Association of β-catenin with P-Smad3 but not LEF-1 dissociates in vitro profibrotic from anti-inflammatory effects of TGF-β1

Journal of Cell Science

Volumn 126, Issue 1, 2013, Pages 67-76

  Tian, Xinrui ^a,b   Zhang, Jianlin ^a,b   Tan, Thian Kui ^a   Lyons, Guy ^c   Zhao, Hong ^a,b   Niu, Bo ^d   Lee, So Ra ^a   Tsatralis, Tania ^a   Zhao, Ye ^a   Wang, Ya ^a   Cao, Qi ^a   Wang, Changqi ^a   Wang, Yiping ^a   Lee, Vincent ^a   Kahn, Michael ^e   Zheng, Guoping ^a   Harris, David C H ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b SHANXI MEDICAL UNIVERSITY   (China)

^c ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^d CAPITAL INSTITUTE OF PEDIATRICS   (China)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Catenin; Epithelial mesenchymal transition; Fibrosis; Inflammation; P Smad3; TGF 1

Indexed keywords

BETA CATENIN; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; LYMPHOID ENHANCER FACTOR 1; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; WNT PROTEIN;

ANIMAL CELL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CELL LINE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FIBROSIS; GENE SILENCING; KIDNEY TUBULE EPITHELIUM; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

ANIMALS; ANTI-INFLAMMATORY AGENTS; BETA CATENIN; BLOTTING, WESTERN; CELL LINE; EPITHELIAL-MESENCHYMAL TRANSITION; IMMUNOPRECIPITATION; LYMPHOID ENHANCER-BINDING FACTOR 1; MICE; MICROSCOPY, FLUORESCENCE; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84875626228     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.103036     Document Type: Article

References (47)

1. Bienz, M. (2005). beta-Catenin: a pivot between cell adhesion and Wnt signalling. Curr. Biol. 15, R64-R67.
2. Blobe, G. C., Schiemann, W. P. and Lodish, H. F. (2000). Role of transforming growth factor beta in human disease. N. Engl. J. Med. 342, 1350-1358.
3. Bogdan, C., Paik, J., Vodovotz, Y. and Nathan, C. (1992). Contrasting mechanisms for suppression of macrophage cytokine release by transforming growth factor-beta and interleukin-10. J. Biol. Chem. 267, 23301-23308.
4. Borok, Z. (2009). Role for alpha3 integrin in EMT and pulmonary fibrosis. J. Clin. Invest. 119, 7-10.
5. Buchert, M., Athineos, D., Abud, H. E., Burke, Z. D., Faux, M. C., Samuel, M. S., Jarnicki, A. G., Winbanks, C. E., Newton, I. P., Meniel, V. S. et al. (2010). Genetic dissection of differential signaling threshold requirements for the Wnt/beta-catenin pathway in vivo. PLoS Genet. 6, e1000816.
6. Chilosi, M., Poletti, V., Zamò, A., Lestani, M., Montagna, L., Piccoli, P., Pedron, S., Bertaso, M., Scarpa, A., Murer, B. et al. (2003). Aberrant Wnt/beta-catenin pathway activation in idiopathic pulmonary fibrosis. Am. J. Pathol. 162, 1495-1502.
7. Chun, T. Y., Chander, P. N., Kim, J. W., Pratt, J. H. and Stier, C. T., Jr (2008).Aldosterone, but not angiotensin II, increases profibrotic factors in kidney of adrenalectomized stroke-prone spontaneously hypertensive rats. Am. J. Physiol. Endocrinol. Metab. 295, E305-E312.
8. Cobas, M., Wilson, A., Ernst, B., Mancini, S. J., MacDonald, H. R., Kemler, R. and Radtke, F. (2004). Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J. Exp. Med. 199, 221-229.
9. Cong, F., Zhang, J., Pao, W., Zhou, P. and Varmus, H. (2003). A protein knockdown strategy to study the function of beta-catenin in tumorigenesis. BMC Mol. Biol. 4, 10.
10. Douglas, I. S., Diaz del Valle, F., Winn, R. A. and Voelkel, N. F. (2006). Beta-catenin in the fibroproliferative response to acute lung injury. Am. J. Respir. Cell Mol. Biol. 34, 274-285.
11. Fuxe, J., Vincent, T. and de Herreros, A. G. (2010). Transcriptional crosstalk between TGFbeta and stem cell pathways in tumor cell invasion: Role of EMT promoting Smad complexes. Cell Cycle 9, 2363-2374.
12. Guo, X. and Wang, X. F. (2009). Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res. 19, 71-88.
13. 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/beta-catenin/CREB binding protein (CBP) signaling reverses pulmonary fibrosis. Proc. Natl. Acad. Sci. USA 107, 14309-14314.
14. Hewitson, T. D. (2009). Renal tubulointerstitial fibrosis: common but never simple. Am. J. Physiol. Renal Physiol. 296, F1239-F1244.
15. Holian, J., Qi, W., Kelly, D. J., Zhang, Y., Mreich, E., Pollock, C. A. and Chen, X. M. (2008). Role of Kruppel-like factor 6 in transforming growth factor-beta1- induced epithelial-mesenchymal transition of proximal tubule cells. Am. J. Physiol. Renal Physiol. 295, F1388-F1396.
16. Hu, D., Fang, W., Han, A., Gallagher, L., Davis, R. J., Xiong, B. and Yang, W. (2008). c-Jun N-terminal kinase 1 interacts with and negatively regulates Wnt/ beta-catenin signaling through GSK3beta pathway. Carcinogenesis 29, 2317-2324.
17. Huber, A. H., Stewart, D. B., Laurents, D. V., Nelson, W. J. and Weis, W. I. (2001). The cadherin cytoplasmic domain is unstructured in the absence of beta-catenin. A possible mechanism for regulating cadherin turnover. J. Biol. Chem. 276, 12301-12309.
18. Humphreys, B. D., Lin, S. L., Kobayashi, A., Hudson, T. E., Nowlin, B. T., Bonventre, J. V., Valerius, M. T., McMahon, A. P. and Duffield, J. S. (2010). Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis. Am. J. Pathol. 176, 85-97.
19. Iwano, M., Plieth, D., Danoff, T. M., Xue, C., Okada, H. and Neilson, E. G. (2002). Evidence that fibroblasts derive from epithelium during tissue fibrosis. J. Clin. Invest. 110, 341-350.
20. Kim, K., Lu, Z. and Hay, E. D. (2002). Direct evidence for a role of beta-catenin/LEF-1 signaling pathway in induction of EMT. Cell Biol. Int. 26, 463-476.
21. 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. et al. (2009a). Epithelial cell alpha3beta1 integrin links beta-catenin and Smad signaling to promote myofibroblast formation and pulmonary fibrosis. J. Clin. Invest. 119, 213-224.
22. Kim, Y., Kugler, M. C., Wei, Y., Kim, K. K., Li, X., Brumwell, A. N. and Chapman, H. A. (2009b). Integrin alpha3beta1-dependent beta-catenin phosphorylation links epithelial Smad signaling to cell contacts. J. Cell Biol. 184, 309-322.
23. Kudo-Saito, C., Shirako, H., Takeuchi, T. and Kawakami, Y. (2009). Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell 15, 195-206.
24. Lan, H. Y. (2003). Tubular epithelial-myofibroblast transdifferentiation mechanisms in proximal tubule cells. Curr. Opin. Nephrol. Hypertens. 12, 25-29.
25. Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A. K. and Flavell, R. A. (2006). Transforming growth factor-beta regulation of immune responses. Annu. Rev. Immunol. 24, 99-146.
26. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
27. Massagué, J. (2000). How cells read TGF-beta signals. Nat. Rev. Mol. Cell Biol. 1, 169-178.
28. 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-beta 1- induced epithelial-to-myofibroblast transition: role for beta-catenin. Am. J. Pathol. 165, 1955-1967.
29. Medici, D., Hay, E. D. and Goodenough, D. A. (2006). Cooperation between snail and LEF-1 transcription factors is essential for TGF-beta1-induced epithelial-mesenchymal transition. Mol. Biol. Cell 17, 1871-1879.
30. Mulroy, T., Xu, Y. and Sen, J. M. (2003). beta-Catenin expression enhances generation of mature thymocytes. Int. Immunol. 15, 1485-1494.
31. Nieto, M. A. (2011). The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu. Rev. Cell Dev. Biol. 27, 347-376.
32. Rastaldi, M. P. (2006). Epithelial-mesenchymal transition and its implications for the development of renal tubulointerstitial fibrosis. J. Nephrol. 19, 407-412.
33. Sahai, E. (2005). Mechanisms of cancer cell invasion. Curr. Opin. Genet. Dev. 15, 87-96.
34. Savagner, P. (2001). Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 23, 912-923.
35. Schmidt-Weber, C. B. and Blaser, K. (2004). Regulation and role of transforming growth factor-beta in immune tolerance induction and inflammation. Curr. Opin. Immunol. 16, 709-716.
36. Takaki, H., Minoda, Y., Koga, K., Takaesu, G., Yoshimura, A. and Kobayashi, T. (2006). TGF-beta1 suppresses IFN-gamma-induced NO production in macrophages by suppressing STAT1 activation and accelerating iNOS protein degradation. Genes Cells 11, 871-882.
37. Tan, T. K., Zheng, G., Hsu, T. T., Wang, Y., Lee, V. W., Tian, X., Wang, Y., Cao, Q., Wang, Y. and Harris, D. C. (2010). Macrophage matrix metalloproteinase-9 mediates epithelial-mesenchymal transition in vitro in murine renal tubular cells. Am.J. Pathol. 176, 1256-1270.
38. Teo, J. L., Ma, H., Nguyen, C., Lam, C. and Kahn, M. (2005). Specific inhibition of CBP/beta-catenin interaction rescues defects in neuronal differentiation caused by a presenilin-1 mutation. Proc. Natl. Acad. Sci. USA 102, 12171-12176.
39. Thornton, T. M., Pedraza-Alva, G., Deng, B., Wood, C. D., Aronshtam, A., Clements, J. L., Sabio, G., Davis, R. J., Matthews, D. E., Doble, B. et al. (2008). Phosphorylation by p38 MAPK as an alternative pathway for GSK3beta inactivation. Science 320, 667-670.
40. Wang, S., Wilkes, M. C., Leof, E. B. and Hirschberg, R. (2010). Noncanonical TGFbeta pathways, mTORC1 and Abl, in renal interstitial fibrogenesis. Am. J. Physiol. Renal Physiol. 298, F142-F149.
41. Werner, F., Jain, M. K., Feinberg, M. W., Sibinga, N. E., Pellacani, A., Wiesel, P., Chin, M. T., Topper, J. N., Perrella, M. A. and Lee, M. E. (2000). Transforming growth factor-beta 1 inhibition of macrophage activation is mediated via Smad3. J. Biol. Chem. 275, 36653-36658.
42. Xu, Y., Banerjee, D., Huelsken, J., Birchmeier, W. and Sen, J. M. (2003). Deletion of beta-catenin impairs T cell development. Nat. Immunol. 4, 1177-1182.
43. Yu, Q., Quinn, W. J., 3rd, Salay, T., Crowley, J. E., Cancro, M. P. and Sen, J. M. (2008). Role of beta-catenin in B cell development and function. J. Immunol. 181, 3777-3783.
44. Zeisberg, M. and Duffield, J. S. (2010). Resolved: EMT produces fibroblasts in the kidney. J. Am. Soc. Nephrol. 21, 1247-1253.
45. Zhang, M., Wang, M., Tan, X., Li, T. F., Zhang, Y. E. and Chen, D. (2010). Smad3 prevents beta-catenin degradation and facilitates beta-catenin nuclear translocation in chondrocytes. J. Biol. Chem. 285, 8703-8710.
46. Zheng, G., Lyons, J. G., Tan, T. K., Wang, Y., Hsu, T. T., Min, D., Succar, L., Rangan, G. K., Hu, M., Henderson, B. R. et al. (2009). Disruption of E-cadherin by matrix metalloproteinase directly mediates epithelial-mesenchymal transition downstream of transforming growth factor-beta1 in renal tubular epithelial cells. Am. J. Pathol. 175, 580-591.
47. Zhou, B., Liu, Y., Kahn, M., Ann, D.K., Han, A., Wang, H., Nguyen, C., Flodby, P., Zhong, Q., Krishnaveni, M. S. et al. (2012). Interactions between beta-catenin and transforming growth factor-beta signaling pathways mediate epithelial-mesenchymal transition and are dependent on the transcriptional co-activator cAMP-response element-binding protein (CREB)-binding protein (CBP). J. Biol. Chem. 287, 7026-7038.