Serine-204 in the linker region of Smad3 mediates the collagen-I response to TGF-β in a cell phenotype-specific manner

Experimental Cell Research

Volumn 319, Issue 19, 2013, Pages 2928-2937

  Browne, J A ^a   Liu, X ^a   Schnaper, H W ^a   Hayashida, T ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Epithelial; ERK MAP kinase; Extracellular matrix; Fibroblast; Fibrosis; Mesenchymal

Indexed keywords

COLLAGEN TYPE 1; MITOGEN ACTIVATED PROTEIN KINASE; SERINE; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; FIBROBLAST; HUMAN; HUMAN CELL; KIDNEY EPITHELIUM; MESANGIUM CELL; MESENCHYME CELL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

EID: 84886586938     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.07.013     Document Type: Article

References (35)

1. Leask A., Abraham D.J. TGF-β signaling and the fibrotic response. FASEB J. 2004, 18:816-827.
2. Runyan C.E., Schnaper H.W., Poncelet A.C. Smad3 and PKCδ mediate TGF-β1-induced collagen I expression in human mesangial cells. Am. J. physiology Renal Physiol. 2003, 285:F413-422.
3. Runyan C.E., Schnaper H.W., Poncelet A.C. The phosphatidylinositol 3-kinase/Akt pathway enhances Smad3-stimulated mesangial cell collagen I expression in response to transforming growth factor-β1. J. Biol. Chem. 2004, 279:2632-2639.
4. Hubchak S.C., Runyan C.E., Kreisberg J.I., Schnaper H.W. Cytoskeletal rearrangement and signal transduction in TGF-β1-stimulated mesangial cell collagen accumulation. J. Am. Soc. Nephrol. 2003, 14:1969-1980.
5. Basu R.K., Hubchak S., Hayashida T., Runyan C.E., Schumacker P.T., Schnaper H.W. Interdependence of HIF-1alpha and TGF-β/Smad3 signaling in normoxic and hypoxic renal epithelial cell collagen expression. Am. J. Physiol. Renal Physiol. 2011, 300:F898-905.
6. Hayashida T., Poncelet A.C., Hubchak S.C., Schnaper H.W. TGF-β1 activates MAP kinase in human mesangial cells: a possible role in collagen expression. Kidney Int. 1999, 56:1710-1720.
7. Hayashida T., Decaestecker M., Schnaper H.W. Cross-talk between ERK MAP kinase and Smad signaling pathways enhances TGF-β-dependent responses in human mesangial cells. FASEB J. 2003, 17:1576-1578.
8. Hayashida T., Wu M.H., Pierce A., Poncelet A.C., Varga J., Schnaper H.W. MAP-kinase activity necessary for TGFβ1-stimulated mesangial cell type I collagen expression requires adhesion-dependent phosphorylation of FAK tyrosine 397. J. Cell Sci. 2007, 120:4230-4240.
9. Hayashida T., Jones J.C., Lee C.K., Schnaper H.W. Loss of β1-integrin enhances TGF-β1-induced collagen expression in epithelial cells via increased αvβ3-integrin and Rac1 activity. J. Biol. Chem. 2010, 285:30741-30751.
10. Fujimoto M., Maezawa Y., Yokote K., Joh K., Kobayashi K., Kawamura H., Nishimura M., Roberts A.B., Saito Y., Mori S. Mice lacking Smad3 are protected against streptozotocin-induced diabetic glomerulopathy. Biochem. Biophys. Res. Commun. 2003, 305:1002-1007.
11. Shi Y. Structural insights on Smad function in TGFβ signaling. Bioessays 2001, 23:223-232.
12. Engel M.E., McDonnell M.A., Law B.K., Moses H.L. Interdependent SMAD and JNK signaling in transforming growth factor-beta-mediated transcription. J. Biol. Chem. 1999, 274:37413-37420.
13. Kretzschmar M., Doody J., Timokhina I., Massague J. A mechanism of repression of TGFβ/Smad signaling by oncogenic Ras. Genes Dev. 1999, 13:804-816.
14. Massague J. Integration of Smad and MAPK pathways: a link and a linker revisited. Genes Dev. 2003, 17:2993-2997.
15. Furukawa F., Matsuzaki K., Mori S., Tahashi Y., Yoshida K., Sugano Y., Yamagata H., Matsushita M., Seki T., Inagaki Y., Nishizawa M., Fujisawa J., Inoue K. p38 MAPK mediates fibrogenic signal through Smad3 phosphorylation in rat myofibroblasts. Hepatology 2003, 38:879-889.
16. Matsuura I., Denissova N.G., Wang G., He D., Long J., Liu F. Cyclin-dependent kinases regulate the antiproliferative function of Smads. Nature 2004, 430:226-231.
17. Liu F. Smad3 phosphorylation by cyclin-dependent kinases. Cytokine Growth Factor Rev. 2006, 17:9-17.
18. Matsuura I., Wang G., He D., Liu F. Identification and characterization of ERK MAP kinase phosphorylation sites in Smad3. Biochemistry 2005, 44:12546-12553.
19. Mori S., Matsuzaki K., Yoshida K., Furukawa F., Tahashi Y., Yamagata H., Sekimoto G., Seki T., Matsui H., Nishizawa M., Fujisawa J., Okazaki K. TGF-β and HGF transmit the signals through JNK-dependent Smad2/3 phosphorylation at the linker regions. Oncogene 2004, 23:7416-7429.
20. Yamagata H., Matsuzaki K., Mori S., Yoshida K., Tahashi Y., Furukawa F., Sekimoto G., Watanabe T., Uemura Y., Sakaida N., Yoshioka K., Kamiyama Y., Seki T., Okazaki K. Acceleration of Smad2 and Smad3 phosphorylation via c-Jun NH(2)-terminal kinase during human colorectal carcinogenesis. Cancer Res. 2005, 65:157-165.
21. Kamaraju A.K., Roberts A.B. 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. 2005, 280:1024-1036.
22. Guo X., Ramirez A., Waddell D.S., Li Z., Liu X., Wang X.F. Axin and GSK3- control Smad3 protein stability and modulate TGF-signaling. Genes Dev. 2008, 22:106-120.
23. Wang G., Matsuura I., He D., Liu F. Transforming growth factor-{β}-inducible phosphorylation of Smad3. J. Biol. Chem. 2009, 284:9663-9673.
24. Millet C., Yamashita M., Heller M., Yu L.R., Veenstra T.D., Zhang Y.E. A negative feedback control of transforming growth factor-beta signaling by glycogen synthase kinase 3-mediated Smad3 linker phosphorylation at Ser-204. J. Biol. Chem. 2009, 284:19808-19816.
25. Matsuzaki K., Kitano C., Murata M., Sekimoto G., Yoshida K., Uemura Y., Seki T., Taketani S., Fujisawa J., Okazaki K. Smad2 and Smad3 phosphorylated at both linker and COOH-terminal regions transmit malignant TGF-β signal in later stages of human colorectal cancer. Cancer Res. 2009, 69:5321-5330.
26. Rahimi R.A., Leof E.B. TGF-β signaling: a tale of two responses. J. Cell. Biochem. 2007, 102:593-608.
27. Wilkes M.C., Leof E.B. Transforming growth factor beta activation of c-Abl is independent of receptor internalization and regulated by phosphatidylinositol 3-kinase and PAK2 in mesenchymal cultures. J. Biol. Chem. 2006, 281:27846-27854.
28. Velden J.L., Alcorn J.F., Guala A.S., Badura E.C., Janssen-Heininger Y.M. c-Jun N-terminal kinase 1 promotes transforming growth factor-β1-induced epithelial-to-mesenchymal transition via control of linker phosphorylation and transcriptional activity of Smad3. Am. J. Respir. Cell Mol. Biol. 2011, 44:571-581.
29. Prokova V., Mavridou S., Papakosta P., Kardassis D. Characterization of a novel transcriptionally active domain in the transforming growth factor beta-regulated Smad3 protein. Nucleic Acids Res. 2005, 33:3708-3721.
30. Wang G., Long J., Matsuura I., He D., Liu F. The Smad3 linker region contains a transcriptional activation domain. Biochem. J. 2005, 386:29-34.
31. Poncelet A.C., de Caestecker M.P., Schnaper H.W. The transforming growth factor-beta/SMAD signaling pathway is present and functional in human mesangial cells. Kidney Int. 1999, 56:1354-1365.
32. Yang Y.C., Piek E., Zavadil J., Liang D., Xie D., Heyer J., Pavlidis P., Kucherlapati R., Roberts A.B., Bottinger E.P. Hierarchical model of gene regulation by transforming growth factor beta. Proc. Natl. Acad. Sci. USA 2003, 100:10269-10274.
33. Racusen L.C., Monteil C., Sgrignoli A., Lucskay M., Marouillat S., Rhim J.G., Morin J.P. Cell lines with extended in vitro growth potential from human renal proximal tubule: characterization, response to inducers, and comparison with established cell lines. J. Lab. Clin. Med. 1997, 129:318-329.
34. Schnaper H.W., Kopp J.B., Poncelet A.C., Hubchak S.C., Stetler-Stevenson W.G., Klotman P.E., Kleinman H.K. Increased expression of extracellular matrix proteins and decreased expression of matrix proteases after serial passage of glomerular mesangial cells. J. Cell Sci. 1996, 109(Pt 10):2521-2528.
35. Gao S., Alarcon C., Sapkota G., Rahman S., Chen P.Y., Goerner N., Macias M.J., Erdjument-Bromage H., Tempst P., Massague J. Ubiquitin ligase Nedd4L targets activated Smad2/3 to limit TGF-β signaling. Mol. Cell 2009, 36:457-468.