Genetic ablation of MicroRNA-33 attenuates inflammation and abdominal aortic aneurysm formation via several anti-inflammatory pathways

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 37, Issue 11, 2017, Pages 2161-2170

  Nakao, Tetsushi ^a   Horie, Takahiro ^a   Baba, Osamu ^a   Nishiga, Masataka ^a   Nishino, Tomohiro ^a   Izuhara, Masayasu ^a   Kuwabara, Yasuhide ^a   Nishi, Hitoo ^a   Usami, Shunsuke ^a   Nakazeki, Fumiko ^a   Ide, Yuya ^a   Koyama, Satoshi ^a   Kimura, Masahiro ^a   Sowa, Naoya ^a   Ohno, Satoko ^b,c   Aoki, Hiroki ^b,c   Hasegawa, Koji ^a   Sakamoto, Kazuhisa ^a   Minatoya, Kenji ^a   Kimura, Takeshi ^a   Ono, Koh ^a   more..

^a KYOTO UNIVERSITY   (Japan)

^b KURUME UNIVERSITY   (Japan)

^c NATIONAL HOSPITAL ORGANIZATION KYOTO MEDICAL CENTER   (Japan)

Author keywords

Aortic aneurysm, abdominal; Bone marrow cells; Inflammation; Matrix metalloproteinase 9; microRNAs

Indexed keywords

ABC TRANSPORTER A1; ALPHA SMOOTH MUSCLE ACTIN; ANGIOTENSIN II; CALCIUM CHLORIDE; GELATINASE B; HIGH DENSITY LIPOPROTEIN; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MICRORNA; MICRORNA 33; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; APOLIPOPROTEIN E; AUTACOID; CCL2 PROTEIN, MOUSE; MIRN33 MICRORNA, HUMAN; MIRN33 MICRORNA, MOUSE; MMP9 PROTEIN, MOUSE;

ABDOMINAL AORTIC ANEURYSM; ABLATION THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CLINICAL ASSESSMENT; CONTROLLED STUDY; GENE EXPRESSION; GENETIC ABLATION; HUMAN; IN VITRO STUDY; MACROPHAGE; MOUSE; NONHUMAN; OUTCOME ASSESSMENT; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; VASCULAR SMOOTH MUSCLE CELL; VASCULITIS; ABDOMINAL AORTA; ANIMAL; AORTIC ANEURYSM, ABDOMINAL; AORTITIS; BLOOD; C57BL MOUSE; CELL LINE; CHEMICALLY INDUCED; DEFICIENCY; DISEASE MODEL; FEMALE; GENETIC PREDISPOSITION; GENETIC TRANSFECTION; GENETICS; KNOCKOUT MOUSE; LESIONS AND DEFECTS; MALE; METABOLISM; PATHOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; TIME FACTOR; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE;

ANGIOTENSIN II; ANIMALS; AORTA, ABDOMINAL; AORTIC ANEURYSM, ABDOMINAL; AORTITIS; APOLIPOPROTEINS E; BONE MARROW TRANSPLANTATION; CALCIUM CHLORIDE; CELL LINE; CHEMOKINE CCL2; CHOLESTEROL, HDL; DILATATION, PATHOLOGIC; DISEASE MODELS, ANIMAL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFLAMMATION MEDIATORS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MACROPHAGES, PERITONEAL; MALE; MATRIX METALLOPROTEINASE 9; MICE, INBRED C57BL; MICE, KNOCKOUT; MICRORNAS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; VASCULAR REMODELING;

EID: 85032968544     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.117.309768     Document Type: Article

References (37)

1. Sakalihasan N, Limet R, Defawe OD. Abdominal aortic aneurysm. Lancet. 2005;365:1577-1589. doi: 10.1016/S0140-6736(05)66459-8.
2. Powell JT, Greenhalgh RM. Clinical practice. Small abdominal aortic aneurysms. N Engl J Med. 2003;348:1895-1901. doi: 10.1056/NEJMcp012641.
3. Peshkova IO, Schaefer G, Koltsova EK. Atherosclerosis and aortic aneurysm-is inflammation a common denominator FEBS J. 2016;283:1636-1652. doi: 10.1111/febs.13634.
4. Meijer CA, Stijnen T, Wasser MN, Hamming JF, van Bockel JH, Lindeman JH; Pharmaceutical Aneurysm Stabilisation Trial Study Group. Doxycycline for stabilization of abdominal aortic aneurysms: A randomized trial. Ann Intern Med. 2013;159:815-823. doi: 10.7326/0003-4819-159-12-201312170-00007.
5. Ailawadi G, Eliason JL, Upchurch GR Jr. Current concepts in the pathogenesis of abdominal aortic aneurysm. J Vasc Surg. 2003;38:584-588.
6. Gokani VJ, Sidloff D, Bath MF, Bown MJ, Sayers RD, Choke E. A retrospective study: Factors associated with the risk of abdominal aortic aneurysm rupture. Vascul Pharmacol. 2015;65-66:13-16. doi:10.1016/j.vph.2014.11.006.
7. 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.
8. 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.
9. 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.
10. Ouimet M, Ediriweera HN, Gundra UM, et al. MicroRNA-33-dependent regulation of macrophage metabolism directs immune cell polarization in atherosclerosis. J Clin Invest. 2015;125:4334-4348. doi: 10.1172/JCI81676.
11. 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.
12. Raffort J, Lareyre F, Clement M, Mallat Z. Micro-RNAs in abdominal aortic aneurysms: Insights from animal models and relevance to human disease. Cardiovasc Res. 2016;110:165-177. doi: 10.1093/cvr/cvw046.
13. Golledge J, van Bockxmeer F, Jamrozik K, McCann M, Norman PE. Association between serum lipoproteins and abdominal aortic aneurysm. Am J Cardiol. 2010;105:1480-1484. doi: 10.1016/j.amjcard.2009.12.076.
14. Mourmoura E, Vasilaki A, Giannoukas A, Michalodimitrakis E, Pavlidis P, Tsezou A. Evidence of deregulated cholesterol efflux in abdominal aortic aneurysm. Acta Histochem. 2016;118:97-108. doi: 10.1016/j.acthis.2015.11.012.
15. Zhao L, Jin H, Yang B, Zhang S, Han S, Yin F, Feng Y. Correlation between ABCA1 gene polymorphism and aopA-I and HDL-C in abdominal aortic aneurysm. Med Sci Monit. 2016;22:172-176. doi:10.12659/MSM.895298.
16. Wanhainen A, Mani K, Vorkapic E, De Basso R, Björck M, Länne T, Wågsäter D. Screening of circulating microRNA biomarkers for prevalence of abdominal aortic aneurysm and aneurysm growth. Atherosclerosis. 2017;256:82-88. doi: 10.1016/j.atherosclerosis.2016.11.007.
17. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000;105:1605-1612. doi: 10.1172/JCI7818.
18. Manning MW, Cassi LA, Huang J, Szilvassy SJ, Daugherty A. Abdominal aortic aneurysms: Fresh insights from a novel animal model of the disease. Vasc Med. 2002;7:45-54. doi: 10.1191/1358863x02vm413ra.
19. Daugherty A, Manning MW, Cassis LA. Antagonism of AT2 receptors augments angiotensin II-induced abdominal aortic aneurysms and atherosclerosis. Br J Pharmacol. 2001;134:865-870. doi: 10.1038/sj.bjp.0704331.
20. Cao RY, Amand T, Ford MD, Piomelli U, Funk CD. The murine angiotensin II-induced abdominal aortic aneurysm model: Rupture risk and inflammatory progression patterns. Front Pharmacol. 2010;1:9. doi: 10.3389/fphar.2010.00009.
21. Longo GM, Xiong W, Greiner TC, Zhao Y, Fiotti N, Baxter BT. Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest. 2002;110:625-632. doi: 10.1172/JCI15334.
22. Wang Y, Krishna S, Golledge J. The calcium chloride-induced rodent model of abdominal aortic aneurysm. Atherosclerosis. 2013;226:29-39. doi: 10.1016/j.atherosclerosis.2012.09.010.
23. Sprague AH, Khalil RA. Inflammatory cytokines in vascular dysfunction and vascular disease. Biochem Pharmacol. 2009;78:539-552. doi: 10.1016/j.bcp.2009.04.029.
24. Yoshimura K, Aoki H, Ikeda Y, Fujii K, Akiyama N, Furutani A, Hoshii Y, Tanaka N, Ricci R, Ishihara T, Esato K, Hamano K, Matsuzaki M. Regression of abdominal aortic aneurysm by inhibition of c-Jun N-terminal kinase. Nat Med. 2005;11:1330-1338. doi: 10.1038/nm1335.
25. Yvan-Charvet L, Pagler TA, Seimon TA, Thorp E, Welch CL, Witztum JL, Tabas I, Tall AR. ABCA1 and ABCG1 protect against oxidative stress-induced macrophage apoptosis during efferocytosis. Circ Res. 2010;106:1861-1869. doi: 10.1161/CIRCRESAHA.110.217281.
26. Goebeler M, Kilian K, Gillitzer R, Kunz M, Yoshimura T, Bröcker EB, Rapp UR, Ludwig S. The MKK6/p38 stress kinase cascade is critical for tumor necrosis factor-alpha-induced expression of monocyte-chemoattractant protein-1 in endothelial cells. Blood. 1999;93:857-865.
27. Domoto K, Taniguchi T, Takaishi H, Takahashi T, Fujioka Y, Takahashi A, Ishikawa Y, Yokoyama M. Chylomicron remnants induce monocyte chemoattractant protein-1 expression via p38 MAPK activation in vascular smooth muscle cells. Atherosclerosis. 2003;171:193-200.
28. Barter PJ, Nicholls S, Rye KA, Anantharamaiah GM, Navab M, Fogelman AM. Antiinflammatory properties of HDL. Circ Res. 2004;95:764-772. doi: 10.1161/01.RES.0000146094.59640.13.
29. Ardans JA, Economou AP, Martinson JM Jr, Zhou M, Wahl LM. Oxidized low-density and high-density lipoproteins regulate the production of matrix metalloproteinase-1 and-9 by activated monocytes. J Leukoc Biol. 2002;71:1012-1018.
30. Tölle M, Pawlak A, Schuchardt M, Kawamura A, Tietge UJ, Lorkowski S, Keul P, Assmann G, Chun J, Levkau B, van der Giet M, Nofer JR. HDLassociated lysosphingolipids inhibit NAD(P)H oxidase-dependent monocyte chemoattractant protein-1 production. Arterioscler Thromb Vasc Biol. 2008;28:1542-1548. doi: 10.1161/ATVBAHA.107.161042.
31. Aiello RJ, Brees D, Bourassa PA, Royer L, Lindsey S, Coskran T, Haghpassand M, Francone OL. Increased atherosclerosis in hyperlipidemic mice with inactivation of ABCA1 in macrophages. Arterioscler Thromb Vasc Biol. 2002;22:630-637.
32. Tang C, Liu Y, Kessler PS, Vaughan AM, Oram JF. The macrophage cholesterol exporter ABCA1 functions as an anti-inflammatory receptor. J Biol Chem. 2009;284:32336-32343. doi: 10.1074/jbc.M109.047472.
33. Steinmetz EF, Buckley C, Shames ML, Ennis TL, Vanvickle-Chavez SJ, Mao D, Goeddel LA, Hawkins CJ, Thompson RW. Treatment with simvastatin suppresses the development of experimental abdominal aortic aneurysms in normal and hypercholesterolemic mice. Ann Surg. 2005;241:92-101.
34. Shiraya S, Miyake T, Aoki M, Yoshikazu F, Ohgi S, Nishimura M, Ogihara T, Morishita R. Inhibition of development of experimental aortic abdominal aneurysm in rat model by atorvastatin through inhibition of macrophage migration. Atherosclerosis. 2009;202:34-40. doi: 10.1016/j.atherosclerosis.2008.03.020.
35. Obad S, dos Santos CO, Petri A, Heidenblad M, Broom O, Ruse C, Fu C, Lindow M, Stenvang J, Straarup EM, Hansen HF, Koch T, Pappin D, Hannon GJ, Kauppinen S. Silencing of microRNA families by seed-targeting tiny LNAs. Nat Genet. 2011;43:371-378. doi: 10.1038/ng.786.
36. van Rooij E, Kauppinen S. Development of microRNA therapeutics is coming of age. EMBO Mol Med. 2014;6:851-864. doi: 10.15252/emmm.201100899.
37. Niesor EJ, Schwartz GG, Perez A, Stauffer A, Durrwell A, Bucklar-Suchankova G, Benghozi R, Abt M, Kallend D. Statin-induced decrease in ATP-binding cassette transporter A1 expression via microRNA33 induction may counteract cholesterol efflux to high-density lipoprotein. Cardiovasc Drugs Ther. 2015;29:7-14. doi:10.1007/s10557-015-6570-0.