TGFβ3 signaling activates transcription of the LEF1 gene to induce epithelial mesenchymal transformation during mouse palate development

Journal of Cell Biology

Volumn 163, Issue 6, 2003, Pages 1291-1301

  Nawshad, Ali ^a   Hay, Elizabeth D ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

catenin; LEF1 transcription; Palate confluence; Smad pathways; Smad2

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; BETA CATENIN; LYMPHOID ENHANCER FACTOR 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; PHOSPHOPROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMAD4 PROTEIN; TRANSFORMING GROWTH FACTOR BETA3; CATNB PROTEIN, MOUSE; CYTOSKELETON PROTEIN; DNA BINDING PROTEIN; LEF1 PROTEIN, MOUSE; SMAD2 PROTEIN; SMAD2 PROTEIN, MOUSE; SMAD4 PROTEIN, MOUSE; TGFB3 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL TRANSFORMATION; EMBRYO; EMBRYO DEVELOPMENT; LASER MICRODISSECTION; MESENCHYME; MESSENGER RNA SYNTHESIS; MOUSE; NONHUMAN; PALATE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CELL DIFFERENTIATION; CELL NUCLEUS; CYTOLOGY; DRUG EFFECT; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MACROMOLECULE; MESODERM; METABOLISM; PREGNANCY; PRENATAL DEVELOPMENT; TRANSACTIVATION;

ANIMALIA;

ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELL NUCLEUS; CYTOSKELETAL PROTEINS; DNA-BINDING PROTEINS; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; LYMPHOID ENHANCER-BINDING FACTOR 1; MACROMOLECULAR SUBSTANCES; MESODERM; MICE; OLIGORIBONUCLEOTIDES, ANTISENSE; PALATE; PREGNANCY; RNA, MESSENGER; SMAD2 PROTEIN; SMAD4 PROTEIN; TRANS-ACTIVATION (GENETICS); TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA3; UP-REGULATION;

EID: 0346102460     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200306024     Document Type: Article

References (67)

1. Abdollah, S., M. Macias-Silva, T. Tsukazaki, H. Hayashi, L. Attisano, and J.L. Wrana. 1997. TβRI phosphorylation of Smad2 on Ser465 and Ser467 is required for Smad2-Smad4 complex formation and signaling. J. Biol. Chem. 272:27678-27685.
2. Adnane, J., E. Seijo, Z. Chen, F. Bizouarn, M. Leal, S.M. Sebti, and T. Munoz-Antonia. 2002. RhoB, not RhoA, represses the transcription of the transforming growth factor β type II receptor by a mechanism involving activator protein 1. J. Biol. Chem. 277:8500-8507.
3. Atcha, F.A., J.E. Munguia, T.W. Li, K. Hovanes, and M.L. Waterman. 2003. A new β-catenin-dependent activation domain in T cell factor. J. Biol. Chem. 278:16169-16175.
4. Attisano, L., and S. Tuen Lee-Hoeflich. 2001. The Smads. Genome Biol. 2:REVIEWS3010.
5. Behrens, J., J.P. von Kries, M. Kuhl, L. Bruhn, D. Wedlich, R. Grosschedl, and W. Birchmeier. 1996. Functional interaction of β-catenin with the transcription factor LEF-1. Nature. 382:638-642.
6. Bhowmick, N.A., M. Ghiassi, A. Bakin, M. Aakre, C.A. Lundquist, M.E. Engel, C.L. Arteaga, and H.L. Moses. 2001. Transforming growth factor-β1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell. 12:27-36.
7. Borbiev, T., S. Nurmukhambetova, F. Liu, A.D. Verin, and J.G. Garcia. 2000. Introduction of C3 exoenzyme into cultured endothelium by lipofectamine. Anal. Biochem. 285:260-264.
8. Boyer, A.S., C.P. Erickson, and R.B. Runyan. 1999. Epithelial-mesenchymal transformation in the embryonic heart is mediated through distinct pertussis toxin-sensitive and TGFβ signal transduction mechanisms. Dev. Dyn. 214:81-91.
9. Brunet, C.L., P.M. Sharpe, and M.W. Ferguson. 1995. Inhibition of TGF-β 3 (but not TGF-β 1 or TGF-β 2) activity prevents normal mouse embryonic palate fusion. Int. J. Dev. Biol. 39:345-355.
10. Cano, A., M.A. Perez-Moreno, I. Rodrigo, A. Locascio, M.J. Blanco, M.G. del Barrio, F. Portillo, and M.A. Nieto. 2000. The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2:76-83.
11. Chow, S., H. Patel, and D.W. Hedley. 2001. Measurement of MAP kinase activation by flow cytometry using phospho-specific antibodies to MEK and ERK: potential for pharmacodynamic monitoring of signal transduction inhibitors. Cytometry. 46:72-78.
12. Cohen, M.M., Jr. 2003. TGF β/Smad signaling system and its pathologic correlates. Am. J. Med. Genet. 116A:1-10.
13. Cui, X.M., and C.F. Shuler. 2000. The TGF-β type III receptor is localized to the medial edge epithelium during palatal fusion. Int. J. Dev. Biol. 44:397-402.
14. Cui, X.M., Y. Chai, J. Chen, T. Yamamoto, Y. Ito, P. Bringas, and C.F. Shuler. 2003. TGF-β3-dependent SMAD2 phosphorylation and inhibition of MEE proliferation during palatal fusion. Dev. Dyn. 227:387-394.
15. Dennler, S., M.J. Goumans, and P. ten Dijke. 2002. Transforming growth factor β signal transduction. J. Leukoc. Biol. 71:731-740.
16. Duan, D., Y. Yue, W. Zhou, B. Labed, T.C. Ritchie, R. Grosschedl, and J.F. Engelhardt. 1999. Submucosal gland development in the airway is controlled by lymphoid enhancer binding factor 1 (LEF1). Development. 126:4441-4453.
17. Eastman, Q., and R. Grosschedl. 1999. Regulation of LEF-1/TCF transcription factors by Wnt and other signals. Curr. Opin. Cell Biol. 11:233-240.
18. Eger, A., A. Stockinger, B. Schaffhauser, H. Beug, and R. Foisner. 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.
19. El-Tanani, M.K., R. Barraclough, M.C. Wilkinson, and P.S. Rudland. 2001. Regulatory region of metastasis-inducing DNA is the binding site for T cell factor-4. Oncogene. 20:1793-1797.
20. Favata, M.F., K.Y. Horiuchi, E.J. Manos, A.J. Daulerio, D.A. Stradley, W.S. Feeser, D.E. Van Dyk, W.J. Pitts, R.A. Earl, F. Hobbs, et al. 1998. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273:18623-18632.
21. Fitchett, J.E., and E.D. Hay. 1989. Medial edge epithelium transforms to mesenchyme after embryonic palatal shelves fuse. Dev. Biol. 131:455-474.
22. Griffith, C.M., and E.D. Hay. 1992. Epithelial-mesenchymal transformation during palatal fusion: carboxyfluorescein traces cells at light and electron microscopic levels. Development. 116:1087-1099.
23. Haertel-Wiesmann, M., Y. Liang, W.J. Fantl, and L.T. Williams. 2000. Regulation of cyclooxygenase-2 and periostin by Wnt-3 in mouse mammary epithelial cells. J. Biol. Chem. 275:32046-32051.
24. Hay, E.D. 1995. An overview of epithelio-mesenchymal transformation. Acta. Anat. (Basel). 154:8-20.
25. Hay, E.D. 2003. Rise and fall of epithelial phenotype. In EMT Concept and Examples from the Vertebrate Embryo. P. Savagner, editor. Landes Bioscience, Georgetown, TX. In press.
26. He, T.C., S. Zhou, L.T. da Costa, J. Yu, K.W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA. 95:2509-2514.
27. Ishitani, T., J. Ninomiya-Tsuji, and K. Matsumoto. 2003. Regulation of lymphoid enhancer factor 1/T-cell factor by mitogen-activated protein kinase-related Nemo-like kinase-dependent phosphorylation in Wnt/β-catenin signaling. Mol. Cell. Biol. 23:1379-1389.
28. Itoh, F., N. Divecha, L. Brocks, L. Oomen, H. Janssen, J. Calafat, S. Itoh, and P. ten Dijke. 2002. The FYVE domain in Smad anchor for receptor activation (SARA) is sufficient for localization of SARA in early endosomes and regulates TGF-β/Smad signalling. Genes Cells. 7:321-331.
29. Itoh, S., M. Thorikay, M. Kowanetz, A. Moustakas, F. Itoh, C.H. Heldin, and P. ten Dijke. 2003. Elucidation of Smad requirement in transforming growth factor-β type 1 receptor-induced responses. J. Biol. Chem. 278:3751-3761.
30. Janda, E., K. Lehmann, I. Killisch, M. Jechlinger, M. Herzig, J. Downward, H. Beug, and S. Grunert. 2002. Ras and TGFβ cooperatively regulate epithelial cell plasticity and metastasis: dissection of Ras signaling pathways. J. Cell Biol. 156:299-313.
31. Kaartinen, V., J.W. Voncken, C. Shuler, D. Warburton, D. Bu, N. Heisterkamp, and J. Groffen. 1995. Abnormal lung development and cleft palate in mice lacking TGF-β 3 indicates defects of epithelial-mesenchymal interaction. Nat. Genet. 11:415-421.
32. Kaartinen, V., L. Haataja, A. Nagy, N. Heisterkamp, and J. Groffen. 2002. TGFβ3-induced activation of RhoA/Rho-kinase pathway is necessary but not sufficient for epithelio-mesenchymal transdifferentiation: implications for palatogenesis. Int. J. Mol. Med. 9:563-570.
33. Kang, P., and K.K. Svoboda. 2002. PI-3 kinase activity is required for epithelial-mesenchymal transformation during palate fusion. Dev. Dyn. 225:316-321.
34. Kim, K., and E.D. Hay. 2001. New evidence that nuclear import of endogenous β-catenin is LEF-1 dependent, while LEF-1 independent import of exogenous β-catenin leads to nuclear abnormalities. Cell Biol. Int. 25:1149-1161.
35. Kim, K., Z. Lu, and E.D. Hay. 2002. Direct evidence for a role of β-catenin/LEF-1 signaling pathway in induction of EMT. Cell Biol. Int. 26:463-476.
36. Kretzschmar, M., J. Doody, I. Timokhina, and J. Massague. 1999. A mechanism of repression of TGFβ/Smad signaling by oncogenic Ras. Genes Dev. 13:804-816.
37. Labbe, E., A. Letamendia, and L. Attisano. 2000. Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-β and wnt pathways. Proc. Natl. Acad. Sci. USA. 97:8358-8363.
38. Lin, H.Y., X.F. Wang, E. Ng-Eaton, R.A. Weinberg, and H.F. Lodish. 1992. Expression cloning of the TGF-β type II receptor, a functional transmembrane serine/threonine kinase. Cell. 68:775-785.
39. Liu, X., F.Q. Wen, T. Kobayashi, S. Abe, Q. Fang, E. Piek, E.P. Bottinger, A.B. Roberts, and S.I. Rennard. 2003. Smad3 mediates the TGF-β-induced contraction of type 1 collagen gels by mouse embryo fibroblasts. Cell Motil. Cytoskeleton. 54:248-253.
40. Lu, J., T.E. Landerholm, J.S. Wei, X.R. Dong, S.P. Wu, X. Liu, K. Nagata, M. Inagaki, and M.W. Majesky. 2001. Coronary smooth muscle differentiation from proepicardial cells requires rhoA-mediated actin reorganization and p160 rho-kinase activity. Dev. Biol. 240:404-418.
41. Lutz, M., and P. Knaus. 2002. Integration of the TGF-β pathway into the cellular signalling network. Cell. Signal. 14:977-988.
42. Miettinen, P.J., R. Ebner, A.R. Lopez, and R. Derynck. 1994. TGF-β induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J. Cell Biol. 127:2021-2036.
43. Morin, P.J., A.B. Sparks, V. Korinek, N. Barker, H. Clevers, B. Vogelstein, and K.W. Kinzler. 1997. Activation of β-catenin-Tcf signaling in colon cancer by mutations in β-catenin or APC. Science. 275:1787-1790.
44. Mulder, K.M. 2000. Role of Ras and Mapks in TGFβ signaling. Cytokine Growth Factor Rev. 11:23-35.
45. Nakajima, Y., E.L. Krug, and R.R. Markwald. 1994. Myocardial regulation of transforming growth factor-β expression by outflow tract endothelium in the early embryonic chick heart. Dev. Biol. 165:615-626.
46. Nishita, M., M.K. Hashimoto, S. Ogata, M.N. Laurent, N. Ueno, H. Shibuya, and K.W. Cho. 2000. Interaction between Wnt and TGF-β signalling pathways during formation of Spemann's organizer. Nature. 403:781-785.
47. Novak, A., S.C. Hsu, C. Leung-Hagesteijn, G. Radeva, J. Papkoff, R. Montesano, C. Roskelley, R. Grosschedl, and S. Dedhar. 1998. Cell adhesion and the integrin-linked kinase regulate the LEF-1 and β-catenin signaling pathways. Proc. Natl. Acad. Sci. USA. 95:4374-4379.
48. Oft, M., K.H. Heider, and H. Beug. 1998. TGFβ signaling is necessary for carcinoma cell invasiveness and metastasis. Curr. Biol. 8:1243-1252.
49. Panopoulou, E., D.J. Gillooly, J.L. Wrana, M. Zerial, H. Stenmark, C. Murphy, and T. Fotsis. 2002. Early endosomal regulation of Smad-dependent signaling in endothelial cells. J. Biol. Chem. 277:18046-18052.
50. Piek, E., A. Moustakas, A. Kurisaki, C.H. Heldin, and P. ten Dijke. 1999. TGF-β type 1 receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J. Cell Sci. 112:4557-4568.
51. Proetzel, G., S.A. Pawlowski, M.V. Wiles, M. Yin, G.P. Boivin, P.N. Howles, J. Ding, M.W. Ferguson, and T. Doetschman. 1995. Transforming growth factor-β 3 is required for secondary palate fusion. Nat. Genet. 11:409-414.
52. Roberts, A.B. 2002. The ever-increasing complexity of TGF-β signaling. Cytokine Growth Factor Rev. 13:3-5.
53. Runyan, R.B., J.D. Potts, and D.L. Weeks. 1992. TGF-β 3-mediated tissue interaction during embryonic heart development. Mol. Reprod. Dev. 32:152-159.
54. Sasaki, T., H. Suzuki, K. Yagi, M. Furuhashi, R. Yao, S. Susa, T. Noda, Y. Arai, K. Miyazono, and M. Kato. 2003. Lymphoid enhancer factor 1 makes cells resistant to transforming growth factor β-induced repression of c-myc. Cancer Res. 63:801-806.
55. Scanlan, M.J., C.M. Gordon, B. Williamson, S.Y. Lee, Y.T. Chen, E. Stockert, A. Jungbluth, G. Ritter, D. Jager, E. Jager, et al. 2002. Identification of cancer/ testis genes by database mining and mRNA expression analysis. Int. J. Cancer. 98:485-492.
56. Shuler, C.F., D.E. Halpern, Y. Guo, and A.C. Sank. 1992. Medial edge epithelium fate traced by cell lineage analysis during epithelial-mesenchymal transformation in vivo. Dev. Biol. 154:318-330.
57. Smith, P.G., C. Roy, Y.N. Zhang, and S. Chauduri. 2003. Mechanical stress increases RhoA activation in airway smooth muscle cells. Am. J. Respir. Cell Mol. Biol. 28:436-442.
58. Sun, D., C.R. Vanderburg, G.S. Odierna, and E.D. Hay. 1998. TGFβ3 promotes transformation of chicken palate medial edge epithelium to mesenchyme in vitro. Development. 125:95-105.
59. Sun, D., C.M. Griffith, and E.D. Hay. 2000. Carboxyfluorescein as a marker at both light and electron microscope levels to follow cell lineage in the embryo. Methods Mol. Biol. 135:357-363.
60. Ten Dijke, P., M.J. Goumans, F. Itoh, and S. Itoh. 2002. Regulation of cell proliferation by Smad proteins. J. Cell. Physiol. 191:1-16.
61. Tsukazaki, T., T.A. Chiang, A.F. Davison, L. Attisano, and J.L. Wrana. 1998. SARA, a FYVE domain protein that recruits Smad2 to the TGFβ receptor. Cell. 95:779-791.
62. Wilde, C., H. Barth, P. Sehr, L. Han, M. Schmidt, I. Just, and K. Aktories. 2002. Interaction of the Rho-ADP-ribosylating C3 exoenzyme with RalA. J. Biol. Chem. 277:14771-14776.
63. Wrana, J.L., L. Attisano, J. Carcamo, A. Zentella, J. Doody, M. Laiho, X.F. Wang, and J. Massague. 1992. TGF β signals through a heteromeric protein kinase receptor complex. Cell. 71:1003-1014.
64. Yu, L., M.C. Hebert, and Y.E. Zhang. 2002. TGF-β receptor-activated p38 MAP kinase mediates Smad-independent TGF-β responses. EMBO J. 21:3749-3759.
65. Zavadil, J., M. Bitzer, D. Liang, Y.C. Yang, A. Massimi, S. Kneitz, E. Piek, and E.P. Bottinger. 2001. Genetic programs of epithelial cell plasticity directed by transforming growth factor-β. Proc. Natl. Acad. Sci. USA. 98:6686-6691.
66. Zhang, L., K. Graziano, T. Pham, C.D. Logsdon, and D.M. Simeone. 2001. Adenovirus-mediated gene transfer of dominant-negative Smad4 blocks TGF-β signaling in pancreatic acinar cells. Am. J. Physiol. Gastrointest. Liver Physiol. 280:G1247-G1253.
67. Zubiaur, M., J. Sancho, C. Terhorst, and D.V. Faller. 1995. A small GTP-binding protein, Rho, associates with the platelet-derived growth factor type-β receptor upon ligand binding. J. Biol. Chem. 270:17221-17228.