MicroRNA-33 Regulates Macrophage Autophagy in Atherosclerosis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 37, Issue 6, 2017, Pages 1058-1067

  Ouimet, Mireille ^a   Ediriweera, Hasini ^a   Afonso, Milessa Silva ^a   Ramkhelawon, Bhama ^b   Singaravelu, Ragunath ^c,d   Liao, Xianghai ^e   Bandler, Rachel C ^a   Rahman, Karishma ^a   Fisher, Edward A ^a   Rayner, Katey J ^a   Pezacki, John P ^c,d   Tabas, Ira ^e   Moore, Kathryn J ^c,f  

^a Marc and Ruti Bell Vascular Biology and Disease Program   (Australia)

^b NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF OTTAWA   (Canada)

^d NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^e Columbia University ^*  (United States)

^f UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

Author keywords

atherosclerosis; autophagy; hydrolysis; lipid droplets; macrophages

Indexed keywords

ABC TRANSPORTER A1; CHLOROQUINE; CHOLESTEROL; FAT DROPLET; MICRORNA; MICRORNA 33; PARAOXON; UNCLASSIFIED DRUG; ATG5 PROTEIN, MOUSE; AUTOPHAGY RELATED PROTEIN 5; LOW DENSITY LIPOPROTEIN RECEPTOR; MIRN33 MICRORNA, HUMAN; MIRN33 MICRORNA, MOUSE;

ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOPHAGY; BIOGENESIS; BONE MARROW DERIVED MACROPHAGE; CATABOLISM; CHOLESTEROL METABOLISM; CLEARANCE; CONTROLLED STUDY; DEGRADATION; GENETICS; HOMEOSTASIS; HYDROLYSIS; IN VIVO STUDY; LIPOLYSIS; LYSOSOME; MOBILIZATION; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; REGULATORY MECHANISM; ANIMAL; C57BL MOUSE; DEFICIENCY; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETIC TRANSFECTION; HUMAN; JURKAT CELL LINE; KNOCKOUT MOUSE; METABOLISM; NECROSIS; PATHOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION;

ANIMALS; ATHEROSCLEROSIS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 5; CHOLESTEROL; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; HUMANS; JURKAT CELLS; LIPID DROPLETS; LYSOSOMES; MACROPHAGES, PERITONEAL; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; NECROSIS; PHENOTYPE; PLAQUE, ATHEROSCLEROTIC; RECEPTORS, LDL; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 85018831750     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.116.308916     Document Type: Article

References (45)

1. Moore KJ, Sheedy FJ, Fisher EA, Macrophages in atherosclerosis: a dynamic balance. Nat Rev Immunol 2013 13 709 721. doi: 10.1038/nri3520.
2. Ouimet M, Autophagy in obesity and atherosclerosis: interrelationships between cholesterol homeostasis, lipoprotein metabolism and autophagy in macrophages and other systems. Biochim Biophys Acta 2013 1831 1124 1133. doi: 10.1016/j.bbalip.2013.03.007.
3. Singh R, Cuervo AM, Autophagy in the cellular energetic balance. Cell Metab 2011 13 495 504. doi: 10.1016/j.cmet.2011.04.004.
4. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM, Czaja MJ, Autophagy regulates lipid metabolism. Nature 2009 458 1131 1135. doi: 10.1038/nature07976.
5. Ouimet M, Franklin V, Mak E, Liao X, Tabas I, Marcel YL, Autophagy regulates cholesterol efflux from macrophage foam cells via lysosomal acid lipase. Cell Metab 2011 13 655 667. doi: 10.1016/j.cmet.2011.03.023.
6. Tabas I, Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol 2010 10 36 46. doi: 10.1038/nri2675.
7. Zang L, Xu Q, Ye Y, Li X, Liu Y, Tashiro S, Onodera S, Ikejima T, Autophagy enhanced phagocytosis of apoptotic cells by oridonin-treated human histiocytic lymphoma U937 cells. Arch Biochem Biophys 2012 518 31 41. doi: 10.1016/j.abb.2011.11.019.
8. Razani B, Feng C, Coleman T, Emanuel R, Wen H, Hwang S, Ting JP, Virgin HW, Kastan MB, Semenkovich CF, Autophagy links inflammasomes to atherosclerotic progression. Cell Metab 2012 15 534 544. doi: 10.1016/j.cmet.2012.02.011.
9. Robinet P, Ritchey B, Smith JD, Physiological difference in autophagic flux in macrophages from 2 mouse strains regulates cholesterol ester metabolism. Arterioscler Thromb Vasc Biol 2013 33 903 910. doi: 10.1161/ATVBAHA.112.301041.
10. Liao X, Sluimer JC, Wang Y, Subramanian M, Brown K, Pattison JS, Robbins J, Martinez J, Tabas I, Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab 2012 15 545 553. doi: 10.1016/j.cmet.2012.01.022.
11. Rayner KJ, Moore KJ, MicroRNA control of high-density lipoprotein metabolism and function. Circ Res 2014 114 183 192. doi: 10.1161/CIRCRESAHA.114.300645.
12. Gupta SK, Thum T, Non-coding RNAs as orchestrators of autophagic processes. J Mol Cell Cardiol 2016 95 26 30. doi: 10.1016/j.yjmcc.2015.11.012.
13. Zhai H, Fesler A, Ju J, MicroRNA: a third dimension in autophagy. Cell Cycle 2013 12 246 250. doi: 10.4161/cc.23273.
14. Feinberg MW, Moore KJ, MicroRNA regulation of atherosclerosis. Circ Res 2016 118 703 720. doi: 10.1161/CIRCRESAHA.115.306300.
15. Bartel DP, MicroRNAs: target recognition and regulatory functions. Cell 2009 136 215 233. doi: 10.1016/j.cell.2009.01.002.
16. Marquart TJ, Allen RM, Ory DS, Baldán A, miR-33 links SREBP-2 induction to repression of sterol transporters. Proc Natl Acad Sci USA 2010 107 12228 12232. doi: 10.1073/pnas.1005191107.
17. Najafi-Shoushtari SH, Kristo F, Li Y, Shioda T, Cohen DE, Gerszten RE, Näär AM, MicroRNA-33 and the SREBP host genes cooperate to control cholesterol homeostasis. Science 2010 328 1566 1569. doi: 10.1126/science.1189123.
18. Rayner KJ, Suárez Y, Dávalos A, Parathath S, Fitzgerald ML, Tamehiro N, Fisher EA, Moore KJ, Fernández-Hernando C, MiR-33 contributes to the regulation of cholesterol homeostasis. Science 2010 328 1570 1573. doi: 10.1126/science.1189862.
19. Ramirez CM, Dávalos A, Goedeke L, Salerno AG, 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 2707 2714. doi: 10.1161/ATVBAHA.111.232066.
20. Gerin I, Clerbaux LA, Haumont O, Lanthier N, Das AK, Burant CF, Leclercq IA, MacDougald OA, Bommer GT, Expression of miR-33 from an SREBP2 intron inhibits cholesterol export and fatty acid oxidation. J Biol Chem 2010 285 33652 33661. doi: 10.1074/jbc.M110.152090.
21. Rottiers V, Najafi-Shoushtari SH, Kristo F, Gurumurthy S, Zhong L, Li Y, Cohen DE, Gerszten RE, Bardeesy N, Mostoslavsky R, Näär AM, MicroRNAs in metabolism and metabolic diseases. Cold Spring Harb Symp Quant Biol 2011 76 225 233. doi: 10.1101/sqb.2011.76.011049.
22. 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 17321 17326. doi: 10.1073/pnas.1008499107.
23. Dávalos A, Goedeke L, Smibert P, miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc Natl Acad Sci USA 2011 108 9232 9237. doi: 10.1073/pnas.1102281108.
24. Rayner KJ, Esau CC, Hussain FN, Inhibition of miR-33a/b in non-human primates raises plasma HDL and lowers VLDL triglycerides. Nature 2011 478 404 407. doi: 10.1038/nature10486.
25. Rottiers V, Obad S, Petri A, Pharmacological inhibition of a microRNA family in nonhuman primates by a seed-targeting 8-mer antimiR. Sci Transl Med 2013 5 212ra162. doi: 10.1126/scitranslmed.3006840.
26. Ouimet M, Ediriweera HN, Gundra UM, MicroRNA-33-dependent regulation of macrophage metabolism directs immune cell polarization in atherosclerosis. J Clin Invest 2015 125 4334 4348. doi: 10.1172/JCI81676.
27. Rayner KJ, Sheedy FJ, Esau CC, Hussain FN, Temel RE, Parathath S, van Gils JM, Rayner AJ, Chang AN, Suarez Y, Fernandez-Hernando C, Fisher EA, Moore KJ, Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J Clin Invest 2011 121 2921 2931. doi: 10.1172/JCI57275.
28. Horie T, Baba O, Kuwabara Y, MicroRNA-33 deficiency reduces the progression of atherosclerotic plaque in ApoE-/-mice. J Am Heart Assoc 2012 1 e003376. doi: 10.1161/JAHA.112.003376.
29. Rotllan N, Ramírez CM, Aryal B, Esau CC, Fernández-Hernando C, Therapeutic silencing of microRNA-33 inhibits the progression of atherosclerosis in Ldlr-/-mice-brief report. Arterioscler Thromb Vasc Biol 2013 33 1973 1977. doi: 10.1161/ATVBAHA.113.301732.
30. Ouimet M, Koster S, Sakowski E, Mycobacterium tuberculosis induces the miR-33 locus to reprogram autophagy and host lipid metabolism. Nat Immunol 2016 17 677 686. doi: 10.1038/ni.3434.
31. Klionsky DJ, Abdalla FC, Abeliovich H, Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012 8 445 544
32. Zang L, He H, Ye Y, Liu W, Fan S, Tashiro S, Onodera S, Ikejima T, Nitric oxide augments oridonin-induced efferocytosis by human histocytic lymphoma U937 cells via autophagy and the NF-κB-COX-2-IL-1β pathway. Free Radic Res 2012 46 1207 1219. doi: 10.3109/10715762.2012.700515.
33. Lai SC, Devenish RJ, LC3-associated phagocytosis (LAP): connections with host autophagy. Cells 2012 1 396 408. doi: 10.3390/cells1030396.
34. Martinez J, Almendinger J, Oberst A, Ness R, Dillon CP, Fitzgerald P, Hengartner MO, Green DR, Microtubule-associated protein 1 light chain 3 alpha (LC3)-associated phagocytosis is required for the efficient clearance of dead cells. Proc Natl Acad Sci USA 2011 108 17396 17401. doi: 10.1073/pnas.1113421108.
35. Allen RM, Marquart TJ, Albert CJ, Suchy FJ, Wang DQ, Ananthanarayanan M, Ford DA, Baldán A, miR-33 controls the expression of biliary transporters, and mediates statin-and diet-induced hepatotoxicity. EMBO Mol Med 2012 4 882 895. doi: 10.1002/emmm.201201228.
36. Ouimet M, Hennessy EJ, van Solingen C, Koelwyn GJ, Hussein MA, Ramkhelawon B, Rayner KJ, Temel RE, Perisic L, Hedin U, Maegdefessel L, Garabedian MJ, Holdt LM, Teupser D, Moore KJ, miRNA targeting of oxysterol-binding protein-like 6 regulates cholesterol trafficking and efflux. Arterioscler Thromb Vasc Biol 2016 36 942 951. doi: 10.1161/ATVBAHA.116.307282.
37. Sanchez AM, Candau RB, Csibi A, Pagano AF, Raibon A, Bernardi H, The role of AMP-activated protein kinase in the coordination of skeletal muscle turnover and energy homeostasis. Am J Physiol Cell Physiol 2012 303 C475 C485. doi: 10.1152/ajpcell.00125.2012.
38. Palmieri M, Impey S, Kang H, di Ronza A, Pelz C, Sardiello M, Ballabio A, Characterization of the CLEAR network reveals an integrated control of cellular clearance pathways. Hum Mol Genet 2011 20 3852 3866. doi: 10.1093/hmg/ddr306.
39. Settembre C, Di Malta C, Polito VA, Garcia Arencibia M, Vetrini F, Erdin S, Erdin SU, Huynh T, Medina D, Colella P, Sardiello M, Rubinsztein DC, Ballabio A, TFEB links autophagy to lysosomal biogenesis. Science 2011 332 1429 1433. doi: 10.1126/science.1204592.
40. Emanuel R, Sergin I, Bhattacharya S, Turner JN, Epelman S, Settembre C, Diwan A, Ballabio A, Razani B, Induction of lysosomal biogenesis in atherosclerotic macrophages can rescue lipid-induced lysosomal dysfunction and downstream sequelae. Arterioscler Thromb Vasc Biol 2014 34 1942 1952. doi: 10.1161/ATVBAHA.114.303342.
41. Le Guezennec X, Brichkina A, Huang YF, Kostromina E, Han W, Bulavin DV, Wip1-dependent regulation of autophagy, obesity, and atherosclerosis. Cell Metab 2012 16 68 80. doi: 10.1016/j.cmet.2012.06.003.
42. Moore KJ, Tabas I, Macrophages in the pathogenesis of atherosclerosis. Cell 2011 145 341 355. doi: 10.1016/j.cell.2011.04.005.
43. Distel E, Barrett TJ, Chung K, Girgis NM, Parathath S, Essau CC, Murphy AJ, Moore KJ, Fisher EA, miR33 inhibition overcomes deleterious effects of diabetes mellitus on atherosclerosis plaque regression in mice. Circ Res 2014 115 759 769. doi: 10.1161/CIRCRESAHA.115.304164.
44. Karunakaran D, Thrush AB, Nguyen MA, Macrophage mitochondrial energy status regulates cholesterol efflux and is enhanced by anti-miR33 in atherosclerosis. Circ Res 2015 117 266 278. doi: 10.1161/CIRCRESAHA.117.305624.
45. Seo YK, Jeon TI, Chong HK, Biesinger J, Xie X, Osborne TF, Genome-wide localization of SREBP-2 in hepatic chromatin predicts a role in autophagy. Cell Metab 2011 13 367 375. doi: 10.1016/j.cmet.2011.03.005.