Vascular Smooth Muscle Cells in Atherosclerosis

Circulation Research

Volumn 118, Issue 4, 2016, Pages 692-702

  Bennett, Martin R ^a   Sinha, Sanjay ^a   Owens, Gary K ^b  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

atherosclerosis; extracellular matrix; interleukin; platelet derived growth factor; smooth muscle

Indexed keywords

ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL WALL; BONE MARROW; CELL AGING; CELL CLONING; CELL DEATH; CELL FUNCTION; CELL MIGRATION; CELL PLASTICITY; CELL POPULATION; CELL PROLIFERATION; CELL STRUCTURE; DISEASE PREDISPOSITION; EMBRYO; HUMAN; NONHUMAN; PRIORITY JOURNAL; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; APOPTOSIS; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOTION; METABOLISM; PATHOLOGY; PHENOTYPE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE;

ANIMALS; APOPTOSIS; ATHEROSCLEROSIS; CELL AGING; CELL DIFFERENTIATION; CELL LINEAGE; CELL MOVEMENT; CELL PROLIFERATION; HUMANS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; PLAQUE, ATHEROSCLEROTIC; SIGNAL TRANSDUCTION;

EID: 84959048825     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.306361     Document Type: Article

References (92)

1. Libby P, Ridker PM, Hansson GK., Progress and challenges in translating the biology of atherosclerosis. Nature 2011 473 317 325. doi: 10.1038/nature10146.
2. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM., Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol 2000 20 1262 1275
3. Tabas I, García-Cardeña G, Owens GK., Recent insights into the cellular biology of atherosclerosis. J Cell Biol 2015 209 13 22. doi: 10.1083/jcb.201412052.
4. Majesky MW., Developmental basis of vascular smooth muscle diversity. Arterioscler Thromb Vasc Biol 2007 27 1248 1258. doi: 10.1161/ATVBAHA.107.141069.
5. Oh J, Richardson JA, Olson EN., Requirement of myocardin-related transcription factor-B for remodeling of branchial arch arteries and smooth muscle differentiation. Proc Natl Acad Sci USA 2005 102 15122 15127. doi: 10.1073/pnas.0507346102.
6. Li J, Zhu X, Chen M, Cheng L, Zhou D, Lu MM, Du K, Epstein JA, Parmacek MS., Myocardin-related transcription factor B is required in cardiac neural crest for smooth muscle differentiation and cardiovascular development. Proc Natl Acad Sci USA 2005 102 8916 8921. doi: 10.1073/pnas.0503741102.
7. Topouzis S, Majesky MW., Smooth muscle lineage diversity in the chick embryo. Two types of aortic smooth muscle cell differ in growth and receptor-mediated transcriptional responses to transforming growth factor-beta. Dev Biol 1996 178 430 445. doi: 10.1006/dbio.1996.0229.
8. Xie WB, Li Z, Shi N, Guo X, Tang J, Ju W, Han J, Liu T, Bottinger EP, Chai Y, Jose PA, Chen SY., Smad2 and myocardin-related transcription factor B cooperatively regulate vascular smooth muscle differentiation from neural crest cells. Circ Res 2013 113 e76 e86. doi: 10.1161/CIRCRESAHA.113.301921.
9. DeBakey ME, Glaeser DH., Patterns of atherosclerosis: effect of risk factors on recurrence and survival-analysis of 11,890 cases with more than 25-year follow-up. Am J Cardiol 2000 85 1045 1053
10. McGill HC Jr, McMahan CA, Herderick EE, Tracy RE, Malcom GT, Zieske AW, Strong JP., Effects of coronary heart disease risk factors on atherosclerosis of selected regions of the aorta and right coronary artery. PDAY Research Group. Pathobiological Determinants of Atherosclerosis in Youth. Arterioscler Thromb Vasc Biol 2000 20 836 845
11. Cheung C, Bernardo AS, Trotter MW, Pedersen RA, Sinha S., Generation of human vascular smooth muscle subtypes provides insight into embryological origin-dependent disease susceptibility. Nat Biotechnol 2012 30 165 173. doi: 10.1038/nbt.2107.
12. Trigueros-Motos L, González-Granado JM, Cheung C, Fernández P, Sánchez-Cabo F, Dopazo A, Sinha S, Andrés V., Embryological-origin-dependent differences in homeobox expression in adult aorta: role in regional phenotypic variability and regulation of NF-κB activity. Arterioscler Thromb Vasc Biol 2013 33 1248 1256. doi: 10.1161/ATVBAHA.112.300539.
13. Alexander MR, Owens GK., Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu Rev Physiol 2012 74 13 40. doi: 10.1146/annurev-physiol-012110-142315.
14. Owens GK, Kumar MS, Wamhoff BR., Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev 2004 84 767 801. doi: 10.1152/physrev.00041.2003.
15. Ackers-Johnson M, Talasila A, Sage AP, Long X, Bot I, Morrell NW, Bennett MR, Miano JM, Sinha S., Myocardin regulates vascular smooth muscle cell inflammatory activation and disease. Arterioscler Thromb Vasc Biol 2015 35 817 828. doi: 10.1161/ATVBAHA.114.305218.
16. Yoshida T, Gan Q, Shang Y, Owens GK., Platelet-derived growth factor-BB represses smooth muscle cell marker genes via changes in binding of MKL factors and histone deacetylases to their promoters. Am J Physiol Cell Physiol 2007 292 C886 C895. doi: 10.1152/ajpcell.00449.2006.
17. Deaton RA, Gan Q, Owens GK., Sp1-dependent activation of KLF4 is required for PDGF-BB-induced phenotypic modulation of smooth muscle. Am J Physiol Heart Circ Physiol 2009 296 H1027 H1037. doi: 10.1152/ajpheart.01230.2008.
18. Pidkovka NA, Cherepanova OA, Yoshida T, Alexander MR, Deaton RA, Thomas JA, Leitinger N, Owens GK., Oxidized phospholipids induce phenotypic switching of vascular smooth muscle cells in vivo and in vitro. Circ Res 2007 101 792 801. doi: 10.1161/CIRCRESAHA.107.152736.
19. Yoshida T, Gan Q, Owens GK., Kruppel-like factor 4, Elk-1, and histone deacetylases cooperatively suppress smooth muscle cell differentiation markers in response to oxidized phospholipids. Am J Physiol Cell Physiol 2008 295 C1175 C1182. doi: 10.1152/ajpcell.00288.2008.
20. Alexander MR, Murgai M, Moehle CW, Owens GK., Interleukin-1β modulates smooth muscle cell phenotype to a distinct inflammatory state relative to PDGF-DD via NF-κB-dependent mechanisms. Physiol Genomics 2012 44 417 429. doi: 10.1152/physiolgenomics.00160.2011.
21. Salmon M, Gomez D, Greene E, Shankman L, Owens GK., Cooperative binding of KLF4, pELK-1, and HDAC2 to a G/C repressor element in the SM22α promoter mediates transcriptional silencing during SMC phenotypic switching in vivo. Circ Res 2012 111 685 696. doi: 10.1161/CIRCRESAHA.112.269811.
22. Yoshida T, Kaestner KH, Owens GK., Conditional deletion of Krüppel-like factor 4 delays downregulation of smooth muscle cell differentiation markers but accelerates neointimal formation following vascular injury. Circ Res 2008 102 1548 1557. doi: 10.1161/CIRCRESAHA.108.176974.
23. Shankman LS, Gomez D, Cherepanova OA, Salmon M, Alencar GF, Haskins RM, Swiatlowska P, Newman AA, Greene ES, Straub AC, Isakson B, Randolph GJ, Owens GK., KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat Med 2015 21 628 637. doi: 10.1038/nm.3866.
24. Vengrenyuk Y, Nishi H, Long X, Ouimet M, Savji N, Martinez FO, Cassella CP, Moore KJ, Ramsey SA, Miano JM, Fisher EA., Cholesterol loading reprograms the microRNA-143/145-myocardin axis to convert aortic smooth muscle cells to a dysfunctional macrophage-like phenotype. Arterioscler Thromb Vasc Biol 2015 35 535 546. doi: 10.1161/ATVBAHA.114.304029.
25. Schrijvers DM, De Meyer GR, Kockx MM, Herman AG, Martinet W., Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler Thromb Vasc Biol 2005 25 1256 1261. doi: 10.1161/01.ATV.0000166517.18801.a7.
26. Gomez D, Owens GK., Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovasc Res 2012 95 156 164. doi: 10.1093/cvr/cvs115.
27. Glass CK, Witztum JL., Atherosclerosis. the road ahead. Cell 2001 104 503 516
28. Koyama H, Raines EW, Bornfeldt KE, Roberts JM, Ross R., Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of Cdk2 inhibitors. Cell 1996 87 1069 1078
29. Li DY, Brooke B, Davis EC, Mecham RP, Sorensen LK, Boak BB, Eichwald E, Keating MT., Elastin is an essential determinant of arterial morphogenesis. Nature 1998 393 276 280. doi: 10.1038/30522.
30. Fukumoto Y, Deguchi JO, Libby P, Rabkin-Aikawa E, Sakata Y, Chin MT, Hill CC, Lawler PR, Varo N, Schoen FJ, Krane SM, Aikawa M., Genetically determined resistance to collagenase action augments interstitial collagen accumulation in atherosclerotic plaques. Circulation 2004 110 1953 1959. doi: 10.1161/01.CIR.0000143174.41810.10.
31. Rohwedder I, Montanez E, Beckmann K, Bengtsson E, Dunér P, Nilsson J, Soehnlein O, Fässler R., Plasma fibronectin deficiency impedes atherosclerosis progression and fibrous cap formation. EMBO Mol Med 2012 4 564 576. doi: 10.1002/emmm.201200237.
32. Gomez D, Shankman LS, Nguyen AT, Owens GK., Detection of histone modifications at specific gene loci in single cells in histological sections. Nat Methods 2013 10 171 177. doi: 10.1038/nmeth.2332.
33. Feil S, Fehrenbacher B, Lukowski R, Essmann F, Schulze-Osthoff K, Schaller M, Feil R., Transdifferentiation of vascular smooth muscle cells to macrophage-like cells during atherogenesis. Circ Res 2014 115 662 667. doi: 10.1161/CIRCRESAHA.115.304634.
34. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R., Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med 2002 8 403 409. doi: 10.1038/nm0402-403.
35. Caplice NM, Bunch TJ, Stalboerger PG, Wang S, Simper D, Miller DV, Russell SJ, Litzow MR, Edwards WD., Smooth muscle cells in human coronary atherosclerosis can originate from cells administered at marrow transplantation. Proc Natl Acad Sci USA 2003 100 4754 4759. doi: 10.1073/pnas.0730743100.
36. Iwata H, Manabe I, Fujiu K, Yamamoto T, Takeda N, Eguchi K, Furuya A, Kuro-o M, Sata M, Nagai R., Bone marrow-derived cells contribute to vascular inflammation but do not differentiate into smooth muscle cell lineages. Circulation 2010 122 2048 2057. doi: 10.1161/CIRCULATIONAHA.110.965202.
37. Yu H, Stoneman V, Clarke M, Figg N, Xin HB, Kotlikoff M, Littlewood T, Bennett M., Bone marrow-derived smooth muscle-like cells are infrequent in advanced primary atherosclerotic plaques but promote atherosclerosis. Arterioscler Thromb Vasc Biol 2011 31 1291 1299. doi: 10.1161/ATVBAHA.110.218578.
38. Bentzon JF, Sondergaard CS, Kassem M, Falk E., Smooth muscle cells healing atherosclerotic plaque disruptions are of local, not blood, origin in apolipoprotein E knockout mice. Circulation 2007 116 2053 2061. doi: 10.1161/CIRCULATIONAHA.107.722355.
39. Bentzon JF, Weile C, Sondergaard CS, Hindkjaer J, Kassem M, Falk E., Smooth muscle cells in atherosclerosis originate from the local vessel wall and not circulating progenitor cells in ApoE knockout mice. Arterioscler Thromb Vasc Biol 2006 26 2696 2702. doi: 10.1161/01.ATV.0000247243.48542.9d.
40. Allahverdian S, Chehroudi AC, McManus BM, Abraham T, Francis GA., Contribution of intimal smooth muscle cells to cholesterol accumulation and macrophage-like cells in human atherosclerosis. Circulation 2014 129 1551 1559. doi: 10.1161/CIRCULATIONAHA.113.005015.
41. Tang Z, Wang A, Yuan F, Yan Z, Liu B, Chu JS, Helms JA, Li S., Differentiation of multipotent vascular stem cells contributes to vascular diseases. Nat Commun 2012 3 875. doi: 10.1038/ncomms1867.
42. Nguyen AT, Gomez D, Bell RD, Smooth muscle cell plasticity: fact or fiction? Circ Res 2013 112 17 22. doi: 10.1161/CIRCRESAHA.112.281048.
43. Buckingham ME, Meilhac SM., Tracing cells for tracking cell lineage and clonal behavior. Dev Cell 2011 21 394 409. doi: 10.1016/j.devcel.2011.07.019.
44. Herring BP, Hoggatt AM, Burlak C, Offermanns S., Previously differentiated medial vascular smooth muscle cells contribute to neointima formation following vascular injury. Vasc Cell 2014 6 21. doi: 10.1186/2045-824X-6-21.
45. Hu Y, Zhang Z, Torsney E, Afzal AR, Davison F, Metzler B, Xu Q., Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice. J Clin Invest 2004 113 1258 1265. doi: 10.1172/JCI19628.
46. Tigges U, Komatsu M, Stallcup WB., Adventitial pericyte progenitor/mesenchymal stem cells participate in the restenotic response to arterial injury. J Vasc Res 2013 50 134 144. doi: 000345524.
47. Coen M, Gabbiani G, Bochaton-Piallat ML., Myofibroblast-mediated adventitial remodeling: an underestimated player in arterial pathology. Arterioscler Thromb Vasc Biol 2011 31 2391 2396. doi: 10.1161/ATVBAHA.111.231548.
48. Sartore S, Chiavegato A, Faggin E, Franch R, Puato M, Ausoni S, Pauletto P., Contribution of adventitial fibroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ Res 2001 89 1111 1121
49. Passman JN, Dong XR, Wu SP, Maguire CT, Hogan KA, Bautch VL, Majesky MW., A sonic hedgehog signaling domain in the arterial adventitia supports resident Sca1+ smooth muscle progenitor cells. Proc Natl Acad Sci USA 2008 105 9349 9354. doi: 10.1073/pnas.0711382105.
50. Hu Y, Davison F, Ludewig B, Erdel M, Mayr M, Url M, Dietrich H, Xu Q., Smooth muscle cells in transplant atherosclerotic lesions are originated from recipients, but not bone marrow progenitor cells. Circulation 2002 106 1834 1839
51. Benditt EP, Benditt JM., Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci USA 1973 70 1753 1756
52. Mikawa T, Fischman DA., Retroviral analysis of cardiac morphogenesis: discontinuous formation of coronary vessels. Proc Natl Acad Sci USA 1992 89 9504 9508
53. Chung IM, Schwartz SM, Murry CE., Clonal architecture of normal and atherosclerotic aorta: implications for atherogenesis and vascular development. Am J Pathol 1998 152 913 923
54. Esner M, Meilhac SM, Relaix F, Nicolas JF, Cossu G, Buckingham ME., Smooth muscle of the dorsal aorta shares a common clonal origin with skeletal muscle of the myotome. Development 2006 133 737 749. doi: 10.1242/dev.02226.
55. Lutgens E, de Muinck ED, Kitslaar PJ, Tordoir JH, Wellens HJ, Daemen MJ., Biphasic pattern of cell turnover characterizes the progression from fatty streaks to ruptured human atherosclerotic plaques. Cardiovasc Res 1999 41 473 479
56. Stemerman MB, Weinstein R, Rowe JW, Maciag T, Fuhro R, Gardner R., Vascular smooth muscle cell growth kinetics in vivo in aged rats. Proc Natl Acad Sci USA 1982 79 3863 3866
57. Hariri RJ, Hajjar DP, Coletti D, Alonso DR, Weksler ME, Rabellino E., Aging and arteriosclerosis. Cell cycle kinetics of young and old arterial smooth muscle cells. Am J Pathol 1988 131 132 136
58. Moon SK, Cha BY, Kim CH., In vitro cellular aging is associated with enhanced proliferative capacity, G1 cell cycle modulation, and matrix metalloproteinase-9 regulation in mouse aortic smooth muscle cells. Arch Biochem Biophys 2003 418 39 48
59. O'Brien ER, Alpers CE, Stewart DK, Ferguson M, Tran N, Gordon D, Benditt EP, Hinohara T, Simpson JB, Schwartz SM., Proliferation in primary and restenotic coronary atherectomy tissue. Implications for antiproliferative therapy. Circ Res 1993 73 223 231
60. Bennett MR, Evan GI, Schwartz SM., Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest 1995 95 2266 2274. doi: 10.1172/JCI117917.
61. Patel VA, Zhang QJ, Siddle K, Soos MA, Goddard M, Weissberg PL, Bennett MR., Defect in insulin-like growth factor-1 survival mechanism in atherosclerotic plaque-derived vascular smooth muscle cells is mediated by reduced surface binding and signaling. Circ Res 2001 88 895 902
62. Matthews C, Gorenne I, Scott S, Figg N, Kirkpatrick P, Ritchie A, Goddard M, Bennett M., Vascular smooth muscle cells undergo telomere-based senescence in human atherosclerosis: effects of telomerase and oxidative stress. Circ Res 2006 99 156 164. doi: 10.1161/01.RES.0000233315.38086.bc.
63. O'Sullivan M, Scott S, McCarthy N, Shapiro LM, Kirkpatrick PJ, MR B., Differential cyclin E expression in human in stent stenosis vascular smooth muscle cells identifies targets for selective anti-restenotic therapy. Cardiovascular Res 2003 60 673 683
64. Bennett MR, Macdonald K, Chan SW, Boyle JJ, Weissberg PL., Cooperative interactions between RB and p53 regulate cell proliferation, cell senescence, and apoptosis in human vascular smooth muscle cells from atherosclerotic plaques. Circ Res 1998 82 704 712
65. Geng YJ, Libby P., Evidence for apoptosis in advanced human atheroma. Colocalization with interleukin-1 beta-converting enzyme. Am J Pathol 1995 147 251 266
66. Boyle JJ, Weissberg PL, Bennett MR., Human macrophage-induced vascular smooth muscle cell apoptosis requires NO enhancement of Fas/Fas-L interactions. Arterioscler Thromb Vasc Biol 2002 22 1624 1630
67. Bennett MR., Apoptosis of vascular smooth muscle cells in vascular remodelling and atherosclerotic plaque rupture. Cardiovasc Res 1999 41 361 368
68. Bauriedel G, Hutter R, Welsch U, Bach R, Sievert H, Lüderitz B., Role of smooth muscle cell death in advanced coronary primary lesions: implications for plaque instability. Cardiovasc Res 1999 41 480 488
69. Kockx MM., Apoptosis in the atherosclerotic plaque: quantitative and qualitative aspects. Arterioscler Thromb Vasc Biol 1998 18 1519 1522
70. Bennett MR., Life and death in the atherosclerotic plaque. Curr Opin Lipidol 2010 21 422 426. doi: 10.1097/MOL.0b013e32833d2bfd.
71. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR., Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med 2006 12 1075 1080. doi: 10.1038/nm1459.
72. Clarke MC, Littlewood TD, Figg N, Maguire JJ, Davenport AP, Goddard M, Bennett MR., Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res 2008 102 1529 1538. doi: 10.1161/CIRCRESAHA.108.175976.
73. Ihling C, Szombathy T, Nampoothiri K, Haendeler J, Beyersdorf F, Uhl M, Zeiher AM, Schaefer HE., Cystic medial degeneration of the aorta is associated with p53 accumulation, Bax upregulation, apoptotic cell death, and cell proliferation. Heart 1999 82 286 293
74. Sawabe M., Vascular aging: from molecular mechanism to clinical significance. Geriatr Gerontol Int 2010 10 suppl 1 S213 S220. doi: 10.1111/j.1447-0594.2010.00603.x.
75. Clarke MC, Talib S, Figg NL, Bennett MR., Vascular smooth muscle cell apoptosis induces interleukin-1-directed inflammation: effects of hyperlipidemia-mediated inhibition of phagocytosis. Circ Res 2010 106 363 372. doi: 10.1161/CIRCRESAHA.109.208389.
76. Bennett MR, Gibson DF, Schwartz SM, Tait JF., Binding and phagocytosis of apoptotic vascular smooth muscle cells is mediated in part by exposure of phosphatidylserine. Circ Res 1995 77 1136 1142
77. Kojima Y, Downing K, Kundu R, Miller C, Dewey F, Lancero H, Raaz U, Perisic L, Hedin U, Schadt E, Maegdefessel L, Quertermous T, Leeper NJ., Cyclin-dependent kinase inhibitor 2B regulates efferocytosis and atherosclerosis. J Clin Invest 2014 124 1083 1097. doi: 10.1172/JCI70391.
78. Zernecke A, Schober A, Bot I, von Hundelshausen P, Liehn EA, Möpps B, Mericskay M, Gierschik P, Biessen EA, Weber C., SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ Res 2005 96 784 791. doi: 10.1161/01.RES.0000162100.52009.38.
79. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O., A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci USA 1995 92 9363 9367
80. Minamino T, Miyauchi H, Yoshida T, Ishida Y, Yoshida H, Komuro I., Endothelial cell senescence in human atherosclerosis: role of telomere in endothelial dysfunction. Circulation 2002 105 1541 1544
81. Ogami M, Ikura Y, Ohsawa M, Matsuo T, Kayo S, Yoshimi N, Hai E, Shirai N, Ehara S, Komatsu R, Naruko T, Ueda M., Telomere shortening in human coronary artery diseases. Arterioscler Thromb Vasc Biol 2004 24 546 550. doi: 10.1161/01.ATV.0000117200.46938.e7.
82. Carracedo J, Merino A, Briceño C, Soriano S, Buendía P, Calleros L, Rodriguez M, Martín-Malo A, Aljama P, Ramírez R., Carbamylated low-density lipoprotein induces oxidative stress and accelerated senescence in human endothelial progenitor cells. FASEB J 2011 25 1314 1322. doi: 10.1096/fj.10-173377.
83. Brouilette S, Singh RK, Thompson JR, Goodall AH, Samani NJ., White cell telomere length and risk of premature myocardial infarction. Arterioscler Thromb Vasc Biol 2003 23 842 846. doi: 10.1161/01.ATV.0000067426.96344.32.
84. Brouilette SW, Moore JS, McMahon AD, Thompson JR, Ford I, Shepherd J, Packard CJ, Samani NJ, West of Scotland Coronary Prevention Study Group Telomere length, risk of coronary heart disease, and statin treatment in the West of Scotland Primary Prevention Study: a nested case-control study. Lancet 2007 369 107 114. doi: 10.1016/S0140-6736(07)60071-3.
85. Panayiotou AG, Nicolaides AN, Griffin M, Tyllis T, Georgiou N, Bond D, Martin RM, Hoppensteadt D, Fareed J, Humphries SE., Leukocyte telomere length is associated with measures of subclinical atherosclerosis. Atherosclerosis 2010 211 176 181. doi: 10.1016/j.atherosclerosis.2010.01.037.
86. Willeit P, Willeit J, Brandstätter A, Ehrlenbach S, Mayr A, Gasperi A, Weger S, Oberhollenzer F, Reindl M, Kronenberg F, Kiechl S., Cellular aging reflected by leukocyte telomere length predicts advanced atherosclerosis and cardiovascular disease risk. Arterioscler Thromb Vasc Biol 2010 30 1649 1656. doi: 10.1161/ATVBAHA.110.205492.
87. Chang E, Harley CB., Telomere length and replicative aging in human vascular tissues. Proc Natl Acad Sci USA 1995 92 11190 11194
88. Nzietchueng R, Elfarra M, Nloga J, Labat C, Carteaux JP, Maureira P, Lacolley P, Villemot JP, Benetos A., Telomere length in vascular tissues from patients with atherosclerotic disease. J Nutr Health Aging 2011 15 153 156
89. Song Y, Shen H, Schenten D, Shan P, Lee PJ, Goldstein DR., Aging enhances the basal production of IL-6 and CCL2 in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2012 32 103 109. doi: 10.1161/ATVBAHA.111.236349.
90. Wang J, Uryga AK, Reinhold J, Figg N, Baker L, Finigan A, Gray K, Kumar S, Clarke M, Bennett M., Vascular smooth muscle cell senescence promotes atherosclerosis and features of plaque vulnerability. Circulation 2015 132 1909 1919. doi: 10.1161/CIRCULATIONAHA.115.016457.
91. Boon RA, Vickers KC., Intercellular transport of microRNAs. Arterioscler Thromb Vasc Biol 2013 33 186 192. doi: 10.1161/ATVBAHA.112.300139.
92. Loyer X, Vion AC, Tedgui A, Boulanger CM., Microvesicles as cell-cell messengers in cardiovascular diseases. Circ Res 2014 114 345 353. doi: 10.1161/CIRCRESAHA.113.300858.