MicroRNA-378 limits activation of hepatic stellate cells and liver fibrosis by suppressing Gli3 expression

Nature Communications

Volumn 7, Issue , 2016, Pages

  Hyun, Jeongeun ^a   Wang, Sihyung ^a   Kim, Jieun ^a   Rao, Kummara Madhusudana ^a   Park, Soo Yong ^a   Chung, Ildoo ^a   Ha, Chang Sik ^a   Kim, Sang Woo ^a   Yun, Yang H ^b   Jung, Youngmi ^a  

^a Pusan National University   (South Korea)

^b University of Akron   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MICRORNA; MICRORNA 378A 3P; MICRORNA 378B; MICRORNA 378D; TRANSCRIPTION FACTOR GLI3; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; CARBON TETRACHLORIDE; CHOLINE; ETHIONINE; G PROTEIN COUPLED RECEPTOR; GLI3 PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; MESSENGER RNA; METHIONINE; MIRN378 MICRORNA, HUMAN; MIRN378 MICRORNA, MOUSE; NANOPARTICLE; NERVE PROTEIN; PROTEIN BINDING; SMO PROTEIN, MOUSE; SMOOTHENED PROTEIN; TRANSCRIPTION FACTOR GLI2;

CELLS AND CELL COMPONENTS; GENE; GENE EXPRESSION; GENETIC MARKER; RNA; TUMOR;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL ACTIVATION; CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; LIVER CELL; LIVER FIBROSIS; MOUSE; NONHUMAN; PATHOGENESIS; SIGNAL TRANSDUCTION; STELLATE CELL; UPREGULATION; ANIMAL; C57BL MOUSE; CHEMISTRY; CHRONIC DISEASE; GENE EXPRESSION REGULATION; GENETICS; HEPATIC STELLATE CELL; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; MALE; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY;

ERINACEIDAE; MUS; ZEA MAYS;

ANIMALS; BASE SEQUENCE; CARBON TETRACHLORIDE; CARCINOMA, HEPATOCELLULAR; CHOLINE; CHRONIC DISEASE; DOWN-REGULATION; ETHIONINE; GENE EXPRESSION REGULATION; HEPATIC STELLATE CELLS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LIVER CIRRHOSIS; MALE; METHIONINE; MICE, INBRED C57BL; MICRORNAS; MOLECULAR SEQUENCE DATA; NANOPARTICLES; NERVE TISSUE PROTEINS; PROTEIN BINDING; RECEPTORS, G-PROTEIN-COUPLED; RNA, MESSENGER; SMOOTHENED RECEPTOR; TRANSCRIPTION FACTOR RELA;

EID: 84961657949     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10993     Document Type: Article

References (68)

1. Kim, Y. et al. Temporal trends in population-based death rates associated with chronic liver disease and liver cancer in the United States over the last 30 years. Cancer 120, 3058-3065 (2014).
2. Bataller, R. & Brenner, D. A. Liver fibrosis. J. Clin. Invest. 115, 209-218 (2005).
3. Kim, V. N. MicroRNA biogenesis: coordinated cropping and dicing. Nat. Rev. Mol. Cell Biol. 6, 376-385 (2005).
4. Bartel, D. P. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233 (2009).
5. Bartel, D. P. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297 (2004).
6. MacFarlane, L.-A. & Murphy, P. R. MicroRNA: biogenesis, function and role in cancer. Curr. Genomics 11, 537-561 (2010).
7. Choi, S. S., Omenetti, A., Syn, W.-K. & Diehl, A. M. The role of Hedgehog signaling in fibrogenic liver repair. Int. J. Biochem. Cell Biol. 43, 238-244 (2011).
8. Omenetti, A., Choi, S., Michelotti, G. & Diehl, A. M. Hedgehog signaling in the liver. J. Hepatol. 54, 366-373 (2011).
9. Jung, Y. et al. Signals from dying hepatocytes trigger growth of liver progenitors. Gut 59, 655-665 (2010).
10. Rangwala, F. et al. Increased production of sonic hedgehog by ballooned hepatocytes. J. Pathol. 224, 401-410 (2011).
11. Chen, Y. et al. Hedgehog controls hepatic stellate cell fate by regulating metabolism. Gastroenterology 143, 1319-1329.e1311 (2012).
12. Yang, L. et al. Sonic hedgehog is an autocrine viability factor for myofibroblastic hepatic stellate cells. J. Hepatol. 48, 98-106 (2008).
13. Shah, P. N., Lopina, S. T. & Yun, Y. H. Blends of novel L-tyrosine based polyurethanes and polyphosphate for potential biomedical applications. J. Appl. Polym. Sci. 114, 3235-3247 (2009).
14. Shah, P. N. & Yun, Y. H. Cellular interactions with biodegradable polyurethanes formulated from L-tyrosine. J. Biomater. Appl. 27, 1017-1031 (2013).
15. Shi, J., Aisaki, K., Ikawa, Y. & Wake, K. Evidence of hepatocyte apoptosis in rat liver after the administration of carbon tetrachloride. Am. J. Pathol. 153, 515-525 (1998).
16. Yin, C., Evason, K. J., Asahina, K. & Stainier, D. Y. Hepatic stellate cells in liver development, regeneration, and cancer. J. Clin. Invest. 123, 1902-1910 (2013).
17. Wunsch, E. et al. Liver expression of sulphotransferase 2A1 enzyme is impaired in patients with primary sclerosing cholangitis: lack of the response to enhanced expression of PXR. J. Immunol. Res. 2015, 1-8 (2015).
18. Bataller, R. & Brenner, D. A. Hepatic stellate cells as a target for the treatment of liver fibrosis. Semin. Liver Dis. 21, 437-452 (2001).
19. Reeves, H. L. & Friedman, S. L. Activation of hepatic stellate cells-a key issue in liver fibrosis. Front. Biosci. 7, 808-826 (2002).
20. Choi, S. S. et al. Hedgehog pathway activation and epithelial-to-mesenchymal transitions during myofibroblastic transformation of rat hepatic cells in culture and cirrhosis. Am. J. Physiol. Gastrointest. Liver Physiol. 297, G1093-G1106 (2009).
21. Friedman, S. L., Roll, F. J., Boyles, J. & Bissell, D. M. Hepatic lipocytes: the principal collagen-producing cells of normal rat liver. Proc. Natl Acad. Sci. USA 82, 8681-8685 (1985).
22. Betel, D., Wilson, M., Gabow, A., Marks, D. S. & Sander, C. The microRNA.org resource: targets and expression. Nucleic Acids Res. 36, D149-D153 (2008).
23. Pritchett, J. et al. Osteopontin is a novel downstream target of SOX9 with diagnostic implications for progression of liver fibrosis in humans. Hepatology 56, 1108-1116 (2012).
24. Kisseleva, T. et al. Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis. Proc. Natl. Acad. Sci. USA 109, 9448-9453 (2012).
25. Friedman, S. L. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 88, 125-172 (2008).
26. Schmittgen, T. D. et al. Real-time PCR quantification of precursor and mature microRNA. Methods 44, 31-38 (2008).
27. Wang, S. et al. Potential role of Hedgehog pathway in liver response to radiation. PLoS ONE 8, e74141 (2013).
28. Bellafante, E. et al. Hepatic-specific activation of peroxisome proliferator-activated receptor γ coactivator-1β protects against steatohepatitis. Hepatology 57, 1343-1356 (2013).
29. Nagalingam, R. S. et al. Deficiency of cardiomyocyte-specific microRNA-378 contributes to the development of cardiac fibrosis involving a transforming growth factor β (TGFβ1)-dependent paracrine mechanism. J. Biol. Chem. 289, 27199-27214 (2014).
30. Suzuki, Y. & Nakayama, M. Differential profiles of genes expressed in neonatal brain of 129X1/SvJ and C57BL/6J mice: A database to aid in analyzing DNA microarrays using nonisogenic gene-targeted mice. DNA Res. 10, 263-275 (2003).
31. Fan, X., Shao, L., Fang, H., Tong, W. & Cheng, Y. Cross-platform comparison of microarray-based multiple-class prediction. PLoS ONE 6, e16067 (2011).
32. Li, W. Q. et al. The rno-miR-34 family is upregulated and targets ACSL1 in dimethylnitrosamine-induced hepatic fibrosis in rats. FEBS J. 278, 1522-1532 (2011).
33. Ameres, S. L. & Zamore, P. D. Diversifying microRNA sequence and function. Nat. Rev. Mol. Cell Biol. 14, 475-488 (2013).
34. Friedman, S. L. et al. Isolated hepatic lipocytes and kupffer cells from normal human liver: morphological and functional characteristics in primary culture. Hepatology 15, 234-243 (1992).
35. Sicklick, J. K. et al. Role for hedgehog signaling in hepatic stellate cell activation and viability. Lab. Invest. 85, 1368-1380 (2005).
36. Xie, G. et al. Hedgehog signalling regulates liver sinusoidal endothelial cell capillarisation. Gut 62, 299-309 (2013).
37. de Almeida Pereira, T. et al. Viral factors induce Hedgehog pathway activation in humans with viral hepatitis, cirrhosis, and hepatocellular carcinoma. Lab. Invest. 90, 1690-1703 (2010).
38. Witek, R. P. et al. Liver cell-derived microparticles activate hedgehog signaling and alter gene expression in hepatic endothelial cells. Gastroenterology 136, 320-330.e322 (2009).
39. Buttitta, L., Mo, R., Hui, C.-C. & Fan, C.-M. Interplays of Gli2 and Gli3 and their requirement in mediating Shh-dependent sclerotome induction. Development 130, 6233-6243 (2003).
40. Hu, M. C. et al. GLI3-dependent transcriptional repression of Gli1, Gli2 and kidney patterning genes disrupts renal morphogenesis. Development 133, 569-578 (2006).
41. Hyun, J., Wang, S., Kim, J., Kim, G. J. & Jung, Y. MicroRNA125b-mediated Hedgehog signaling influences liver regeneration by chorionic plate-derived mesenchymal stem cells. Sci. Rep. 5, 14135 (2015).
42. Oeckinghaus, A. & Ghosh, S. The NF-κB family of transcription factors and its regulation. Cold Spring Harb. Perspect. Biol. 1, a000034 (2009).
43. Ghosh, S., May, M. J. & Kopp, E. B. NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol. 16, 225-260 (1998).
44. Roderburg, C. et al. Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology 53, 209-218 (2011).
45. Ma, X., Buscaglia, L. E. B., Barker, J. R. & Li, Y. MicroRNAs in NF-κB signaling. J. Mol. Cell Biol. 3, 159-166 (2011).
46. Bruix, J., Boix, L., Sala, M. & Llovet, J. M. Focus on hepatocellular carcinoma. Cancer Cell 5, 215-219 (2004).
47. Ascha, M. S. et al. The incidence and risk factors of hepatocellular carcinoma in patients with nonalcoholic steatohepatitis. Hepatology 51, 1972-1978 (2010).
48. Chan, I. S. et al. Paracrine Hedgehog signaling drives metabolic changes in hepatocellular carcinoma. Cancer Res. 72, 6344-6350 (2012).
49. Huang, S. et al. Activation of the hedgehog pathway in human hepatocellular carcinomas. Carcinogenesis 27, 1334-1340 (2006).
50. Zhao, W. et al. Activated hepatic stellate cells promote hepatocellular carcinoma development in immunocompetent mice. Int. J. Cancer 129, 2651-2661 (2011).
51. Amann, T. et al. Activated hepatic stellate cells promote tumorigenicity of hepatocellular carcinoma. Cancer Sci. 100, 646-653 (2009).
52. Carloni, V., Luong, T. V. & Rombouts, K. Hepatic stellate cells and extracellular matrix in hepatocellular carcinoma: more complicated than ever. Liver Int. 34, 834-843 (2014).
53. Li, L., Gao, Q., Wang, X. & Guo, Z. [miR-378 suppresses HBV-related hepatocellular carcinoma tumor growth by directly targeting the insulin-like growth factor 1 receptor]. Zhonghua Gan Zang Bing Za Zhi 21, 609-613 (2013).
54. An, J. et al. A genetic variant in primary miR-378 is associated with risk and prognosis of hepatocellular carcinoma in a Chinese population. PLoS ONE 9, e93707 (2014).
55. Tu, X. et al. MicroRNA-101 suppresses liver fibrosis by targeting TGFβ signaling pathway. J. Pathol. 234, 46-59 (2014).
56. Su, S. et al. miR-142-5p and miR-130a-3p are regulated by IL-4 and IL-13 and control profibrogenic macrophage program. Nat. Commun. 6, 8523 (2015).
57. Ditto, A. J., Shah, P. N., Gump, L. R. & Yun, Y. H. Nanospheres formulated from L-tyrosine polyphosphate exhibiting sustained release of polyplexes and in vitro controlled transfection properties. Mol. Pharm. 6, 986-995 (2009).
58. Ditto, A. J. et al. In vivo gene delivery with l-tyrosine polyphosphate nanoparticles. Mol. Pharm. 10, 1836-1844 (2013).
59. Yang, B. B., Lum, P. K., Hayashi, M. M. & Roskos, L. K. Polyethylene glycol modification of filgrastim results in decreased renal clearance of the protein in rats. J. Pharm. Sci. 93, 1367-1373 (2004).
60. Yi, H.-S. et al. Treatment with 4-methylpyrazole modulated stellate cells and natural killer cells and ameliorated liver fibrosis in mice. PLoS ONE 10, e0127946 (2015).
61. Suh, Y. G. et al. CD11b+ Gr1+ bone marrow cells ameliorate liver fibrosis by producing interleukin-10 in mice. Hepatology 56, 1902-1912 (2012).
62. Philips, G. M. et al. Hedgehog signaling antagonist promotes regression of both liver fibrosis and hepatocellular carcinoma in a murine model of primary liver cancer. PLoS ONE 6, e23943 (2011).
63. Horiguchi, N. et al. Cell type-dependent pro-and anti-inflammatory role of signal transducer and activator of transcription 3 in alcoholic liver injury. Gastroenterology 134, 1148-1158 (2008).
64. Radaeva, S. et al. Natural killer cells ameliorate liver fibrosis by killing activated stellate cells in nkg2d-dependent and tumor necrosis factor-related apoptosisinducing ligand-dependent manners. Gastroenterology 130, 435-452 (2006).
65. cip1: Regulation by SOCS3. Biochem. Biophys. Res. Commun. 338, 1943-1949 (2005).
66. Smedsrød, B. & Pertoft, H. Preparation of pure hepatocytes and reticuloendothelial cells in high yield from a single rat liver by means of Percoll centrifugation and selective adherence. J. Leukoc. Biol. 38, 213-230 (1985).
67. Jeong, D. et al. MicroRNA-124 links p53 to the NF-κB pathway in B-cell lymphomas. Leukemia 29, 1868-1874 (2015).
68. Ozpolat, B., Sood, A. & Lopez-Berestein, G. Nanomedicine based approaches for the delivery of siRNA in cancer. J. Intern. Med. 267, 44-53 (2010).