Transforming growth factor-β1 induces epithelial-mesenchymal transition and integrin α3β1-mediated cell migration of HSC-4 human squamous cell carcinoma cells through Slug

Journal of Biochemistry

Volumn 153, Issue 3, 2013, Pages 303-315

  Saito, Daishi ^a,b   Kyakumoto, Seiko ^a   Chosa, Naoyuki ^a   Ibi, Miho ^c   Takahashi, Noriko ^a   Okubo, Naoto ^c   Sawada, Shunsuke ^a   Ishisaki, Akira ^a   Kamo, Masaharu ^a  

^a IWATE MEDICAL UNIVERSITY   (Japan)

^b School of Dentistry   (Japan)

^c Department of Tumor Biology   (Japan)

Author keywords

EMT; integrin 3 1; migration; squamous cell carcinoma; TGF

Indexed keywords

BETA CATENIN; CYTOKERATIN 18; FIBRONECTIN; FOCAL ADHESION KINASE INHIBITOR; NERVE CELL ADHESION MOLECULE; SMAD2 PROTEIN; TRANSCRIPTION FACTOR SLUG; TRANSFORMING GROWTH FACTOR BETA1; UVOMORULIN; VERY LATE ACTIVATION ANTIGEN 3; VIMENTIN;

ARTICLE; CANCER CELL CULTURE; CELL MIGRATION; CELL STIMULATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUTH SQUAMOUS CELL CARCINOMA; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEOMICS; UPREGULATION;

BLOTTING, WESTERN; CADHERINS; CARCINOMA, SQUAMOUS CELL; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRIN ALPHA3BETA1; MICROSCOPY, CONFOCAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SMAD7 PROTEIN; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84874334375     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvs144     Document Type: Article

References (56)

1. Wang, X., Sun, W., Bai, J., Ma, L., Yu, Y., Geng, J., Qi, J., Shi, Z., and Fu, S. (2009) Growth inhibition induced by transforming growth factor-b1 in human oral squamous cell carcinoma. Mol. Biol. Rep. 36, 861-869
2. Ikushima, H. and Miyazono, K. (2010) TGFb signalling:a complex web in cancer progression. Nat. Rev. Cancer 10, 415-424
3. Meulmeester, E. and Dijke, T.P. (2011) The dynamic roles of TGF-b in cancer. J. Pathol. 223, 205-218
4. Mu, Y., Gudey, S.K., and Landström, M. (2012) Non-Smad signaling pathways. Cell Tissue Res. 347, 11-20
5. Miyazawa, K., Shinozaki, M., Hara, T., Furuya, T., and Miyazono, K. (2002) Two major Smad pathways in TGF-b superfamily signalling. Genes Cells 7, 1191-1204
6. Sabe, H. (2011) Cancer early dissemination: Cancerous epithelial-mesenchymal transdifferentiation and transforming growth factor b signaling. J. Biochem. 149, 633-639
7. Saitoh, M. and Miyazawa, K. (2012) Transcriptional and post-transcriptional regulation in TGF-b-mediated epithelial-mesenchymal transition. J. Biochem. 151, 563-571
8. Micalizzi, D.S., Farabaugh, S.M., and Ford, H.L. (2010) Epithelial-mesenchymal transition in cancer: Parallels between normal development and tumor progression. J. Mamm. Gland Biol. Neoplasia 15, 117-134
9. Chen, Y.S., Mathias, R.A., Mathivanan, S., Kapp, E.A., Moritz, R.L., Zhu, H.J., and Simpson, R.J. (2011) Proteomics profiling of Madin-Darby canine kidney plasma membranes reveals Wnt-5 a involvement during oncogenic H-Ras/TGF-b-mediated epithelialmesenchymal transition. Mol. Cell. Proteomics 10, M110.001131
10. Jing, Y., Han, Z., Zhang, S., Liu, Y., and Wei, L. (2011) Epithelial-mesenchymal transition in tumor microenvironment. Cell Biosci. 1, 29
11. Thiery, J.P. and Sleeman, J.P. (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142
12. Kim, K., Lu, Z., and Hay, E.D. (2002) Direct evidence for a role of b-catenin/LEF-1 signaling pathway in induction of EMT. Cell Biol. Int. 26, 463-476
13. Chilosi, M., Poletti, V., Zamó, A., Lestani, M., Montagna, L., Piccoli, P., Pedron, S., Bertaso, M., Scarpa, A., Murer, B., Cancellieri, A., Maestro, R., Semenzato, G., and Dogurioni, C. (2003) Aberrant Wnt/b-catenin pathway activation in idiopathic pulmonary fibrosis. American J. Pathol. 162, 1495-1502
14. Jamora, C., DasGupta, R., Kocieniewski, P., and Fuchs, E. (2003) Links between signal transduction, transcription and adhesion in epithelial bud development. Nature 422, 317-322
15. Savagner, P. (2001) Leaving the neighborhood: Molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 23, 912-923
16. Nelson, W.J. and Nusse, R. (2004) Convergence of Wnt, b-catenin, and cadherin pathways. Science 303, 1483-1487
17. Uraguchi, M., Morikawa, M., Shirakawa, M., Sanada, K., and Imai, K. (2004) Activation of WNT family expression and signaling in squamous cell carcinomas of the oral cavity. J. Dent. Res. 83, 327-332
18. Korkaya, H., Liu, S., and Wicha, M.S. (2011) Breast cancer stem cells, cytokine networks, and the tumor microenvironment. J. Clin. Invest. 121, 3804-3809
19. Zeisberg, M. and Neilson, E.G. (2009) Biomarkers for epithelial- mesenchymal transitions. J. Clin. Invest. 119, 1429-1437
20. Peinado, H., Olmeda, D., and Cano, A. (2007) Snail, Zeb and bHLH factors in tumour progression: An alliance against the epithelial phenotype? Nat. Rev. Cancer 7, 415-428
21. Batlle, E., Sancho, E., Franci, C., Dominguez, D., Monfar, M., Baulida, J., and Garcia De, H.A. (2000) The transcription factor Snail is a repressor of E-cadherin gene expression in the epithelial tumour cells. Nat. Cell Biol. 2, 84-89
22. Medici, D., Hay, E.D., and Olsen, B.R. (2008) Snail and Slug promote epithelial-mesenchymal transition through b-catenin-T-cell factor-4-dependent expression of transforming growth factor-b3. Mol. Biol. Cell 19, 4875-4887
23. Yang, J., Mani, S.A., Donaher, J.L., Ramaswamy, S., Itzykson, R.A., Come, C., Savagner, P., Gitelman, I., Richardson, A., and Weinberg, R.A. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939
24. Hader, C., Marlier, A., and Cantley, L. (2010) Mesenchymal-epithelial transition in epithelial response to injury: The role of Foxc2. Oncogene 29, 1031-1040
25. Fuxe, J., Vincent, T., and de Herreros, A. (2010) Transcriptional crosstalk between TGF-b and stem cell pathways in tumor cell invasion: Role of EMT promoting Smad complexes. Cell Cycle 15, 2363-2374
26. Lawler, J., Sunday, M., Thibert, V., Duquette, M., George, E.L., Rayburn, H., and Hynes, R.O. (1998) Thrombospondin-1 is required for normal murine pulmonary homeostasis and its absence causes pneumonia, J. Clin. Invest. 101, 982-992
27. Yee, K.O., Connolly, C.M., Duquette, M., Kazerounian, S., Washington, R., and Lawler, J. (2009) The effect of thrombospondin-1 on breast cancer metastasis. Breast Cancer Res. Treat. 114, 85-96
28. Smith, H.W. and Marshall, C.J. (2010) Regulation of cell signalling by uPAR. Nat. Rev. Mol. Cell Biol. 11, 23-36
29. Oh, J.E., Kook, J.-K., and Min, B.M. (2005) ßig-h3 induces keratinocyte differentiation via modulation of involucrin and transglutaminase expression through the integrin a3b1 and the phosphatidylinositol 3-kinase/Akt signaling pathway. J. Biol. Chem. 280, 21629-21637
30. de longh, R.U., Wederell, E., Lovicu, F.J., and McAvoy, J.W. (2005) Transforming growth factor-b-induced epithelial-mesenchymal transition in the lens: A model for cataract formation. Cells Tissues Organs 179, 43-55
31. Ungefroren, H., Sebens, S., Seidl, D., Lehnert, H., and Hass, R. (2011) Interaction of tumor cells with the microenvironment. Cell Commun. Signal 9, 18
32. Richter, P., Umbreit, C., Franz, M., Berndt, A., Grimm, S., Uecker, A., Böhmer, F.D., Kosmehl, H., and Berndt, A. (2010) EGF/TGFb1 co-stimulation of oral squamous cell carcinoma cells causes an epithelial-mesenchymal transition cell phenotype expressing laminin 332. J. Oral Pathol. Med. 40, 46-54
33. Takayama, S., Hatori, M., Kurihara, Y., Kinugasa, Y., Shirota, T., and Shintani, S. (2009) Inhibition of TGF-b1 suppresses motility and invasiveness of oral squamous cell carcinoma cell lines via modulation of integrins and down-regulation of matrix-metalloproteinases. Oncology Rep. 21, 205-210
34. Qiao, B., Johnson, N.W., and Gao, J. (2010) Epithelial-mesenchymal transition in oral squamous cell carcinoma triggered by transforming growth factor-b1 is Snail family-dependent and correlates with matrix metalloproteinase-2 and -9 expressions. Int. J. Oncol. 37, 663-668
35. Nakao, A., Afrakhte, M., Morén, A., Nakayama, T., Christian, J.L., Heuchel, R., Itoh, S., Kawabata, M., Heldin, N.E., Heldin, C.H., and ten Dijke, P. (1997) Identification of Smad7, a TGFb-inducible antagonist of TGF-b signalling. Nature 389, 631-635
36. Hocevar, B.A., Brown, T.L., and Howe, P.H. (1999) TGF-b induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. EMBO J. 18, 1345-1356
37. Akiyoshi, S., Ishii, M., Nemoto, N., Kawabata, M., Aburatani, H., and Miyazono, K. (2001) Targets of transcriptional regulation by transforming growth factor-beta: Expression profile analysis using oligonucleotide arrays. Jpn. J. Cancer Res. 92, 257-268
38. Lauffenburger, D.A. and Horwitz, A.F. (1996) Cell migration:a physically integrated molecular process. Cell 84, 359-369
39. Mierke, C.T., Kollmannsberger, P., Zitterbart, D.P., Smith, J., Fabry, B., and Goldmann, W.H. (2008) Mechano-coupling and regulation of contractility by the vinculin tail domain. Biophys. J. 94, 661-670
40. Ezzell, R.M., Goldmann, W.H., Wang, N., Parashurama, N., and Ingber, D.E. (1997) Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton. Exp. Cell Res. 231, 14-26
41. Humphries, J.D., Wang, P., Streuli, C., Geiger, B., Humphries, M.J., and Ballestrem, C. (2007) Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 179, 1043-1057
42. Ren, B., Yee, K.O., Lawler, J., and Khosravi-Far, R. (2006) Regulation of tumor angiogenesis by thrombospondin-1. Biochim. Biophys. Acta 1765, 178-188
43. Reinboth, B., Thomas, J., Hanssen, E., and Gibson, M.A. (2006) ßig-h3 interacts directly with biglycan and decorin, promotes collagen VI aggregation, and participates in ternary complexing with these macromolecules. J. Boil. Chem. 281, 7816-7824
44. Elices, M.J., Urry, L.A., and Hemler, M.E. (1991) Receptor functions for the integrin VLA-3: Fibronectin, collagen, and laminin binding are differentially influenced by Arg-Gly-Asp peptide and by divalent cations. J. Cell Biol. 112, 169-181
45. Wei, Y., Eble, J.A., Wang, Z., Kreidberg, J.A., and Chapman, H.A. (2001) Urokinase receptors promote b1 integrin function through interactions with integrin a3b1. Mol. Biol. Cell 12, 2975-2986
46. Heijink, I.H., Postma, D.S., Noordhoek, J.A., Broekema, M., and Kapus, A. (2010) House dust mitepromoted epithelial-to-mesenchymal transition in human bronchial epithelium. Am. J. Respir. Cell Mol. Biol. 42, 69-79
47. Chandler, H.L., Colitz, C.M., Lu, P., Saville, W.J., and Kusewitt, D.F. (2007) The role of the Slug transcription factor in cell migration during corneal re-epithelialization in the dog. Exp. Eye Res. 84, 400-411
48. Chen, Z., Zhang, D., Yue, F., Zheng, M., Kovacevic, Z., and Richardson, D.R. (2012) The iron chelators Dp44mT and DFO inhibit TGF-b-induced epithelialmesenchymal transition via up-regulation of N-Myc downstream-regulated gene 1 (NDRG1). J. Biol. Chem. 287, 17016-17028
49. Taki, M., Verschueren, K., Yokoyama, K., Nagayama, M., and Kamata, N. (2006) Involvement of Ets-1 transcription factor in inducing matrix metalloproteinase-2 expression by epithelial-mesenchymal transition in human squamous carcinoma cells. Int. J. Oncol. 28, 487-496
50. Lamouille, S., Connolly, E., Smyth, J.W., Akhurst, R.J., and Derynck, R. (2012) TGF-b-induced activation of mTOR complex 2 drives epithelial-mesenchymal transition and cell invasion. J. Cell Sci. 125, 1259-1273
51. Bakin, A.V., Rinehart, C., Tomlinson, A.K., and Arteaga, C.L. (2002) p38 mitogen-activated protein kinase is required for TGFb-mediated fibroblastic transdifferentiation and cell migration. J. Cell Sci. 115, 3193-3206
52. Aomatsu, K., Arao, T., Abe, K., Kodama, A., Sugioka, K., Matsumoto, K., Kudo, K., Kimura, H., Fujita, Y., Hayashi, H., Nagai, T., Shimomura, Y., and Nishio, K. (2012) Slug is upregulated during wound healing and regulates cellular phenotypes in corneal epithelial cells. Invest. Ophthalmol. Vis. Sci. 53, 751-756
53. Pocheć, E., Lityń ska, A., Amoresano, A., and Casbarra, A. (2003) Glycosylation profile of integrin a3b1 changes with melanoma progression. Biochim. Biophys. Acta 1643, 113-123
54. Frame, M.C., Patel, H., Serrels, B., Lietha, D., and Eck, M.J. (2010) The FERM domain: Organizing the structure and function of FAK. Nat. Rev. Mol. Cell Biol. 11, 802-814
55. Mitra, S.K., Hanson, D.A., and Schlaepfer, D.D. (2005) Focal adhesion kinase: In command and control of cell motility. Nat. Rev. Mol. Cell Biol. 6, 56-68
56. Narumiya, S., Tanji, M., and Ishizaki, T. (2009) Rho signaling, ROCK and mDia1, in transformation, metastasis and invasion. Cancer Metastasis Rev. 28, 65-76