miR-223 inhibits lipid deposition and inflammation by suppressing toll-like receptor 4 signaling in macrophages

International Journal of Molecular Sciences

Volumn 16, Issue 10, 2015, Pages 24965-24982

  Wang, Jun ^a   Bai, Xiaojun ^a   Song, Qiang ^a   Fan, Fenling ^a   Hu, Zhi ^a   Cheng, Gesheng ^a   Zhang, Yushun ^a  

^a XI'AN JIAOTONG UNIVERSITY   (China)

Author keywords

Atherosclerosis; Inflammatory; Lipid accumulation; MiR 223; PI3K AKT; TLR4

Indexed keywords

CHOLESTEROL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MICRORNA 223; NITRIC OXIDE; TOLL LIKE RECEPTOR 4; TRIACYLGLYCEROL; MICRORNA; MIRN223 MICRORNA, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INFLAMMATION; LIPID DIET; LIPID STORAGE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; GENETICS; KNOCKOUT MOUSE; LIPID METABOLISM; MACROPHAGE; METABOLISM; PHYSIOLOGY; RAW 264.7 CELL LINE;

ANIMALS; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; INFLAMMATION; INTERLEUKIN-6; LIPID METABOLISM; MACROPHAGES; MICE; MICE, KNOCKOUT; MICRORNAS; RAW 264.7 CELLS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84944754560     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms161024965     Document Type: Article

References (51)

1. Di Tullio, M.R.; Russo, C.; Jin, Z.; Sacco, R.L.; Mohr, J.; Homma, S. Aortic arch plaques and risk of recurrent stroke and death. Circulation 2009, 119, 2376-2382.
2. Wang, G.; Kim, R.Y.; Imhof, I.; Honbo, N.; Luk, F.S.; Li, K.; Kumar, N.; Zhu, B.-Q.; Eberlé, D.; Ching, D. The immunosuppressant FTY720 prolongs survival in a mouse model of diet-induced coronary atherosclerosis and myocardial infarction. J. Cardiovasc. Pharmacol. 2014, 63, 132-143.
3. Graceffa, A. Preclinical atherosclerosis, metabolic syndrome and risk of cardiovascular events. Int. J. Sci. 2014, 3, 33-42.
4. Yahagi, K.; Davis, H.R.; Arbustini, E.; Virmani, R. Sex differences in coronary artery disease: Pathological observations. Atherosclerosis 2015, 239, 260-267.
5. Raul, C.M.; Antonio, C.A.L. Development of anti-atherosclerosis therapy based on the inflammatory and proliferative aspects of the disease. Curr. Pharm. Des. 2015, 21, 1196-1204.
6. Tian, G.-P.; Tang, Y.-Y.; He, P.-P.; Lv, Y.-C.; Ouyang, X.-P.; Zhao, G.-J.; Tang, S.-L.; Wu, J.-F.; Wang, J.-L.; Peng, J. The effects of miR-467b on lipoprotein lipase (LPL) expression, pro-inflammatory cytokine, lipid levels and atherosclerotic lesions in apolipoprotein E knockout mice. Biochem. Biophys. Res. Commun. 2014, 443, 428-434.
7. Feng, X.; Yuan, Y.; Wang, C.; Feng, J.; Yuan, Z.; Zhang, X.; Sui, W.; Hu, P.; Zheng, P.; Ye, J. Autophagy involved in lipopolysaccharide-induced foam cell formation is mediated by adipose differentiation-related protein. Lipids Health Dis. 2014, 13, 1-9.
8. Westerterp, M.; Murphy, A.J.; Wang, M.; Pagler, T.A.; Vengrenyuk, Y.; Kappus, M.S.; Gorman, D.J.; Nagareddy, P.R.; Zhu, X.; Abramowicz, S. Deficiency of ATP-binding cassette transporters A1 and G1 in macrophages increases inflammation and accelerates atherosclerosis in mice. Circ. Res. 2013, 112, 1456-1465.
9. Mullick, A.E.; Tobias, P.S.; Curtiss, L.K. Toll-like receptors and atherosclerosis. Immunol. Res. 2006, 34, 193-209.
10. Pasterkamp, G.; van Keulen, J.; de Kleijn, D. Role of Toll-like receptor 4 in the initiation and progression of atherosclerotic disease. Eur. J. Clin. Investig. 2004, 34, 328-334.
11. Higashimori, M.; Tatro, J.B.; Moore, K.J.; Mendelsohn, M.E.; Galper, J.B.; Beasley, D. Role of Toll-Like receptor 4 in intimal foam cell accumulation in apolipoprotein E-Deficient mice. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 50-57.
12. Zhang, X.; Xie, Y.; Zhou, H.; Xu, Y.; Liu, J.; Xie, H.; Yan, J. Involvement of TLR4 in oxidized LDL/ β2GPI/Anti-β2GPI-induced transformation of macrophages to foam cells. J. Atheroscler. Thromb. 2014, 21, 1140-1151.
13. Ding, Y.; Subramanian, S.; Montes, V.N.; Goodspeed, L.; Wang, S.; Han, C.; Teresa, A.S.; Kim, J.; O'Brien, K.D.; Chait, A. Toll-like receptor 4 deficiency decreases atherosclerosis but does not protect against inflammation in obese low-density lipoprotein receptor-Deficient mice. Arterioscler. Thromb. Vasc. Biol. 2012, 32, 1596-1604.
14. Katsargyris, A.; Klonaris, C.; Tsiodras, S.; Bastounis, E.; Giannopoulos, A.; Theocharis, S. Statin treatment is associated with reduced toll-like receptor 4 immunohistochemical expression on carotid atherosclerotic plaques: A novel effect of statins. Vascular 2011, 19, 320-326.
15. Ayyappan, J.P.; Abraham, A. Targeting TLR4/MAPKs signaling pathway: A better option for therapeutic inhibition of atherosclerosis. World J. Immunol. 2014, 4, 116-121.
16. Dangwal, S.; Thum, T. microRNA therapeutics in cardiovascular disease models. Annu. Rev. Pharmacol. Toxicol. 2014, 54, 185-203.
17. Sheikh, M.S.A.; Xia, K.; Li, F.; Deng, X.; Salma, U.; Deng, H.; Liu, W.; Yang, T.-L.; Peng, J. Circulating miR-765 and miR-149: Potential noninvasive diagnostic biomarkers for geriatric coronary artery disease patients. Biomed. Res. Int. 2015, 2015, doi:10.1155/2015/740301.
18. Nazari-Jahantigh, M.; Wei, Y.; Noels, H.; Akhtar, S.; Zhou, Z.; Koenen, R.R.; Heyll, K.; Gremse, F.; Kiessling, F.; Grommes, J. MicroRNA-155 promotes atherosclerosis by repressing Bcl6 in macrophages. J. Clin. Investig. 2012, 122, 4190-4202.
19. Jiang, W.; Ni, Q.; Tan, L.; Kong, L.; Lu, Y.; Xu, X. The microRNA-146a/b attenuates acute small-for-size liver graft injury in rats. Liver Int. 2015, 35, 914-924.
20. Liu, G.; Friggeri, A.; Yang, Y.; Park, Y.J.; Tsuruta, Y.; Abraham, E. miR-147, a microRNA that is induced upon Toll-like receptor stimulation, regulates murine macrophage inflammatory responses. Proc. Natl. Acad. Sci. USA 2009, 106, 15819-15824.
21. Kong, H.; Yin, F.; He, F.; Omran, A.; Li, L.; Wu, T.; Wang, Y.; Peng, J. The effect of miR-132, miR-146a, and miR-155 on MRP8/TLR4-induced astrocyte-related inflammation. J. Mol. Neurosci. 2015, 57, 28-37.
22. Chen, Y.; Chen, J.; Wang, H.; Shi, J.; Wu, K.; Liu, S.; Liu, Y.; Wu, J. HCV-induced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1. PLoS Pathog. 2013, 9, e1003248.
23. Fabbri, M.; Paone, A.; Calore, F.; Galli, R.; Gaudio, E.; Santhanam, R.; Lovat, F.; Fadda, P.; Mao, C.; Nuovo, G.J.; et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. USA 2012, 109, E2110-E2116.
24. He, J.; He, Y.; Chen, D.; Yu, B.; Mao, X.; Zheng, P.; Yu, J.; Huang, Z.; Luo, J. miR-628, a microRNA that is induced by Toll-like receptor stimulation, regulates porcine innate immune responses. Sci. Rep. 2015, 5, doi:10.1038/srep12226.
25. Fordham, J.B.; Naqvi, A.R.; Nares, S. Regulation of miR-24, miR-30b, and miR-142-3p during macrophage and dendritic cell differentiation potentiates innate immunity. J. Leukoc. Biol. 2015, 98, 195-207.
26. Haneklaus, M.; Gerlic, M.; O'Neill, L.A.; Masters, S.L. miR-223: Infection, inflammation and cancer. J. Intern. Med. 2013, 274, 215-226.
27. Ferland-McCollough, D.; Ozanne, S.; Siddle, K.; Willis, A.; Bushell, M. The involvement of microRNAs in Type2 diabetes. Biochem. Soc. Trans. 2010, 38, 1565-1570.
28. Paraskevi, A.; Theodoropoulos, G.; Papaconstantinou, I.; Mantzaris, G.; Nikiteas, N.; Gazouli, M. Circulating microRNA in inflammatory bowel disease. J. Crohn's Colitis 2012, 6, 900-904.
29. Pinatel, E.M.; Orso, F.; Penna, E.; Cimino, D.; Elia, A.R.; Circosta, P.; Dentelli, P.; Brizzi, M.F.; Provero, P.; Taverna, D. miR-223 is a coordinator of breast cancer progression as revealed by bioinformatics predictions. PLoS ONE 2014, 9, e84859.
30. Chen, Q.; Wang, H.; Liu, Y.; Song, Y.; Lai, L.; Han, Q.; Cao, X.; Wang, Q. Inducible microRNA-223 down-regulation promotes TLR-triggered IL-6 and IL-1β production in macrophages by targeting STAT3. PLoS ONE 2012, 7, e42971.
31. Liu, Y.; Wang, R.; Jiang, J.; Yang, B.; Cao, Z.; Cheng, X. miR-223 is upregulated in monocytes from patients with tuberculosis and regulates function of monocyte-derived macrophages. Mol. Immunol. 2015, 67, 475-481.
32. Sugatani, T.; Hruska, K.A. MicroRNA-223 is a key factor in osteoclast differentiation. J. Cell. Biochem. 2007, 101, 996-999.
33. Fazi, F.; Rosa, A.; Fatica, A.; Gelmetti, V.; de Marchis, M.L.; Nervi, C.; Bozzoni, I. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPα regulates human granulopoiesis. Cell 2005, 123, 819-831.
34. Taibi, F.; Metzinger-Le Meuth, V.; M'Baya-Moutoula, E.; Djelouat, M.; Louvet, L.; Bugnicourt, J.M.; Poirot, S.; Bengrine, A.; Chillon, J.M.; Massy, Z.A.; et al. Possible involvement of microRNAs in vascular damage in experimental chronic kidney disease. Biochim. Biophys. Acta 2014, 1842, 88-98.
35. Zeller, I.; Srivastava, S. Macrophage functions in atherosclerosis. Circ. Res. 2014, 115, e83-e85.
36. Moore, K.J.; Tabas, I. Macrophages in the pathogenesis of atherosclerosis. Cell 2011, 145, 341-355.
37. Calippe, B.; Douin-Echinard, V.; Laffargue, M.; Laurell, H.; Rana-Poussine, V.; Pipy, B.; Guery, J.C.; Bayard, F.; Arnal, J.F.; Gourdy, P. Chronic estradiol administration in vivo promotes the proinflammatory response of macrophages to TLR4 activation: involvement of the phosphatidylinositol 3-kinase pathway. J. Immunol. 2008, 180, 7980-7988.
38. Libby, P. Inflammation in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2012, 32, 2045-2051.
39. Xue, Y.; Wei, Z.; Ding, H.; Wang, Q.; Zhou, Z.; Zheng, S.; Zhang, Y.; Hou, D.; Liu, Y.; Zen, K.; et al. MicroRNA-19b/221/222 induces endothelial cell dysfunction via suppression of PGC-1α in the progression of atherosclerosis. Atherosclerosis 2015, 241, 671-681.
40. Cengiz, M.; Yavuzer, S.; Avci, B.K.; Yuruyen, M.; Yavuzer, H.; Dikici, S.A.; Karatas, O.F.; Ozen, M.; Uzun, H.; Ongen, Z. Circulating miR-21 and eNOS in subclinical atherosclerosis in patients with hypertension. Clin. Exp. Hypertens. 2015, doi:10.3109/10641963.2015.1036064.
41. Fish, J.E.; Cybulsky, M.I. ApoE attenuates atherosclerosis via miR-146a. Circ. Res. 2015, 117, 3-6.
42. Koga, J.-I.; Aikawa, M. Molecular imaging of macrophages in atherosclerosis. In Cardiovascular Imaging; Springer: Cham, Switzerland, 2015; pp. 65-78.
43. Ishikawa, Y.; Satoh, M.; Itoh, T.; Minami, Y.; Takahashi, Y.; Akamura, M. Local expression of Toll-like receptor 4 at the site of ruptured plaques in patients with acute myocardial infarction. Clin. Sci. 2008, 115, 133-140.
44. Den Dekker, W.K.; Cheng, C.; Pasterkamp, G.; Duckers, H.J. Toll like receptor 4 in atherosclerosis and plaque destabilization. Atherosclerosis 2010, 209, 314-320.
45. 4 amplifies NF-κB activation in mouse macrophages by reducing SOCS1 inhibition of MyD88 expression. J. Clin. Investig. 2011, 121, 671-682.
46. Ni, M.; Wang, Y.; Zhang, M.; Zhang, P.F.; Ding, S.F.; Liu, C.X.; Liu, X.L.; Zhao, Y.X.; Zhang, Y. Atherosclerotic plaque disruption induced by stress and lipopolysaccharide in apolipoprotein E knockout mice. Am. J. Physiol. Heart Circ. Physiol. 2009, 296, H1598-H1606.
47. Xu, C.-Q.; Liu, B.-J.; Wu, J.-F.; Xu, Y.-C.; Duan, X.-H.; Cao, Y.-X.; Dong, J.-C. Icariin attenuates LPS-induced acute inflammatory responses: Involvement of PI3K/Akt and NF-κB signaling pathway. Eur. J. Pharmacol. 2010, 642, 146-153.
48. Kamo, N.; Ke, B.; Busuttil, R.W.; Kupiec-Weglinski, J.W. PTEN-mediated Akt/β-Catenin/foxo1 signaling regulates innate immune responses in mouse liver ischemia/reperfusion injury. Hepatology 2013, 57, 289-298.
49. Lee, W.J. IGF-I exerts an anti-inflammatory effect on skeletal muscle cells through down-regulation of TLR4 signaling. Immune Netw. 2011, 11, 223-226.
50. Joo, S.-Y.; Song, Y.-A.; Park, Y.-L.; Myung, E.; Chung, C.-Y.; Park, K.-J.; Cho, S.-B.; Lee, W.-S.; Kim, H.-S.; Rew, J.-S. Epigallocatechin-3-gallate inhibits LPS-induced NF-κB and MAPK signaling pathways in bone marrow-derived macrophages. Gut Liver 2012, 6, 188-196.
51. Yu, C.-H.; Xu, C.-F.; Li, Y.-M. Association of MicroRNA-223 expression with hepatic ischemia/reperfusion injury in mice. Dig. Dis. Sci. 2009, 54, 2362-2366.