Reassessing the Mechanisms of Acute Coronary Syndromes: The "vulnerable Plaque" and Superficial Erosion

Circulation Research

Volumn 124, Issue 1, 2019, Pages 150-160

  Libby, Peter ^a   Pasterkamp, Gerard ^c   Crea, Filippo ^d   Jang, Ik Kyung ^b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^d FONDAZIONE POLICLINICO UNIVERSITARIO A GEMELLI IRCCS   (Italy)

Author keywords

acute coronary syndrome; atherosclerosis; macrophages; monocytes; neutrophils; thrombosis

Indexed keywords

PATTERN RECOGNITION RECEPTOR;

ACUTE CORONARY SYNDROME; ATHEROSCLEROTIC PLAQUE; BASEMENT MEMBRANE; CELL DEATH; CELL TRANSFORMATION; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY THROMBOSIS; ENDOTHELIAL TO MESENCHYMAL TRANSITION; ENDOTHELIUM CELL; EXTRACELLULAR TRAP; HUMAN; INNATE IMMUNITY; MACROPHAGE; MONOCYTE; NEUTROPHIL; NONHUMAN; PATHOPHYSIOLOGY; PERSONALIZED MEDICINE; POINT OF CARE TESTING; PRIORITY JOURNAL; REVIEW; ANIMAL; CORONARY ARTERY DISEASE; CORONARY BLOOD VESSEL; METABOLISM; PATHOLOGY; PROGNOSIS; RISK ASSESSMENT; RISK FACTOR; RUPTURE; SIGNAL TRANSDUCTION; VASCULAR REMODELING;

ACUTE CORONARY SYNDROME; ANIMALS; CORONARY ARTERY DISEASE; CORONARY VESSELS; HUMANS; PLAQUE, ATHEROSCLEROTIC; PROGNOSIS; RISK ASSESSMENT; RISK FACTORS; RUPTURE, SPONTANEOUS; SIGNAL TRANSDUCTION; VASCULAR REMODELING;

EID: 85059499070     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.118.311098     Document Type: Review

References (70)

1. Bentzon JF, Otsuka F, Virmani R, Falk E. Mechanisms of plaque formation and rupture. Circ Res. 2014;114:1852-1866. doi: 10.1161/ CIRCRESAHA.114.302721
2. Libby P. Mechanisms of acute coronary syndromes and their implications for therapy. N Engl J Med. 2013;368:2004-2013. doi: 10.1056/ NEJMra1216063
3. Drake TA, Morrissey JH, Edgington TS. Selective cellular expression of tissue factor in human tissues. Implications for disorders of hemostasis and thrombosis. Am J Pathol. 1989;134:1087-1097.
4. Wilcox JN, Smith KM, Schwartz SM, Gordon D. Localization of tissue factor in the normal vessel wall and in the atherosclerotic plaque. Proc Natl Acad Sci USA. 1989;86:2839-2843.
5. Mach F, Schönbeck U, Bonnefoy JY, Pober JS, Libby P. Activation of monocyte/macrophage functions related to acute atheroma complication by ligation of CD40: induction of collagenase, stromelysin, and tissue factor. Circulation. 1997;96:396-399.
6. Schönbeck U, Mach F, Sukhova GK, Herman M, Graber P, Kehry MR, Libby P. CD40 ligation induces tissue factor expression in human vascular smooth muscle cells. Am J Pathol. 2000;156:7-14. doi: 10.1016/S0002-9440(10)64699-8
7. Libby P, Theroux P. Pathophysiology of coronary artery disease. Circulation. 2005;111:3481-3488. doi: 10.1161/CIRCULATIONAHA.105.537878
8. Nilsson J. Atherosclerotic plaque vulnerability in the statin era. Eur Heart J. 2017;38:1638-1644. doi: 10.1093/eurheartj/ehx143
9. Lee SE, Chang HJ, Sung JM, et al. Effects of statins on coronary atherosclerotic plaques: the PARADIGM (Progression of AtheRosclerotic PlAque DetermIned by Computed TomoGraphic Angiography Imaging) study. JACC Cardiovasc Imaging. 2018;11:1475-1484.
10. Bohula EA, Giugliano RP, Leiter LA, Verma S, Park JG, Sever PS, Pineda AL, Honarpour N, Wang H, Murphy SA, Keech A, Pedersen TR, Sabatine MS. Inflammatory and cholesterol risk in the FOURIER trial (Further Cardiovascular Outcomes Research With PCSK9 Inhibition in Patients With Elevated Risk). Circulation. 2018;138:131-140.
11. Pradhan AD, Aday AW, Rose LM, Ridker PM. Residual inflammatory risk on treatment with PCSK9 inhibition and statin therapy. Circulation. 2018;138:141-149.
12. Libby P, Pasterkamp G. Requiem for the 'vulnerable plaque'. Eur Heart J. 2015;36:2984-2987. doi: 10.1093/eurheartj/ehv349
13. Pasterkamp G, den Ruijter HM, Libby P. Temporal shifts in clinical presentation and underlying mechanisms of atherosclerotic disease. Nat Rev Cardiol. 2017;14:21-29. doi: 10.1038/nrcardio.2016.166
14. Falk E, Shah PK, Fuster V. Coronary plaque disruption. Circulation. 1995;92:657-671.
15. Davies MJ. Stability and instability: two faces of coronary atherosclerosis. The Paul Dudley White Lecture 1995. Circulation. 1996;94:2013-2020.
16. Virmani R, Burke AP, Farb A, Kolodgie FD. Pathology of the unstable plaque. Prog Cardiovasc Dis. 2002;44:349-356.
17. Stone GW, Maehara A, Lansky AJ, de Bruyne B, Cristea E, Mintz GS, Mehran R, McPherson J, Farhat N, Marso SP, Parise H, Templin B, White R, Zhang Z, Serruys PW; PROSPECT Investigators. A prospective natural-history study of coronary atherosclerosis. N Engl J Med. 2011;364:226-235. doi: 10.1056/NEJMoa1002358
18. Kubo T, Maehara A, Mintz GS, et al. The dynamic nature of coronary artery lesion morphology assessed by serial virtual histology intravascular ultrasound tissue characterization. J Am Coll Cardiol. 2010;55:1590-1597. doi: 10.1016/j.jacc.2009.07.078
19. Chang HJ, Lin FY, Lee SE, et al. Coronary atherosclerotic precursors of acute coronary syndromes. J Am Coll Cardiol. 2018;71:2511-2522. doi: 10.1016/j.jacc.2018.02.079
20. Farb A, Burke AP, Tang AL, Liang TY, Mannan P, Smialek J, Virmani R. Coronary plaque erosion without rupture into a lipid core. A frequent cause of coronary thrombosis in sudden coronary death. Circulation. 1996;93:1354-1363.
21. Arbustini E, Dal Bello B, Morbini P, Burke AP, Bocciarelli M, Specchia G, Virmani R. Plaque erosion is a major substrate for coronary thrombosis in acute myocardial infarction. Heart. 1999;82:269-272.
22. Kolodgie FD, Burke AP, Farb A, Weber DK, Kutys R, Wight TN, Virmani R. Differential accumulation of proteoglycans and hyaluronan in culprit lesions: insights into plaque erosion. Arterioscler Thromb Vasc Biol. 2002;22:1642-1648.
23. Kolodgie FD, Burke AP, Wight TN, Virmani R. The accumulation of specific types of proteoglycans in eroded plaques: a role in coronary thrombosis in the absence of rupture. Curr Opin Lipidol. 2004;15:575-582.
24. Virmani R, Burke AP, Farb A. Plaque rupture and plaque erosion. Thromb Haemost. 1999;82(suppl 1):1-3.
25. Hu S, Yonetsu T, Jia H, et al. Residual thrombus pattern in patients with ST-segment elevation myocardial infarction caused by plaque erosion versus plaque rupture after successful fibrinolysis: an optical coherence tomography study. J Am Coll Cardiol. 2014;63:1336-1338. doi: 10.1016/j.jacc.2013.11.025
26. Jia H, Abtahian F, Aguirre AD, et al. In vivo diagnosis of plaque erosion and calcified nodule in patients with acute coronary syndrome by intravascular optical coherence tomography. J Am Coll Cardiol. 2013;62:1748-1758. doi: 10.1016/j.jacc.2013.05.071
27. Ferrante G, Nakano M, Prati F, Niccoli G, Mallus MT, Ramazzotti V, Montone RA, Kolodgie FD, Virmani R, Crea F. High levels of systemic myeloperoxidase are associated with coronary plaque erosion in patients with acute coronary syndromes: a clinicopathological study. Circulation. 2010;122:2505-2513. doi: 10.1161/CIRCULATIONAHA.110.955302
28. Partida RA, Libby P, Crea F, Jang IK. Plaque erosion: a new in vivo diagnosis and a potential major shift in the management of patients with acute coronary syndromes. Eur Heart J. 2018;39:2070-2076. doi: 10.1093/eurheartj/ehx786
29. Libby P. How does lipid lowering prevent coronary events? New insights from human imaging trials. Eur Heart J. 2015;36:472-474. doi: 10.1093/eurheartj/ehu510
30. Libby P, Ganz P, Schoen FJ, Lee RT. The vascular biology of the acute coronary syndromes. In: Topol EJ, ed. Acute Coronary Syndromes. 2nd ed. New York, NY: Marcel Dekker Inc; 2000:33-57.
31. Lindsey ML, Libby P. Matrix metalloproteinases in cardiovascular diseases. In: Brinckerhoff CE, ed. Matrix Metalloproteinases in Health and Disease. Singapore: World Scientific Publishing; 2017:187-225.
32. Rajavashisth TB, Liao JK, Galis ZS, Tripathi S, Laufs U, Tripathi J, Chai NN, Xu XP, Jovinge S, Shah PK, Libby P. Inflammatory cytokines and oxidized low density lipoproteins increase endothelial cell expression of membrane type 1-matrix metalloproteinase. J Biol Chem. 1999;274:11924-11929.
33. Sugiyama S, Kugiyama K, Aikawa M, Nakamura S, Ogawa H, Libby P. Hypochlorous acid, a macrophage product, induces endothelial apoptosis and tissue factor expression: involvement of myeloperoxidase-mediated oxidant in plaque erosion and thrombogenesis. Arterioscler Thromb Vasc Biol. 2004;24:1309-1314. doi: 10.1161/01.ATV.0000131784.50633.4f
34. Tricot O, Mallat Z, Heymes C, Belmin J, Lesèche G, Tedgui A. Relation between endothelial cell apoptosis and blood flow direction in human atherosclerotic plaques. Circulation. 2000;101:2450-2453.
35. Yamamoto E, Thondapu V, Poon E, Sugiyama T, Fracassi F, Dijkstra J, Lee H, Ooi A, Barlis P, Jang IK. Endothelial shear stress and plaque erosion: a computational fluid dynamics and optical coherence tomography study [published online ahead of print August 28, 2018]. JACC Cardiovasc Imaging. doi: 10.1016/j.jcmg.2018.07.024. https://www.clinicalkey.com/ service/content/pdf/watermarked/1-s2.0-S1936878X18307307.pdf? ocale=en-US.
36. Mullick AE, Tobias PS, Curtiss LK. Modulation of atherosclerosis in mice by Toll-like receptor 2. J Clin Invest. 2005;115:3149-3156. doi: 10.1172/JCI25482
37. Mullick AE, Soldau K, Kiosses WB, Bell TA 3rd, Tobias PS, Curtiss LK. Increased endothelial expression of Toll-like receptor 2 at sites of disturbed blood flow exacerbates early atherogenic events. J Exp Med. 2008;205:373-383. doi: 10.1084/jem.20071096
38. Franck G, Mawson T, Sausen G, et al. Flow perturbation mediates neutrophil recruitment and potentiates endothelial injury via TLR2 in mice: implications for superficial erosion. Circ Res. 2017;121:31-42. doi: 10.1161/CIRCRESAHA.117.310694
39. Bentzon JF, Falk E. Plaque erosion: new insights from the road less travelled. Circ Res. 2017;121:8-10. doi: 10.1161/CIRCRESAHA.117.311218
40. Quillard T, Araújo HA, Franck G, Shvartz E, Sukhova G, Libby P. TLR2 and neutrophils potentiate endothelial stress, apoptosis and detachment: implications for superficial erosion. Eur Heart J. 2015;36:1394-1404. doi: 10.1093/eurheartj/ehv044
41. Giannotta M, Trani M, Dejana E. VE-cadherin and endothelial adherens junctions: active guardians of vascular integrity. Dev Cell. 2013;26:441-454. doi: 10.1016/j.devcel.2013.08.020
42. Taylor KR, Trowbridge JM, Rudisill JA, Termeer CC, Simon JC, Gallo RL. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J Biol Chem. 2004;279:17079-17084. doi: 10.1074/jbc.M310859200
43. Scheibner KA, Lutz MA, Boodoo S, Fenton MJ, Powell JD, Horton MR. Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J Immunol. 2006;177:1272-1281.
44. Quillard T, Franck G, Mawson T, Folco E, Libby P. Mechanisms of erosion of atherosclerotic plaques. Curr Opin Lipidol. 2017;28:434-441. doi: 10.1097/MOL.0000000000000440
45. Bertheloot D, Latz E. HMGB1, IL-1α, IL-33 and S100 proteins: dualfunction alarmins. Cell Mol Immunol. 2017;14:43-64. doi: 10.1038/ cmi.2016.34
46. Laman JD, Schoneveld AH, Moll FL, van Meurs M, Pasterkamp G. Significance of peptidoglycan, a proinflammatory bacterial antigen in atherosclerotic arteries and its association with vulnerable plaques. Am J Cardiol. 2002;90:119-123.
47. Nijhuis MM, Pasterkamp G, Sluis NI, de Kleijn DP, Laman JD, Ulfman LH. Peptidoglycan increases firm adhesion of monocytes under flow conditions and primes monocyte chemotaxis. J Vasc Res. 2007;44:214-222. doi: 10.1159/000100420
48. Wright HL, Moots RJ, Bucknall RC, Edwards SW. Neutrophil function in inflammation and inflammatory diseases. Rheumatology (Oxford). 2010;49:1618-1631. doi: 10.1093/rheumatology/keq045
49. Borregaard N, Sørensen OE, Theilgaard-Mönch K. Neutrophil granules: a library of innate immunity proteins. Trends Immunol. 2007;28:340-345. doi: 10.1016/j.it.2007.06.002
50. Naegelen I, Beaume N, Plançon S, Schenten V, Tschirhart EJ, Bréchard S. Regulation of neutrophil degranulation and cytokine secretion: a novel model approach based on linear fitting. J Immunol Res. 2015;2015:817038. doi: 10.1155/2015/817038
51. Folco EJ, Mawson TL, Vromman A, Bernardes-Souza B, Franck G, Persson O, Nakamura M, Newton G, Luscinskas FW, Libby P. Neutrophil extracellular traps induce endothelial cell activation and tissue factor production through Interleukin-1α and Cathepsin G. Arterioscler Thromb Vasc Biol. 2018;38:1901-1912. doi: 10.1161/ATVBAHA. 118.311150
52. Fuchs TA, Brill A, Duerschmied D, Schatzberg D, Monestier M, Myers DD Jr, Wrobleski SK, Wakefield TW, Hartwig JH, Wagner DD. Extracellular DNA traps promote thrombosis. Proc Natl Acad Sci USA. 2010;107:15880-15885. doi: 10.1073/pnas.1005743107
53. Martinod K, Wagner DD. Thrombosis: tangled up in NETs. Blood. 2014;123:2768-2776. doi: 10.1182/blood-2013-10-463646
54. Chow OA, von Köckritz-Blickwede M, Bright AT, Hensler ME, Zinkernagel AS, Cogen AL, Gallo RL, Monestier M, Wang Y, Glass CK, Nizet V. Statins enhance formation of phagocyte extracellular traps. Cell Host Microbe. 2010;8:445-454. doi: 10.1016/j.chom.2010.10.005
55. Franck G, Mawson TL, Folco EJ, et al. Roles of PAD4 and NETosis in experimental atherosclerosis and arterial injury: implications for superficial erosion. Circ Res. 2018;123:33-42. doi: 10.1161/CIRCRESAHA.117.312494
56. Soehnlein O, Bazioti V, Westerterp M. A PAD 4 plaque erosion. Circ Res. 2018;123:6-8. doi: 10.1161/CIRCRESAHA.118.313110
57. Chen PY, Qin L, Barnes C, Charisse K, Yi T, Zhang X, Ali R, Medina PP, Yu J, Slack FJ, Anderson DG, Kotelianski V, Wang F, Tellides G, Simons M. FGF regulates TGF-β signaling and endothelial-to-mesenchymal transition via control of let-7 miRNA expression. Cell Rep. 2012;2:1684-1696. doi: 10.1016/j.celrep.2012.10.021
58. Cooley BC, Nevado J, Mellad J, et al. TGF-β signaling mediates endothelial-to-mesenchymal transition (EndMT) during vein graft remodeling. Sci Transl Med. 2014;6:227ra34. doi: 10.1126/scitranslmed.3006927
59. Wesseling M, Sakkers TR, de Jager SCA, Pasterkamp G, Goumans MJ. The morphological and molecular mechanisms of epithelial/endothelialto-mesenchymal transition and its involvement in atherosclerosis. Vascul Pharmacol. 2018;106:1-8. doi: 10.1016/j.vph.2018.02.006
60. Evrard SM, Lecce L, Michelis KC, et al. Endothelial to mesenchymal transition is common in atherosclerotic lesions and is associated with plaque instability. Nat Commun. 2016;7:11853. doi: 10.1038/ncomms11853
61. Schreiner PJ, Jacobs DR Jr, Wong ND, Kiefe CI. Twenty-five year secular trends in lipids and modifiable risk factors in a population-based biracial cohort: the Coronary Artery Risk Development in Young Adults (CARDIA) study, 1985-2011. J Am Heart Assoc. 2016;5:e003384.
62. Hopstock LA, Bønaa KH, Eggen AE, Grimsgaard S, Jacobsen BK, Løchen ML, Mathiesen EB, Njølstad I, Wilsgaard T. Longitudinal and secular trends in total cholesterol levels and impact of lipid-lowering drug use among Norwegian women and men born in 1905-1977 in the population-based Tromsø Study 1979-2016. BMJ Open. 2017;7:e015001. doi: 10.1136/bmjopen-2016-015001
63. Niccoli G, Montone RA, Di Vito L, Gramegna M, Refaat H, Scalone G, Leone AM, Trani C, Burzotta F, Porto I, Aurigemma C, Prati F, Crea F. Plaque rupture and intact fibrous cap assessed by optical coherence tomography portend different outcomes in patients with acute coronary syndrome. Eur Heart J. 2015;36:1377-1384. doi: 10.1093/eurheartj/ehv029
64. Prati F, Uemura S, Souteyrand G, Virmani R, Motreff P, Di Vito L, Biondi-Zoccai G, Halperin J, Fuster V, Ozaki Y, Narula J. OCT-based diagnosis and management of STEMI associated with intact fibrous cap. JACC Cardiovasc Imaging. 2013;6:283-287. doi: 10.1016/j.jcmg.2012.12.007
65. Jia H, Dai J, Hou J, Xing L, Ma L, Liu H, Xu M, Yao Y, Hu S, Yamamoto E, Lee H, Zhang S, Yu B, Jang IK. Effective anti-thrombotic therapy without stenting: intravascular optical coherence tomography-based management in plaque erosion (the EROSION study). Eur Heart J. 2017;38:792-800. doi: 10.1093/eurheartj/ehw381
66. Jia H, Kubo T, Akasaka T, Yu B. Optical coherence tomography guidance in management of acute coronary syndrome caused by plaque erosion. Circ J. 2018;82:302-308. doi: 10.1253/circj.CJ-17-1373
67. Braunwald E. Coronary plaque erosion: recognition and management. JACC Cardiovasc Imaging. 2013;6:288-289. doi: 10.1016/j.jcmg.2013.01.003
68. Libby P. Superficial erosion and the precision management of acute coronary syndromes: not one-size-fits-all. Eur Heart J. 2017;38:801-803. doi: 10.1093/eurheartj/ehw599
69. Niccoli G, Montone RA, Cataneo L, Cosentino N, Gramegna M, Refaat H, Porto I, Burzotta F, Trani C, Leone AM, Severino A, Crea F. Morphological-biohumoral correlations in acute coronary syndromes: pathogenetic implications. Int J Cardiol. 2014;171:463-466. doi: 10.1016/j.ijcard.2013.12.238
70. Chandran S, Watkins J, Abdul-Aziz A, Shafat M, Calvert PA, Bowles KM, Flather MD, Rushworth SA, Ryding AD. Inflammatory differences in plaque erosion and rupture in patients with ST-segment elevation myocardial infarction. J Am Heart Assoc. 2017;6:e005868.