Novel hepatic microRNAs upregulated in human nonalcoholic fatty liver disease

Physiological Reports

Volumn 4, Issue 1, 2016, Pages

  Soronen, Jarkko ^a,b   Yki Järvinen, Hannele ^b,c   Zhou, You ^b   Sädevirta, Sanja ^b,c   Sarin, Antti Pekka ^a,c   Leivonen, Marja ^d   Sevastianova, Ksenia ^b,c   Perttilä, Julia ^b   Laurila, Pirkka Pekka ^a   Sigruener, Alexander ^e   Schmitz, Gerd ^e   Olkkonen, Vesa M ^b,f  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b MINERVA FOUNDATION INSTITUTE FOR MEDICAL RESEARCH   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

^d HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^e UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^f UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Hepatocyte; immortalized human hepatocytes; liver biopsy; microarray; microRNA; nonalcoholic fatty liver disease

Indexed keywords

MICRORNA;

ADULT; BIOSYNTHESIS; CELL CULTURE; CROSS-SECTIONAL STUDY; FEMALE; HEPG2 CELL LINE; HUMAN; LIVER; LIVER CELL; MALE; METABOLISM; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY; PHYSIOLOGY; TRANSFORMED CELL LINE; UPREGULATION;

ADULT; CELL LINE, TRANSFORMED; CELLS, CULTURED; CROSS-SECTIONAL STUDIES; FEMALE; HEP G2 CELLS; HEPATOCYTES; HUMANS; LIVER; MALE; MICRORNAS; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; UP-REGULATION;

EID: 84987648111     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/PHY2.12661     Document Type: Article

References (65)

1. Alisi, A., L. Da Sacco, G. Bruscalupi, F. Piemonte, N. Panera, R. De Vito, et al. 2011. Mirnome analysis reveals novel molecular determinants in the pathogenesis of diet-induced nonalcoholic fatty liver disease. Lab. Invest. 91:283–293.
2. Bakan, I., and M. Laplante. 2012. Connecting mTORC1 signaling to SREBP-1 activation. Curr. Opin. Lipidol. 23:226–234.
3. Baker, S. S., R. D. Baker, W. Liu, N. J. Nowak, and L. Zhu. 2010. Role of alcohol metabolism in non-alcoholic steatohepatitis. PLoS One 5:e9570.
4. Bellentani, S., F. Scaglioni, M. Marino, and G. Bedogni. 2010. Epidemiology of non-alcoholic fatty liver disease. Dig. Dis. 28:155–161.
5. Braunersreuther, V., G. L. Viviani, F. Mach, and F. Montecucco. 2012. Role of cytokines and chemokines in non-alcoholic fatty liver disease. World J. Gastroenterol. 18:727–735.
6. Castro, R. E., D. M. Ferreira, M. B. Afonso, P. M. Borralho, M. V. Machado, H. Cortez-Pinto, et al. 2013. miR-34a/ SIRT1/p53 is suppressed by ursodeoxycholic acid in the rat liver and activated by disease severity in human nonalcoholic fatty liver disease. J. Hepatol. 58:119–125.
7. Cazanave, S. C., J. L. Mott, N. A. Elmi, S. F. Bronk, H. C. Masuoka, M. R. Charlton, et al. 2011. A role for miR-296 in the regulation of lipoapoptosis by targeting PUMA. J. Lipid Res. 52:1517–1525.
8. Cheung, O., P. Puri, C. Eicken, M. J. Contos, F. Mirshahi, J. W. Maher, et al. 2008. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression. Hepatology 48:1810–1820.
9. Choi, Y. M., S. An, E. M. Lee, K. Kim, S. J. Choi, J. S. Kim, et al. 2012. CYP1A1 is a target of miR-892a-mediated posttranscriptional repression. Int. J. Oncol. 41:331–336.
10. Dooley, S., and P. ten Dijke. 2012. TGF-beta in progression of liver disease. Cell Tissue Res. 347:245–256.
11. Ferreira, D. M., A. L. Simao, C. M. Rodrigues, and R. E. Castro. 2014. Revisiting the metabolic syndrome and paving the way for microRNAs in non-alcoholic fatty liver disease. FEBS J. 281:2503–2524.
12. Fukuhara, T., and Y. Matsuura. 2013. Role of miR-122 and lipid metabolism in HCV infection. J. Gastroenterol. 48:169–176.
13. Ge, Y., K. Zhao, Y. Qi, X. Min, Z. Shi, X. Qi, et al. 2013. Serum microRNA expression profile as a biomarker for the diagnosis of pertussis. Mol. Biol. Rep. 40:1325–1332.
14. Gutschner, T., M. Hämmerle, N. Pazaitis, N. Bley, E. Fiskin, H. Uckelmann, et al. 2014. Insulin-like growth factor 2 mRNA-binding protein 1 (IGF2BP1) is an important protumorigenic factor in hepatocellular carcinoma. Hepatology 59:1900–1911.
15. Jiang, M., R. Broering, M. Trippler, J. Wu, E. Zhang, X. Zhang, et al. 2014. MicroRNA-155 controls Toll-like receptor 3-and hepatitis C virus-induced immune responses in the liver. J. Viral Hepat. 21:99–110.
16. Kida, K., M. Nakajima, T. Mohri, Y. Oda, S. Takagi, T. Fukami, et al. 2011. PPARalpha is regulated by miR-21 and miR-27b in human liver. Pharm. Res. 28:2467–2476.
17. Kleiner, D. E., E. M. Brunt, M. Van Natta, C. Behling, M. J. Contos, O. W. Cummings, et al. 2005. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41:1313–1321.
18. Kohjima, M., M. Enjoji, N. Higuchi, M. Kato, K. Kotoh, T. Yoshimoto, et al. 2007. Re-evaluation of fatty acid metabolism-related gene expression in nonalcoholic fatty liver disease. Int. J. Mol. Med. 20:351–358.
19. Kohjima, M., N. Higuchi, M. Kato, K. Kotoh, T. Yoshimoto, T. Fujino, et al. 2008. SREBP-1c, regulated by the insulin and AMPK signaling pathways, plays a role in nonalcoholic fatty liver disease. Int. J. Mol. Med. 21:507–511.
20. Kotronen, A., J. Westerbacka, R. Bergholm, K. H. Pietilainen, and H. Yki-Jarvinen. 2007. Liver fat in the metabolic syndrome. J. Clin. Endocrinol. Metab. 92:3490–3497.
21. Lakner, A. M., N. M. Steuerwald, T. L. Walling, S. Ghosh, T. Li, I. H. McKillop, et al. 2012. Inhibitory effects of microRNA 19b in hepatic stellate cell-mediated fibrogenesis. Hepatology 56:300–310.
22. Lankisch, T. O., T. Voigtlander, M. P. Manns, A. Holzmann, S. Dangwal, and T. Thum. 2014. MicroRNAs in the bile of patients with biliary strictures after liver transplantation. Liver Transpl. 20:673–678.
23. Li, Z., X. Gu, Y. Fang, J. Xiang, and Z. Chen. 2012. microRNA expression profiles in human colorectal cancers with brain metastases. Oncol. Lett. 3:346–350.
24. Li, B., Z. Zhang, H. Zhang, K. Quan, Y. Lu, D. Cai, et al. 2014a. Aberrant miR199a-5p/ Caveolin1/ PPARalpha axis in hepatic steatosis. J. Mol. Endocrinol. 53:393–403.
25. Li, Z., G. Xu, Y. Qin, C. Zhang, H. Tang, Y. Yin, et al. 2014b. Ghrelin promotes hepatic lipogenesis by activation of mTOR-PPARgamma signaling pathway. Proc. Natl Acad. Sci. USA 111:13163–13168.
26. Liu, L., J. Zou, Q. Wang, F. Q. Yin, W. Zhang, and L. Li. 2014. Novel microRNAs expression of patients with chemotherapy drug-resistant and chemotherapy-sensitive epithelial ovarian cancer. Tumour Biol. 35:7713–7717.
27. Lopez-Vicario, C., A. Gonzalez-Periz, B. Rius, E. Moran Salvador, V. Garcia-Alonso, J. J. Lozano, et al. 2014. Molecular interplay between Delta5/Delta6 desaturases and long-chain fatty acids in the pathogenesis of non-alcoholic steatohepatitis. Gut 63:344–355.
28. Lu, Z. M., Y. F. Lin, L. Jiang, L. S. Chen, X. N. Luo, X. H. Song, et al. 2014. Micro-ribonucleic acid expression profiling and bioinformatic target gene analyses in laryngeal carcinoma. Onco Targets Ther. 7:525–533.
29. Mairinger, F. D., S. Ting, R. Werner, R. F. Walter, T. Hager, C. Vollbrecht, et al. 2014. Different micro-RNA expression profiles distinguish subtypes of neuroendocrine tumors of the lung: results of a profiling study. Mod. Pathol. 27:1632– 1640.
30. Martinez-Ramos, R., J. R. Garcia-Lozano, J. M. Lucena, M. J. Castillo-Palma, F. Garcia-Hernandez, M. C. Rodriguez, et al. 2014. Differential expression pattern of microRNAs in CD4+ and CD19+ cells from asymptomatic patients with systemic lupus erythematosus. Lupus 23:353–359.
31. Mazzoccoli, G., M. Vinciguerra, J. Oben, R. Tarquini, and S. De Cosmo. 2014. Non-alcoholic fatty liver disease: the role of nuclear receptors and circadian rhythmicity. Liver Int. 34:1133–1152.
32. Meli, R., G. Mattace Raso, and A. Calignano. 2014. Role of innate immune response in non-alcoholic Fatty liver disease: metabolic complications and therapeutic tools. Front Immunol. 5:177.
33. Min, H. K., A. Kapoor, M. Fuchs, F. Mirshahi, H. Zhou, J. Maher, et al. 2012. Increased hepatic synthesis and dysregulation of cholesterol metabolism is associated with the severity of nonalcoholic fatty liver disease. Cell Metab. 15:665–674.
34. Morita, M., S. P. Gravel, L. Hulea, O. Larsson, M. Pollak, J. St-Pierre, et al. 2015. mTOR coordinates protein synthesis, mitochondrial activity and proliferation. Cell Cycle 14:473– 480.
35. Naik, A., R. Kosir, and D. Rozman. 2013. Genomic aspects of NAFLD pathogenesis. Genomics 102:84–95.
36. Ogawa, T., M. Enomoto, H. Fujii, Y. Sekiya, K. Yoshizato, K. Ikeda, et al. 2012. MicroRNA-221/222 upregulation indicates the activation of stellate cells and the progression of liver fibrosis. Gut 61:1600–1609.
37. Pasquinelli, A. E. 2012. MicroRNAs and their targets: recognition, regulation and an emerging reciprocal relationship. Nat. Rev. Genet. 13:271–282.
38. Perry, R. J., V. T. Samuel, K. F. Petersen, and G. I. Shulman. 2014. The role of hepatic lipids in hepatic insulin resistance and type 2 diabetes. Nature 510:84–91.
39. Pettinelli, P., T. Del Pozo, J. Araya, R. Rodrigo, A. V. Araya, G. Smok, et al. 2009. Enhancement in liver SREBP-1c/ PPAR-alpha ratio and steatosis in obese patients: correlations with insulin resistance and n-3 long-chain polyunsaturated fatty acid depletion. Biochim. Biophys. Acta 1792:1080–1086.
40. Pirola, C. J., T. Fernandez Gianotti, G. O. Castano, P. Mallardi, J. San Martino, M. Mora Gonzalez Lopez Ledesma, et al. 2014. Circulating microRNA signature in non-alcoholic fatty liver disease: from serum non-coding RNAs to liver histology and disease pathogenesis. Gut 64:800–812.
41. Pogribny, I. P., A. Starlard-Davenport, V. P. Tryndyak, T. Han, S. A. Ross, I. Rusyn, et al. 2010. Difference in expression of hepatic microRNAs miR-29c, miR-34a, miR155, and miR-200b is associated with strain-specific susceptibility to dietary nonalcoholic steatohepatitis in mice. Lab. Invest. 90:1437–1446.
42. Rottiers, V., and A. M. Naar. 2012. MicroRNAs in metabolism and metabolic disorders. Nat. Rev. Mol. Cell Biol. 13:239– 250.
43. Samanez, C. H., S. Caron, O. Briand, H. Dehondt, I. Duplan, F. Kuipers, et al. 2012. The human hepatocyte cell lines IHH and HepaRG: models to study glucose, lipid and lipoprotein metabolism. Arch. Physiol. Biochem. 118:102–111.
44. Sand, M., M. Skrygan, D. Sand, D. Georgas, T. Gambichler, S. A. Hahn, et al. 2013. Comparative microarray analysis of microRNA expression profiles in primary cutaneous malignant melanoma, cutaneous malignant melanoma metastases, and benign melanocytic nevi. Cell Tissue Res. 351:85–98.
45. Sarma, N. J., V. Tiriveedhi, J. S. Crippin, W. C. Chapman, and T. Mohanakumar. 2014. Hepatitis C virus-induced changes in microRNA 107 (miRNA-107) and miRNA-449a modulate CCL2 by targeting the interleukin-6 receptor complex in hepatitis. J. Virol. 88:3733–3743.
46. Schultze, S. M., B. A. Hemmings, M. Niessen, and O. Tschopp. 2012. PI3K/AKT, MAPK and AMPK signalling: protein kinases in glucose homeostasis. Expert Rev. Mol. Med. 14:e1.
47. Selbach, M., B. Schwanhausser, N. Thierfelder, Z. Fang, R. Khanin, and N. Rajewsky. 2008. Widespread changes in protein synthesis induced by microRNAs. Nature 455:58– 63.
48. Sharma, M., F. Urano, and A. Jaeschke. 2012. Cdc42 and Rac1 are major contributors to the saturated fatty acid-stimulated JNK pathway in hepatocytes. J. Hepatol. 56:192–198.
49. Sobolewski, C., N. Calo, D. Portius, and M. Foti. 2015. MicroRNAs is fatty liver disease. Semin. Liver Dis. 35:12–25.
50. Taniguchi, C. M., K. Ueki, and R. Kahn. 2005. Complementary roles of IRS-1 and IRS-2 in the hepatic regulation of metabolism. J. Clin. Invest. 115:718–727.
51. Trajkovski, M., J. Hausser, J. Soutschek, B. Bhat, A. Akin, M. Zavolan, et al. 2011. MicroRNAs 103 and 107 regulate insulin sensitivity. Nature 474:649–653.
52. Tsang, J., J. Zhu, and A. van Oudenaarden. 2007. MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol. Cell 26:753– 767.
53. Tyagi, S., P. Gupta, A. S. Saini, C. Kaushal, and S. Sharma. 2011. The peroxisome proliferator-activated receptor: a family of nuclear receptors role in various diseases. J. Adv. Pharm. Technol. Res. 2:236–240.
54. Vasudevan, S., Y. Tong, and J. A. Steitz. 2007. Switching from repression to activation: microRNAs can up-regulate translation. Science 318:1931–1934.
55. Videla, L. A., and P. Pettinelli. 2012. Misregulation of PPAR functioning and its pathogenic consequences associated with nonalcoholic fatty liver disease in human obesity. PPAR Res. 2012:107434.
56. Vinciguerra, M., C. Veyrat-Durebex, M. A. Moukil, L. Rubbia Brandt, F. Rohner-Jeanrenaud, and M. Foti. 2008. PTEN down-regulation by unsaturated fatty acids triggers hepatic steatosis via an NF-kappaBp65/mTOR-dependent mechanism. Gastroenterology 134:268–280.
57. Vinciguerra, M., A. Sgroi, C. Veyrat-Durebex, L. RubbiaBrandt, L. H. Buhler, and M. Foti. 2009. Unsaturated fatty acids inhibit the expression of tumor suppressor phosphatase and tensin homolog (PTEN) via microRNA-21 up-regulation in hepatocytes. Hepatology 49:1176–1184.
58. Wang, W., G. Xu, C. L. Ding, L. J. Zhao, P. Zhao, H. Ren, et al. 2013. All-trans retinoic acid protects hepatocellular carcinoma cells against serum-starvation-induced cell death by upregulating collagen 8A2. FEBS J. 280:1308–1319.
59. Wen, J., and J. R. Friedman. 2012. miR-122 regulates hepatic lipid metabolism and tumor suppression. J. Clin. Invest. 122:2773–2776.
60. White, D. L., F. Kanwal, and H. B. El-Serag. 2012. Association between nonalcoholic fatty liver disease and risk for hepatocellular cancer, based on systematic review. Clin. Gastroenterol. Hepatol. 10:1342–1359.e1342
61. Whittaker, R., P. A. Loy, E. Sisman, E. Suyama, P. Aza-Blanc, R. S. Ingermanson, et al. 2010. Identification of MicroRNAs that control lipid droplet formation and growth in hepatocytes via high-content screening. J. Biomol. Screen. 15:798–805.
62. Williams, M. D., and G. M. Mitchell. 2012. MicroRNAs in insulin resistance and obesity. Exp. Diabetes Res. 2012:484696.
63. Yki-Järvinen, H. 2014. Non-alcoholic fatty liver disease as a cause and a consequence of metabolic syndrome. Lancet Diabetes Endocrinol. 2:901–910.
64. Zhang, Z., Y. Zha, W. Hu, Z. Huang, Z. Gao, Y. Zang, et al. 2013. The autoregulatory feedback loop of microRNA-21/ programmed cell death protein 4/activation protein-1 (MiR21/PDCD4/AP-1) as a driving force for hepatic fibrosis development. J. Biol. Chem. 288:37082–37093.
65. Zheng, J., C. Wu, Z. Xu, P. Xia, P. Dong, B. Chen, et al. 2014. Hepatic stellate cell is activated by microRNA-181b via PTEN/Akt pathway. Mol. Cell. Biochem. 398:1–9.