Transforming growth factor-β (TGF-β) directly activates the JAK1-STAT3 axis to induce hepatic fibrosis in coordination with the SMAD pathway

Journal of Biological Chemistry

Volumn 292, Issue 10, 2017, Pages 4302-4312

  Tang, Liu Ya ^a   Heller, Mary ^a   Meng, Zhaojing ^b   Yu, Li Rong ^b,c   Tang, Yi ^a   Zhou, Ming ^b   Zhang, Ying E ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; GENES; PHOSPHORYLATION; PROTEINS;

BINDING PROTEINS; BIOLOGICAL EFFECTS; GENE EXPRESSION PROFILING; HEPATIC FIBROSIS; HEPATIC STELLATE CELLS; LIVER FIBROSIS; NOVO PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

GENE EXPRESSION;

JANUS KINASE 1; SMAD PROTEIN; STAT3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; JAK1 PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; EMBRYO; GENE EXPRESSION PROFILING; GENE TARGETING; HEPATIC STELLATE CELL; LIVER FIBROSIS; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; ANIMAL; CELL CULTURE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; LIVER CIRRHOSIS; MAMMALIAN EMBRYO; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; EMBRYO, MAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEPATIC STELLATE CELLS; JANUS KINASE 1; LIVER CIRRHOSIS; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMAD PROTEINS; STAT3 TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA;

EID: 85015072762     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.773085     Document Type: Article

References (36)

1. Morikawa, M., Derynck, R., and Miyazono, K. (2016) TGF-β and the TGF-β family: context-dependent roles in cell and tissue physiology. Cold Spring Harb. Perspect. Biol. 8, a021873
2. Fabregat, I., Moreno-Càceres, J., Sánchez, A., Dooley, S., Dewidar, B., Giannelli, G., Ten Dijke, P., and IT-LIVER Consortium (2016) TGF-β signalling and liver disease. FEBS J. 283, 2219-2232
3. Hata, A., and Chen, Y. G. (2016) TGF-β signaling from receptors to Smads. Cold Spring Harb. Perspect. Biol. 8, a022061
4. Zhang, Y. E. (2016) Non-Smad signaling pathways of the TGF-β family. Cold Spring Harb. Perspect. Biol. 9, a022129
5. Yang, Y. A., Zhang, G. M., Feigenbaum, L., and Zhang, Y. E. (2006) Smad3 reduces susceptibility to hepatocarcinoma by sensitizing hepatocytes to apoptosis through downregulation of Bcl-2. Cancer Cell 9, 445-457
6. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
7. Yamashita, M., Fatyol, K., Jin, C., Wang, X., Liu, Z., and Zhang, Y. E. (2008) TRAF6 mediates Smad-independent activation of JNK and p38 by TGF-β. Mol. Cell 31, 918-924
8. Shibuya, H., Iwata, H., Masuyama, N., Gotoh, Y., Yamaguchi, K., Irie, K., Matsumoto, K., Nishida, E., and Ueno, N. (1998) Role of TAK1 and TAB1 in BMP signaling in early Xenopus development. EMBO J. 17, 1019-1028
9. Sorrentino, A., Thakur, N., Grimsby, S., Marcusson, A., von Bulow, V., Schuster, N., Zhang, S., Heldin, C. H., and Landström, M. (2008) The type I TGF-β receptor engages TRAF6 to activate TAK1 in a receptor kinase-independent manner. Nat. Cell Biol. 10, 1199-1207
10. Yu, L., Hébert, M. C., and Zhang, Y. E. (2002) TGF-β receptor-activated p38 MAP kinase mediates Smad-independent TGF-β responses. EMBO J. 21, 3749-3759
11. Harrison, D. A. (2012) The Jak/STAT pathway. Cold Spring Harb. Perspect. Biol. 4, a011205
12. Inagaki-Ohara, K., Kondo, T., Ito, M., and Yoshimura, A. (2013) SOCS, inflammation, and cancer. JAKSTAT 2, e24053
13. Kusaba, M., Nakao, K., Goto, T., Nishimura, D., Kawashimo, H., Shibata, H., Motoyoshi, Y., Taura, N., Ichikawa, T., Hamasaki, K., and Eguchi, K. (2007) Abrogation of constitutive STAT3 activity sensitizes human hepatoma cells to TRAIL-mediated apoptosis. J. Hepatol. 47, 546-555
14. Yamamoto, T., Matsuda, T., Muraguchi, A., Miyazono, K., and Kawabata, M. (2001) Cross-talk between IL-6 and TGF-β signaling in hepatoma cells. FEBS Lett. 492, 247-253
15. Zauberman, A., Lapter, S., and Zipori, D. (2001) Smad proteins suppress CCAAT/enhancer-binding protein (C/EBP) β- and STAT3-mediated transcriptional activation of the haptoglobin promoter. J. Biol. Chem. 276, 24719-24725
16. Wang, G., Yu, Y., Sun, C., Liu, T., Liang, T., Zhan, L., Lin, X., and Feng, X. H. (2016) STAT3 selectively interacts with Smad3 to antagonize TGF-β. Oncogene 35, 4388-4398
17. Yoon, J. H., Sudo, K., Kuroda, M., Kato, M., Lee, I. K., Han, J. S., Nakae, S., Imamura, T., Kim, J., Ju, J. H., Kim, D. K., Matsuzaki, K., Weinstein, M., Matsumoto, I., Sumida, T., and Mamura, M. (2015) Phosphorylation status determines the opposing functions of Smad2/Smad3 as STAT3 cofactors in TH17 differentiation. Nat. Commun. 6, 7600
18. Coffer, P., Lutticken, C., van Puijenbroek, A., Klop-de Jonge, M., Horn, F., and Kruijer, W. (1995) Transcriptional regulation of the junB promoter: analysis of STAT-mediated signal transduction. Oncogene 10, 985-994
19. Kojima, H., Nakajima, K., and Hirano, T. (1996) IL-6-inducible complexes on an IL-6 response element of the junB promoter contain Stat3 and 36 kDa CRE-like site binding protein. Oncogene 12, 547-554
20. Jonk, L. J., Itoh, S., Heldin, C. H., ten Dijke, P., and Kruijer, W. (1998) Identification and functional characterization of a Smad binding element (SBE) in the JunB promoter that acts as a transforming growth factor-β, activin, and bone morphogenetic protein-inducible enhancer. J. Biol. Chem. 273, 21145-21152
21. Cong, M., Iwaisako, K., Jiang, C., and Kisseleva, T. (2012) Cell signals influencing hepatic fibrosis. Int. J. Hepatol. 2012, 158547
22. Carpino, G., Morini, S., Ginanni Corradini, S., Franchitto, A., Merli, M., Siciliano, M., Gentili, F., Onetti Muda, A., Berloco, P., Rossi, M., Attili, A. F., and Gaudio, E. (2005) α-SMA expression in hepatic stellate cells and quantitative analysis of hepatic fibrosis in cirrhosis and in recurrent chronic hepatitis after liver transplantation. Dig. Liver Dis. 37, 349-356
23. Tang, Y., Kitisin, K., Jogunoori, W., Li, C., Deng, C. X., Mueller, S. C., Ressom, H. W., Rashid, A., He, A. R., Mendelson, J. S., Jessup, J. M., Shetty, K., Zasloff, M., Mishra, B., Reddy, E. P., et al. (2008) Progenitor/stem cells give rise to liver cancer due to aberrant TGF-β and IL-6 signaling. Proc. Natl. Acad. Sci. U.S.A. 105, 2445-2450
24. Liu, Y., Liu, H., Meyer, C., Li, J., Nadalin, S., Königsrainer, A., Weng, H., Dooley, S., and ten Dijke, P. (2013) Transforming growth factor-β (TGF-β)-mediated connective tissue growth factor (CTGF) expression in hepatic stellate cells requires Stat3 signaling activation. J. Biol. Chem. 288, 30708-30719
25. Yang, Y., Pan, X., Lei, W., Wang, J., Shi, J., Li, F., and Song, J. (2006) Regulation of transforming growth factor-β 1-induced apoptosis and epithelial-to-mesenchymal transition by protein kinase A and signal transducers and activators of transcription 3. Cancer Res. 66, 8617-8624
26. Xu, M. Y., Hu, J. J., Shen, J., Wang, M. L., Zhang, Q. Q., Qu, Y., and Lu, L. G. (2014) Stat3 signaling activation crosslinking of TGF-β1 in hepatic stellate cell exacerbates liver injury and fibrosis. Biochim. Biophys. Acta 1842, 2237-2245
27. Chung, C. D., Liao, J., Liu, B., Rao, X., Jay, P., Berta, P., and Shuai, K. (1997) Specific inhibition of Stat3 signal transduction by PIAS3. Science 278, 1803-1805
28. Kroy, D. C., Beraza, N., Tschaharganeh, D. F., Sander, L. E., Erschfeld, S., Giebeler, A., Liedtke, C., Wasmuth, H. E., Trautwein, C., and Streetz, K. L. (2010) Lack of interleukin-6/glycoprotein 130/signal transducers and activators of transcription-3 signaling in hepatocytes predisposes to liver steatosis and injury in mice. Hepatology 51, 463-473
29. Mair, M., Zollner, G., Schneller, D., Musteanu, M., Fickert, P., Gumhold, J., Schuster, C., Fuchsbichler, A., Bilban, M., Tauber, S., Esterbauer, H., Kenner, L., Poli, V., Blaas, L., Kornfeld, J. W., et al. (2010) Signal transducer and activator of transcription 3 protects from liver injury and fibrosis in a mouse model of sclerosing cholangitis. Gastroenterology 138, 2499-2508
30. Wang, H., Lafdil, F., Kong, X., and Gao, B. (2011) Signal transducer and activator of transcription 3 in liver diseases: a novel therapeutic target. Int. J. Biol. Sci. 7, 536-550
31. Meng, F., Wang, K., Aoyama, T., Grivennikov, S. I., Paik, Y., Scholten, D., Cong, M., Iwaisako, K., Liu, X., Zhang, M., Osterreicher, C. H., Stickel, F., Ley, K., Brenner, D. A., and Kisseleva, T. (2012) Interleukin-17 signaling in inflammatory, Kupffer cells, and hepatic stellate cells exacerbates liver fibrosis in mice. Gastroenterology 143, 765-776.e1-3
32. Liu, Y., Festing, M. H., Hester, M., Thompson, J. C., and Weinstein, M. (2004) Generation of novel conditional and hypomorphic alleles of the Smad2 gene. Genesis 40, 118-123
33. Yang, X., Letterio, J. J., Lechleider, R. J., Chen, L., Hayman, R., Gu, H., Roberts, A. B., and Deng, C. (1999) Targeted disruption of SMAD3 results in impaired mucosal immunity and diminished T cell responsiveness to TGF-β. EMBO J. 18, 1280-1291
34. Millet, C., Yamashita, M., Heller, M., Yu, L. R., Veenstra, T. D., and Zhang, Y. E. (2009) A negative feedback control of transforming growth factor-β signaling by glycogen synthase kinase 3-mediated Smad3 linker phosphorylation at Ser-204. J. Biol. Chem. 284, 19808-19816
35. Mellacheruvu, D., Wright, Z., Couzens, A. L., Lambert, J. P., St-Denis, N. A., Li, T., Miteva, Y. V., Hauri, S., Sardiu, M. E., Low, T. Y., Halim, V. A., Bagshaw, R. D., Hubner, N. C., Al-Hakim, A., Bouchard, A., et al. (2013) The CRAPome: a contaminant repository for affinity purification-mass spectrometry data. Nat. Methods 10, 730-736
36. Allalou, A., and Wählby, C. (2009) BlobFinder, a tool for fluorescence microscopy image cytometry. Comput. Methods Programs Biomed. 94, 58-65