubin MA and Day ML: Posttranslational truncation and inactivation of human E-cadherin distinguishes prostate cancer from matched normal prostate. Cancer Res 61: 489-492, 2001. (Pubitemid 32128604)
11. Guilford P, Hopkins J, Harraway J, McLeod M, McLeod N, Harawira P, Taite H, Scoular R, Miller A and Reeve AE: E-Cadherin germline mutations in familial gastric cancer. Nature 392: 402-405, 1998.
12. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, del Barrio MG, Portillo F and Nieto MA: The transcription factor SNAIL controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2: 76-83, 2000.
13. Batlle E, Sancho E, Franci C, Dominguez D, Monfar M, Baulida J and Garcia De Herreros A: The transcription factor SNAIL is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat Cell. Biol 2: 84-89, 2000.
14. Mueller N, Reinacher-Schick A, Baldus S, van Hengel J, Berx G, Baar A, van Roy F, Schmiegel W and Schwarte-Waldhoff I: SMAD4 induces the tumor suppressor E-cadherin and P-cadherin in colon carcinoma cells. Oncogene 21: 6049-6058, 2002.
15. Hahn SA, Schutte M, Hoque ATM, Moskaluk CA, da Costa LT, Rozenblum E, Weinstein CL, Fischer A, Yeo CJ, Hruban RH and Kern SE: DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271: 350-353, 1996. (Pubitemid 3021510)
16. Miyaki M, Iijima T, Konishi M, Sakai K, Ishii A, Yasuno M, Hishima T, Koike M, Shitara N, Iwama T, Utsunomiya J, Kuroki T and Mori T: Higher frequency of SMAD4 gene mutation in human colorectal cancer with distant metastasis. Oncogene 18: 3098-3103, 1999. (Pubitemid 29261230)
17. Maitra A, Molberg K, Albores-Saavedra J and Lindberg G: Loss of DPC4 expression in colonic adenocarcinomas correlates with the presence of metastatic disease. Am J Pathol 157: 1105-1111, 2000.
18. Riggins GJ, Kinzler KW, Vogelstein B and Thiagalingam S: Frequency of SMAD gene mutations in human cancer. Cancer Res 57: 2578-2580, 1997. (Pubitemid 27283760)
19. Massague J and Chen YG: Controlling TGF-beta signaling. Genes Dev 14: 627-644, 2000.
20. Massague J, Seoane J and Wotton D: SMAD transcription factors. Genes Dev 19: 2783-2810, 2005.
21. Hocevar BA, Brown TL and Howe PH: TGF-beta induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, SMAD4-independent pathway. EMBO J 18, 1345-1356, 1999.
22. Sirard C, Kim S, Mirtsos C, Tadich P, Hoodless PA, Itie A, Maxson R, Wrana, JL and Mak TW: Targeted disruption in murine cells reveals variable requirement for SMAD4 in transforming growth factor beta-related signaling. J Biol Chem 275: 2063-2070, 2000. (Pubitemid 30060834)
23. Fink SP, Swinler SE, Lutterbaugh JD, Massague J, Thiagalingam S, Kinzler KW, Vogelstein B, Willson JK and Markowitz S: Transforming growth factor-beta-induced growth inhibition in a SMAD4 mutant colon adenoma cell line. Cancer Res 61: 256-260, 2001. (Pubitemid 32109247)
24. Pardali K and Moustakas A: Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. Biochim Biophys Acta 1775: 21-62, 2007. (Pubitemid 44881193)
25. Zavadil J and Bottinger EP: TGF beta and epithelial-to-mesenchymal transitions. Oncogene 24: 5764-5774, 2005.
26. Schwarte-Waldhoff I, Volpert OV, Bouck NP, Sipos B, Hahn SA, Klein-Scory S, Luettges J, Kloppel G, Graeven U, Eilert-Micus C, Hintelmann A and Schmiegel W: SMAD4/DPC4-mediated tumor suppression through suppression of angiogenesis. Proc Natl Acad Sci USA 97: 9624-9629, 2000. (Pubitemid 30650826)
27. Schwarte-Waldhoff I, Klein S, Blass-Kampmann S, Hintelmann A, Eilert C, Dreschers S, Kalthoff H, Hahn SA and Schmiegel W: DPC4/SMAD4-mediated tumor suppression of colon carcinoma cells is associated with reduced urokinase expression. Oncogene 18: 3152-3158, 1999. (Pubitemid 29261236)
28. Zapatka M, Zboralski D, Radacz Y, Bockmann M, Arnold C, Schoneck A, Hoppe S, Tannapfel A, Schmiegel W, Simon-Assmann P and Schwarte-Waldhoff I: Basement membrane component laminin-5 is a target of the tumor suppressor SMAD4. Oncogene 26: 1417-1427, 2007. (Pubitemid 46340807)
29. Baldus SE, Zirbes TK, Engel S, Hanisch FG, Monig SP, Lorenzen J, Glossmann J, Fromm S, Thiele J, Pichlmaier H and Dienes HP: Correlation of the immunohistochemical reactivity of mucin peptide cores MUC1 and MUC2 with the histopathological subtype and prognosis of gastric carcinomas. Int J Cancer 79: 133-138, 1998. (Pubitemid 28201683)
30. Moll R, Mitze M, Frixen UH and Birchmeier W: Differential loss of E-cadherin expression in infiltrating ductal and lobular breast carcinomas. Am J Pathol 143: 1731-1742, 1993. (Pubitemid 24058276)
31. Herrman H and Aebli U: Intermediate filaments: Molecular structure, assembly mechanism and integration into functionally distinct intracellular scaffolds. Annu Rev Biochem 73: 749-789, 2004.
32. Polley AC, Mulholland F, Pin C, Williams EA, Bradburn DM, Mills SJ, Mathers JC and Johnson IT: Proteomic analysis reveals field-wide changes in protein expression in the morphologically normal mucosa of patients with colorectal neoplasia. Cancer Res 66: 6553-6562, 2006. (Pubitemid 44085610)
33. Kaihara T, Kawamata H, Imura J, Fujii S, Kitajima K, Omotehara F, Maeda N, Nakamura T and Fujimori T: Redifferentiation and ZO-1 re-expression in liver-metastasized colorectal cancer: Possible association with epidermal growth factor receptor-induced tyrosine phosphorylation of ZO-1. Cancer Sci 94: 166-172, 2003. (Pubitemid 36575876)
34. Athman R, Louvard D and Robine S: Villin enhances hepatocyte growth factor-induced actin cytoskeleton remodeling in epithelial cells. Mol Biol Cell 14: 4641-4653, 2003.
35. Nusrat A, Delp C and Madara JL: Intestinal epithelial restitution. Characterization of a cell culture model and mapping of cytoskeletal elements in migrating cells. J Clin Invest 89: 1501-1511, 1992.
36. Schwarte-Waldhoff I and Schmiegel W: SMAD4 transcriptional pathways and angio-genesis. Int J Gastrointest Cancer 31: 47-59, 2002.
37. Siegel PM and Massague J: Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat Rev Cancer 3: 807-821, 2003.
38. Subramanian G, Schwarz RE, Higgins L, McEnroe G, Chakravarty S, Dugar S and Reiss M: Targeting endogenous transforming growth factor beta receptor signaling in SMAD4-deficient human pancreatic carcinoma cells inhibits their invasive phenotypel. Cancer Res 64: 5200-5211, 2004. (Pubitemid 39006539)
39. Deckers M, van Dinther M, Buijs J, Que I, Ladwik C, van der Pluijm G and ten Dijke P: The tumor suppressor SMAD4 is required for transforming growth factor beta-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells. Cancer Res 66: 2202-2209, 2006. (Pubitemid 43294931)
40. Piek E, Moustakas A, Kurisaki A, Heldin CH and ten Dijke P: TGF-β type I receptor/ALK-5 and SMAD proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J Cell Sci 112: 4557-4568, 1999. (Pubitemid 30034805)
41. Valcourt U, Kowanetz M, Niimi H, Heldin CH and Moustakas A: TGF-beta and the SMAD signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol Biol Cell 16: 1987-2002, 2005.
42. Levy L and Hill CS: SMAD4 dependency defines two classes of transforming growth factor beta (TGF-β) target genes and distinguishes TGF-β-induced epithelial-mesenchymal transition from its antiproliferative and migratory responses. Mol Cell Biol 25: 8108-8125, 2005. (Pubitemid 41263004)
43. Shiou SR, Singh AB, Moorthy K, Datta PK, Washington MK, Beauchamp D and Dhawan P: SMAD4 regulates claudin-1 expression in a TGF-β-independent manner in colon cancer cells. Cancer Res 67: 1571-1579, 2007. (Pubitemid 46383381)