Macrophage Mitochondrial Energy Status Regulates Cholesterol Efflux and Is Enhanced by Anti-miR33 in Atherosclerosis

Circulation Research

Volumn 117, Issue 3, 2015, Pages 266-278

  Karunakaran, Denuja ^a   Thrush, A Brianne ^b   Nguyen, My Anh ^a,b   Richards, Laura ^a   Geoffrion, Michele ^a   Singaravelu, Ragunath ^b,c   Ramphos, Eleni ^a   Shangari, Prakriti ^a   Ouimet, Mireille ^d   Pezacki, John P ^b,c   Moore, Kathryn J ^d   Perisic, Ljubica ^e   Maegdefessel, Lars ^e   Hedin, Ulf ^e   Harper, Mary Ellen ^b   Rayner, Katey J ^a,b  

^a UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

atherosclerosis; cholesterol; macrophages; microRNA 33, mouse; mitochondria

Indexed keywords

ABC TRANSPORTER A1; ADENOSINE TRIPHOSPHATE; ANTISENSE OLIGONUCLEOTIDE; APOLIPOPROTEIN E; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MICRORNA; MICRORNA 33A; MICRORNA 33B; MITOCHONDRIAL TRANSCRIPTION FACTOR A; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN; PROTEIN SLC25A25; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PYRUVATE DEHYDROGENASE KINASE 4; TRANSCRIPTION FACTOR NRF1; UNCLASSIFIED DRUG; AMINO ACID TRANSPORTER; CALCIUM BINDING PROTEIN; CHOLESTEROL; MIRN33 MICRORNA, MOUSE; PROTEIN SERINE THREONINE KINASE; SLC25A25 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTISENSE THERAPY; AORTA DISEASE; AORTIC SINUS LESION; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CAROTID ATHEROSCLEROSIS; CELL ENERGY; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME INHIBITION; GENE CONTROL; HEART PROTECTION; HUMAN; HUMAN CELL; MACROPHAGE; MITOCHONDRIAL GENE; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE THERAPY; GENETICS; HEK293 CELL LINE; METABOLISM; MITOCHONDRION; NUCLEOTIDE SEQUENCE; PERITONEUM MACROPHAGE; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY;

ADENOSINE TRIPHOSPHATE; AMINO ACID TRANSPORT SYSTEMS, ACIDIC; ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BASE SEQUENCE; CALCIUM-BINDING PROTEINS; CELL LINE; CHOLESTEROL; GENE EXPRESSION REGULATION; GENETIC THERAPY; HEK293 CELLS; HUMANS; MACROPHAGES; MACROPHAGES, PERITONEAL; MICE; MICE, INBRED C57BL; MICRORNAS; MITOCHONDRIA; OLIGONUCLEOTIDES, ANTISENSE; PROTEIN-SERINE-THREONINE KINASES; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANSCRIPTION FACTORS;

EID: 84937554657     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.117.305624     Document Type: Article

References (40)

1. Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell. 2011;145:341-355. doi: 10.1016/j.cell.2011.04.005.
2. Rader DJ, Tall AR. The not-so-simple HDL story: Is it time to revise the HDL cholesterol hypothesis? Nat Med. 2012;18:1344-1346. doi: 10.1038/nm.2937.
3. Rosenson RS, Brewer HB Jr, Davidson WS, Fayad ZA, Fuster V, Goldstein J, Hellerstein M, Jiang XC, Phillips MC, Rader DJ, Remaley AT, Rothblat GH, Tall AR, Yvan-Charvet L. Cholesterol efflux and atheroprotection: advancing the concept of reverse cholesterol transport. Circulation. 2012;125:1905-1919. doi: 10.1161/CIRCULATIONAHA.111.066589.
4. Rohatgi A, Khera A, Berry JD, Givens EG, Ayers CR, Wedin KE, Neeland IJ, Yuhanna IS, Rader DR, de Lemos JA, Shaul PW. HDL cholesterol efflux capacity and incident cardiovascular events. N Engl J Med. 2014;371:2383-2393. doi: 10.1056/NEJMoa1409065.
5. Allen AM, Taylor JM, Graham A. Mitochondrial (dys)function and regulation of macrophage cholesterol efflux. Clin Sci (Lond). 2013;124:509-515. doi: 10.1042/CS20120358.
6. Nunnari J, Suomalainen A. Mitochondria: in sickness and in health. Cell. 2012;148:1145-1159. doi: 10.1016/j.cell.2012.02.035.
7. Allen AM, Graham A. Mitochondrial function is involved in regulation of cholesterol efflux to apolipoprotein (apo)A-I from murine RAW 264.7 macrophages. Lipids Health Dis. 2012;11:169. doi: 10.1186/1476-511X-11-169.
8. Vats D, Mukundan L, Odegaard JI, Zhang L, Smith KL, Morel CR, Wagner RA, Greaves DR, Murray PJ, Chawla A. Oxidative metabolism and PGC-1beta attenuate macrophage-mediated inflammation. Cell Metab. 2006;4:13-24. doi: 10.1016/j.cmet.2006.05.011.
9. van Rooij E, Olson EN. MicroRNA therapeutics for cardiovascular disease: opportunities and obstacles. Nat Rev Drug Discov. 2012;11:860-872. doi: 10.1038/nrd3864.
10. Thum T. MicroRNA therapeutics in cardiovascular medicine. EMBO Mol Med. 2012;4:3-14. doi: 10.1002/emmm.201100191.
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. Nguyen MA, Karunakaran D, Rayner KJ. Unlocking the door to new therapies in cardiovascular disease: microRNAs hold the key. Curr Cardiol Rep. 2014;16:539. doi: 10.1007/s11886-014-0539-7.
13. 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.
14. 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.
15. Horie T, Baba O, Kuwabara Y, et al. 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.
16. 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.
17. 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.
18. Dávalos A, Goedeke L, Smibert P, et al. miR-33a/b contribute to the regulation of fatty acid metabolism and insulin signaling. Proc Natl Acad Sci U S A. 2011;108:9232-9237. doi: 10.1073/pnas.1102281108.
19. Wang N, Silver DL, Thiele C, Tall AR. ATP-binding cassette transporter A1 (ABCA1) functions as a cholesterol efflux regulatory protein. J Biol Chem. 2001;276:23742-23747. doi: 10.1074/jbc.M102348200.
20. Anunciado-Koza RP, Zhang J, Ukropec J, Bajpeyi S, Koza RA, Rogers RC, Cefalu WT, Mynatt RL, Kozak LP. Inactivation of the mitochondrial carrier SLC25A25 (ATP-Mg2+/Pi transporter) reduces physical endurance and metabolic efficiency in mice. J Biol Chem. 2011;286:11659-11671. doi: 10.1074/jbc.M110.203000.
21. Finck BN, Kelly DP. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J Clin Invest. 2006;116:615-622. doi: 10.1172/JCI27794.
22. Majer M, Popov KM, Harris RA, Bogardus C, Prochazka M. Insulin downregulates pyruvate dehydrogenase kinase (PDK) mRNA: potential mechanism contributing to increased lipid oxidation in insulin-resistant subjects. Mol Genet Metab. 1998;65:181-186. doi: 10.1006/mgme.1998.2748.
23. Ramírez CM, Goedeke L, Rotllan N, Yoon JH, Cirera-Salinas D, Mattison JA, Suárez Y, de Cabo R, Gorospe M, Fernández-Hernando C. MicroRNA 33 regulates glucose metabolism. Mol Cell Biol. 2013;33:2891-2902. doi: 10.1128/MCB.00016-13.
24. -/- mice-brief report. Arterioscler Thromb Vasc Biol. 2013;33:1973-1977. doi: 10.1161/ATVBAHA.113.301732.
25. Rayner KJ, Esau CC, Hussain FN, et al. Inhibition of miR-33a/b in nonhuman primates raises plasma HDL and lowers VLDL triglycerides. Nature. 2011;478:404-407. doi: 10.1038/nature10486.
26. Li AC, Binder CJ, Gutierrez A, Brown KK, Plotkin CR, Pattison JW, Valledor AF, Davis RA, Willson TM, Witztum JL, Palinski W, Glass CK. Differential inhibition of macrophage foam-cell formation and atherosclerosis in mice by PPARalpha, beta/delta, and gamma. J Clin Invest. 2004;114:1564-1576. doi: 10.1172/JCI18730.
27. 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.
28. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98:115-124. doi: 10.1016/S0092-8674(00)80611-X.
29. Higgins CF. ABC transporters: physiology, structure and mechanism-an overview. Res Microbiol. 2001;152:205-210.
30. Lee JY, Karwatsky J, Ma L, Zha X. ABCA1 increases extracellular ATP to mediate cholesterol efflux to ApoA-I. Am J Physiol Cell Physiol. 2011;301:C886-C894. doi: 10.1152/ajpcell.00042.2011.
31. Fernández-Hernando C, Suárez Y, Rayner KJ, Moore KJ. MicroRNAs in lipid metabolism. Curr Opin Lipidol. 2011;22:86-92. doi: 10.1097/MOL.0b013e3283428d9d.
32. Yu E, Calvert PA, Mercer JR, et al. Mitochondrial DNA damage can promote atherosclerosis independently of reactive oxygen species through effects on smooth muscle cells and monocytes and correlates with higherrisk plaques in humans. Circulation. 2013;128:702-712. doi: 10.1161/CIRCULATIONAHA.113.002271.
33. Handschin C, Spiegelman BM. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev. 2006;27:728-735. doi: 10.1210/er.2006-0037.
34. Handschin C, Spiegelman BM. The role of exercise and PGC1alpha in inflammation and chronic disease. Nature. 2008;454:463-469. doi: 10.1038/nature07206.
35. Kleiner S, Mepani RJ, Laznik D, Ye L, Jurczak MJ, Jornayvaz FR, Estall JL, Chatterjee Bhowmick D, Shulman GI, Spiegelman BM. Development of insulin resistance in mice lacking PGC-1α in adipose tissues. Proc Natl Acad Sci U S A. 2012;109:9635-9640. doi: 10.1073/pnas.1207287109.
36. Ling C, Del Guerra S, Lupi R, Rönn T, Granhall C, Luthman H, Masiello P, Marchetti P, Groop L, Del Prato S. Epigenetic regulation of PPARGC1A in human type 2 diabetic islets and effect on insulin secretion. Diabetologia. 2008;51:615-622. doi: 10.1007/s00125-007-0916-5.
37. McCarthy C, Lieggi NT, Barry D, Mooney D, de Gaetano M, James WG, McClelland S, Barry MC, Escoubet-Lozach L, Li AC, Glass CK, Fitzgerald DJ, Belton O. Macrophage PPAR gamma Co-activator-1 alpha participates in repressing foam cell formation and atherosclerosis in response to conjugated linoleic acid. EMBO Mol Med. 2013;5:1443-1457. doi: 10.1002/emmm.201302587.
38. Marquart TJ, Allen RM, Ory DS, Baldán A. miR-33 links SREBP-2 induction to repression of sterol transporters. Proc Natl Acad Sci U S A. 2010;107:12228-12232. doi: 10.1073/pnas.1005191107.
39. Goedeke L, Salerno A, Ramírez CM, Guo L, Allen RM, Yin X, Langley SR, Esau C, Wanschel A, Fisher EA, Suárez Y, Baldán A, Mayr M, Fernández-Hernando C. Long-term therapeutic silencing of miR-33 increases circulating triglyceride levels and hepatic lipid accumulation in mice. EMBO Mol Med. 2014;6:1133-1141. doi: 10.15252/emmm.201404046.
40. Horie T, Nishino T, Baba O, et al. MicroRNA-33b knock-in mice for an intron of sterol regulatory element-binding factor 1 (Srebf1) exhibit reduced HDL-C in vivo. Sci Rep. 2014;4:5312. doi: 10.1038/srep05312.