The epithelial-mesenchymal transition: New insights in signaling, development, and disease

Journal of Cell Biology

Volumn 172, Issue 7, 2006, Pages 973-981

  Lee, Jonathan M ^a   Dedhar, Shoukat ^b,c   Kalluri, Raghu ^d,e,f   Thompson, Erik W ^g,h  

^a UNIVERSITY OF OTTAWA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c BRITISH COLUMBIA CANCER AGENCY   (Canada)

^d BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^g UNIVERSITY OF MELBOURNE   (Australia)

^h ST VINCENT'S INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MARKER;

CANCER; CELL ACTIVATION; CELL ADHESION; CELL COMMUNICATION; CELL TRANSFORMATION; CYTOLOGY; EMBRYO DEVELOPMENT; EPITHELIUM CELL; FIBROSIS; GENE TARGETING; HUMAN; IN VIVO STUDY; MESENCHYME; METAZOON; NEOPLASM; NONHUMAN; ORGANOGENESIS; PATHOLOGY; PRIORITY JOURNAL; SHORT SURVEY; SIGNAL TRANSDUCTION;

ANIMALS; CELL DIFFERENTIATION; EPITHELIAL CELLS; EPITHELIUM; FEMALE; HUMANS; MESODERM; NEOPLASM INVASIVENESS; NEOPLASMS; SIGNAL TRANSDUCTION;

METAZOA;

EID: 33645302628     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200601018     Document Type: Short Survey

References (58)

1. Barrallo-Gimeno, A., and M.A. Nieto. 2005. The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development. 132:3151-3161.
2. Bates, R.C. 2005. Colorectal cancer progression: integrin alphavbeta6 and the epithelial-mesenchymal transition (EMT). Cell Cycle. 4:1350-1352.
3. Bissell, M.J., D. Farson, and A.S. Tung. 1977. Cell shape and hexose transport in normal and virus-transformed cells in culture. J. Supramol. Struct. 6:1-12.
4. Brabletz, T., A. Jung, S. Reu, M. Porzner, F. Hlubek, L.A. Kunz-Schughart, R. Knuechel, and T. Kirchner. 2001. Variable beta-catenin expression in colorectal cancers indicates tumor progression driven by the tumor environment. Proc. Natl. Acad. Sci. USA. 98:10356-10361.
5. Brabletz, T., A. Jung, S. Spaderna, F. Hlubek, and T. Kirchner. 2005. Opinion: migrating cancer stem cells - an integrated concept of malignant tumour progression. Nat. Rev. Cancer. 5:744-749.
6. Brembeck, F.H., T. Schwarz-Romond, J. Bakkers, S. Wilhelm, M. Hammerschmidt, and W. Birchmeier. 2004. Essential role of BCL9-2 in the switch between beta-catenin's adhesive and transcriptional functions. Genes Dev. 18:2225-2230.
7. Burridge, K., and K. Wennerberg. 2004. Rho and Rac take center stage. Cell. 116:167-179.
8. Carlsson, P., and M. Mahlapuu. 2002. Forkhead transcription factors: key players in development and metabolism. Dev. Biol. 250:1-23.
9. Castanon, I., and M.K. Baylies. 2002. A Twist in fate: evolutionary comparison of Twist structure and function. Gene. 287:11-22.
10. Cavallaro, U., and G. Christofori. 2004. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat. Rev. Cancer. 4:118-132.
11. Chen, C.S., M. Mrksich, S. Huang, G.M. Whitesides, and D.E. Ingber. 1997. Geometric control of cell life and death. Science. 276:1425-1428.
12. Chu, Y.S., O. Eder, W.A. Thomas, I. Simcha, F. Pincet, A. Ben-Ze'ev, E. Perez, J.P. Thiery, and S. Dufour. 2005. Prototypical type-I E-cadherin and type-II cadherin-7 mediate very distinct adhesiveness through their extracellular domain. J. Biol. Chem. 281:365-373.
13. Chu, Y.S., W.A. Thomas, O. Eder, F. Pincet, E. Perez, J.P. Thiery, and S. Dufour. 2004. Force measurements in E-cadherin-mediated cell doublets reveal rapid adhesion strengthened by actin cytoskeleton remodeling through Rac and Cdc42. J. Cell Biol. 167:1183-1194.
14. Condeelis, J., and J.E. Segall. 2003. Intravital imaging of cell movement in tumours. Nat. Rev. Cancer. 3:921-930.
15. De Craene, B., B. Gilbert, C. Stove, E. Bruyneel, F. van Roy, and G. Berx. 2005. The transcription factor snail induces tumor cell invasion through modulation of the epithelial cell differentiation program. Cancer Res. 65:6237-6244.
16. De Robertis, E.M., O. Wessely, M. Oelgeschlager, B. Brizuela, E. Pera, J. Larrain, J. Abreu, and D. Bachiller. 2001. Molecular mechanisms of cell-cell signaling by the Spemann-Mangold organizer. Int. J. Dev. Biol. 45:189-197.
17. Dominguez, D., B. Montserrat-Sentis, A. Virgos-Soler, S. Guaita, J. Grueso, M. Porta, I. Puig, J. Baulida, C. Franci, and A. Garcia de Herreros. 2003. Phosphorylation regulates the subcellular location and activity of the snail transcriptional repressor. Mol. Cell. Biol. 23:5078-5089.
18. Ezratty, E.J., M.A. Partridge, and G.G. Gundersen. 2005. Microtubule-induced focal adhesion disassembly is mediated by dynamin and focal adhesion kinase. Nat. Cell Biol. 7:581-590.
19. Folkman, J., and A. Moscona. 1978. Role of cell shape in growth control. Nature. 273:345-349.
20. Fujita, N., D.L. Jaye, M. Kajita, C. Geigerman, C.S. Moreno, and P.A. Wade. 2003. MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell. 113:207-219.
21. Giri, D.K., M. Ali-Seyed, L.Y. Li, D.F. Lee, P. Ling, G. Bartholomeusz, S.C. Wang, and M.C. Hung. 2005. Endosomal transport of ErbB-2: mechanism for nuclear entry of the cell surface receptor. Mol. Cell. Biol. 25:11005-11018.
22. Gumbiner, B.M. 2005. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6:622-634.
23. Hay, E.D. 2005. The mesenchymal cell, its role in the embryo, and the remarkable signaling mechanisms that create it. Dev. Dyn. 233:706-720.
24. Huang, X., and J.P. Saint-Jeannet. 2004. Induction of the neural crest and the opportunities of life on the edge. Dev. Biol. 275:1-11.
25. Iwano, M., A. Fischer, H. Okada, D. Plieth, C. Xue, T.M. Danoff, and E.G. Neilson. 2001. Conditional abatement of tissue fibrosis using nucleoside analogs to selectively corrupt DNA replication in transgenic fibroblasts. Mol. Ther. 3:149-159.
26. Iwano, M., D. Plieth, T.M. Danoff, C. Xue, H. Okada, and E.G. Neilson. 2002. Evidence that fibroblasts derive from epithelium during tissue fibrosis. J. Clin. Invest. 110:341-350.
27. Kalluri, R., and E.G. Neilson. 2003. Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest. 112:1776-1784.
28. Kim, M.Y., T. Zhang, and W.L. Kraus. 2005. Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev. 19:1951-1967.
29. Lo, H.W., S.C. Hsu, M. Ali-Seyed, M. Gunduz, W. Xia, Y. Wei, G. Bartholomeusz, J.Y. Shih, and M.C. Hung. 2005a. Nuclear interaction of EGFR and STAT3 in the activation of the iNOS/NO pathway. Cancer Cell. 7:575-589.
30. Lo, H.W., W. Xia, Y. Wei, M. Ali-Seyed, S.F. Huang, and M.C. Hung. 2005b. Novel prognostic value of nuclear epidermal growth factor receptor in breast cancer. Cancer Res. 65:338-348.
31. Lochter, A., A. Srebrow, C.J. Sympson, N. Terracio, Z. Werb, and M.J. Bissell. 1997. Misregulation of stromelysin-1 expression in mouse mammary tumor cells accompanies acquisition of stromelysin-1-dependent invasive properties. J. Biol. Chem. 272:5007-5015.
32. Masszi, A., L. Fan, L. Rosivall, C.A. McCulloch, O.D. Rotstein, I. Mucsi, and A. Kapus. 2004. Integrity of cell-cell contacts is a critical regulator of TGF-beta 1-induced epithelial-to-myofibroblast transition: role for beta-catenin. Am. J. Pathol. 165:1955-1967.
33. Moody, S.E., D. Perez, T.C. Pan, C.J. Sarkisian, C.P. Portocarrero, C.J. Sterner, K.L. Notorfrancesco, R.D. Cardiff, and L.A. Chodosh. 2005. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell. 8:197-209.
34. Nawshad, A., D. Lagamba, A. Polad, and E.D. Hay. 2005. Transforming growth factor-beta signaling during epithelial-mesenchymal transformation: implications for embryogenesis and tumor metastasis. Cells Tissues Organs. 179:11-23.
35. Neilson, E.G. 2005. Setting a trap for tissue fibrosis. Nat. Med. 11:373-374.
36. Newgreen, D.F., and S.J. McKeown. 2005. Neural crest cells migration. In Rise and Fall of Epithelial Phenotype: Concepts of Epithelial-Mesenchymal Transition. P. Savagner, editor. Landes Bioscience, Texas. 29-39.
37. Nishitani, Y., M. Iwano, Y. Yamaguchi, K. Harada, K. Nakatani, Y. Akai, T. Nishino, H. Shiiki, M. Kanauchi, Y. Saito, and E.G. Neilson. 2005. Fibroblast-specific protein 1 is a specific prognostic marker for renal survival in patients with IgAN. Kidney Int. 68:1078-1085.
38. Paszek, M.J., N. Zahir, K.R. Johnson, J.N. Lakins, G.I. Rozenberg, A. Gefen, C.A. Reinhart-King, S.S. Margulies, M. Dembo, D. Boettiger, et al. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell. 8:241-254.
39. Radice, G.L., M.C. Ferreira-Cornwell, S.D. Robinson, H. Rayburn, L.A. Chodosh, M. Takeichi, and R.O. Hynes. 1997. Precocious mammary gland development in P-cadherin-deficient mice. J. Cell Biol. 139:1025-1032.
40. Radisky, D.C., D.D. Levy, L.E. Littlepage, H. Liu, C.M. Nelson, J.E. Fata, D. Leake, E.L. Godden, D.G. Albertson, M.A. Nieto, et al. 2005. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature. 436:123-127.
41. Rosivatz, E., K.F. Becker, E. Kremmer, C. Schott, K. Blechschmidt, H. Hofler, and M. Sarbia. 2005. Expression and nuclear localization of Snail, an E-cadherin repressor, in adenocarcinomas of the upper gastrointestinal tract. Virchows Arch. 17:1-11.
42. Shook, D., and R. Keller. 2003. Mechanisms, mechanics and function of epithelial-mesenchymal transitions in early development. Mech. Dev. 120:1351-1383.
43. Somasiri, A., J.S. Nielsen, N. Makretsov, M.L. McCoy, L. Prentice, C.B. Gilks, S.K. Chia, K.A. Gelmon, D.B. Kershaw, D.G. Huntsman, et al. 2004. Overexpression of the anti-adhesin podocalyxin is an independent predictor of breast cancer progression. Cancer Res. 64:5068-5073.
44. Sternlicht, M.D., A. Lochter, C.J. Sympson, B. Huey, J.P. Rougier, J.W. Gray, D. Pinkel, M.J. Bissell, and Z. Werb. 1999. The stromal proteinase MMP3/stromelysin-1 promotes mammary carcinogenesis. Cell. 98:137-146.
45. Tarin, D., E.W. Thompson, and D.F. Newgreen. 2005. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res. 65:5996-6000.
46. Thiery, J.P. 2002. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer. 2:442-454.
47. Thiery, J.P., and R. Huang. 2005. Linking epithelial-mesenchymal transition to the well-known polarity protein Par6. Dev. Cell. 8:456-458.
48. Thompson, E.W., D.F. Newgreen, and D. Tarin. 2005. Carcinoma invasion and metastasis: a role for epithelial-mesenchymal transition? Cancer Res. 65:5991-5995.
49. Thomson, S., E. Buck, F. Petti, G. Griffin, E. Brown, N. Ramnarine, K.K. Iwata, N. Gibson, and J.D. Haley. 2005. Epithelial to mesenchymal transition is a determinant of sensitivity of non-small-cell lung carcinoma cell lines and xenografts to epidermal growth factor receptor inhibition. Cancer Res. 65:9455-9462.
50. van Es, J.H., N. Barker, and H. Clevers. 2003. You Wnt some, you lose some: oncogenes in the Wnt signaling pathway. Curr. Opin. Genet. Dev. 13:28-33.
51. Wang, Z., D. Shen, D.W. Parsons, A. Bardelli, J. Sager, S. Szabo, J. Ptak, N. Silliman, B.A. Peters, M.S. van der Heijden, et al. 2004. Mutational analysis of the tyrosine phosphatome in colorectal cancers. Science. 304:1164-1166.
52. Weaver, V.M., S. Lelievre, J.N. Lakins, M.A. Chrenek, J.C. Jones, F. Giancotti, Z. Werb, and M.J. Bissell. 2002. beta4 integrin-dependent formation of polarized three-dimensional architecture confers resistance to apoptosis in normal and malignant mammary epithelium. Cancer Cell. 2:205-216.
53. Willipinski-Stapelfeldt, B., S. Riethdorf, V. Assmann, U. Woelfl e, T. Rau, G. Sauter, J. Heukeshoven, and K. Pantel. 2005. Changes in cytoskeletal protein composition indicative of an epithelial-mesenchymal transition in human micrometastatic and primary breast carcinoma cells. Clin. Cancer Res. 11:8006-8014.
54. Xue, C., D. Plieth, C. Venkov, C. Xu, and E.G. Neilson. 2003. The gatekeeper effect of epithelial-mesenchymal transition regulates the frequency of breast cancer metastasis. Cancer Res. 63:3386-3394.
55. Yang, J., S.A. Mani, J.L. Donaher, S. Ramaswamy, R.A. Itzykson, C. Come, P. Savagner, I. Gitelman, A. Richardson, and R.A. Weinberg. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell. 117:927-939.
56. Zavadil, J., and E.P. Bottinger. 2005. TGF-beta and epithelial-to- mesenchymal transitions. Oncogene. 24:5764-5774.
57. Zavadil, J., L. Cermak, N. Soto-Nieves, and E.P. Bottinger. 2004. Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J. 23:1155-1165.
58. Zhou, B.P., J. Deng, W. Xia, J. Xu, Y.M. Li, M. Gunduz, and M.C. Hung. 2004. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat. Cell Biol. 6:931-940.