β-Catenin and Smad3 regulate the activity and stability of myocardin-related transcription factor during epithelial-myofibroblast transition

Molecular Biology of the Cell

Volumn 22, Issue 23, 2011, Pages 4472-4485

  Charbonney, Emmanuel ^a,b   Speight, Pam ^a,b   Masszi, András ^a,b   Nakano, Hiroyasu ^c   Kapus, András ^a,b  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; MYOCARDIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; EPITHELIUM CELL; MYOFIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RAT;

ACTINS; ADHERENS JUNCTIONS; ANIMALS; BETA CATENIN; CADHERINS; CELLS, CULTURED; EPITHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; MYOFIBROBLASTS; PROMOTER REGIONS, GENETIC; PROTEIN STABILITY; RATS; SERUM RESPONSE FACTOR; SMAD3 PROTEIN; SWINE; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA;

EID: 82655173709     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-04-0335     Document Type: Article

References (64)

1. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA (2009). Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. J Clin Invest 119, 1438-1449.
2. Attisano L, Labbe E (2004). TGFbeta and Wnt pathway cross-talk. Cancer Metastasis Rev 23, 53-61.
3. Badorff C, Seeger FH, Zeiher AM, Dimmeler S (2005). Glycogen synthase kinase 3beta inhibits myocardin-dependent transcription and hypertrophy induction through site-specific phosphorylation. Circ Res 97, 645-654. (Pubitemid 41416333)
4. Bowley E, O'Gorman DB, Gan BS (2007). Beta-catenin signaling in fibroproliferative disease. J Surg Res 138, 141-150.
5. Busche S, Descot A, Julien S, Genth H, Posern G (2008). Epithelial cell-cell contacts regulate SRF-mediated transcription via Rac-actin-MAL signalling. J Cell Sci 121, 1025-1035. (Pubitemid 351639421)
6. Busche S, Kremmer E, Posern G (2010). E-cadherin regulates MAL-SRF-mediated transcription in epithelial cells. J Cell Sci 123, 2803-2809.
7. Cheon S, Poon R, Yu C, Khoury M, Shenker R, Fish J, Alman BA (2005). Prolonged beta-catenin stabilization and tcf-dependent transcriptional activation in hyperplastic cutaneous wounds. Lab Invest 85, 416-425. (Pubitemid 40333158)
8. Cheon SS, Cheah AY, Turley S, Nadesan P, Poon R, Clevers H, Alman BA (2002). beta-Catenin stabilization dysregulates mesenchymal cell proliferation, motility, and invasiveness and causes aggressive fibromatosis and hyperplastic cutaneous wounds. Proc Natl Acad Sci USA 99, 6973-6978. (Pubitemid 34526242)
9. Cho IJ, Kim YW, Han CY, Kim EH, Anderson RA, Lee YS, Lee CH, Hwang SJ, Kim SG (2010). E-Cadherin antagonizes transforming growth factor beta1 gene induction in hepatic stellate cells by inhibiting RhoA-dependent Smad3 phosphorylation. Hepatology 52, 2053-2064.
10. 3β. J Biol Chem 283, 35337-35353.
11. Deng H, Dokshin GA, Lei J, Goldsmith AM, Bitar KN, Fingar DC, Hershenson MB, Bentley JK (2008). Inhibition of glycogen synthase kinase-3beta is sufficient for airway smooth muscle hypertrophy. J Biol Chem 283, 10198-10207.
12. Doble BW, Woodgett JR (2003). GSK-3: tricks of the trade for a multi-tasking kinase. J Cell Sci 116, 1175-1186. (Pubitemid 36410657)
13. Du KL, Chen M, Li J, Lepore JJ, Mericko P, Parmacek MS (2004). Megakaryoblastic leukemia factor-1 transduces cytoskeletal signals and induces smooth muscle cell differentiation from undifferentiated embryonic stem cells. J Biol Chem 279, 17578-17586. (Pubitemid 38560522)
14. Elberg G, Chen L, Elberg D, Chan MD, Logan CJ, Turman MA (2008). MKL1 mediates TGF-beta1-induced alpha-smooth muscle actin expression in human renal epithelial cells. Am J Physiol Renal Physiol 294, F1116-F1128.
15. Fan L et al. (2007). Cell contact-dependent regulation of epithelial-myofi- broblast transition via the rho-rho kinase-phospho-myosin pathway. Mol Biol Cell 18, 1083-1097. (Pubitemid 46399511)
16. Fuxe J, Vincent T, de Herreros AG (2010). Transcriptional crosstalk between TGFbeta and stem cell pathways in tumor cell invasion: role of EMT promoting Smad complexes. Cell Cycle 9.
17. Gosens R, Meurs H, Schmidt M (2008). The GSK-3/beta-catenin-signalling axis in smooth muscle and its relationship with remodelling. Naunyn Schmiedebergs Arch Pharmacol 378, 185-191. (Pubitemid 351977640)
18. Hu B, Wu Z, Phan SH (2003). Smad3 mediates transforming growth factor-beta-induced alpha-smooth muscle actin expression. Am J Respir Cell Mol Biol 29, 397-404. (Pubitemid 37093999)
19. Hua F, Zhou J, Liu J, Zhu C, Cui B, Lin H, Liu Y, Jin W, Yang H, Hu Z (2010). Glycogen synthase kinase-3beta negatively regulates TGF-beta1 and angiotensin II-mediated cellular activity through interaction with Smad3. Eur J Pharmacol 644, 17-23.
20. Johansen FE, Prywes R (1993). Identification of transcriptional activation and inhibitory domains in serum response factor (SRF) by using GAL4-SRF constructs. Mol Cell Biol 13, 4640-4647.
21. Kalluri R, Weinberg RA (2009). The basics of epithelial-mesenchymal transition. J Clin Invest 119, 1420-1428.
22. Kamaraju AK, Roberts AB (2005). Role of Rho/ROCK and p38 MAP kinase pathways in transforming growth factor-beta-mediated Smad-dependent growth inhibition of human breast carcinoma cells in vivo. J Biol Chem 280, 1024-1036.
23. Kapoor M, Liu S, Shi-wen X, Huh K, McCann M, Denton CP, Woodgett JR, Abraham DJ, Leask A (2008). GSK-3beta in mouse fibroblasts controls wound healing and fibrosis through an endothelin-1-dependent mechanism. J Clin Invest 118, 3279-3290.
24. Kim KK 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.
25. Kim Y, Kugler MC, Wei Y, Kim KK, Li X, Brumwell AN, Chapman HA (2009b). Integrin alpha3beta1-dependent beta-catenin phosphorylation links epithelial Smad signaling to cell contacts. J Cell Biol 184, 309-322.
26. Kolligs FT, Hu G, Dang CV, Fearon ER (1999). Neoplastic transformation of RK3E by mutant beta-catenin requires deregulation of Tcf/Lef transcription but not activation of c-myc expression. Mol Cell Biol 19, 5696-5706. (Pubitemid 29339926)
27. Lei S, Dubeykovskiy A, Chakladar A, Wojtukiewicz L, Wang TC (2004). The murine gastrin promoter is synergistically activated by transforming growth factor-beta/Smad and Wnt signaling pathways. J Biol Chem 279, 42492-42502. (Pubitemid 39372133)
28. Liebner S, Cattelino A, Gallini R, Rudini N, Iurlaro M, Piccolo S, Dejana E (2004). Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J Cell Biol 166, 359-367. (Pubitemid 39031239)
29. Liu Y (2010). New insights into epithelial-mesenchymal transition in kidney fibrosis. J Am Soc Nephrol 21, 212-222.
30. Masszi A, Di Ciano C, Sirokmany G, Arthur WT, Rotstein OD, Wang J, McCulloch CA, Rosivall L, Mucsi I, Kapus A (2003). Central role for Rho in TGF-beta1-induced alpha-smooth muscle actin expression during epithelial-mesenchymal transition. Am J Physiol Renal Physiol 284, F911-F924. (Pubitemid 36443575)
31. Masszi A, Fan L, Rosivall L, McCulloch CA, Rotstein OD, Mucsi I, 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. (Pubitemid 39578374)
32. Masszi A, Kapus A (2011). Smaddening complexity: the role of Smad3 in epithelial-myofibroblast transition. Cells Tissues Organs 193, 41-52.
33. Masszi A, Speight P, Charbonney E, Lodyga M, Nakano H, Szaszi K, Kapus A (2010). Fate-determining mechanisms in epithelial-myofibroblast transition: major inhibitory role for Smad3. J Cell Biol 188, 383-399.
34. Meng XM, Huang XR, Chung AC, Qin W, Shao X, Igarashi P, Ju W, Bottinger EP, Lan HY (2010). Smad2 protects against TGF-beta/Smad3-mediated renal fibrosis. J Am Soc Nephrol 21, 1477-1487.
35. Miralles F, Posern G, Zaromytidou AI, Treisman R (2003). Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113, 329-342. (Pubitemid 36556115)
36. Morita T, Mayanagi T, Sobue K (2007). Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling. J Cell Biol 179, 1027-1042. (Pubitemid 350223496)
37. Muehlich S, Wang R, Lee SM, Lewis TC, Dai C, Prywes R (2008). Serum-induced phosphorylation of the serum response factor coactivator MKL1 by the extracellular signal-regulated kinase 1/2 pathway inhibits its nuclear localization. Mol Cell Biol 28, 6302-6313.
38. Ng YY, Huang TP, Yang WC, Chen ZP, Yang AH, Mu W, Nikolic-Paterson DJ, Atkins RC, Lan HY (1998). Tubular epithelial-myofibroblast transdifferentiation in progressive tubulointerstitial fibrosis in 5/6 nephrectomized rats. Kidney Int 54, 864-876. (Pubitemid 28397404)
39. Olson EN, Nordheim A (2010). Linking actin dynamics and gene transcription to drive cellular motile functions. Nat Rev Mol Cell Biol 11, 353-365.
40. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA (2008). Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 68, 3645-3654.
41. Poncelet AC, Schnaper HW, Tan R, Liu Y, Runyan CE (2007). Cell phenotype-specific down-regulation of Smad3 involves decreased gene activation as well as protein degradation. J Biol Chem 282, 15534-15540. (Pubitemid 47093313)
42. Roberts AB, Tian F, Byfield SD, Stuelten C, Ooshima A, Saika S, Flanders KC (2006). Smad3 is key to TGF-beta-mediated epithelial-to-mesenchymal transition, fibrosis, tumor suppression and metastasis. Cytokine Growth Factor Rev 17, 19-27. (Pubitemid 43117513)
43. Samarin SN, Ivanov AI, Flatau G, Parkos CA, Nusrat A (2007). Rho/ROCK-II signaling mediates disassembly of epithelial apical junctions. Mol Biol Cell 18, 3429-3439. (Pubitemid 47378682)
44. Sasazuki T et al. (2002). Identification of a novel transcriptional activator, BSAC, by a functional cloning to inhibit tumor necrosis factor-induced cell death. J Biol Chem 277, 28853-28860.
45. Sebe A, Masszi A, Zulys M, Yeung T, Speight P, Rotstein OD, Nakano H, Mucsi I, Szaszi K, Kapus A (2008). Rac, PAK and p38 regulate cell contact-dependent nuclear translocation of myocardin-related transcription factor. FEBS Lett 582, 291-298.
46. Shafer SL, Towler DA (2009). Transcriptional regulation of SM22alpha by Wnt3a: convergence with TGFbeta(1)/Smad signaling at a novel regulatory element. J Mol Cell Cardiol 46, 621-635.
47. Sun Q, Chen G, Streb JW, Long X, Yang Y, Stoeckert CJ Jr, Miano JM (2006). Defining the mammalian CArGome. Genome Res 16, 197-207. (Pubitemid 43200268)
48. Surendran K, McCaul SP, Simon TC (2002). A role for Wnt-4 in renal fibrosis. Am J Physiol Renal Physiol 282, F431-F441. (Pubitemid 34654531)
49. Surendran K, Schiavi S, Hruska KA (2005). Wnt-dependent beta-catenin signaling is activated after unilateral ureteral obstruction, and recombinant secreted frizzled-related protein 4 alters the progression of renal fibrosis. J Am Soc Nephrol 16, 2373-2384. (Pubitemid 41725055)
50. Tamiya S, Liu L, Kaplan HJ (2010). Loss of cell-cell contact initiates epithelial-mesenchymal transition and proliferation of retinal pigment epithelial cells. Invest Ophthalmol Vis Sci 51, 2755-2763.
51. Tian YC, Phillips AO (2002). Interaction between the transforming growth factor-beta type II receptor/Smad pathway and beta-catenin during transforming growth factor-beta1-mediated adherens junction disassembly. Am J Pathol 160, 1619-1628. (Pubitemid 34525642)
52. Tomasek JJ, McRae J, Owens GK, Haaksma CJ (2005). Regulation of alpha-smooth muscle actin expression in granulation tissue myofibroblasts is dependent on the intronic CArG element and the transforming growth factor-beta1 control element. Am J Pathol 166, 1343-1351. (Pubitemid 40586506)
53. Tomasek JJ, Vaughan MB, Kropp BP, Gabbiani G, Martin MD, Haaksma CJ, Hinz B (2006). Contraction of myofibroblasts in granulation tissue is dependent on Rho/Rho kinase/myosin light chain phosphatase activity. Wound Repair Regen 14, 313-320. (Pubitemid 43979261)
54. Vartiainen MK, Guettler S, Larijani B, Treisman R (2007). Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316, 1749-1752. (Pubitemid 46988550)
55. Wang DZ, Li S, Hockemeyer D, Sutherland L, Wang Z, Schratt G, Richardson JA, Nordheim A, Olson EN (2002). Potentiation of serum response factor activity by a family of myocardin-related transcription factors. Proc Natl Acad Sci USA 99, 14855-14860. (Pubitemid 35334573)
56. Wendt MK, Allington TM, Schiemann WP (2009). Mechanisms of the epithelial-mesenchymal transition by TGF-beta. Future Oncol 5, 1145-1168.
57. Xie P, Fan Y, Zhang H, Zhang Y, She M, Gu D, Patterson C, Li H (2009). CHIP represses myocardin-induced smooth muscle cell differentiation via ubiquitin-mediated proteasomal degradation. Mol Cell Biol 29, 2398-2408.
58. Xie WB, Li Z, Miano JM, Long X, Chen SY (2011). Smad3-mediated myocardin silencing, a novel mechanism governing the initiation of smooth muscle differentiation. J Biol Chem 286, 15050-15057.
59. Zaromytidou AI, Miralles F, Treisman R (2006). MAL and ternary complex factor use different mechanisms to contact a common surface on the serum response factor DNA-binding domain. Mol Cell Biol 26, 4134-4148. (Pubitemid 43788016)
60. Zeisberg M, Neilson EG (2009). Biomarkers for epithelial-mesenchymal transitions. J Clin Invest 119, 1429-1437.
61. Zhang M, Lee CH, Luo DD, Krupa A, Fraser D, Phillips A (2007). Polarity of response to transforming growth factor-beta1 in proximal tubular epithelial cells is regulated by beta-catenin. J Biol Chem 282, 28639-28647. (Pubitemid 47606061)
62. Zhang M, Wang M, Tan X, Li TF, Zhang YE, Chen D (2010). Smad3 prevents beta-catenin degradation and facilitates beta-catenin nuclear translocation in chondrocytes. J Biol Chem 285, 8703-8710.
63. Zhao Y, Geverd DA (2002). Regulation of Smad3 expression in bleomycin-induced pulmonary fibrosis: a negative feedback loop of TGF-beta signaling. Biochem Biophys Res Commun 294, 319-323. (Pubitemid 34694096)
64. Zheng G 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.