EPIGENETIC REGULATION OF REVERSE CHOLESTEROL TRANSPORT: THE ROLE OF MICRO-RNAS


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Micro-RNAs are a group of small non-coding RNA molecules regulating target genes at the post-transcriptional level. Micro-RNAs are involved in the control of many pathophysiological processes, including dyslipidemia, the main risk factor for atherosclerosis. Current evidence suggests micro-RNAs to be a new class of epigenetic regulators controlling the metabolism of high-density lipoprotein cholesterol (HDL-C), which makes a significant contribution to the pathophysiology of atherosclerosis. Accumulated data suggest micro-RNA, in particular, miR-33, miR-27, miR-144, miR-758 and miR-20, to be involved in the post-transcriptional control of ABCA1, ABCG1 and SCARB1 genes regulatory network of the reverse cholesterol transport (RCT). These micro-RNAs have been shown to be central players in disrupting the path of RCT, leading to the development of atherosclerosis. This article presents the latest data on the participation of the corresponding micro-RNA at different stages of both HDL metabolism and the pathway of RCT. Some of the limitations on the therapeutic potential of micro-RNA and the prospects for transferring to the clinical plane the results of experimental studies on their participation in the regulation of RCT are also discussed.

Full Text

Restricted Access

About the authors

K. A Aitbaev

Scientific Research Institute of Molecular Biology and Medicine

Bishkek, Kyrgyzstan

R. R Tuhvatshin

I.K. Akhunbaev Kyrgyz State Medical Academy

Bishkek, Kyrgyzstan

V. V Fomin

I.M.Sechenov First Moscow State Medical University, Healthcare Ministry of Russia (Sechenov University)

Moscow, Russian Federation

I. T Murkamilov

I.K. Akhunbaev Kyrgyz State Medical Academy; First President of Russia B.N. Yeltsin Kyrgyz Russian Slavic University

Email: murkamilov.i@mail.ru
Bishkek, Kyrgyzstan

M. T Talaibekov

First President of Russia B.N. Yeltsin Kyrgyz Russian Slavic University

Bishkek, Kyrgyzstan

References

  1. Barter P., Gotto A.M., LaRosa J.C., Maroni J., Szarek M., Grundy S.M., Kastelein J.J., Bittner V., Fruchartet J.C. Treating to New Targets Investigators. HDL cholesterol, very low levels of LDL cholesterol, and cardiovascular events. N. Engl. J. Med. 2007; 357: 1301-10. https://doi.org/10.1056/NEJMoa064278.
  2. Rye K.A., Bursill C.A., Lambert G., Tabet F., Barter PJ. The metabolism and anti-atherogenic properties of HDL. J. Lipid Res. 2009; 50: 195-200. https:// doi.org/10.1194/jlr.R800034-JLR200.
  3. Phillips M.C. Molecular mechanisms of cellular cholesterol efflux. J. Biol. Chem. 2014; 289 (35): 24020-9. https://doi.org/10.1074/jbc.R114.583658.
  4. Щелкунова Т.А., Морозов И.А., Рубцов П.М., Самоходская Л.М., Андрианова И.В., Собенин И.А., Орехов А.Н., Смирнов А.Н. Изменения в уровне экспрессии генов в интиме аорты в ходе атерогенеза. Биохимия. 2013; 78 (5): 610-9. (Shchelkunova TA., Smirnov A.N., Morozov I.A., Rubtsov P.M., Samokhodskaya L.M., Andrianova I.V., Sobenin I.A., Orekhov A.N. Changes in levels of gene expression in human aortal intima during atherogenesis. Biochemistry (Moscow). 2013; 78 (5): 610-9 (in Russian)]
  5. Душкин М.И. Макрофаги и атеросклероз: патофизиологические основы и терапевтические аспекты. Бюллетень СО РАМН. 2006; 26 (120): 47-55. [Dushkin M.I. Macrophages and atherosclerosis: pathophysiological bases and therapeutic aspects. Bulletin of SB RAMS. 2006; 26 (120): 47-55 (in Russian))
  6. Acton S., Rigotti A., Landschulz K.T, Xu S., Hobbs H.H., Krieger M. Identification of scavenger receptor SR-BI as a high density lipoprotein receptor. Science. 1996; 271 (5248): 518-20. https://doi. org/10.1126/science.271.5248.518.
  7. Chiang J.Y. Bile acids: regulation of synthesis. J. Lipid Res. 2009; 50 (10): 1955-66. https://doi. org/10.1194/jlr.R900010-JLR200.
  8. Esteller A. Physiology of bile secretion. World J. Gastroenterol. 2008; 14 (37): 5641-9. https://doi. org/10.3748/wjg.14.5641.
  9. AIM-HIGH Investigators, Boden W.E., Probstfield J.L., Anderson T., Chaitman B.R., Desvignes-Nickens P., Koprowicz K., McBride R., Teo K., Weintraub W. Niacin in patients with low HDL cholesterol levels receiving intensive statin therapy. N. Engl. J. Med. 2011; 365 (24): 2255-67. https://doi. org/10.1056/NEJMoa1107579.
  10. Annema W., Tietge U.J. Regulation of reverse cholesterol transport - a comprehensive appraisal of available animal studies. Nutr Metab (Lond). 2012; 9 (1): 25. https://doi.org/10.1186/1743-7075-9-25.
  11. Grefhorst A., Elzinga B.M., Voshol PJ., Plösch T., Kok T, Bloks VW, van der Sluijs F. H., Havekes L.M., Romijn J.A., Verkade H.J., Kuiperset F. Stimulation of lipogenesis by pharmacological activation of the liver X receptor leads to production of large, triglyceride-rich very low density lipoprotein particles. J. Biol. Chem. 2002; 277 (37): 34182-90. https://doi.org/10.1074/jbc.M204887200.
  12. Rottiers V, Näär A.M. MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol. Cell. Biol. 2012; 13 (4): 239-50. https://doi.org/10.1038/nrm3313.
  13. Andreou I., Sun X., Stone PH., Edelman E.R., Feinberget M.W. MiRNAs in atherosclerotic plaque initiation, progression, and rupture. Trends Mol. Med. 2015; 21 (5): 307-18. https://doi.org/10.1016/j. molmed.2015.02.003.
  14. Krol J., Loedige I., Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet. 2010; 11 (9): 597-610. https://doi.org/10.1038/nrg2843.
  15. Moore A.C., Winkjer J.S, Tseng TT. Bioinformatics Resources for MicroRNA Discovery. Biomark Insights. 2016; 10 (suppl 4): 53-8.
  16. Lu M., Zhang Q., Deng M., Miao J., Guo Y., Gao W., Cui Q. An analysis of human microRNA and disease associations. PLoS ONE. 2008; 3: e3420. https://doi.org/10.1371/journal.pone.0003420.
  17. Li Y., Qiu C., Tu J., Geng B., Yang J., Jiang T., Cui Q. HMDD v2.0.: a database for experimentally supported human microRNA and disease associations. Nucleic Acids Res. 2014; 42: 1070-4. https:// doi.org/10.1093/nar/gkt1023.
  18. Jiang Q., Wang Y., Hao Y., Juan L., Teng M., Zhang X., Li M., Wang G., Liu Y MiR2Disease: a manually curated database for microRNA deregulation in human disease. Nucleic Acids Res. 2009; 37: 98-104. https://doi.org/10.1093/nar/gkn714.
  19. Filipowicz W, Bhattacharyya S.N., Sonenberg N. Mechanisms of posttranscriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet. 2008; 9 (2): 102-14. https://doi.org/10.1038/nrg2290.
  20. Matkovich S.J., Van Booven D.J., Eschenbacher W.H., Dorn G.W 2nd. RISC RNA sequencing for context-specific identification of in vivo microRNA targets. Circ Res. 2011; 108 (1): 18-26. https://doi. org/10.1161/CIRCRESAHA.110.233528.
  21. Vickers K.C., Palmisano B.T., Shoucri B.M., Shamburek R.D., Remaley A.T. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat Cell. Biol. 2011; 13 (4): 423-33. https://doi.org/10.1038/ncb2210.
  22. Pan S., Yang X., Jia Y., Li R., Zhao R. Microvesicle-shuttled miR-130b reduces fat deposition in recipient primary cultured porcine adipocytes by inhibiting PPAR-g expression. J. Cell. Physiol. 2014; 229 (5): 631-9. https://doi.org/10.1002/jcp.24486.
  23. Christian P., Su Q. MicroRNA regulation of mitochondrial and ER stress signaling pathways: implications for lipoprotein metabolism in metabolic syndrome. Am J. Physiol. Endocrinol. Metab. 2014; 307 (9): 729-37 https://doi.org/10.1152/ajpendo.00194.2014.
  24. Rayner K.J., Suârez Y., Dâvalos A., Parathath S., Fitzgerald M.L., Tamehiro N., Fisher E.A., Moore K.J., Fernândez-Hernando C. MiR-33 contributes to the regulation of cholesterol homeostasis. Science. 2010; 328 (5985): 1570-3. https://doi.org/10.1126/ science.1189862.
  25. Elmen J., Lindow M., Silahtaroglu A., Bak M., Christensen M., Lind-Thomsen A., Hedtjärn M., Hansen J.B., Hansen H.F, Straarup E.M., McCullagh K., Kearney P., Kauppinen S. Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to up-regulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Res 2008; 36 (4): 1153-62. https:// doi.org/10.1093/nar/gkm1113.
  26. Soh J., Iqbal J., Queiroz J., FernandezHernando C., Hussain M.M. MicroRNA-30c reduces hyperlipidemia and atherosclerosis in mice by decreasing lipid synthesis and lipoprotein secretion. Nat Med. 2013;(7): 892-900. https://doi.org/10.1038/nm.3200.
  27. Esau C., Davis S., Murray S.F., Yu X.X., Pandey S.K., Pear M., Watts L., Booten S.L., Graham M., McKay R., Subramaniam A., Propp S., Lollo B.A., Freier S., Bennett C.F., Bhanot S., Monia B.P. MiR-122 regulation of lipid metabolism revealed by in vivo antisense targeting. Cell Metab. 2006; 3: 87-98. https://doi.org/10.1016/j.cmet.2006.01.005.
  28. Elmen J., Lindow M., Schutz S., Lawrence M., Petri A., Obad S., Lindholm M., Hedtjarn M., Hansen H.F., Berger U., Gullans S., Kearney P., Sarnow P., Straarup E.M., Kauppinen S. LNAmediated microRNA silencing in non-human primates. Nature. 2008; 452: 896-9. https://doi.org/10.1038/nature06783.
  29. Horie T., Ono K., Horiguchi M., Nishi H., Nakamura T, Nagao K., Kinoshita M., Kuwabara Y, Marusawa H., Iwanaga Y, Hasegawa K., Yokode M., Kimura T., Kita T. MicroRNA-33 encoded by an intron of sterol regulatory element-binding protein 2 (Srebp2) regulates HDL in vivo. Proc Natl Acad Sci USA. 2010; 107 (40): 17321-6. https://doi.org/10.1073/pnas.1008499107.
  30. Ramirez C.M., Dávalos A., Goedeke L., Salerno A.G., Warrier N., Cirera-Salinas D., Suárez Y., Fernández-Hernando C. MicroRNA-758 regulates cholesterol efflux through posttranscriptional repression of ATP-binding cassette transporter A1. Arterioscler Thromb Vasc Biol. 2011; 31 (11): 2707-14. https:// doi.org/10.1161/ATVBAHA.111.232066.
  31. Hosin A.A., Prasad A., Viiri L.E., Davies A.H., Shalhoub J. MicroRNAs in atherosclerosis. J. Vasc Res. 2014; 51 (5): 338-49. https://doi.org/10.1159/000368193.
  32. Назаренко М.С., Марков А.В., Лебедев И.Н., Слепцов А.А., Фролов А.В., Барбараш О.Л.,Барбараш Л.С., Пузырев В.П. Профиль метилирования ДНК в тканях сосудистого русла при атеросклерозе. Молекулярная биология. 2013; 47 (3): 398-404. https://doi.org/10.7868/ S0026898413030099
  33. Moore K.J., Rayner K.J., Suárez Y, Fernández-Hernando C. MicroRNAs and cholesterol metabolism. Trends Endocrinol Metab. 2010; 21 (12): 699-706. https://doi.org/10.1016/j.tem.2010.08.008.
  34. Horton J.D., Goldstein J.L., Brown M.S. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Invest. 2002;(9): 1125-31. https://doi.org/10.1172/JCI0215593.
  35. Rayner K.J., Sheedy F.J., Esau C.C., Hussain FN., Temel R.E., Parathath S., van Gils J.M., Rayner A.J., Chang A.N., Suarez Y., Fernandez-Hernando C., Fisher E.A., Moore K.J. Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J. Clin. Invest. 2011; 121 (7): 2921-31. https://doi.org/10.1172/JCI57275.
  36. Rayner K.J., Esau C.C., Hussain FN., McDaniel A.L., Marshall S.M., van Gils J.M., Ray T.D., Sheedy F.J., Goedeke L., Liu X., Khatsenko O.G., Kaimal V, Lees C.J., Fernandez-Hernando C., Fisher E.A., Temel R.E., Moore K.J. Inhibition of miR-33a/b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature. 2011; 478 (7369): 404-7. https://doi.org/10.1038/nature10486.
  37. Allen R.M., Marquart T.J., Albert C.J., Suchy F.J., Wang D.Q., Ananthanarayanan M., Ford D.A., Baldân A. MiR-33 controls the expression of biliary transporters, and mediates statin- and diet-induced hepatotoxicity. EMBO Mol Med. 2012; 4 (9): 882-95. https://doi.org/10.1002/emmm.201201228.
  38. Scherrer D.Z., Zago VH., Parra E.S., Avansini S., Panzoldo N.B., Alexandre F, Baracat J., Nakandakare E.R., Quintäo E.C., de Faria E.C. Asymptomatic individuals with high HDL-C levels overexpress ABCA1 and ABCG1 and present miR-33a dysregulation in peripheral blood mononuclear cells. Gene. 2015; 570 (1): 50-6. https://doi. org/10.1016/j.gene.2015.05.074.
  39. Horie T., Baba O., Kuwabara Y., Chujo Y., Watanabe S., Kinoshita M., Horiguchi M., Nakamura T., Chonabayashi K., Hishizawa M., Hasegawa K., Kume N., Yokode M., Kita T., Kimura T., Ono K. MicroRNA-33 deficiency reduces the progression of atherosclerotic plaque in ApoE-/- mice. J. Am. Heart Assoc. 2012; 1 (6): e003376. https://doi. org/10.1161/JAHA.112.003376.
  40. Rotllan N., Ramirez C.M., Aryal B., Esau C.C., Fernández-Hernando C. Therapeutic silencing of microRNA-33 inhibits the progression of atherosclerosis in Ldlr-/- mice-brief report. Arterioscler Thromb Vasc Biol. 2013; 33 (8): 1973-7. https://doi. org/10.1161/ATVBAHA.113.301732.
  41. Marquart T.J., Wu J., Lusis A.J., Baldán A. Anti-miR-33 therapy does not alter the progression of atherosclerosis in low density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2013; 33 (3): 455-8. https://doi.org/10.1161/ATVBAHA.112.300639.
  42. Chen W.J., Yin K., Zhao G.J., Fu Y.C., Tang C.K. The magic and mystery of microRNA-27 in atherosclerosis. Atherosclerosis. 2012; 222 (2): 314323. https:// doi.org/10.1016/j.atherosclerosis.2012.01.020.
  43. Xie W., Li L., Zhang M., Cheng H.P., Gong D., Lv Y.C., Yao F., He P.P., Ouyang X.P., Lan G., Liu D., Zhao Z.W., Tan Y.L., Zheng X.L., Yin W.D., Tang C.K. MicroRNA-27 prevents Atherosclerosis by Suppressing Lipoprotein Lipase-Induced Lipid Accumulation and Inflammatory Response in Apolipoprotein E Knockout Mice. PLoS One. 2016; 11 (6): e0157085. https://doi.org/10.1371/journal.pone.0157085.
  44. Li T., Cao H., Zhuang J., Wan J., Guan M., Yu B., Li X., Zhang W. Identification of miR-130a, miR-27b and miR-210 as serum biomarkers for atherosclerosis obliterans. Clin Chim Acta. 2011; 412 (1-2): 66-70. https://doi.org/10.1016/j.cca.2010.09.029.
  45. Shirasaki T., Honda M., Shimakami T., Horii R., Yamashita T, Sakai Y, Sakai A., Okada H., Watanabe R., Murakami S., Yi M., Lemon S.M., Kaneko S. MicroRNA-27a regulates lipid metabolism and inhibits hepatitis C virus replication in human hepatoma cells. J. Virol. 2013; 87 (9): 5270-86. https://doi.org/10.1128/JVI.03022-12.
  46. Kang M.H., Zhang L.H., Wijesekara N., de Haan W., Butland S., Bhattacharjee A., Hayden M.R. Regulation of ABCA1 protein expression and function in hepatic and pancreatic islet cells by miR-145. Arterioscler Thromb Vasc Biol. 2013; 33 (12): 2724-32. https://doi.org/10.1161/ATVBAHA.113.302004.
  47. Zhang M., Wu J.F., Chen WJ., Tang S.L., Mo Z.C., Tang Y.Y., Li Y., Wang J.L., Liu X.Y, Peng J., Chen K., He P.P., Lv Y.C., Ouyang X.P., Yao F, Tang D.P., Cayabyab F.S., Zhang D.W., Zheng X.L., Tian D.P., CK Tang C.K. MicroRNA-27a/b regulates cellular cholesterol efflux, influx and esterification/hydrolysis in THP-1 macrophages. Atherosclerosis. 2014; 234 (1): 54-64. https:// doi.org/10.1016/j.atherosclerosis.2014.02.008.
  48. Goedeke L., Rotllan N., Ramirez C.M., Aranda J.F., Canfrán-Duque A., Araldi E., Fernández-Hernando A., Langhi C., de Cabo R., Baldán A., Suárez Y., FernándezHernando C. MiR-27b inhibits LDLR and ABCA1 expression but does not influence plasma and hepatic lipid levels in mice. Atherosclerosis. 215; 243 (2): 499-509. https://doi.org/10.1016/j. atherosclerosis.2015.09.033.
  49. Vickers K.C., Shoucri B.M., Levin M.G., Wu H., Pearson D.S., Osei-Hwedieh D., Collins F.S, Remaley A.T., Sethupathy P. MicroRNA-27b is a regulatory hub in lipid metabolism and is altered in dyslipidemia. Hepatology. 2013; 57 (2): 533-42. https://doi. org/10.1002/hep.25846.
  50. Boon R.A., Hergenreider E., Dimmeler S. Atheroprotective mechanisms of shear stress-regulated mi-croRNAs. Thromb Haemost. 2016; 108 (4): 616-20. https://doi.org/10.1160/TH12-07-0491.
  51. Degoma E.M., Rader D.J. Novel HDL directed pharmacotherapeutic strategies. Nat Rev Cardiol. 2011; 8 (5): 266-77. https://doi.org/10.1038/nrcardio.2010.200.
  52. De Aguiar Vallim T.Q., Tarling E.J., Kim T, Civelek M., Baldán A., Esau C., Edwards PA. MicroRNA-144 regulates hepatic ATP binding cassette transporter A1 and plasma high-density lipoprotein after activation of the nuclear receptor farnesoid X receptor. Circ Res. 2013; 112 (12): 1602-12. https:// doi.org/10.1161/CIRCRESAHA.112.300648.
  53. Ramirez C.M., Rotllan N., Vlassov A.V, Dávalos A., Li M., Goedeke L., Aranda J.F., Salinas C.-D., Araldi E., Salerno A., Wanschel A., Zavadil J., Castrillo A., Kim J., Suârez Y, Fernândez-Hernando C. Control of cholesterol metabolism and plasma high density lipoprotein levels by microRNA-144. Circ Res. 2013; 112 (12): 1592-1601. https://doi.org/10.1161/ CIRCRESAHA.112.300626.
  54. Hu Y.W., Hu Y.R., Zhao J.Y., Li S.F., Ma X., Wu S.G., Lu J.B., Qiu Y.R., Sha Y.H., Wang Y.C., Gao J.J., Zheng L., Wang Q. 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. https://doi.org/10.1371/journal.pone.0094997.
  55. Ansell B.J., Navab M., Hama S., Kamranpour N., Fonarow G., Hough G., Rahmani S., Mottahedeh R., Dave R., Reddy S.T, Fogelman A.M. Inflammatory/ antiinflammatory properties of high-density lipoprotein distinguish patients from control subjects better than high-density lipoprotein cholesterol levels and are favorably affected by simvastatin treatment. Circulation. 2003; 108 (22): 2751-6. https://doi. org/10.1161/01.CIR.0000103624.14436.4B.
  56. Rayner K.J., Fernandez-Hernando C., Moore K.J. MicroRNAs regulating lipid metabolism in athero-genesis. Thromb Haemost. 2012; 107 (4): 642-7. https://doi.org/10.1160/TH11-10-0694.
  57. Mandolini C., Santovito D., Marcantonio P., Buttitta F., Bucci M., Ucchino S., Mezzetti A., Cipollone F Identification of microRNAs 758 and 33b as potential modulators of ABCA1 expression in human atherosclerotic plaques. Nutr Metab Cardiovasc Dis. 2015; 25 (2): 202-9. https://doi.org/10.1016/j. numecd.2014.09.005.
  58. Li B.R., Xia L.Q., Liu J., Liao L.L., Zhang Y., Deng M., Zhong H.J., Feng T.T, He P.P., Ouyang X.P. MiR-758-5p regulates cholesterol uptake via targeting the CD36 3'UTR. Biochem Biophys Res Commun. 2017; 494 (1-2): 384-9. https://doi.org/10.1016/j. bbrc.2017.09.150.
  59. Can U., Buyukinan M., Yerlikaya FH. The investigation of circulating microRNAs associated with lipid metabolism in childhood obesity. Pediatr Obes. 2016; 11 (3): 228-34. https://doi.org/10.1111/ijpo.12050.
  60. Liang B., Wang X., Song X., Bai R., Yang H., Yang Z., Xiao C., Bian Y. MicroRNA-20a/b regulates cholesterol efflux through posttranscriptional repression of ATP-binding cassette transporter A1. Biochim Biophys Acta. 2017; 1862 (9): 929-38. https://doi. org/10.1016/j.bbalip.2017.06.002.
  61. Brandt J.M., Djouadi F, Kelly D.P Fatty acids activate transcription of the muscle carnitine. Palmitoyl transferase I gene in cardiac myocytes via the peroxisome proliferatoractivated receptoralpha. J. Biol. Chem. 1998; 273 (37): 23786-92. https://doi. org/10.1074/jbc.273.37.23786.
  62. Rigotti A., Miettinen H.E., Krieger M. The role of the high-density lipoprotein receptor SR-BI in the lipid metabolism of endocrine and other tissues. Endocr Rev 2003; 24 (3): 357-87. https://doi. org/10.1210/er.2001-0037
  63. Kocher O., Birrane G., Tsukamoto K., Fenske S., Yesilaltay A., Pal R., Daniels K., Ladias J.A., Krieger M. In vitro and in vivo analysis of the binding of the C terminus of the HDL receptor scavenger receptor class B, type I (SR-BI), to the PDZ1 domain of its adaptor protein PDZK1. J. Biol. Chem. 2010; 285 (45): 34999-5010. https://doi.org/10.1074/jbc. M110.164418.
  64. Hu Z., Shen WJ., Kraemer F.B., Azhar S. MicroRNAs 125a and 455 repress lipoprotein-supported steroidogenesis by targeting scavenger receptor class B type I in steroidogenic cells. Mol Cell Biol. 2012; 32 (24): 5035-5045. https://doi.org/10.1128/ MCB.01002-12.
  65. Wang L., Jia X.J., Jiang H.J., Du Y., Yang F., Si S.Y., Hong B. MicroRNAs 185, 96, and 223 repress selective high-density lipoprotein cholesterol uptake through posttranscriptional inhibition. Mol. Cell. Biol. 2013; 33 (10): 1956-64. https://doi. org/10.1128/MCB.01580-12.
  66. Mysore R., Zhou Y., Sádevirta S., Savolainen-Peltonen H., Nidhina Haridas P.A., Soronen J., Leivonen M., Sarin A.P., FischerPosovszky P., Wabitsch M., Yki-Järvinen H., Olkkonen V.M. MicroRNA-192* impairs adipocyte triglyceride storage. Biochim Biophys Acta. 2016; 1861 (4): 342-51. https://doi. org/10.1016/j.bbalip.2015.12.019.
  67. Paulusma C.C., Folmer D.E., Ho-Mok K.S., de Waart D.R., Hilarius P.M., Verhoeven A.J., Oude Elferink R.P. ATP8B1 requires an accessory protein for endoplasmic reticulum exit and plasma membrane lipid flippase activity. Hepatology. 2008; 47 (1): 268-78. https://doi.org/10.1002/hep.21950.
  68. Li T., Francl J.M., Boehme S., Chiang J.Y. Regulation of cholesterol and bile acid homeostasis by the cholesterol 7a-hydroxylase/steroid response element binding protein 2/microRNA-33a axis in mice. Hepatology 2013; 58 (3): 1111-21. https:// doi.org/10.1002/hep.26427.
  69. Lai L., Azzam K.M., Lin WC., Rai P, Lowe J.M., Gabor K.A., Madenspacher J.H., Aloor J.J., Parks J.S., Näär A.M., Fessler M.B. MicroRNA-33 regulates the Innate Immune Response via ATP Binding Cassette Transporter-mediated Remodeling of Membrane Microdomains. J. Biol. Chem. 2016; 291 (37): 19651-60. https://doi.org/10.1074/jbc.M116.723056.
  70. Демина Е.П., Мирошникова В.В., Шварцман А.Л. Роль АВС-транспортеров А1 и G1 - ключевые белков обратного транспорта холестерина - в развитии атеросклероза. Молекулярная биология. 2016; 50 (2): 223-30. https://doi. org/10.7868/S002689841602004X

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies