Generic placeholder image

Current Protein & Peptide Science

Editor-in-Chief

ISSN (Print): 1389-2037
ISSN (Online): 1875-5550

Review Article

Reverse cholesterol transport-related miRNAs and their regulation by natural functional compounds

Author(s): Ziyang Lian, Bobo Zhu, Chuyuan Lei, Wen Zhao, Qingsheng Huang, Chunmei Jiang, Mingliang Jin, Junling Shi* and Dongyan Shao*

Volume 20, Issue 10, 2019

Page: [1004 - 1011] Pages: 8

DOI: 10.2174/1389203720666190827143218

Price: $65

Abstract

Cardiovascular disease (CVD) is the biggest killer globally and atherosclerosis (AS) is the major trigger to this pathology. Abnormal cholesterol homeostasis is the starting point of AS, especially the aggregation of macrophage foam cells in the intra-arterial subcutaneous region. Reverse cholesterol transport (RCT) can remove excess cholesterol from macrophages and transport it to the liver for excretion, making this process vital to alleviate AS. MicroRNAs (miRNAs) are small, noncoding RNAs that play critical roles in various diseases including AS, by regulating post-transcriptional gene expression. Many natural compounds can exert anti-atherosclerotic effects by regulating different miRNAs that are implicated in RCT. Hence, targeting these miRNAs using natural functional compounds may be a safe, novel, and promising strategy to prevent and treat AS. This review describes the miRNAs involved in RCT and the potential uses of natural compounds to target RCT-related miRNAs to modulate AS.

Keywords: Reverse cholesterol transport, microRNA, natural functional compounds, atherosclerosis, macrophage, homeostasis.

Next »
Graphical Abstract
[1]
Alaarg, A.; Senders, M.L.; Varela-Moreira, A.; Pérez-Medina, C.; Zhao, Y.; Tang, J.; Fay, F.; Reiner, T.; Fayad, Z.A.; Hennink, W.E. A systematic comparison of clinically viable nanomedicines targeting HMG-CoA reductase in inflammatory atherosclerosis. J. Control. Release, 2017, 262S016836591730723X
[2]
Shao, D.; Lian, Z.; Di, Y.; Lei, Z.; Rajoka, M.S.R.; Zhang, Y.; Jie, K.; Jiang, C.; Shi, J. Dietary compounds have potential in controlling atherosclerosis by modulating macrophage cholesterol metabolism and inflammation via miRNA. NPJ Sci. Food, 2018, 2(1), 13-21.
[3]
Karunakaran, D.; Rayner, K.J. Macrophage miRNAs in atherosclerosis. Biochim. Biophys. Acta Biomembr., 2016, 1861(12 Pt B), 2087-2093.
[4]
Lewis, B.P.; Burge, C.B.; Bartel, D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are MicroRNA targets. Cell, 2005, 120(1), 1-20.
[5]
Friedman, R.; Farh, K.; Bartel, D. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res., 2008, 19(1), 92-105.
[6]
Bladé, C.; Baselga‐Escudero, L.; Salvadó, M.J.; Arola‐Arnal, A. miRNAs, polyphenols, and chronic disease. Mol. Nutr. Food Res., 2013, 57(1), 58-70.
[7]
Baselga-Escudero, L. Bladã©, C.; Ribas-Latre, A.; Casanova, E.; Salvadã3, M.J.; Arola, L.; Arola-Arnal, A. Grape seed proanthocyanidins repress the hepatic lipid regulators miR-33 and miR-122 in rats. Mol. Nutr. Food Res., 2012, 56(11), 1636-1646.
[8]
Han, Q.A.; Yan, C.; Wang, L.; Li, G.; Xu, Y.; Xia, X. Urolithin A attenuates ox-LDL-induced endothelial dysfunction partly by modulating microRNA-27 and ERK/PPAR-γ pathway. Mol. Nutr. Food Res., 2016, 60(9), 1933-1943.
[9]
Gosslau, A.; Li, S.; Ho, C.T.; Chen, K.Y.; Rawson, N.E. The importance of natural product characterization in studies of their anti-inflammatory activity. Mol. Nutr. Food Res., 2011, 55(1), 74-82.
[10]
Libby, P.; Ridker, P.M.; Hansson, G.K. Inflammation in atherosclerosis: From pathophysiology to practice. J. Am. Coll. Cardiol., 2009, 54(23), 2129-2138.
[11]
Wildgruber, M.; Lee, H.; Chudnovskiy, A.; Yoon, T.J.; Etzrodt, M.; Pittet, M.J.; Nahrendorf, M.; Croce, K.; Libby, P.; Weissleder, R. Monocyte subset dynamics in human atherosclerosis can be profiled with magnetic nano-sensors. PLoS One, 2009, 4(5)e5663
[12]
Moore, K.J.; Sheedy, F.J.; Fisher, E.A. Macrophages in atherosclerosis: A dynamic balance. Nat. Rev. Immunol., 2013, 13(10), 709-721.
[13]
Mclaren, J.E.; Michael, D.R.; Ashlin, T.G.; Ramji, D.P. Cytokines, macrophage lipid metabolism and foam cells: Implications for cardiovascular disease therapy. Prog. Lipid Res., 2011, 50(4), 331-347.
[14]
Yu, X.H.; Zhang, D.W.; Zheng, X.L.; Tang, C.K. Cholesterol transport system: An integrated cholesterol transport model involved in atherosclerosis. Prog. Lipid Res., 2019, 73, 65-91.
[15]
Yuan, Y.; Li, P.; Ye, J. Lipid homeostasis and the formation of macrophage-derived foam cells in atherosclerosis. Proteins Cells, 2012, 03(3), 173-181.
[16]
Chistiakov, D.A.; Bobryshev, Y.V.; Orekhov, A.N. Macrophage-mediated cholesterol handling in atherosclerosis. J. Cell. Mol. Med., 2016, 20(1), 17-28.
[17]
Oram, J.F.; Heinecke, J.W. ATP-binding cassette transporter A1: A cell cholesterol exporter that protects against cardiovascular disease. Physiol. Rev., 2005, 85(4), 1343-1372.
[18]
Nan, W.; Debin, L.; Wengen, C.; Fumihiko, M.; Tall, A.R. ATP-binding cassette transporters G1 and G4 mediate cellular cholesterol efflux to high-density lipoproteins. Proc. Natl. Acad. Sci. USA, 2004, 101(26), 9774-9779.
[19]
Maria Pia, A.; Francesca, Z.; Billheimer, J.T.; Nan, W.; Rader, D.J.; Phillips, M.C.; Rothblat, G.H. The roles of different pathways in the release of cholesterol from macrophages. J. Lipid Res., 2007, 48(11), 2453-2462.
[20]
May, B.; Joerg, H.; Mukaddes, B.B.; Anne, E.; Moore, K.J.; Franz, R. Selective uptake of HDL cholesteryl esters and cholesterol efflux from mouse peritoneal macrophages independent of SR-BI. J. Lipid Res., 2006, 47(11), 2408-2421.
[21]
Li, K.; Ching, D.; Fu, S.L.; Raffai, R.L. Apolipoprotein E enhances MicroRNA-146a in monocytes and macrophages to suppress nuclear factor-κB–driven inflammation and atherosclerosis novelty and significance. Circ. Res., 2015, 117(1) e1
[22]
Brown, M.S.; Goldstein, J.L. How LDL receptors influence cholesterol and atherosclerosis. Sci. Am., 1984, 251(5), 58-66.
[23]
Esteller, A. Physiology of bile secretion. World J. Gastroenterol., 2008, 14(37), 5641.
[24]
Vrins, C.; Vink, E.; Vandenberghe, K.E.; Frijters, R.; Seppen, J.; Groen, A.K. The sterol transporting heterodimer ABCG5/ABCG8 requires bile salts to mediate cholesterol efflux. FEBS Lett., 2007, 581(24), 4616-4620.
[25]
Paulusma, C.C.; Folmer, D.E.; Homok, K.S.; De, D.W.; Hilarius, P.M.; Verhoeven, A.J.; Oude, R.E. ATP8B1 requires an accessory protein for endoplasmic reticulum exit and plasma membrane lipid flippase activity. Hepatology, 2010, 47(1), 268-278.
[26]
Feinberg, M.W.; Moore, K.J. MicroRNA regulation of atherosclerosis. Circ. Res., 2016, 118(4), 703.
[27]
Rader, D.J. Molecular regulation of HDL metabolism and function: Implications for novel therapies. J. Clin. Invest., 2006, 116(12), 3090-3100.
[28]
Lewis, G.F.; Rader, D.J. New insights into the regulation of HDL metabolism and reverse cholesterol transport. Circ. Res., 2005, 96(12), 1221-1232.
[29]
Selbach, M.; Schwanhausser, B.; Thierfelder, N.; Fang, Z.; Khanin, R.; Rajewsky, N. Widespread changes in protein synthesis induced by microRNAs. Nature, 2008, 455(7209), 58-63.
[30]
Tong, A.W.; Nemunaitis, J. Modulation of miRNA activity in human cancer: A new paradigm for cancer gene therapy? Cancer Gene Ther., 2008, 15(6), 341-355.
[31]
Isabelle, G.; Laure-Alix, C.; Olivier, H.; Nicolas, L.; Das, A.K.; Burant, C.F.; Leclercq, I.A.; Macdougald, O.A.; Bommer, G.T. Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation. J. Biol. Chem., 2010, 285(44), 33652.
[32]
Rayner, K.J.; Sheedy, F.J.; Esau, C.C. Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J. Clin. Invest., 2011, 54(5), 2921-2931.
[33]
S., Hani N.S.; Fjoralba, K.; Yingxia, L.; Toshi, S.; Cohen, D.E.; Gerszten, R.E.; Näär, A.M. MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science, 2010, 328(5985), 1566-1569.
[34]
Lv, Y.C.; Tang, Y.Y.; Peng, J.; Zhao, G.J.; Yang, J.; Yao, F.; Ouyang, X.P.; He, P.P.; Xie, W.; Tan, Y.L. MicroRNA-19b promotes macrophage cholesterol accumulation and aortic atherosclerosis by targeting ATP-binding cassette transporter A1. Atherosclerosis, 2014, 236(1), 215-226.
[35]
Dongliang, W.; Min, X.; Xiao, Y.; Dan, L.; Lei, W.; Yuxuan, X.; Tianru, J.; Wenhua, L. Gut microbiota metabolism of anthocyanin promotes reverse cholesterol transport in mice via repressing miRNA-10b. Circ. Res., 2012, 111(8), 967-981.
[36]
Sun, D.; Zhang, J.; Xie, J.; Wei, W.; Chen, M.; Xiang, Z. MiR-26 controls LXR-dependent cholesterol efflux by targeting ABCA1 and ARL7. FEBS Lett., 2012, 586(10), 1472-1479.
[37]
Ramirez, C.M.; Dávalos, A.; Goedeke, L.; Salerno, A.G.; Warrier, N.; Cirerasalinas, D.; Suárez, Y.; Fernándezhernando, C. MicroRNA-758 regulates cholesterol efflux through posttranscriptional repression of ATP-binding cassette transporter A1. Arterioscler. Thromb. Vasc. Biol., 2011, 31(11), 2707-2714.
[38]
Alexandre, W.; Hani, N.S.; Lifeng, W.; Leigh, G.; Sumita, S.; Delemos, A.S.; Black, J.C.; Ramírez, C.M.; Yingxia, L.; Ryan, T. Genome-wide identification of microRNAs regulating cholesterol and triglyceride homeostasis. Nat. Med., 2015, 21(11), 1290-1297.
[39]
Dávalos, A.; Goedeke, L.; Smibert, P.; Ramírez, C.M.; Warrier, N.P.; Andreo, U.; Cirera-Salinas, D.; Rayner, K.; Suresh, U.; Pastor-Pareja, J.C. miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc. Natl. Acad. Sci. USA, 2011, 108(22), 9232-9237.
[40]
Ramirez, C.M.; Goedeke, L.; Rotllan, N.; Yoon, J.H.; Cirera-Salinas, D.; Mattison, J.A.; Suarez, Y.; de Cabo, R.; Gorospe, M.; Fernandez-Hernando, C. MicroRNA 33 regulates glucose metabolism. Mol. Cell. Biol., 2013, 33(15), 2891-2902.
[41]
Fernández-Hernando, C.; Moore, K.J. MicroRNA modulation of cholesterol homeostasis. Arterioscler. Thromb. Vasc. Biol., 2011, 31(11), 2378-2382.
[42]
Rayner, K.J.; Yajaira, S.; Alberto, D.; Saj, P.; Fitzgerald, M.L.; Norimasa, T.; Fisher, E.A.; Moore, K.J.; Carlos, F.H. MiR-33 contributes to the regulation of cholesterol homeostasis. Science, 2010, 328(5985), 1570-1573.
[43]
Ediriweera, H. Therapeutic targeting of miR-33 in atherosclerosis; Dissertations & Theses - Gradworks, 2014.
[44]
Greenow, K.; Pearce, N.J.; Ramji, D.P. The key role of apolipoprotein E in atherosclerosis. J. Mol. Med., 2005, 83(5), 329-342.
[45]
Rotllan, N.; Price, N.; Pati, P.; Goedeke, L.; Fernandez-Hernando, C. microRNAs in lipoprotein metabolism and cardiometabolic disorders. Atherosclerosis, 2016, 246, 352-360.
[46]
Ramírez, C.M.; Noemi, R.; Vlassov, A.V.; Alberto, D.; Mu, L.; Leigh, G.; Aranda, J.F.; Daniel, C.S.; Elisa, A.; Alessandro, S. Control of cholesterol metabolism and plasma high-density lipoprotein levels by microRNA-144. Circ. Res., 2013, 112(12), 1592-1601.
[47]
Takahiro, H.; Osamu, B.; Yasuhide, K.; Yoshimasa, C.; Shin, W.; Minako, K.; Masahito, H.; Tomoyuki, N.; Kazuhisa, C.; Masakatsu, H. MicroRNA-33 deficiency reduces the progression of atherosclerotic plaque in ApoE-/- mice. J. Am. Heart Assoc., 2012, 1(6), e003376-e003392.
[48]
Bidzhekov, K.; Gan, L.; Denecke, B.; Rostalsky, A.; Hristov, M.; Koeppel, T.A.; Zernecke, A.; Weber, C. microRNA expression signatures and parallels between monocyte subsets and atherosclerotic plaque in humans. Thromb. Haemost., 2012, 107(04), 619-625.
[49]
Fei, M. Mordicin MD28 increases ABCA1 expression by down-regulating miR-23b-3p; , 2015. In complete
[50]
Kim, J.; Yoon, H.; Ramírez, C.M.; Lee, S.M.; Hoe, H.S.; Fernández-Hernando, C.; Kim, J. miR-106b impairs cholesterol efflux and increases Aβ levels by repressing ABCA1 expression. Exp. Neurol., 2012, 235(2), 476-483.
[51]
Leigh, G.; Noemi, R.; Alberto, C.D.; Aranda, J.F.; Ramírez, C.M.; Elisa, A.; Chin-Sheng, L.; Anderson, N.N.; Alexandre, W.; Rafael, D.C. MicroRNA-148a regulates LDL receptor and ABCA1 expression to control circulating lipoprotein levels. Nat. Med., 2015, 21(11), 1280-1289.
[52]
de Aguiar Vallim, T.Q.; Tarling, E.J.; Kim, T.; Civelek, M.; Baldán, Á.; Esau, C.; Edwards, P.A. 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), 1602-1612.
[53]
Goedeke, L.; Rotllan, N.; Ramírez, C.M.; Aranda, J.F.; Canfrán-Duque, A.; Araldi, E.; Fernández-Hernando, A.; Langhi, C.; Cabo, R.D.; Baldán, Á. miR-27b inhibits LDLR and ABCA1 expression but does not influence plasma and hepatic lipid levels in mice. Atherosclerosis, 2015, 243(2), 499-509.
[54]
Svenja, M.; Yvonne, B.; Emma, T.; Kosal, S.; Boisvert, W.A. MicroRNA 302a is a novel modulator of cholesterol homeostasis and atherosclerosis. Arterioscler. Thromb. Vasc. Biol., 2015, 35(2), 323-331.
[55]
Kang, M.H.; Lin-Hua, Z.; Nadeeja, W.; Willeke, D.H.; Stefanie, B.; Alpana, B.; 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), 2724-2732.
[56]
Adlakha, Y.K.; Khanna, S.; Singh, R.; Singh, V.P.; 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-e791.
[57]
Wang, D.; Yan, X.; Xia, M.; Yang, Y.; Li, D.; Li, X.; Song, F.; Ling, W. Coenzyme Q10 promotes macrophage cholesterol efflux by regulation of the activator protein-1/miR-378/ATP-binding cassette transporter G1-signaling pathway. Arterioscler. Thromb. Vasc. Biol., 2014, 34(9), 1860-1870.
[58]
Kim, T.H.; Kim, I.; Kim, E.M.; Park, H.E.; Park, E.H.; Kang, K.; Kim, C.W.; Kim, J.M.; Ihm, S.H.; Chang, K. MicroRNA 18a is a novel regulator of reverse cholesterol transport and potential therapeutic targets in atherosclerosis. Atherosclerosis, 2017, 263, e111-e112.
[59]
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), 518-520.
[60]
Li, W.; Xiao-Jian, J.; Hua-Jun, J.; Yu, D.; Fan, Y.; Shu-Yi, S.; Bin, H. MicroRNAs 185, 96, and 223 repress selective high-density lipoprotein cholesterol uptake through posttranscriptional inhibition. Mol. Cell. Biol., 2013, 33(10), 1956-1964.
[61]
Vickers, K.C.; Landstreet, S.R.; Levin, M.G.; Shoucri, B.M.; Toth, C.L.; Taylor, R.C.; Palmisano, B.T.; Fatiha, T.; Cui, H.L.; Kerry-Anne, R. MicroRNA-223 coordinates cholesterol homeostasis. Proc. Natl. Acad. Sci. USA, 2014, 111(40), 14518-14523.
[62]
Zhigang, H.; Wen-Jun, S.; Kraemer, F.B.; Salman, A. 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.
[63]
Ren, K.; Zhu, X.; Zheng, Z.; Mo, Z.C.; Peng, X.S.; Zeng, Y.Z.; Ou, H.X.; Zhang, Q.H.; Qi, H.Z.; Zhao, G.J. MicroRNA-24 aggravates atherosclerosis by inhibiting selective lipid uptake from HDL cholesterol via the post-transcriptional repression of scavenger receptor class B type I. Atherosclerosis, 2018, 270, 57-67.
[64]
Tall, A.R.; Yvancharvet, L.; Terasaka, N.; Pagler, T.; Wang, N. HDL, ABC transporters, and cholesterol efflux: Implications for the treatment of atherosclerosis. Cell Metab., 2008, 7(5), 365-375.
[65]
Huajun, J.; Jin, Z.; Yu, D.; Xiaojian, J.; Fan, Y.; Shuyi, S.; Li, W.; Bin, H. microRNA-185 modulates low density lipoprotein receptor expression as a key posttranscriptional regulator. Atherosclerosis, 2015, 243(2), 523-532.
[66]
Allen, R.M.; Marquart, T.J.; Albert, C.J.; Suchy, F.J.; Wang, D.Q.; Ananthanarayanan, M.; Ford, D.A.; Baldã, N.A. miR-33 controls the expression of biliary transporters, and mediates statin- and diet-induced hepatotoxicity. EMBO Mol. Med., 2012, 4(9), 882-895.
[67]
Kamisako, T.; Ogawa, H. Regulation of biliary cholesterol secretion is associated with abcg5 and abcg8 expressions in the rats: Effects of diosgenin and ethinyl estradiol. Hepatol. Res., 2003, 26(4), 348-352.
[68]
Matsumoto, N.; Okushio, K.Y. Effect of black tea polyphenols on plasma lipids in cholesterol-fed rats. J. Nutr. Sci. Vitaminol., 1998, 44(2), 337-342.
[69]
Zern, T.L.; Wood, R.J.; Christine, G.; West, K.L.; Yanzhu, L.; Dimple, A.; Shachter, N.S.; Maria Luz, F. Grape polyphenols exert a cardioprotective effect in pre- and postmenopausal women by lowering plasma lipids and reducing oxidative stress. J. Nutr., 2005, 135(8), 1911-1917.
[70]
Li, Y.; Kong, D.; Wang, Z.; Sarkar, F.H. Regulation of microRNAs by natural agents: An emerging field in chemoprevention and chemotherapy research. Pharm. Res., 2010, 27(6), 1027-1041.
[71]
Perumal, Y.; Dharmarajan, S. Betulinic acid and its derivatives: A review on their biological properties. Curr. Med. Chem., 2005, 12(6), 657-666.
[72]
Zhao, G.J.; Tang, S.L.; Lv, Y.C.; Ouyang, X.P.; He, P.P.; Yao, F.; Chen, W.J.; Lu, Q.; Tang, Y.Y.; Zhang, M. Antagonism of betulinic acid on LPS-mediated inhibition of ABCA1 and cholesterol efflux through inhibiting nuclear factor-kappaB signaling pathway and miR-33 expression. PLoS One, 2013, 8(9), e74782-e74783.
[73]
Hong, W.; Shengjie, B.; Yang, C.S. Green tea polyphenol EGCG suppresses lung cancer cell growth through upregulating miR-210 expression caused by stabilizing HIF-1α. Carcinogenesis, 2011, 32(12), 1881-1889.
[74]
Yin, J.; Huang, F.; Yi, Y.; Yin, L.; Peng, D. EGCG attenuates atherosclerosis through the Jagged-1/Notch pathway. Int. J. Mol. Med., 2016, 37(2), 398-406.
[75]
Lv, Y.C.; Yang, J.; Yao, F.; Xie, W.; Tang, Y.Y.; Ouyang, X.P.; He, P.P.; Tan, Y.L.; Li, L.; Zhang, M. Diosgenin inhibits atherosclerosis via suppressing the MiR-19b-induced downregulation of ATP-binding cassette transporter A1. Atherosclerosis, 2015, 240(1), 80-89.
[76]
Wang, Z.; Yun-Cheng, L.; Tang, C.K.; Yao, F.; Wang, Z.B.; Liu, L.S.; Guang-Hui, Y.I.; Yang, Y.Z. Experimental studies on anti-atherosclerosis effects of Momordica charantia L in rabbits. Chin. J. Pathophysiol., 2005, 21(3), 514-518.
[77]
Song, Y.M.; Zuo, W.; Guo, Z.Y.; Zhang, X.L.; Jun, M. Effects of momordicin on atherogenesis of apolipoprotein e knockout mice and expression of intestinal cholesterol transport related genes. Chin. J. Arterioscler., 2009. Incomplete
[78]
Allen, R.M.; Vickers, K.C. Coenzyme Q10 increases cholesterol efflux and inhibits atherosclerosis through microRNAs. Arterioscler. Thromb. Vasc. Biol., 2014, 34(9), 1795-1797.
[79]
Su, D.; Zhang, R.; Hou, F.; Chi, J.; Huang, F.; Yan, S.; Liu, L.; Deng, Y.; Wei, Z.; Zhang, M. Lychee pulp phenolics ameliorate hepatic lipid accumulation by reducing miR-33 and miR-122 expression in mice fed a high-fat diet. Food Funct., 2017, 8(2), 808-815.

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy