Inhibiting miR-21 attenuates experimental hepatic fibrosis by suppressing both the ERK1 pathway in HSC and hepatocyte EMT

Clinical Science

Volumn 130, Issue 16, 2016, Pages 1469-1480

  Wu, Kaiming ^a   Ye, Changhong ^a   Lin, Lin ^a   Chu, Yimin ^b   Ji, Meng ^a   Dai, Weiping ^a   Zeng, Xin ^a   Lin, Yong ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b Shanghai Jiao Tong University School of Medicine   (China)

Author keywords

Epithelial mesenchymal transition (EMT); Extracellular signal regulated kinase1 (ERK1) signalling pathway; Hepatic fibrosis; Hepatic stellate cell (HSC); Hepatocyte; MiR 21

Indexed keywords

ADENOVIRUS VECTOR; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; HYDROXYPROLINE; MICRORNA 21; MITOGEN ACTIVATED PROTEIN KINASE 3; SPROUTY 2 PROTEIN; SPROUTY PROTEIN; UNCLASSIFIED DRUG; MICRORNA; MIRN21 MICRORNA, HUMAN; MIRN21 MICRORNA, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; CONTROLLED STUDY; DISEASE SEVERITY; EPITHELIAL MESENCHYMAL TRANSITION; EXPERIMENTAL LIVER FIBROSIS; GENE EXPRESSION REGULATION; HEPATIC STELLATE CELL; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MAJOR CLINICAL STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; SIGNAL TRANSDUCTION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ANIMAL; CYTOLOGY; ENZYMOLOGY; GENETICS; LIVER CIRRHOSIS; METABOLISM; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; EPITHELIAL-MESENCHYMAL TRANSITION; HEPATIC STELLATE CELLS; HEPATOCYTES; HUMANS; LIVER CIRRHOSIS; MALE; MICRORNAS; MITOGEN-ACTIVATED PROTEIN KINASE 3; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION;

EID: 85014331274     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20160334     Document Type: Article

References (43)

1. Friedman, S.L. (2008) Mechanisms of hepatic fibrogenesis. Gastroenterology 134, 1655-1669.
2. Hernandez-Gea, V. and Friedman, S.L. (2011) Pathogenesis of liver fibrosis. Annu. Rev. Pathol. 6, 425-456.
3. Castera, L. (2012) Noninvasive methods to assess liver disease in patients with hepatitis B or C. Gastroenterology 142, 1293-1302.
4. DeLeve, L.D., Valla, D.C., Garcia-Tsao, G., and American Association for the Study Liver Diseases. (2009) Vascular disorders of the liver. Hepatology 49, 1729-1764.
5. Friedman, S.L. (2004) Stellate cells: a moving target in hepatic fibrogenesis. Hepatology 40, 1041-1043.
6. Friedman, S.L. (1993) Seminars in medicine of the Beth Israel Hospital, Boston. The cellular basis of hepatic fibrosis. Mechanisms and treatment strategies. N. Engl. J. Med. 328, 1828-1835.
7. Tacke, F. and Weiskirchen, R. (2012) Update on hepatic stellate cells: pathogenic role in liver fibrosis and novel isolation techniques. Expert. Rev. Gastroenterol. Hepatol. 6, 67-80.
8. Lee, S.J., Kim, K.H. and Park, K.K. (2014) Mechanisms of fibrogenesis in liver cirrhosis: the molecular aspects of epithelial-mesenchymal transition. World. J. Hepatol. 6, 207-216.
9. Pinzani, M. (2011) Epithelial-mesenchymal transition in chronic liver disease: fibrogenesis or escape from death? J. Hepatol. 55, 459-465.
10. Ikegami, T., Zhang, Y. and Matsuzaki, Y. (2007) Liver fibrosis: possible involvement of EMT. Cells Tissues Organs 185, 213-221.
11. Zeisberg, M., Yang, C., Martino, M., Duncan, M.B., Rieder, F., Tanjore, H. and Kalluri, R. (2007) Fibroblasts derive from hepatocytes in liver fibrosis via epithelial to mesenchymal transition. J. Biol. Chem. 282, 23337-23347.
12. Mann, D.A. and Smart, D.E. (2002) Transcriptional regulation of hepatic stellate cell activation. Gut 50, 891-896.
13. Zhang, F., Kong, D.S., Zhang, Z.L., Lei, N., Zhu, X.J., Zhang, X.P., Chen, L., Lu, Y. and Zheng, S.Z. (2013) Tetramethylpyrazine induces G0/G1 cell cycle arrest and stimulates mitochondrial-mediated and caspase-dependent apoptosis through modulating ERK/p53 signaling in hepatic stellate cells in vitro. Apoptosis 18, 135-149.
14. Zhong, W., Shen, W.F., Ning, B.F., Hu, P.F., Lin, Y., Yue, H.Y., Yin, C., Hou, J.L., Chen, Y.X., Zhang, J.P. et al. (2009) Inhibition of extracellular signal-regulated kinase 1 by adenovirus mediated small interfering RNA attenuates hepatic fibrosis in rats. Hepatology 50, 1524-1536.
15. Yue, H.Y., Yin, C., Hou, J.L., Zeng, X., Chen, Y.X., Zhong, W., Hu, P.F., Deng, X., Tan, Y.X., Zhang, J.P. et al. (2010) Hepatocyte nuclear factor 4alpha attenuates hepatic fibrosis in rats. Gut 59, 236-246.
16. Pedersen, I.M., Cheng, G., Wieland, S., Volinia, S., Croce, C.M., Chisari, F.V. and David, M. (2007) Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 449, 919-922.
17. Png, K.J., Halberg, N., Yoshida, M. and Tavazoie, S.F. (2011) A microRNA regulon that mediates endothelial recruitment and metastasis by cancer cells. Nature 481, 190-194.
18. He, Y., Huang, C., Sun, X., Long, X.R., Lv, X.W. and Li, J. (2012) MicroRNA-146a modulates TGF-beta1-induced hepatic stellate cell proliferation by targeting SMAD4. Cell. Signal. 24, 1923-1930.
19. Xin, X., Zhang, Y., Liu, X., Xin, H., Cao, Y. and Geng, M. (2014) MicroRNA in hepatic fibrosis and cirrhosis. Front. Biosci. (Landmark Ed) 19, 1418-1424.
20. Dong, S., Ma, W., Hao, B., Hu, F., Yan, L., Yan, X., Wang, Y., Chen, Z. and Wang, Z. (2014) MicroRNA-21 promotes cardiac fibrosis and development of heart failure with preserved left ventricular ejection fraction by up-regulating Bcl-2. Int. J. Clin. Exp. Pathol. 7, 565-574.
21. Thum, T., Gross, C., Fiedler, J., Fischer, T., Kissler, S., Bussen, M., Galuppo, P., Just, S., Rottbauer, W., Frantz, S. et al. (2008) MicroRNA-21 contributes to myocardial disease by stimulating MAP kinase signalling in fibroblasts. Nature 456, 980-984.
22. Marquez, R.T., Wendlandt, E., Galle, C.S., Keck, K. and McCaffrey, A.P. (2010) MicroRNA-21 is upregulated during the proliferative phase of liver regeneration, targets Pellino-1, and inhibits NF-kappaB signaling. Am. J. Physiol. Gastrointest. Liver. Physiol. 298, G535-G541.
23. Ling, M., Li, Y., Xu, Y., Pang, Y., Shen, L., Jiang, R., Zhao, Y., Yang, X., Zhang, J., Zhou, J. et al. (2012) Regulation of miRNA-21 by reactive oxygen species-activated ERK/NF-?B in arsenite-induced cell transformation. Free. Radic. Biol. Med. 52, 1508-1518.
24. Marquez, R.T., Bandyopadhyay, S., Wendlandt, E.B., Keck, K., Hoffer, B.A., Icardi, M.S., Christensen, R.N., Schmidt, W.N. and McCaffrey, A.P. (2010) Correlation between microRNA expression levels and clinical parameters associated with chronic hepatitis C viral infection in humans. Lab. Invest. 90, 1727-1736.
25. Zhao, J., Tang, N., Wu, K., Dai, W., Ye, C., Shi, J., Zhang, J., Ning, B., Zeng, X. and Lin, Y. (2014) MiR-21 simultaneously regulates ERK1 signaling in HSC activation and hepatocyte EMT in hepatic fibrosis. PloS One 9, e108005.
26. Haraguchi, T., Ozaki, Y. and Iba, H. (2009) Vectors expressing efficient RNA decoys achieve the long-term suppression of specific microRNA activity in mammalian cells. Nucleic Acids Res. 37, e43.
27. Hollensen, A.K., Bak, R.O., Haslund, D. and Mikkelsen, J.G. (2013) Suppression of microRNAs by dual-targeting and clustered Tough Decoy inhibitors. RNA Biol. 10, 406-414.
28. Sakurai, F., Furukawa, N., Higuchi, M., Okamoto, S., Ono, K., Yoshida, T., Kondoh, M., Yagi, K., Sakamoto, N., Katayama, K. et al. (2012) Suppression of hepatitis C virus replicon by adenovirus vector-mediated expression of Tough Decoy RNA against miR-122a. Virus Res. 165, 214-218.
29. Chen, S.W., Chen, Y.X., Zhang, X.R., Qian, H., Chen, W.Z. and Xie, W.F. (2008) Targeted inhibition of platelet-derived growth factor receptor-beta subunit in hepatic stellate cells ameliorates hepatic fibrosis in rats. Gene Ther. 15, 1424-1435.
30. Dai, W., Zhao, J., Tang, N., Zeng, X., Wu, K., Ye, C., Shi, J., Lu, C., Ning, B., Zhang, J. et al. (2015) MicroRNA-155 attenuates activation of hepatic stellate cell by simultaneously preventing EMT process and ERK1 signalling pathway. Liver Int. 35, 1234-1243.
31. Mitchell, P.S., Parkin, R.K., Kroh, E.M., Fritz, B.R., Wyman, S.K., Pogosova-Agadjanyan, E.L., Peterson, A., Noteboom, J., O'Briant, K.C., Allen, A. et al. (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. U.S.A. 105, 10513-10518.
32. Hu, J., Chen, C., Liu, Q., Liu, B., Song, C., Zhu, S., Wu, C., Liu, S., Yu, H., Yao, D. et al. (2015) The role of the miR-31/FIH1 pathway in TGF-β-induced liver fibrosis. Clin. Sci. (Lond) 129, 305-317.
33. Sinigaglia, A., Lavezzo, E., Trevisan, M., Sanavia, T., Di Camillo, B., Peta, E., Scarpa, M., Castagliuolo, I., Guido, M., Sarcognato, S. et al. (2015) Changes in microRNA expression during disease progression in patients with chronic viral hepatitis. Liver Int. 35, 1324-1333.
34. Noetel, A., Kwiecinski, M., Elfimova, N., Huang, J. and Odenthal, M. (2012) MicroRNA are central players in anti- and profibrotic gene regulation during liver fibrosis. Front. Physiol. 3, 49.
35. Su, S., Zhao, Q., He, C., Huang, D., Liu, J., Chen, F., Chen, J., Liao, J.Y., Cui, X., Zeng, Y. et al. (2015) miR-142-5p and miR-130a-3p are regulated by IL-4 and IL-13 and control profibrogenic macrophage program. Nat. Commun. 6, 8523.
36. Okada, H., Honda, M., Campbell, J.S., Takegoshi, K., Sakai, Y., Yamashita, T., Shirasaki, T., Takabatake, R., Nakamura, M., Tanaka, T. et al. (2015) Inhibition of microRNA-214 ameliorates hepatic fibrosis and tumor incidence in platelet-derived growth factor C transgenic mice. Cancer Sci. 106, 1143-1152.
37. Zhu, B., Wei, X.X., Wang, T.B., Zhou, Y.C., Liu, A.M. and Zhang, G.W. (2015) Increased miR-16 expression induced by hepatitis C virus infection promotes liver fibrosis through downregulation of hepatocyte growth factor and Smad7. Arch. Virol. 160, 2043-2050.
38. Tomita, K., Teratani, T., Suzuki, T., Shimizu, M., Sato, H., Narimatsu, K., Okada, Y., Kurihara, C., Irie, R., Yokoyama, H. et al. (2014) Free cholesterol accumulation in hepatic stellate cells: mechanism of liver fibrosis aggravation in nonalcoholic steatohepatitis in mice. Hepatology 59, 154-169.
39. Lakner, A.M., Steuerwald, N.M., Walling, T.L., Ghosh, S., Li, T., McKillop, I.H., Russo, M.W., Bonkovsky, H.L. and Schrum, L.W. (2012) Inhibitory effects of microRNA 19b in hepatic stellate cell-mediated fibrogenesis. Hepatology 56, 300-310.
40. Kwiecinski, M., Elfimova, N., Noetel, A., Töx, U., Steffen, H.M., Hacker, U., Nischt, R., Dienes, H.P. and Odenthal, M. (2012) Expression of platelet-derived growth factor-C and insulin-like growth factor I in hepatic stellate cells is inhibited by miR-29. Lab. Invest. 92, 978-987.
41. Li, J., Ghazwani, M., Zhang, Y., Lu, J., Li, J., Fan, J., Gandhi, C.R. and Li, S. (2013) miR-122 regulates collagen production via targeting hepatic stellate cells and suppressing P4HA1 expression. J. Hepatol. 58, 522-528.
42. Zhang, J., Jiao, J., Cermelli, S., Muir, K., Jung, K.H., Zou, R., Rashid, A., Gagea, M., Zabludoff, S., Kalluri, R. et al. (2015) miR-21 inhibition reduces liver fibrosis and prevents tumor development by inducing apoptosis of CD24+ progenitor cells. Cancer Res. 75, 1859-1867.
43. He, X., Xie, J., Zhang, D., Su, Q., Sai, X., Bai, R., Chen, C., Luo, X., Gao, G. and Pan, W. (2015) Recombinant adeno-associated virus-mediated inhibition of microRNA-21 protects mice against the lethal schistosome infection by repressing both IL-13 and transforming growth factor beta 1 pathways. Hepatology 61, 2008-2017.