Chronic miR-29 antagonism promotes favorable plaque remodeling in atherosclerotic mice

EMBO Molecular Medicine

Volumn 8, Issue 6, 2016, Pages 643-653

  Ulrich, Victoria ^a   Rotllan, Noemi ^a   Araldi, Elisa ^a   Luciano, Amelia ^a   Skroblin, Philipp ^c   Abonnenc, Mélanie ^c   Perrotta, Paola ^a   Yin, Xiaoke ^c   Bauer, Ashley ^a   Leslie, Kristen L ^a   Zhang, Pei ^a   Aryal, Binod ^a   Montgomery, Rusty L ^b   Thum, Thomas ^d,e   Martin, Kathleen ^a   Suarez, Yajaira ^a   Mayr, Manuel ^c   Fernandez Hernando, Carlos ^a   Sessa, William C ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MiRagen Therapeutics   (United States)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Atherosclerosis; LNA; miR 29; Plaque; Stability

Indexed keywords

MICRORNA 29; COL3A1 PROTEIN, MOUSE; COLLAGEN TYPE 1; COLLAGEN TYPE 3; COLLAGEN TYPE I, ALPHA 1 CHAIN; MICRORNA; MIRN29 MICRORNA, MOUSE;

ANALYSIS OF VARIANCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BIOACCUMULATION; CENTRIFUGATION; CONTROLLED STUDY; DENSITOMETRY; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC CONSERVATION; GENETIC TRANSFECTION; HOMEOSTASIS; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; MALE; MORPHOLOGY; MORPHOMETRICS; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; TISSUE DISTRIBUTION; TRANSCRIPTION REGULATION; VASCULAR REMODELING; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; METABOLISM; PATHOLOGY;

ANIMALS; ATHEROSCLEROSIS; COLLAGEN TYPE I; COLLAGEN TYPE III; DISEASE MODELS, ANIMAL; MICE; MICRORNAS;

EID: 84964715579     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.15252/emmm.201506031     Document Type: Article

References (46)

1. Abela GS, Aziz K (2005) Cholesterol crystals cause mechanical damage to biological membranes: a proposed mechanism of plaque rupture and erosion leading to arterial thrombosis. Clin Cardiol 28: 413-420
2. Abonnenc M, Nabeebaccus AA, Mayr U, Barallobre-Barreiro J, Dong X, Cuello F, Sur S, Drozdov I, Langley SR, Lu R et al (2013) Extracellular matrix secretion by cardiac fibroblasts: role of microRNA-29b and microRNA-30c. Circ Res 113: 1138-1147
3. Aikawa M, Rabkin E, Okada Y, Voglic SJ, Clinton SK, Brinckerhoff CE, Sukhova GK, Libby P (1998) Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: a potential mechanism of lesion stabilization. Circulation 97: 2433-2444
4. Ambros V (2004) The functions of animal microRNAs. Nature 431: 350-355
5. Arroyo LH, Lee RT (1999) Mechanisms of plaque rupture: mechanical and biologic interactions. Cardiovasc Res 41: 369-375
6. Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136: 215-233
7. Boon RA, Seeger T, Heydt S, Fischer A, Hergenreider E, Horrevoets AJ, Vinciguerra M, Rosenthal N, Sciacca S, Pilato M et al (2011) MicroRNA-29 in aortic dilation: implications for aneurysm formation. Circ Res 109: 1115-1119
8. Chamley-Campbell J, Campbell GR, Ross R (1979) The smooth muscle cell in culture. Physiol Rev 59: 1-61
9. Chen KC, Wang YS, Hu CY, Chang WC, Liao YC, Dai CY, Juo SH (2011) OxLDL up-regulates microRNA-29b, leading to epigenetic modifications of MMP-2/MMP-9 genes: a novel mechanism for cardiovascular diseases. FASEB J 25: 1718-1728
10. Choi H, Fermin D, Nesvizhskii AI (2008) Significance analysis of spectral count data in label-free shotgun proteomics. Mol Cell Proteomics 7: 2373-2385
11. Davies MJ, Richardson PD, Woolf N, Katz DR, Mann J (1993) Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content. Br Heart J 69: 377-381
12. Ekman M, Bhattachariya A, Dahan D, Uvelius B, Albinsson S, Sward K (2013) Mir-29 repression in bladder outlet obstruction contributes to matrix remodeling and altered stiffness. PLoS ONE 8: e82308
13. Elmen J, Lindow M, Silahtaroglu A, Bak M, Christensen M, Lind-Thomsen A, Hedtjarn M, Hansen JB, Hansen HF, Straarup EM et al (2008) Antagonism of microRNA-122 in mice by systemically administered LNA-antimiR leads to up-regulation of a large set of predicted target mRNAs in the liver. Nucleic Acids Res 36: 1153-1162
14. Fernandez-Hernando C, Jozsef L, Jenkins D, Di Lorenzo A, Sessa WC (2009) Absence of Akt1 reduces vascular smooth muscle cell migration and survival and induces features of plaque vulnerability and cardiac dysfunction during atherosclerosis. Arterioscler Thromb Vasc Biol 29: 2033-2040
15. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat Rev Genet 9: 102-114
16. Galis ZS, Sukhova GK, Lark MW, Libby P (1994) Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Investig 94: 2493-2503
17. Gimbrone MA, Jr, Cybulsky MI, Kume N, Collins T, Resnick N (1995) Vascular endothelium. An integrator of pathophysiological stimuli in atherogenesis. Ann N Y Acad Sci 748: 122-131; discussion 131-122
18. Han W, Han Y, Liu X, Shang X (2015) Effect of miR-29a Inhibition on Ventricular Hypertrophy Induced by Pressure Overload. Cell Biochem Biophys 71: 821-826
19. Heidenreich PA, Trogdon JG, Khavjou OA, Butler J, Dracup K, Ezekowitz MD, Finkelstein EA, Hong Y, Johnston SC, Khera A et al (2011) Forecasting the future of cardiovascular disease in the United States: a policy statement from the American Heart Association. Circulation 123: 933-944
20. Heinrich J, Schulte H, Schonfeld R, Kohler E, Assmann G (1995) Association of variables of coagulation, fibrinolysis and acute-phase with atherosclerosis in coronary and peripheral arteries and those arteries supplying the brain. Thromb Haemost 73: 374-379
21. Hullinger TG, Montgomery RL, Seto AG, Dickinson BA, Semus HM, Lynch JM, Dalby CM, Robinson K, Stack C, Latimer PA et al (2012) Inhibition of miR-15 protects against cardiac ischemic injury. Circ Res 110: 71-81
22. ISTH Steering Committee for World Thrombosis Day (2014) Thrombosis: a major contributor to the global disease burden. J Thromb Haemost 12: 1580-1590
23. James EN, Delany AM, Nair LS (2014) Post-transcriptional regulation in osteoblasts using localized delivery of miR-29a inhibitor from nanofibers to enhance extracellular matrix deposition. Acta Biomater 10: 3571-3580
24. Kolodgie FD, Burke AP, Farb A, Gold HK, Yuan J, Narula J, Finn AV, Virmani R (2001) The thin-cap fibroatheroma: a type of vulnerable plaque: the major precursor lesion to acute coronary syndromes. Curr Opin Cardiol 16: 285-292
25. Li Z, Hassan MQ, Jafferji M, Aqeilan RI, Garzon R, Croce CM, van Wijnen AJ, Stein JL, Stein GS, Lian JB (2009) Biological functions of miR-29b contribute to positive regulation of osteoblast differentiation. J Biol Chem 284: 15676-15684
26. Liu Y, Taylor NE, Lu L, Usa K, Cowley AW Jr, Ferreri NR, Yeo NC, Liang M (2010) Renal medullary microRNAs in Dahl salt-sensitive rats: miR-29b regulates several collagens and related genes. Hypertension 55: 974-982
27. Maegdefessel L, Azuma J, Toh R, Merk DR, Deng A, Chin JT, Raaz U, Schoelmerich AM, Raiesdana A, Leeper NJ et al (2012) Inhibition of microRNA-29b reduces murine abdominal aortic aneurysm development. J Clin Investig 122: 497-506
28. Maurer B, Stanczyk J, Jungel A, Akhmetshina A, Trenkmann M, Brock M, Kowal-Bielecka O, Gay RE, Michel BA, Distler JH et al (2010) MicroRNA-29, a key regulator of collagen expression in systemic sclerosis. Arthritis Rheum 62: 1733-1743
29. Melo SF, Fernandes T, Barauna VG, Matos KC, Santos AA, Tucci PJ, Oliveira EM (2014) Expression of MicroRNA-29 and Collagen in Cardiac Muscle after Swimming Training in Myocardial-Infarcted Rats. Cell Physiol Biochem 33: 657-669
30. Merk DR, Chin JT, Dake BA, Maegdefessel L, Miller MO, Kimura N, Tsao PS, Iosef C, Berry GJ, Mohr FW et al (2012) miR-29b participates in early aneurysm development in Marfan syndrome. Circ Res 110: 312-324
31. Montgomery RL, Yu G, Latimer PA, Stack C, Robinson K, Dalby CM, Kaminski N, van Rooij E (2014) MicroRNA mimicry blocks pulmonary fibrosis. EMBO Mol Med 6: 1347-1356
32. Moran AE, Tzong KY, Forouzanfar MH, Rothy GA, Mensah GA, Ezzati M, Murray CJ, Naghavi M (2014) Variations in ischemic heart disease burden by age, country, and income: the Global Burden of Diseases, Injuries, and Risk Factors 2010 study. Global Heart 9: 91-99
33. Nikkari ST, O'Brien KD, Ferguson M, Hatsukami T, Welgus HG, Alpers CE, Clowes AW (1995) Interstitial collagenase (MMP-1) expression in human carotid atherosclerosis. Circulation 92: 1393-1398
34. van Rooij E, Sutherland LB, Thatcher JE, DiMaio JM, Naseem RH, Marshall WS, Hill JA, Olson EN (2008) Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci USA 105: 13027-13032
35. Schwenke DC, Carew TE (1989) Initiation of atherosclerotic lesions in cholesterol-fed rabbits. I. Focal increases in arterial LDL concentration precede development of fatty streak lesions. Arteriosclerosis 9: 895-907
36. Sengupta S, den Boon JA, Chen IH, Newton MA, Stanhope SA, Cheng YJ, Chen CJ, Hildesheim A, Sugden B, Ahlquist P (2008) MicroRNA 29c is down-regulated in nasopharyngeal carcinomas, up-regulating mRNAs encoding extracellular matrix proteins. Proc Natl Acad Sci USA 105: 5874-5878
37. Shekhonin BV, Domogatsky SP, Idelson GL, Koteliansky VE, Rukosuev VS (1987) Relative distribution of fibronectin and type I, III, IV, V collagens in normal and atherosclerotic intima of human arteries. Atherosclerosis 67: 9-16
38. Small DM, Bond MG, Waugh D, Prack M, Sawyer JK (1984) Physicochemical and histological changes in the arterial wall of nonhuman primates during progression and regression of atherosclerosis. J Clin Investig 73: 1590-1605
39. Sukhova GK, Schonbeck U, Rabkin E, Schoen FJ, Poole AR, Billinghurst RC, Libby P (1999) Evidence for increased collagenolysis by interstitial collagenases-1 and -3 in vulnerable human atheromatous plaques. Circulation 99: 2503-2509
40. Takahashi M, Eda A, Fukushima T, Hohjoh H (2012) Reduction of type IV collagen by upregulated miR-29 in normal elderly mouse and klotho-deficient, senescence-model mouse. PLoS ONE 7: e48974
41. Tracy RE (1984) The kind of plaque that underlies a coronary thrombus. Am J Forensic Med Pathol 5: 15-18
42. Yang Z, Wu L, Zhu X, Xu J, Jin R, Li G, Wu F (2013) MiR-29a modulates the angiogenic properties of human endothelial cells. Biochem Biophys Res Commun 434: 143-149
43. Zhang P, Huang A, Ferruzzi J, Mecham RP, Starcher BC, Tellides G, Humphrey JD, Giordano FJ, Niklason LE, Sessa WC (2012a) Inhibition of microRNA-29 enhances elastin levels in cells haploinsufficient for elastin and in bioengineered vessels-brief report. Arterioscler Thromb Vasc Biol 32: 756-759
44. Zhang P, Huang A, Morales-Ruiz M, Starcher BC, Huang Y, Sessa WC, Niklason LE, Giordano FJ (2012b) Engineered zinc-finger proteins can compensate genetic haploinsufficiency by transcriptional activation of the wild-type allele: application to Willams-Beuren syndrome and supravalvular aortic stenosis. Hum Gene Ther 23: 1186-1199
45. Zhang XY, Shen BR, Zhang YC, Wan XJ, Yao QP, Wu GL, Wang JY, Chen SG, Yan ZQ, Jiang ZL (2013) Induction of thoracic aortic remodeling by endothelial-specific deletion of microRNA-21 in mice. PLoS ONE 8: e59002
46. Zhou J, Chew M, Ravn HB, Falk E (1999) Plaque pathology and coronary thrombosis in the pathogenesis of acute coronary syndromes. Scand J Clin Lab Invest Suppl 230: 3-11