Smad7 regulates compensatory hepatocyte proliferation in damaged mouse liver and positively relates to better clinical outcome in human hepatocellular carcinoma

Clinical Science

Volumn 128, Issue 11, 2015, Pages 761-774

  Feng, Teng ^a   Dzieran, Johanna ^a   Gu, Xing ^b   Marhenke, Silke ^c   Vogel, Arndt ^c   Machida, Keigo ^d   Weiss, Thomas S ^e   Ruemmele, Petra ^e   Kollmar, Otto ^f   Hoffmann, Patrick ^f   Grässer, Friedrich ^f   Allgayer, Heike ^a   Fabian, Jasmin ^a   Weng, Hong Lei ^a   Teufel, Andreas ^g   Maass, Thorsten ^g   Meyer, Christoph ^a   Lehmann, Ulrich ^c   Zhu, Cheng ^h   Mertens, Peter R ^h   Gao, Chun Fang ^b   Dooley, Steven ^a   Meindl Beinker, Nadja M ^a   more..

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e UNIVERSITY OF REGENSBURG   (Germany)

^f SAARLAND UNIVERSITY   (Germany)

^g UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^h OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Hepatocellular carcinoma (HCC); Human tissue; Liver cancer; Transforming growth factor (TGF ); Y box protein 1 (YB 1)

Indexed keywords

FUMARYLACETOACETASE; MESSENGER RNA; SMAD7 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; Y BOX BINDING PROTEIN 1; YBX1 PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER INHIBITION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSTASIS; DISEASE FREE SURVIVAL; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HEPATOCELLULAR CARCINOMA CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER CELL; LIVER CELL CARCINOMA; LIVER INJURY; MAJOR CLINICAL STUDY; MALE; MIDDLE AGED; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; OVERALL SURVIVAL; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; TUMOR VOLUME; 129 MOUSE; ANIMAL; CELL CULTURE; CONFOCAL MICROSCOPY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEPG2 CELL LINE; KNOCKOUT MOUSE; LIVER DISEASE; LIVER TUMOR; METABOLISM; MULTIVARIATE ANALYSIS; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEP G2 CELLS; HEPATOCYTES; HUMANS; LIVER DISEASES; LIVER NEOPLASMS; MALE; MICE, 129 STRAIN; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MIDDLE AGED; MULTIVARIATE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SMAD7 PROTEIN; SURVIVAL ANALYSIS; TRANSFORMING GROWTH FACTOR BETA; Y-BOX-BINDING PROTEIN 1;

EID: 84930985155     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20140606     Document Type: Article

References (44)

1. Ferlay, J., Soerjomataram, I.I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., Parkin, D.M., Forman, D.D. and Bray, F. (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int. J. Cancer 136, E359-E386
2. Dooley, S. and ten Dijke, P. (2012) TGF-beta in progression of liver disease. Cell Tissue Res. 347, 245-256
3. Karkampouna, S., Ten Dijke, P., Dooley, S. and Julio, M.K. (2012) TGFbeta signaling in liver regeneration. Curr. Pharm. Des. 18, 4103-4113
4. Chen, C.L., Tsukamoto, H., Liu, J.C., Kashiwabara, C., Feldman, D., Sher, L., Dooley, S., French, S.W., Mishra, L., Petrovic, L. et al. (2013) Reciprocal regulation by TLR4 and TGF-beta in tumor-initiating stem-like cells. J. Clin. Invest. 123, 2832-2849
5. Miyazono, K., ten Dijke, P. and Heldin, C.H. (2000) TGF-beta signaling by Smad proteins. Adv. Immunol. 75, 115-157
6. Reichl, P., Haider, C., Grubinger, M. and Mikulits, W. (2012) TGF-beta in epithelial to mesenchymal transition and metastasis of liver carcinoma. Curr. Pharm. Des. 18, 4135-4147
7. Baek, H.J., Pishvaian, M.J., Tang, Y., Kim, T.H., Yang, S., Zouhairi, M.E., Mendelson, J., Shetty, K., Kallakury, B., Berry, D.L. et al. (2011) Transforming growth factor-beta adaptor, beta2-spectrin, modulates cyclin dependent kinase 4 to reduce development of hepatocellular cancer. Hepatology 53, 1676-1684
8. Nagata, H., Hatano, E., Tada, M., Murata, M., Kitamura, K., Asechi, H., Narita, M., Yanagida, A., Tamaki, N., Yagi, S. et al. (2009) Inhibition of c-Jun NH2-terminal kinase switches Smad3 signaling from oncogenesis to tumor- suppression in rat hepatocellular carcinoma. Hepatology 49, 1944-1953
9. Dooley, S., Hamzavi, J., Ciuclan, L., Godoy, P., Ilkavets, I., Ehnert, S., Ueberham, E., Gebhardt, R., Kanzler, S., Geier, A. et al. (2008) Hepatocyte-specific Smad7 expression attenuates TGF-beta-mediated fibrogenesis and protects against liver damage. Gastroenterology 135, 642-659
10. Dooley, S., Hamzavi, J., Breitkopf, K., Wiercinska, E., Said, H.M., Lorenzen, J., Ten Dijke, P. and Gressner, A.M. (2003) Smad7 prevents activation of hepatic stellate cells and liver fibrosis in rats. Gastroenterology 125, 178-191
11. Chen, Y.K., Huang, A.H., Cheng, P.H., Yang, S.H. and Lin, L.M. (2013) Overexpression of Smad proteins, especially Smad7, in oral epithelial dysplasias. Clin. Oral Investig. 17, 921-932
12. Osawa, H., Nakajima, M., Kato, H., Fukuchi, M. and Kuwano, H. (2004) Prognostic value of the expression of Smad6 and Smad7, as inhibitory Smads of the TGF-beta superfamily, in esophageal squamous cell carcinoma. Anticancer Res. 24, 3703-3709
13. Theohari, I., Giannopoulou, I., Magkou, C., Nomikos, A., Melissaris, S. and Nakopoulou, L. (2012) Differential effect of the expression of TGF-beta pathway inhibitors, Smad-7 and Ski, on invasive breast carcinomas: relation to biologic behavior. APMIS 120, 92-100
14. Huang, Q., Liu, L., Liu, C.H., Shao, F., Xie, F., Zhang, C.H. and Hu, S.Y. (2012) Expression of Smad7 in cholangiocarcinoma: prognostic significance and implications for tumor metastasis. Asian Pac. J. Cancer Prev. 13, 5161-5165
15. Park, Y.N., Chae, K.J., Oh, B.K., Choi, J., Choi, K.S. and Park, C. (2004) Expression of Smad7 in hepatocellular carcinoma and dysplastic nodules: resistance mechanism to transforming growth factor-beta. Hepatogastroenterology 51, 396-400
16. Wang, J., Zhao, J., Chu, E.S., Mok, M.T., Go, M.Y., Man, K., Heuchel, R., Lan, H.Y., Chang, Z., Sung, J.J. and Yu, J. (2013) Inhibitory role of Smad7 in hepatocarcinogenesis in mice and in vitro. J. Pathol. 230, 441-452
17. Xia, H., Ooi, L.L. and Hui, K.M. (2013) MicroRNA-216a/217-induced epithelial-mesenchymal transition targets PTEN and SMAD7 to promote drug resistance and recurrence of liver cancer. Hepatology 58, 629-641
18. Grompe, M., al-Dhalimy, M., Finegold, M., Ou, C.N., Burlingame, T., Kennaway, N.G. and Soriano, P. (1993) Loss of fumarylacetoacetate hydrolase is responsible for the neonatal hepatic dysfunction phenotype of lethal albino mice. Genes Dev. 7, 2298-2307
19. Kuhn, R., Schwenk, F., Aguet, M. and Rajewsky, K. (1995) Inducible gene targeting in mice. Science 269, 1427-1429
20. Fleenor, D.E. and Kaufman, R.E. (1993) Characterization of the DNase I hypersensitive site 3' of the human beta globin gene domain. Blood 81, 2781-2790
21. Li, Q. and Stamatoyannopoulos, G. (1994) Hypersensitive site 5 of the human beta locus control region functions as a chromatin insulator. Blood 84, 1399-1401
22. Blessing, M., Nanney, L.B., King, L.E., Jones, C.M. and Hogan, B.L. (1993) Transgenic mice as a model to study the role of TGF-beta-related molecules in hair follicles. Genes Dev. 7, 204-215
23. Gorski, K., Carneiro, M. and Schibler, U. (1986) Tissue-specific in vitro transcription from the mouse albumin promoter. Cell 47, 767-776
24. Werner, S., Weinberg, W., Liao, X., Peters, K.G., Blessing, M., Yuspa, S.H., Weiner, R.L. and Williams, L.T. (1993) Targeted expression of a dominant-negative FGF receptor mutant in the epidermis of transgenic mice reveals a role of FGF in keratinocyte organization and differentiation. EMBO J. 12, 2635-2643
25. Sauer, B. and Henderson, N. (1988) Site-specific DNA recombination in mammalian cells by the Cre recombinase of bacteriophage P1. Proc. Natl. Acad. Sci. U.S.A. 85, 5166-5170
26. Pluck, A. and Klasen, C. (2009) Generation of chimeras by microinjection. Methods Mol. Biol. 561, 199-217
27. Damm, G., Pfeiffer, E., Burkhardt, B., Vermehren, J., Nüssler, A.K. and Weiss, T.S. (2013) Human parenchymal and non-parenchymal liver cell isolation, culture and characterization. Hepatol. Int. 7, 951-958
28. Stopa, M., Benes, V., Ansorge, W., Gressner, A.M. and Dooley, S. (2000) Genomic locus and promoter region of rat Smad7, an important antagonist of TGFbeta signaling. Mamm. Genome 11, 169-176
29. Bettstetter, M., Dechant, S., Ruemmele, P., Vogel, C., Kurz, K., Morak, M., Keller, G., Holinski-Feder, E., Hofstaedter, F. and Dietmaier, W. (2008) MethyQESD, a robust and fast method for quantitative methylation analyses in HNPCC diagnostics using formalin-fixed and paraffin-embedded tissue samples. Lab. Invest. 88, 1367-1375
30. Marhenke, S., Buitrago-Molina, L.E., Endig, J., Orlik, J., Schweitzer, N., Klett, S., Longerich, T., Geffers, R., Sanchez Munoz, A., Dorrell, C. et al. (2014) p21 promotes sustained liver regeneration and hepatocarcinogenesis in chronic cholestatic liver injury. Gut 63, 1501-1512
31. Mertens, P.R., Martin, I.V., Frye, B.C., Rauen, T., Strauch, S., Pabst, M. and Geier, A. (2012) Rat Mrp2 gene expression is regulated by an interleukin-1beta-stimulated biphasic response with enhanced transcription and subcellular shuttling of YB-1. Eur. J. Cell Biol. 91, 533-541
32. Camp, R.L., Dolled-Filhart, M. and Rimm, D.L. (2004) X-tile: a new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization. Clin. Cancer Res. 10, 7252-7259
33. Dzieran, J., Fabian, J., Feng, T., Coulouarn, C., Ilkavets, I., Kyselova, A., Breuhahn, K., Dooley, S. and Meindl-Beinker, N.M. (2013) Comparative analysis of TGF-beta/Smad signaling dependent cytostasis in human hepatocellular carcinoma cell lines. PLoS ONE 8, e72252
34. Dooley, S., Said, H.M., Gressner, A.M., Floege, J., En-Nia, A. and Mertens, P.R. (2006) Y-box protein-1 is the crucial mediator of antifibrotic interferon-gamma effects. J. Biol. Chem. 281, 1784-1795
35. Tang, Y., Katuri, V., Dillner, A., Mishra, B., Deng, C.X. and Mishra, L. (2003) Disruption of transforming growth factor-beta signaling in ELF beta-spectrin-deficient mice. Science 299, 574-577
36. Matsuzaki, K., Date, M., Furukawa, F., Tahashi, Y., Matsushita, M., Sugano, Y., Yamashiki, N., Nakagawa, T., Seki, T., Nishizawa, M. et al. (2000) Regulatory mechanisms for transforming growth factor beta as an autocrine inhibitor in human hepatocellular carcinoma: implications for roles of smads in its growth. Hepatology 32, 218-227
37. Yamamura, Y., Hua, X., Bergelson, S. and Lodish, H.F. (2000) Critical role of Smads and AP-1 complex in transforming growth factor-beta -dependent apoptosis. J. Biol. Chem. 275, 36295-36302
38. Zhang, H., Ozaki, I., Mizuta, T., Hamajima, H., Yasutake, T., Eguchi, Y., Ideguchi, H., Yamamoto, K. and Matsuhashi, S. (2006) Involvement of programmed cell death 4 in transforming growth factor-beta1-induced apoptosis in human hepatocellular carcinoma. Oncogene 25, 6101-6112
39. Matsuzaki, K., Date, M., Furukawa, F., Tahashi, Y., Matsushita, M., Sakitani, K., Yamashiki, N., Seki, T., Saito, H., Nishizawa, M. et al. (2000) Autocrine stimulatory mechanism by transforming growth factor beta in human hepatocellular carcinoma. Cancer Res. 60, 1394-1402
40. Higashi, K., Inagaki, Y., Suzuki, N., Mitsui, S., Mauviel, A., Kaneko, H. and Nakatsuka, I. (2003) Y-box-binding protein YB-1 mediates transcriptional repression of human alpha 2(I) collagen gene expression by interferon-gamma. J. Biol. Chem. 278, 5156-5162
41. Higashi, K., Tomigahara, Y., Shiraki, H., Miyata, K., Mikami, T., Kimura, T., Moro, T., Inagaki, Y. and Kaneko, H. (2011) A novel small compound that promotes nuclear translocation of YB-1 ameliorates experimental hepatic fibrosis in mice. J. Biol. Chem. 286, 4485-4492
42. Inagaki, Y., Kushida, M., Higashi, K., Itoh, J., Higashiyama, R., Hong, Y.Y., Kawada, N., Namikawa, K., Kiyama, H., Bou-Gharios, G. et al. (2005) Cell type-specific intervention of transforming growth factor beta/Smad signaling suppresses collagen gene expression and hepatic fibrosis in mice. Gastroenterology 129, 259-268
43. Yasen, M., Kajino, K., Kano, S., Tobita, H., Yamamoto, J., Uchiumi, T., Kon, S., Maeda, M., Obulhasim, G., Arii, S. and Hino, O. (2005) The up-regulation of Y-box binding proteins (DNA binding protein A and Y-box binding protein-1) as prognostic markers of hepatocellular carcinoma. Clin. Cancer Res. 11, 7354-7361
44. Tacke, F., Kanig, N., En-Nia, A., Kaehne, T., Eberhardt, C.S., Shpacovitch, V., Trautwein, C. and Mertens, P.R. (2011) Y-box protein-1/p18 fragment identifies malignancies in patients with chronic liver disease. BMC Cancer 11, 185