MicroRNA-101 overexpression by IL-6 and TNF-α inhibits cholesterol efflux by suppressing ATP-binding cassette transporter A1 expression

Experimental Cell Research

Volumn 336, Issue 1, 2015, Pages 33-42

  Zhang, Nan ^a   Lei, Jia Yan ^a   Lei, Han ^a   Ruan, Xiongzhong ^b,c   Liu, Qing ^b   Chen, Yaxi ^b   Huang, Wei ^a  

^a THE FIRST AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^b CHONGQING MEDICAL UNIVERSITY   (China)

^c ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

ABCA1; Atherosclerosis; ATP binding cassette transporter A1; Cholesterol; IL 6; Inflammation; MicroRNA; MiR 101; MiRNA; NAFLD; Non alcoholic fatty liver disease; TNF

Indexed keywords

ABC TRANSPORTER A1; DEOXYRIBODIPYRIMIDINE PHOTOLYASE; INTERLEUKIN 6; LENTIVIRUS VECTOR; LIPID; LOW DENSITY LIPOPROTEIN; LUCIFERASE; MESSENGER RNA; MICRORNA 101; TUMOR NECROSIS FACTOR ALPHA; 3' UNTRANSLATED REGION; ABCA1 PROTEIN, HUMAN; CHOLESTEROL; MICRORNA; MIRN101 MICRORNA, HUMAN;

3' UNTRANSLATED REGION; ARTICLE; CELL LINE; CHOLESTEROL TRANSPORT; HEPATOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; INFLAMMATION; MACROPHAGE; NONALCOHOLIC FATTY LIVER; PRIORITY JOURNAL; PROTEIN EXPRESSION; STAINING; UPREGULATION; WESTERN BLOTTING; CARCINOMA, HEPATOCELLULAR; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; GENETICS; LIVER NEOPLASMS; METABOLISM; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

3' UNTRANSLATED REGIONS; ATP BINDING CASSETTE TRANSPORTER 1; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELLS, CULTURED; CHOLESTEROL; HUMANS; INTERLEUKIN-6; LIVER NEOPLASMS; LUCIFERASES; MACROPHAGES; MICRORNAS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84943391651     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2015.05.023     Document Type: Article

References (35)

1. Chen Y., Chen Y., Zhao L., Chen Y., Mei M., Li Q., et al. Inflammatory stress exacerbates hepatic cholesterol accumulation via disrupting cellular cholesterol export. J. Gastroenterol. Hepatol. 2012, 27(5):974-984.
2. Mao M., Lei H., Liu Q., Chen Y., Zhao L., Li Q., et al. Effects of miR-33a-5P on ABCA1/G1-mediated cholesterol efflux under inflammatory stress in THP-1 macrophages. PloS One 2014, 9(10):e109722.
3. Chen Y., Ruan X.Z., Li Q., Huang A., Moorhead J.F., Powis S.H., et al. Inflammatory cytokines disrupt LDL-receptor feedback regulation and cause statin resistance: a comparative study in human hepatic cells and mesangial cells. Am. J. Physiol.-Ren. Physiol. 2007, 293(3):F680-F687.
4. Ruan X.Z., Moorhead J.F., Tao J.L., Ma K.L., Wheeler D.C., Powis S.H., et al. Mechanisms of dysregulation of low-density lipoprotein receptor expression in vascular smooth muscle cells by inflammatory cytokines. Arterioscler. Thromb. Vasc. Biol. 2006, 26(5):1150-1155.
5. Ong J.P., Younossi Z.M. Epidemiology and natural history of NAFLD and NASH. Clin. Liver Dis. 2007, 11(1):1-16.
6. Hansson G.K. Inflammation, atherosclerosis, and coronary artery disease. N. Engl. J. Med. 2005, 352(16):1685-1695.
7. Langmann T., Klucken J., Reil M., Liebisch G., Luciani M.-F., Chimini G., et al. Molecular cloning of the human ATP-binding cassette transporter 1 (hABC1): evidence for sterol-dependent regulation in macrophages. Biochem. Biophys. Res. Commun. 1999, 257(1):29-33.
8. Yin K., Liao d-f, Tang C.-k ATP-binding membrane cassette transporter A1 (ABCA1): a possible link between inflammation and reverse cholesterol transport. Mol. Med. 2010, 16(9-10):438.
9. Wang N., Silver D.L., Costet P., Tall A.R. Specific binding of ApoA-I, enhanced cholesterol efflux, and altered plasma membrane morphology in cells expressing ABC1. J. Biol. Chem. 2000, 275(42):33053-33058.
10. L.R. Brunham, M.H. Kang, C. Van Karnebeek, S.N. Sadananda, J.A. Collins, L.-H. Zhang, et al. Clinical, Biochemical and Molecular Characterization of Novel Mutations in ABCA1 in Families with Tangier Disease (2014).
11. Liu Y., Tang C. Regulation of ABCA1 functions by signaling pathways. Biochim. Biophys. Acta (BBA)-Mol. Cell Biol. Lipids 2012, 1821(3):522-529.
12. Sun D., Zhang J., Xie J., Wei W., Chen M., Zhao X. MiR-26 controls LXR-dependent cholesterol efflux by targeting ABCA1 and ARL7. FEBS Lett. 2012, 586(10):1472-1479.
13. Elfimova N., Ommer K., Schlattjan M., Sowa J.P., Wedemeyer I., Vantler M., et al. miR-101 in steatosis and steatohepatitis of non-alcoholic fatty liver disease (NAFLD). J. Hepatol. 2013, 58:502-508. [Meeting Abstract].
14. Frankel L.B., Wen J., Lees M., Høyer-Hansen M., Farkas T., Krogh A., et al. microRNA-101 is a potent inhibitor of autophagy. EMBO J. 2011, 30(22):4628-4641.
15. Rayner K.J., Moore K.J. MicroRNA control of high-density lipoprotein metabolism and function. Circ. Res. 2014, 114(1):183-192.
16. Ismael F.O., Proudfoot J.M., Brown B.E., van Reyk D.M., Croft K.D., Davies M.J., et al. Comparative reactivity of the myeloperoxidase-derived oxidants HOCl and HOSCN with low-density lipoprotein (LDL): implications for foam cell formation in atherosclerosis. Arch. Biochem. Biophys. 2015, 573:40-51.
17. Wang C., Yan Y., Hu L., Zhao L., Yang P., Moorhead J.F., et al. Rapamycin-mediated CD36 translational suppression contributes to alleviation of hepatic steatosis. Biochem. Biophys. Res. Commun. 2014, 447(1):57-63.
18. Wang C., Hu L., Zhao L., Yang P., Moorhead J.F., Varghese Z., et al. Inflammatory stress increases hepatic CD36 translational efficiency via activation of the mTOR signalling pathway. PloS One 2014, 9(7):e103071.
19. Narang M.A., Dumas R., Ayer L.M., Gravel R.A. Reduced histone biotinylation in multiple carboxylase deficiency patients: a nuclear role for holocarboxylase synthetase. Hum. Mol. Genet. 2004, 13(1):15-23.
20. Oishi K., Uchida D., Ohkura N., Horie S. PPARα deficiency augments a ketogenic diet-induced circadian PAI-1 expression possibly through PPARγ activation in the liver. Biochem. Biophys. Res. Commun. 2010, 401(2):313-318.
21. Sankaranarayanan S., Kellner-Weibel G., DE La Llera-Moya M., Phillips M.C., Asztalos B.F., Bittman R., et al. A sensitive assay for ABCA1-mediated cholesterol efflux using BODIPY-cholesterol. J. Lipid Res. 2011, 52(12):2332-2340.
22. Zhang J., Cai S., Peterson B.R., Kris-Etherton P.M. Heuvel JPV. Development of a cell-based, high-throughput screening assay for cholesterol efflux using a fluorescent mimic of cholesterol. Assay Drug Dev. Technol. 2011, 9(2):136-146.
23. Wang L., Zhang X., Jia L.T., Hu S.J., Zhao J., Yang J.D., et al. c-Myc-mediated epigenetic silencing of MicroRNA-101 contributes to dysregulation of multiple pathways in hepatocellular carcinoma. Hepatology 2014, 59(5):1850-1863.
24. Tu X., Zhang H., Zhang J., Zhao S., Zheng X., Zhang Z., et al. MicroRNA-101 suppresses liver fibrosis by targeting TGFβ signaling pathway. J. Pathol. 2014, 234(1):46-59. http://dx.doi.org/10.1002/path.4373.
25. Gao Y., Liu F., Fang L., Cai R., Zong C., Qi Y. Genkwanin Inhibits Proinflammatory Mediators Mainly through the Regulation of miR-101/MKP-1/MAPK Pathway in LPS-Activated Macrophages. PloS One 2014, 9(5):e96741.
26. Xaus J., Comalada M., Valledor A.F., Cardó M., Herrero C., Soler C., et al. Molecular mechanisms involved in macrophage survival, proliferation, activation or apoptosis. Immunobiology 2001, 204(5):543-550.
27. Ramirez C.M., Dávalos A., Goedeke L., Salerno A.G., Warrier N., Cirera-Salinas D., et al. MicroRNA-758 regulates cholesterol efflux through posttranscriptional repression of ATP-binding cassette transporter A1. Arterioscler. Thromb. Vasc. Biol. 2011, 31(11):2707-2714.
28. Ramírez C.M., Rotllan N., Vlassov A.V., Dávalos A., Li M., Goedeke L., et al. Control of cholesterol metabolism and plasma high-density lipoprotein levels by microRNA-144. Circ. Res. 2013, 112(12):1592-1601.
29. Adlakha Y., Khanna S., Singh R., Singh V., Agrawal A., Saini N. Pro-apoptotic miRNA-128-2 modulates ABCA1, ABCG1 and RXRα expression and cholesterol homeostasis. Cell Death Dis. 2013, 4(8):e780.
30. Kang M.H., Zhang L.-H., Wijesekara N., de Haan W., Butland S., Bhattacharjee A., et al. Regulation of ABCA1 protein expression and function in hepatic and pancreatic islet cells by miR-145. Arterioscler. Thromb. Vasc. Biol. 2013, 33(12):2724-2732.
31. Hu Y.-W., Hu Y.-R., Zhao J.-Y., Li S.-F., Ma X., Wu S.-G., et al. An agomir of miR-144-3p accelerates plaque formation through impairing reverse cholesterol transport and promoting pro-inflammatory cytokine production. PloS One 2014, 9(4):e94997.
32. Wang J.M., Zhou J.J., Zheng Q., Gan H., Wang H. Dialysis method alters the expression of MicroRNA-33a and its target genes ABCA1, ABCG1 in THP-1 macrophages. Ther. Apheresis Dial. 2014, 18(1):44-50.
33. Zhang M., Wu J.-F., Chen W.-J., Tang S.-L., Mo Z.-C., Tang Y.-Y., et al. MicroRNA-27 a/b regulates cellular cholesterol efflux, influx and esterification/hydrolysis in THP-1 macrophages. Atherosclerosis 2014, 234(1):54-64.
34. Zhao R., Feng J., He G. miR-613 regulates cholesterol efflux by targeting LXRα and ABCA1 in PPARγ activated THP-1 macrophages. Biochem. Biophys. Res. Commun. 2014, 448(3):329-334.
35. Lv Y.-C., Tang Y.-Y., Peng J., Zhao G.-J., Yang J., Yao F., et al. MicroRNA-19b promotes macrophage cholesterol accumulation and aortic atherosclerosis by targeting ATP-binding cassette transporter A1. Atherosclerosis 2014, 236(1):215-226.