Down-regulation of miR-192-5p protects from oxidative stress-induced acute liver injury

Clinical Science

Volumn 130, Issue 14, 2016, Pages 1197-1207

  Roy, Sanchari ^a   Benz, Fabian ^a   Alder, Jan ^a   Bantel, Heike ^b   Janssen, Joern ^a   Vucur, Mihael ^a   Gautheron, Jeremie ^a   Schneider, Anne ^a   Schüller, Florian ^a   Loosen, Sven ^a   Luedde, Mark ^c   Koch, Alexander ^a   Tacke, Frank ^a   Luedde, Tom ^a   Trautwein, Christian ^a   Roderburg, Christoph ^a  

^a RWTH AACHEN UNIVERSITY   (Germany)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c UNIVERSITY OF KIEL   (Germany)

Author keywords

Acute liver failure; Critical illness; Ischaemia reperfusion; MiR 192 5p; Serum

Indexed keywords

MICRORNA; MICRORNA 192 5P; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; HOMEODOMAIN PROTEIN; MIRN192 MICRORNA, MOUSE; REPRESSOR PROTEIN; ZFHX1B PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DEATH; CONTROLLED STUDY; CRITICALLY ILL PATIENT; DOWN REGULATION; GENE EXPRESSION; IN VITRO STUDY; LIVER CELL; LIVER INJURY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REPERFUSION INJURY; TUNEL ASSAY; UPREGULATION; ANIMAL; BLOOD; C57BL MOUSE; CELL CULTURE; CHEMICAL AND DRUG INDUCED LIVER INJURY; HUMAN; PHYSIOLOGY;

ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; CELLS, CULTURED; CHEMICAL AND DRUG INDUCED LIVER INJURY; DOWN-REGULATION; HOMEODOMAIN PROTEINS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; OXIDATIVE STRESS; REPRESSOR PROTEINS;

EID: 84994317794     PISSN: 01435221     EISSN: 14708736     Source Type: Journal    
DOI: 10.1042/CS20160216     Document Type: Article

References (42)

1. Kloosterman, W.P. and Plasterk, R.H. (2006) The diverse functions of microRNAs in animal development and disease. Dev. Cell 11, 441-450
2. Ambros, V. (2004) The functions of animal microRNAs. Nature 431, 350-355
3. Roderburg, C., Urban, G.W., Bettermann, K., Vucur, M., Zimmermann, H., Schmidt, S., Janssen, J., Koppe, C., Knolle, P., Castoldi, M. et al. (2011) Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology 53, 209-218
4. Reid, G., Kirschner, M.B. and van Zandwijk, N. (2011) Circulating microRNAs: association with disease and potential use as biomarkers. Crit. Rev. Oncol. Hematol. 80, 193-208
5. Pineau, P., Volinia, S., McJunkin, K., Marchio, A., Battiston, C., Terris, B., Mazzaferro, V., Lowe, S.W., Croce, C.M. and Dejean, A. (2010) miR-221 overexpression contributes to liver tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 107, 264-269
6. Tacke, F., Roderburg, C., Benz, F., Cardenas, D.V., Luedde, M., Hippe, H.J., Frey, N., Vucur, M., Gautheron, J., Koch, A. et al. (2014) Levels of circulating miR-133a are elevated in sepsis and predict mortality in critically ill patients. Crit. Care Med. 42, 1096-1104
7. Roderburg, C., Luedde, M., Vargas Cardenas, D., Vucur, M., Mollnow, T., Zimmermann, H.W., Koch, A., Hellerbrand, C., Weiskirchen, R., Frey, N. et al. (2013) miR-133a mediates TGF-beta-dependent derepression of collagen synthesis in hepatic stellate cells during liver fibrosis. J. Hepatol. 58, 736-742
8. Wang, K., Zhang, S., Marzolf, B., Troisch, P., Brightman, A., Hu, Z., Hood, L.E. and Galas, D.J. (2009) Circulating microRNAs, potential biomarkers for drug-induced liver injury. Proc. Natl. Acad. Sci. U.S.A. 106, 4402-4407
9. Nagano, T., Higashisaka, K., Kunieda, A., Iwahara, Y., Tanaka, K., Nagano, K., Abe, Y., Kamada, H., Tsunoda, S., Nabeshi, H. et al. (2013) Liver-specific microRNAs as biomarkers of nanomaterial-induced liver damage. Nanotechnology 24, 405102
10. Church, R.J., Otieno, M., McDuffie, J.E., Singh, B., Sonee, M., Hall, L., Watkins, P.B., Ellinger-Ziegelbauer, H. and Harrill, AH. (2016) Beyond miR-122: identification of microRNA alterations in blood during a time course of hepatobiliary injury and biliary hyperplasia in rats. Toxicol. Sci. 150, 3-14
11. Tryndyak, V.P., Latendresse, J.R., Montgomery, B., Ross, S.A., Beland, F.A., Rusyn, I. and Pogribny, I.P. (2012) Plasma microRNAs are sensitive indicators of inter-strain differences in the severity of liver injury induced in mice by a choline-and folate-deficient diet. Toxicol. App. Pharmacol. 262, 52-59
12. van der Meer, A.J., Farid, W.R., Sonneveld, M.J., de Ruiter, P.E., Boonstra, A., van Vuuren, A.J., Verheij, J., Hansen, B.E., de Knegt, R.J., van der Laan, L.J. and Janssen, H.L. (2013) Sensitive detection of hepatocellular injury in chronic hepatitis C patients with circulating hepatocyte-derived microRNA-122. J. Viral Hepat. 20, 158-166
13. Starkey Lewis, P.J., Dear, J., Platt, V., Simpson, K.J., Craig, D.G., Antoine, D.J., French, N.S., Dhaun, N., Webb, D.J., Costello, E.M. et al. (2011) Circulating microRNAs as potential markers of human drug-induced liver injury. Hepatology 54, 1767-1776
14. Hu, J., Wang, Z., Tan, C.J., Liao, B.Y., Zhang, X., Xu, M., Dai, Z., Qiu, S.J., Huang, X.W., Sun, J. et al. (2013) Plasma microRNA, a potential biomarker for acute rejection after liver transplantation. Transplantation 95, 991-999
15. Krauskopf, J., Caiment, F., Claessen, S.M., Johnson, K.J., Warner, R.L., Schomaker, S.J., Burt, D.A., Aubrecht, J. and Kleinjans, J.C. (2015) Application of high-throughput sequencing to circulating microRNAs reveals novel biomarkers for drug-induced liver injury. Toxicol. Sci. 143, 268-276
16. Jenkins, R.H., Martin, J., Phillips, A.O., Bowen, T. and Fraser, D.J. (2012) Transforming growth factor beta1 represses proximal tubular cell microRNA-192 expression through decreased hepatocyte nuclear factor DNA binding. Biochem. J. 443, 407-416
17. Silakit, R., Loilome, W., Yongvanit, P., Chusorn, P., Techasen, A., Boonmars, T., Khuntikeo, N., Chamadol, N., Pairojkul, C. and Namwat, N. (2014) Circulating miR-192 in liver fluke-associated cholangiocarcinoma patients: a prospective prognostic indicator. J. Hepatobiliary Pancreat. Sci. 21, 864-872
18. Luedde, T., Assmus, U., Wustefeld, T., Meyerzu Vilsendorf, A., Roskams, T., Schmidt-Supprian, M., Rajewsky, K., Brenner, D.A., Manns, M.P., Pasparakis, M. and Trautwein, C. (2005) Deletion of IKK2 in hepatocytes does not sensitize these cells to TNF-induced apoptosis but protects from ischemia/reperfusion injury. J. Clin. Invest. 115, 849-859
19. Vucur, M., Reisinger, F., Gautheron, J., Janssen, J., Roderburg, C., Cardenas, D.V., Kreggenwinkel, K., Koppe, C., Hammerich, L., Hakem, R. et al. (2013) RIP3 inhibits inflammatory hepatocarcinogenesis but promotes cholestasis by controlling caspase-8-and JNK-dependent compensatory cell proliferation. Cell Rep 4, 776-790
20. Bettermann, K., Vucur, M., Haybaeck, J., Koppe, C., Janssen, J., Heymann, F., Weber, A., Weiskirchen, R., Liedtke, C., Gassler, N. et al. (2010) TAK1 suppresses a NEMO-dependent but NF-kappaB-independent pathway to liver cancer. Cancer Cell 17, 481-496
21. Roderburg, C., Benz, F., Vargas Cardenas, D., Koch, A., Janssen, J., Vucur, M., Gautheron, J., Schneider, A.T., Koppe, C., Kreggenwinkel, K. et al. (2015) Elevated miR-122 serum levels are an independent marker of liver injury in inflammatory diseases. Liver Int 35, 1172-1184
22. Gautheron, J., Pescatore, A., Fusco, F., Esposito, E., Yamaoka, S., Agou, F., Ursini, M.V. and Courtois, G. (2010) Identification of a new NEMO/TRAF6 interface affected in incontinentia pigmenti pathology. Hum. Mol. Genet. 19, 3138-3149
23. Benz, F., Roderburg, C., Vargas Cardenas, D., Vucur, M., Gautheron, J., Koch, A., Zimmermann, H., Janssen, J., Nieuwenhuijsen, L., Luedde, M. et al. (2013) U6 is unsuitable for normalization of serum miRNA levels in patients with sepsis or liver fibrosis. Exp. Mol. Med. 45, e42
24. Roy, S., Benz, F., Vargas Cardenas, D., Vucur, M., Gautheron, J., Schneider, A., Hellerbrand, C., Pottier, N., Alder, J., Tacke, F. et al. (2015) miR-30c and miR-193 are a part of the TGF-beta-dependent regulatory network controlling extracellular matrix genes in liver fibrosis. J. Dig. Dis. 16, 513-524
25. John, K., Hadem, J., Krech, T., Wahl, K., Manns, M.P., Dooley, S., Batkai, S., Thum, T., Schulze-Osthoff, K. and Bantel, H. (2014) MicroRNAs play a role in spontaneous recovery from acute liver failure. Hepatology 60, 1346-1355
26. Takahashi, Y., Ganster, R.W., Gambotto, A., Shao, L., Kaizu, T., Wu, T., Yagnik, G.P., Nakao, A., Tsoulfas, G., Ishikawa, T. et al. (2002) Role of NF-kappaB on liver cold ischemia-reperfusion injury. Am. J. Physiol. Gastrointest. Liver Physiol. 283, G1175-G1184
27. Meng, X.M., Tang, P.M., Li, J. and Lan, H.Y. (2015) TGF-beta/Smad signaling in renal fibrosis. Front. Physiol. 6, 82
28. Teoh, N., Field, J., Sutton, J. and Farrell, G. (2004) Dual role of tumor necrosis factor-alpha in hepatic ischemia-reperfusion injury: studies in tumor necrosis factor-alpha gene knockout mice. Hepatology 39, 412-421
29. Luedde, T., Kaplowitz, N. and Schwabe, R.F. (2014) Cell death and cell death responses in liver disease: mechanisms and clinical relevance. Gastroenterology 147, 765-783
30. Gautheron, J., Vucur, M., Reisinger, F., Cardenas, D.V., Roderburg, C., Koppe, C., Kreggenwinkel, K., Schneider, A.T., Bartneck, M., Neumann, U.P. et al. (2014) A positive feedback loop between RIP3 and JNK controls non-alcoholic steatohepatitis. EMBO Mol. Med. 6, 1062-1074
31. Zhang, W., Wang, M., Xie, H.Y., Zhou, L., Meng, X.Q., Shi, J. and Zheng, S. (2007) Role of reactive oxygen species in mediating hepatic ischemia-reperfusion injury and its therapeutic applications in liver transplantation. Transplant. Proc. 39, 1332-1337
32. Rubinfeld, H., Kammer, A., Cohen, O., Gorshtein, A., Cohen, Z.R., Hadani, M., Werner, H. and Shimon, I. (2014) IGF1 induces cell proliferation in human pituitary tumors - functional blockade of IGF1 receptor as a novel therapeutic approach in non-functioning tumors. Mol. Cell. Endocrinol. 390, 93-101
33. Qiuping, Z., Jie, X., Youxin, J., Qun, W., Wei, J., Chun, L., Jin, W., Yan, L., Chunsong, H., Mingzhen, Y. et al. (2005) Selectively frequent expression of CXCR5 enhances resistance to apoptosis in CD8(+)CD34(+) T cells from patients with T-cell-lineage acute lymphocytic leukemia. Oncogene 24, 573-584
34. Shen, J.Z., Zhang, Y.Y., Fu, H.Y., Wu, D.S. and Zhou, H.R. (2014) Overexpression of microRNA-143 inhibits growth and induces apoptosis in human leukemia cells. Oncol. Rep. 31, 2035-2042
35. Dasgupta, P., Rizwani, W., Pillai, S., Davis, R., Banerjee, S., Hug, K., Lloyd, M., Coppola, D., Haura, E. and Chellappan, S.P. (2011) ARRB1-mediated regulation of E2F target genes in nicotine-induced growth of lung tumors. J. Natl. Cancer Inst. 103, 317-333
36. Qi, S., Song, Y., Peng, Y., Wang, H., Long, H., Yu, X., Li, Z., Fang, L., Wu, A., Luo, W. et al. (2012) ZEB2 mediates multiple pathways regulating cell proliferation, migration, invasion, and apoptosis in glioma. PLoS One 7, e38842
37. Clarke, J.D., Sharapova, T., Lake, A.D., Blomme, E., Maher, J. and Cherrington, N.J. (2014) Circulating microRNA 122 in the methionine and choline-deficient mouse model of non-alcoholic steatohepatitis. J. Appl. Toxicol. 34, 726-732
38. Kim, T., Veronese, A., Pichiorri, F., Lee, T.J., Jeon, Y.J., Volinia, S., Pineau, P., Marchio, A., Palatini, J., Suh, S.S. et al. p53 regulates epithelial-mesenchymal transition through microRNAs targeting ZEB1 and ZEB2. J. Exp. Med. 208, 875-883
39. Techasen, A., Namwat, N., Loilome, W., Duangkumpha, K., Puapairoj, A., Saya, H. and Yongvanit, P Tumor necrosis factor-alpha modulates epithelial mesenchymal transition mediators ZEB2 and S100A4 to promote cholangiocarcinoma progression. J. Hepatobiliary Pancreat. Sci. 21, 703-711
40. Janssen, H.L., Reesink, H.W., Lawitz, E.J., Zeuzem, S., Rodriguez-Torres, M., Patel, K., van der Meer, A.J., Patick, A.K., Chen, A., Zhou, Y. et al. (2013) Treatment of HCV infection by targeting microRNA. N. Engl. J. Med. 368, 1685-1694
41. Krauskopf, J., Caiment, F., Claessen, S.M., Johnson, K.J., Warner, R.L., Schomaker, S.J., Burt, D.A., Aubrecht, J. and Kleinjans, J.C. (2015) Application of high-throughput sequencing to circulating microRNAs reveals novel biomarkers for drug-induced liver injury. Toxicol. Sci. 143, 268-276
42. Bala, S., Petrasek, J., Mundkur, S., Catalano, D., Levin, I., Ward, J., Alao, H., Kodys, K. and Szabo, G. (2012) Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology 56, 1946-1957