Interactions between β-catenin and transforming growth factor-β signaling pathways mediate epithelial- mesenchymal transition and are dependent on the transcriptional co-activator cAMP-response element-binding protein (CREB)-binding protein (CBP)

Journal of Biological Chemistry

Volumn 287, Issue 10, 2012, Pages 7026-7038

  Zhou, Beiyun ^a   Liu, Yixin ^a   Kahn, Michael ^b   Ann, David K ^c   Han, Arum ^a   Wang, Hongjun ^a   Nguyen, Cu ^b   Flodby, Per ^a   Zhong, Qian ^a   Krishnaveni, Manda S ^a   Liebler, Janice M ^a   Minoo, Parviz ^a   Crandall, Edward D ^a   Borok, Zea ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALVEOLAR EPITHELIAL CELLS; BINDING PROTEINS; BIOLOGICAL PROCESS; CAMP-RESPONSE ELEMENT-BINDING PROTEINS; CHROMATIN IMMUNOPRECIPITATION; CO-IMMUNOPRECIPITATIONS; COLOCALIZATION; COMPLEX FORMATIONS; DIRECT INTERACTIONS; EPITHELIAL PROLIFERATION; EPITHELIAL-MESENCHYMAL TRANSITION; OVER-EXPRESSION; PULMONARY FIBROSIS; SIGNALING PATHWAYS; SMALL MOLECULES; SMOOTH MUSCLE ACTINS; SPECIFIC INHIBITORS; TRANSCRIPTIONAL CO-ACTIVATORS; TRANSFORMING GROWTH FACTORS;

CHEMICAL ACTIVATION; PROTEINS; SIGNALING;

PIGMENTS;

ALPHA SMOOTH MUSCLE ACTIN; BETA CATENIN; COLLAGEN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; SMAD3 PROTEIN; T CELL FACTOR PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA1; WNT PROTEIN;

ADULT; ALPHA SMOOTH MUSCLE ACTIN GENE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE; HUMAN; HUMAN TISSUE; LUNG ALVEOLUS EPITHELIUM; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION;

ACTINS; BETA CATENIN; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL LINE; CELL PROLIFERATION; CREB-BINDING PROTEIN; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; HUMANS; PULMONARY FIBROSIS; PYRIMIDINONES; SIGNAL TRANSDUCTION; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84863229401     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.276311     Document Type: Article

References (59)

1. Whitman, M. (1998) Smads and early developmental signaling by the TGFβ superfamily. Genes Dev. 12, 2445-2462
2. Labbé, E., Lock, L., Letamendia, A., Gorska, A. E., Gryfe, R., Gallinger, S., Moses, H. L., and Attisano, L. (2007) Transcriptional cooperation between the transforming growth factor-β and Wnt pathways in mammary and intestinal tumorigenesis. Cancer Res. 67, 75-84 (Pubitemid 46142761)
3. Nishita, M., Hashimoto, M. K., Ogata, S., Laurent, M. N., Ueno, N., Shibuya, H., and Cho, K. W. (2000) Interaction between Wnt and TGF-βsignaling pathways during formation of Spemann's organizer. Nature 403, 781-785 (Pubitemid 30111840)
4. Labbé, E., Letamendia, A., and Attisano, L. (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. U.S.A. 97, 8358-8363 (Pubitemid 30639677)
5. Furuhashi, M., Yagi, K., Yamamoto, H., Furukawa, Y., Shimada, S., Nakamura, Y., Kikuchi, A., Miyazono, K., and Kato, M. (2001) Axin facilitates Smad3 activation in the transforming growth factor β signaling pathway. Mol. Cell. Biol. 21, 5132-5141 (Pubitemid 32656409)
6. Tian, X., Du, H., Fu, X., Li, K., Li, A., and Zhang, Y. (2009) Smad4 restoration leads to a suppression of Wnt/β-catenin signaling activity and migration capacity in human colon carcinoma cells. Biochem. Biophys. Res. Commun. 380, 478-483
7. Dong, Y., Drissi, H., Chen, M., Chen, D., Zuscik, M. J., Schwarz, E. M., and O'Keefe, R. J. (2005) Wnt-mediated regulation of chondrocyte maturation: modulation by TGF-β. J. Cell. Biochem. 95, 1057-1068 (Pubitemid 41420151)
8. Minoo, P., and Li, C. (2010) Cross-talk between transforming growth factor-β and Wingless/Int pathways in lung development and disease. Int J Biochem. Cell Biol. 42, 809-812
9. Lei, S., Dubeykovskiy, A., Chakladar, A., Wojtukiewicz, L., and Wang, T. C. (2004) The murine gastrin promoter is synergistically activated by transforming growth factor-β/Smad and Wnt signaling pathways. J. Biol. Chem. 279, 42492-42502 (Pubitemid 39372133)
10. Masszi, A., Fan, L., Rosivall, L., McCulloch, C. A., Rotstein, O. D., Mucsi, I., and Kapus, A. (2004) Integrity of cell-cell contacts is a critical regulator of TGF-β1-induced epithelial-to-myofibroblast transition: role for β-catenin. Am. J. Pathol. 165, 1955-1967 (Pubitemid 39578374)
11. Tian, Y. C., and Phillips, A. O. (2002) Interaction between the transforming growth factor-β type II receptor/Smad pathway and β-catenin during transforming growth factor-β1-mediated adherens junction disassembly. Am. J. Pathol. 160, 1619-1628 (Pubitemid 34525642)
12. Kim, Y., Kugler, M. C., Wei, Y., Kim, K. K., Li, X., Brumwell, A. N., and Chapman, H. A. (2009) Integrin α3β1-dependent β-catenin phosphorylation links epithelial Smad signaling to cell contacts. J. Cell Biol. 184, 309-322
13. Thiery, J. P., and Sleeman, J. P. (2006) Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142 (Pubitemid 43278296)
14. Zavadil, J., and Böttinger, E. P. (2005) TGF-β and epithelial-to-mesenchymal transitions. Oncogene 24, 5764-5774
15. Thiery, J. P., Acloque, H., Huang, R. Y., and Nieto, M. A. (2009) Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890
16. Willis, B. C., Liebler, J. M., Luby-Phelps, K., Nicholson, A. G., Crandall, E. D., du Bois, R. M., and Borok, Z. (2005) Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor- β1: potential role in idiopathic pulmonary fibrosis. Am. J. Pathol. 166, 1321-1332 (Pubitemid 40586504)
17. Tanjore, H., Xu, X. C., Polosukhin, V. V., Degryse, A. L., Li, B., Han, W., Sherrill, T. P., Plieth, D., Neilson, E. G., Blackwell, T. S., and Lawson, W. E. (2009) Contribution of epithelial-derived fibroblasts to bleomycin-induced lung fibrosis. Am. J. Respir. Crit. Care Med. 180, 657-665
18. Kim, K. K., Kugler, M. C., Wolters, P. J., Robillard, L., Galvez, M. G., Brumwell, A. N., Sheppard, D., and Chapman, H. A. (2006) Alveolar epithelial cell mesenchymal transition develops in vivo during pulmonary fibrosis and is regulated by the extracellular matrix. Proc. Natl. Acad. Sci. U.S.A. 103, 13180-13185 (Pubitemid 44338936)
19. Sime, P. J., Xing, Z., Graham, F. L., Csaky, K. G., and Gauldie, J. (1997) Adenovector-mediated gene transfer of active transforming growth factor- β1 induces prolonged severe fibrosis in rat lung. J. Clin. Invest. 100, 768-776 (Pubitemid 27371693)
20. Roberts, A. B., Tian, F., Byfield, S. D., Stuelten, C., Ooshima, A., Saika, S., and Flanders, K. C. (2006) Smad3 is key to TGF-β-mediated epithelial-tomesenchymal transition, fibrosis, tumor suppression, and metastasis. Cytokine Growth Factor Rev. 17, 19-27 (Pubitemid 43117513)
21. Willis, B. C., and Borok, Z. (2007) TGF-β-induced EMT: mechanisms and implications for fibrotic lung disease. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L525-L534 (Pubitemid 47358808)
22. Bergeron, A., Soler, P., Kambouchner, M., Loiseau, P., Milleron, B., Valeyre, D., Hance, A. J., and Tazi, A. (2003) Cytokine profiles in idiopathic pulmonary fibrosis suggest an important role for TGF-beta and IL-10. Eur. Respir. J. 22, 69-76 (Pubitemid 36896473)
23. Khalil, N., Parekh, T. V., O'Connor, R., Antman, N., Kepron, W., Yehaulaeshet, T., Xu, Y. D., and Gold, L. I. (2001) Regulation of the effects of TGF-β1 by activation of latent TGF-β1 and differential expression of TGF-β receptors (TβR-I and TβR-II) in idiopathic pulmonary fibrosis. Thorax 56, 907-915 (Pubitemid 33097184)
24. Shi, Y., and Massagué, J. (2003) Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700 (Pubitemid 36724933)
25. Flanders, K. C. (2004) Smad3 as a mediator of the fibrotic response. Int. J. Exp. Pathol. 85, 47-64
26. Valcourt, U., Kowanetz, M., Niimi, H., Heldin, C. H., and Moustakas, A. (2005) TGF-β and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol. Biol. Cell 16, 1987-2002 (Pubitemid 40471965)
27. Masszi, A., Speight, P., Charbonney, E., Lodyga, M., Nakano, H., Szászi, K., and Kapus, A. (2010) Fate-determining mechanisms in epithelial-myofibroblast transition: major inhibitory role for Smad3. J. Cell Biol. 188, 383-399
28. Kim, K., Lu, Z., and Hay, E. D. (2002) Direct evidence for a role of β-catenin/LEF-1 signaling pathway in induction of EMT. Cell Biol. Int 26, 463-476 (Pubitemid 34762099)
29. LaGamba, D., Nawshad, A., and Hay, E. D. (2005) Microarray analysis of gene expression during epithelial-mesenchymal transformation. Dev Dyn 234, 132-142 (Pubitemid 41192757)
30. Moustakas, A., and Heldin, C. H. (2007) Signaling networks guiding epithelial- mesenchymal transitions during embryogenesis and cancer progression. Cancer Sci 98, 1512-1520 (Pubitemid 47308444)
31. Chilosi, M., Poletti, V., Zamò, A., Lestani, M., Montagna, L., Piccoli, P., Pedron, S., Bertaso, M., Scarpa, A., Murer, B., Cancellieri, A., Maestro, R., Semenzato, G., and Doglioni, C. (2003) Aberrant Wnt/β-catenin pathway activation in idiopathic pulmonary fibrosis. Am. J. Pathol. 162, 1495-1502 (Pubitemid 36512831)
32. Königshoff, M., Balsara, N., Pfaff, E. M., Kramer, M., Chrobak, I., Seeger, W., and Eickelberg, O. (2008) Functional Wnt signaling is increased in idiopathic pulmonary fibrosis. PLoS One 3, e2142
33. Königshoff, M., Kramer, M., Balsara, N., Wilhelm, J., Amarie, O. V., Jahn, A., Rose, F., Fink, L., Seeger, W., Schaefer, L., Günther, A., and Eickelberg, O. (2009) WNT1-inducible signaling protein-1 mediates pulmonary fibrosis in mice and is upregulated in humans with idiopathic pulmonary fibrosis. J. Clin. Invest. 119, 772-787
34. Yang, I. V., Burch, L. H., Steele, M. P., Savov, J. D., Hollingsworth, J. W., McElvania-Tekippe, E., Berman, K. G., Speer, M. C., Sporn, T. A., Brown, K. K., Schwarz, M. I., and Schwartz, D. A. (2007) Gene expression profiling of familial and sporadic interstitial pneumonia. Am. J. Respir. Crit. Care Med. 175, 45-54 (Pubitemid 46105308)
35. Selman, M., Pardo, A., Barrera, L., Estrada, A., Watson, S. R., Wilson, K., Aziz, N., Kaminski, N., and Zlotnik, A. (2006) Gene expression profiles distinguish idiopathic pulmonary fibrosis from hypersensitivity pneumonitis. Am. J. Respir. Crit. Care Med. 173, 188-198 (Pubitemid 43187891)
36. Königshoff, M., and Eickelberg, O. (2010) WNT signaling in lung disease: a failure or a regeneration signal? Am. J. Respir. Cell Mol. Biol. 42, 21-31
37. Medici, D., Hay, E. D., and Olsen, B. R. (2008) Snail and Slug promote epithelial-mesenchymal transition through β-catenin-T-cell factor-4-dependent expression of transforming growth factor-β3. Mol. Biol. Cell 19, 4875-4887
38. Nawshad, A., Medici, D., Liu, C. C., and Hay, E. D. (2007) TGFβ3 inhibits E-cadherin gene expression in palate medial-edge epithelial cells through a Smad2-Smad4-LEF1 transcription complex. J. Cell Sci. 120, 1646-1653 (Pubitemid 46831794)
39. Kim, K. K., Wei, Y., Szekeres, C., Kugler, M. C., Wolters, P. J., Hill, M. L., Frank, J. A., Brumwell, A. N., Wheeler, S. E., Kreidberg, J. A., and Chapman, H. A. (2009) Epithelial cell α3β1 integrin links β-catenin and Smad signaling to promote myofibroblast formation and pulmonary fibrosis. J. Clin. Invest. 119, 213-224
40. Henderson, W. R., Jr., Chi, E. Y., Ye, X., Nguyen, C., Tien, Y. T., Zhou, B., Borok, Z., Knight, D. A., and Kahn, M. (2010) Inhibition of Wnt/β- catenin/CREB-binding protein (CBP) signaling reverses pulmonary fibrosis. Proc. Natl. Acad. Sci. U.S.A. 107, 14309-14314
41. Zhou, B., Zhong, Q., Minoo, P., Li, C., Ann, D. K., Frenkel, B., Morrisey, E. E., Crandall, E. D., and Borok, Z. (2008) Foxp2 inhibits Nkx2.1-mediated transcription of SP-C via interactions with the Nkx2.1 homeodomain. Am. J. Respir. Cell Mol. Biol. 38, 750-758 (Pubitemid 351841578)
42. Han, M. K., Swigris, J., Liu, L., Bartholmai, B., Murray, S., Giardino, N., Thompson, B., Frederick, M., Li, D., Schwarz, M., Limper, A., Flaherty, K., and Martinez, F. J. (2010) Gender influences health-related quality of life in IPF. Respiratory Med. 104, 724-730
43. Klein, P. S., and Melton, D. A. (1996)Amolecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. U.S.A. 93, 8455-8459 (Pubitemid 26269579)
44. Kiela, P. R., LeSueur, J., Collins, J. F., and Ghishan, F. K. (2003) Transcriptional regulation of the rat NHE3 gene. Functional interactions between GATA-5 and Sp family transcription factors. J. Biol. Chem. 278, 5659-5668 (Pubitemid 36800809)
45. Gottardi, C. J., and Gumbiner, B. M. (2004) Role for ICAT in β-catenin-dependent nuclear signaling and cadherin functions. Am. J. Physiol. Cell Physiol. 286, C747-C756 (Pubitemid 38543802)
46. Staal, F. J., Noort Mv, M., Strous, G. J., and Clevers, H. C. (2002) Wnt signals are transmitted through N-terminally dephosphorylated β-catenin. EMBO Reports 3, 63-68 (Pubitemid 34144817)
47. van Noort, M., Weerkamp, F., Clevers, H. C., and Staal, F. J. (2007) Wnt signaling and phosphorylation status of β-catenin: importance of the correct antibody tools. Blood 110, 2778-2779 (Pubitemid 47523216)
48. Ma, H., Nguyen, C., Lee, K. S., and Kahn, M. (2005) Differential roles for the coactivators CBP and p300 on TCF/β-catenin-mediated survivin gene expression. Oncogene 24, 3619-3631 (Pubitemid 40756231)
49. Felton, V. M., Borok, Z., and Willis, B. C. (2009) N-acetylcysteine inhibits alveolar epithelial-mesenchymal transition. Am. J. Physiol. Lung Cell Mol. Physiol. 297, L805-L812
50. Jinnin, M., Ihn, H., and Tamaki, K. (2006) Characterization of SIS3, a novel specific inhibitor of Smad3, and its effect on transforming growth factor- β1-induced extracellular matrix expression. Mol. Pharmacol. 69, 597-607 (Pubitemid 43121957)
51. Hu, B., Wu, Z., and Phan, S. H. (2003) Smad3 mediates transforming growth factor-β-induced α-smooth muscle actin expression. Am. J. Respir. Cell Mol. Biol. 29, 397-404 (Pubitemid 37093999)
52. Kawasaki, H., Eckner, R., Yao, T. P., Taira, K., Chiu, R., Livingston, D. M., and Yokoyama, K. K. (1998) Distinct roles of the co-activators p300 and CBP in retinoic-acid-induced F9-cell differentiation. Nature 393, 284-289 (Pubitemid 28261730)
53. Roth, J. F., Shikama, N., Henzen, C., Desbaillets, I., Lutz, W., Marino, S., Wittwer, J., Schorle, H., Gassmann, M., and Eckner, R. (2003) Differential role of p300 and CBP acetyltransferase during myogenesis: p300 acts upstream of MyoD and Myf5. EMBO J. 22, 5186-5196 (Pubitemid 37222038)
54. Kalkhoven, E. (2004) CBP and p300: HATs for different occasions. Biochem. Pharmacol. 68, 1145-1155
55. Emami, K. H., Nguyen, C., Ma, H., Kim, D. H., Jeong, K. W., Eguchi, M., Moon, R. T., Teo, J. L., Oh, S. W., Kim, H. Y., Moon, S. H., Ha, J. R., and Kahn, M. (2004) A small molecule inhibitor of β-catenin/CREB-binding protein transcription. Proc. Natl. Acad. Sci. U.S.A. 101, 12682-12687 (Pubitemid 39122083)
56. Brown, K. A., Pietenpol, J. A., and Moses, H. L. (2007) A tale of two proteins: differential roles and regulation of Smad2 and Smad3 in TGF-βsignaling. J. Cell. Biochem. 101, 9-33 (Pubitemid 46652569)
57. Flanders, K. C., Major, C. D., Arabshahi, A., Aburime, E. E., Okada, M. H., Fujii, M., Blalock, T. D., Schultz, G. S., Sowers, A., Anzano, M. A., Mitchell, J. B., Russo, A., and Roberts, A. B. (2003) Interference with transforming growth factor-β/ Smad3 signaling results in accelerated healing of wounds in previously irradiated skin. Am. J. Pathol. 163, 2247-2257 (Pubitemid 37466469)
58. Kasai, H., Allen, J. T., Mason, R. M., Kamimura, T., and Zhang, Z. (2005) TGF-β1 induces human alveolar epithelial to mesenchymal cell transition (EMT). Respir Res 6, 56
59. Li, M., Krishnaveni, M. S., Li, C., Zhou, B., Xing, Y., Banfalvi, A., Li, A., Lombardi, V., Akbari, O., Borok, Z., and Minoo, P. (2011) Epitheliumspecific deletion of TGF-β receptor type II protects mice from bleomycininduced pulmonary fibrosis. J. Clin. Invest. 121, 277-287