The Role of Matrix Metalloproteinases in the Progression and Vulnerabilization of Coronary Atherosclerotic Plaques

1. Newby AC. Dual role of matrix metalloproteinases (matrixins) in intimal thickening and atherosclerotic plaque rupture. Physiol Rev. 2005;85:1-31. doi: 10.1152/physrev.00048.2003.10.1152/physrev.00048.2003Search in Google Scholar

2. Spinale FG. Matrix metalloproteinases: regulation and dysregulation in the failing heart. Circ Res. 2002;90:520-30. doi: 10.1161/01.res.0000013290.12884.a3.10.1161/01.RES.0000013290.12884.A3Search in Google Scholar

3. Shah PK. Inflammation, metalloproteinases, and increased proteolysis: an emerging pathophysiological paradigm in aortic aneurysm. Circulation. 1997;96:2115-2117. doi: 10.1161/01.cir.96.7.2115.10.1161/01.CIR.96.7.2115Search in Google Scholar

4. Ho-Tin-Noé B, Michel JB. Initiation of angiogenesis in atherosclerosis: smooth muscle cells as mediators of the angiogenic response to atheroma formation. Trends Cardiovasc Med. 2011;21:183-187. doi: 10.1016/j.tcm.2012.05.007.10.1016/j.tcm.2012.05.007Search in Google Scholar

5. Kaperonis EA, Liapis CD, Kakisis JD, Dimitroulis D, Papavassiliou VG. Inflammation and atherosclerosis. Eur J Vasc Endovasc Surg. 2006;31:386-393. doi: 10.1016/j. ejvs.2005.11.001.Search in Google Scholar

6. Bäck M, Ketelhuth DF, Agewall S. Matrix metalloproteinases in atherothrombosis. Prog Cardiovasc Dis. 2010;52:410-428. doi: 10.1016/j.pcad.2009.12.00210.1016/j.pcad.2009.12.002Search in Google Scholar

7. Yabluchanskiy A, Ma Y, Iyer RP, Hall ME, Lindsey ML. Matrix metalloproteinase-9: Many shades of function in cardiovascular disease. Physiology. 2013;28:391–403. doi: 10.1152/physiol.00029.2013.10.1152/physiol.00029.2013Search in Google Scholar

8. Marino-Puertas L, Goulas T, Gomis-Rüth FX. Matrix metalloproteinases outside vertebrates. Biochim Biophys Acta Mol Cell Res. 2017;1864:2026-2035. doi: 10.1016/j. bbamcr.2017.04.003.Search in Google Scholar

9. Benjamin MM, Khalil RA. Matrix metalloproteinase inhibitors as investigative tools in the pathogenesis and management of vascular disease. Exp Suppl. 2012;103:209-279. doi: 10.1007/978-3-0348-0364-9_7.10.1007/978-3-0348-0364-9_7Search in Google Scholar

10. Olejarz W, Łacheta D, Kubiak-Tomaszewska G. Matrix Metalloproteinases as Biomarkers of Atherosclerotic Plaque Instability. Int J Mol Sci. 2020;21:3946. doi: 10.3390/ijms21113946.10.3390/ijms21113946Search in Google Scholar

11. Borkakoti N. Structural studies of matrix metalloproteinases. J Mol Med. 2000;78:261–268. doi: 10.1007/s001090000113.10.1007/s001090000113Search in Google Scholar

12. Spinale FG, Coker ML, Heung LJ, et al. A matrix metalloproteinase induction/activation system exists in the human left ventricular myocardium and is upregulated in heart failure. Circulation. 2000;102:1944-1949. doi: 10.1161/01. cir.102.16.1944.Search in Google Scholar

13. Stewart JA Jr, Wei CC, Brower GL, Rynders PE, Hankes GH, Dillon AR, Lucchesi PA, Janicki JS, Dell’Italia LJ. Cardiac mast cell- and chymase-mediated matrix metalloproteinase activity and left ventricular remodeling in mitral regurgitation in the dog. J Mol Cell Cardiol. 2003;35:311-319. doi: 10.1016/s0022-2828(03)00013-0.10.1016/S0022-2828(03)00013-0Search in Google Scholar

14. Liu P, Sun M, Sader S. Matrix metalloproteinases in cardiovascular disease. Can J Cardiol. 2006;22 Suppl B:25B-30B. doi: 10.1016/s0828-282x(06)70983-7.10.1016/S0828-282X(06)70983-7Search in Google Scholar

15. Ehrmann M, Clausen T. Proteolysis as a regulatory mechanism. Annu Rev Genet. 2004;38:709-24. doi: 10.1146/annurev. genet.38.072902.093416.Search in Google Scholar

16. Lambert E, Dassé E, Haye B, Petitfrère E. TIMPs as multifacial proteins. Crit Rev Oncol Hematol. 2004;49:187-98. doi: 10.1016/j.critrevonc.2003.09.008.10.1016/j.critrevonc.2003.09.008Search in Google Scholar

17. Simon F, Bergeron D, Larochelle S, Lopez-Vallé CA, Genest H, Armour A, Moulin VJ. Enhanced secretion of TIMP-1 by human hypertrophic scar keratinocytes could contribute to fibrosis. Burns. 2012;38:421-427. doi: 10.1016/j.burns.2011.09.001.10.1016/j.burns.2011.09.001Search in Google Scholar

18. Swiderski RE, Dencoff JE, Floerchinger CS, Shapiro SD, Hunninghake GW. Differential expression of extracellular matrix remodeling genes in a murine model of bleomycin-induced pulmonary fibrosis. Am J Pathol. 1998;152:821-828.Search in Google Scholar

19. McLennan SV, Wang XY, Moreno V, Yue DK, Twigg SM. Connective tissue growth factor mediates high glucose effects on matrix degradation through tissue inhibitor of matrix metalloproteinase type 1: implications for diabetic nephropathy. Endocrinology. 2004;145:5646-5655. doi: 10.1210/en.2004-0436.10.1210/en.2004-0436Search in Google Scholar

20. Knight BE, Kozlowski N, Havelin J, et al. TIMP-1 Attenuates the Development of Inflammatory Pain Through MMP-Dependent and Receptor-Mediated Cell Signaling Mechanisms. Front Mol Neurosci. 2019;12:220. doi: 10.3389/fnmol.2019.00220.10.3389/fnmol.2019.00220Search in Google Scholar

21. Arpino V, Brock M, Gill SE. The role of TIMPs in regulation of extracellular matrix proteolysis. Matrix Biol. 2015;44-46:247-54. doi: 10.1016/j.matbio.2015.03.005.10.1016/j.matbio.2015.03.005Search in Google Scholar

22. Gill SE, Pape MC, Khokha R, Watson AJ, Leco KJ. A null mutation for tissue inhibitor of metalloproteinases-3 (Timp-3) impairs murine bronchiole branching morphogenesis. Dev Biol. 2003;261:313-323. doi: 10.1016/s0012-1606(03)00318-x.10.1016/S0012-1606(03)00318-XSearch in Google Scholar

23. Gill SE, Pape MC, Leco KJ. Tissue inhibitor of metalloproteinases 3 regulates extracellular matrix--cell signaling during bronchiole branching morphogenesis. Dev Biol. 2006;298:540-554. doi: 10.1016/j.ydbio.2006.07.004.10.1016/j.ydbio.2006.07.00416890932Search in Google Scholar

24. Tian H, Cimini M, Fedak PW, Altamentova S, Fazel S, Huang ML, Weisel RD, Li RK. TIMP-3 deficiency accelerates cardiac remodeling after myocardial infarction. J Mol Cell Cardiol. 2007;43:733-743. doi: 10.1016/j.yjmcc.2007.09.003.10.1016/j.yjmcc.2007.09.00317945252Search in Google Scholar

25. Basu R, Lee J, Morton JS, Takawale A, Fan D, Kandalam V, Wang X, Davidge ST, Kassiri Z. TIMP3 is the primary TIMP to regulate agonist-induced vascular remodelling and hypertension. Cardiovasc Res. 2013;98:360-371. doi: 10.1093/cvr/cvt067.10.1093/cvr/cvt06723524300Search in Google Scholar

26. Takawale A, Fan D, Basu R, Shen M, Parajuli N, Wang W, Wang X, Oudit GY, Kassiri Z. Myocardial recovery from ischemiareperfusion is compromised in the absence of tissue inhibitor of metalloproteinase 4. Circ Heart Fail. 2014;7:652-662. doi: 10.1161/CIRCHEARTFAILURE.114.001113.10.1161/CIRCHEARTFAILURE.114.00111324842912Search in Google Scholar

27. Watanabe-Takano H, Takano K, Sakamoto A, et al. DA-Raf-dependent inhibition of the Ras-ERK signaling pathway in type 2 alveolar epithelial cells controls alveolar formation. Proc Natl Acad Sci U S A. 2014;111:E2291-300. doi: 10.1073/pnas.1321574111.10.1073/pnas.1321574111405057824843139Search in Google Scholar

28. Shynlova O, Bortolini MAT, Alarab M. Genes responsible for vaginal extracellular matrix metabolism are modulated by women’s reproductive cycle and menopause. International Braz J Urol. 2013;39:257-267. doi: 10.1590/S1677-5538. IBJU.2013.02.15Search in Google Scholar

29. Kyle DJ, Harvey AG, Shih B, Tan KT, Chaudhry IH, Bayat A. Identification of molecular phenotypic descriptors of breast capsular contracture formation using informatics analysis of the whole genome transcriptome. Wound Repair Regen. 2013;21:762-769. doi: 10.1111/wrr.12077.10.1111/wrr.1207723941504Search in Google Scholar

30. Magdalena K, Magdalena K, Grazyna S. The Role of Matrix Metalloproteinase-3 In the Development of Atherosclerosis and Cardiovascular Events. EJIFCC. 2006;17:2-5.Search in Google Scholar

31. Yoon YW, Kwon HM, Hwang KC, et al. Upstream regulation of matrix metalloproteinase by EMMPRIN; extracellular matrix metalloproteinase inducer in advanced atherosclerotic plaque. Atherosclerosis. 2005;180:37-44. doi: 10.1016/j. atherosclerosis.2004.11.021.Search in Google Scholar

32. Wang X, Khalil RA. Matrix metalloproteinases, vascular remodeling, and vascular disease. Adv. Pharmacol. 2018;81:241–330. doi: 10.1016/bs.apha.2017.08.002.10.1016/bs.apha.2017.08.002576587529310800Search in Google Scholar

33. Kowara M, Cudnoch-Jedrzejewska A, Opolski G, Wlodarski P. MicroRNA regulation of extracellular matrix components in the process of atherosclerotic plaque destabilization. Clin. Exp. Pharmacol. Physiol. 2017;44:711–718. doi: 10.1111/1440-1681.12772.10.1111/1440-1681.1277228440887Search in Google Scholar

34. Newby AC. Metalloproteinase production from macrophages—A perfect storm leading to atherosclerotic plaque rupture and myocardial infarction. Exp. Physiol. 2016;101:1327–1337. doi: 10.1113/EP085567.10.1113/EP08556726969796Search in Google Scholar

35. Chen Q, Wang Q, Zhu J, Xiao Q, Zhang L. Reactive oxygen species: Key regulators in vascular health and diseases. Br. J. Pharmacol. 2018;175:1279–1292. doi: 10.1111/bph.13828.10.1111/bph.13828586702628430357Search in Google Scholar

36. Newby AC. Metalloproteinase expression in monocytes and macrophages and its relationship to atherosclerotic plaque instability. Arterioscler. Thromb. Vasc. Biol. 2008;28:2108– 2114. doi: 10.1161/ATVBAHA.108.173898.10.1161/ATVBAHA.108.17389818772495Search in Google Scholar

37. Amato B, Compagna R, Amato M, et al. Adult vascular wall resident multipotent vascular stem cells, matrix metalloproteinases, and arterial aneurysms. Stem Cells Int. 2015;2015:434962. doi: 10.1155/2015/434962.10.1155/2015/434962438185225866513Search in Google Scholar

38. Mott JD, Werb Z. Regulation of matrix biology by matrix metalloproteinases. Curr. Opin. Cell Biol. 2004;16:558–564. doi: 10.1016/j.ceb.2004.07.010.10.1016/j.ceb.2004.07.010277544615363807Search in Google Scholar

39. Chistiakov DA, Myasoedova VA, Melnichenko AA, Grechko AV, Orekhov AN. Calcifying matrix vesicles and atherosclerosis. Biomed. Res. Int. 2017;2017:7463590. doi: 10.1155/2017/7463590.10.1155/2017/7463590569739229238720Search in Google Scholar

40. Gaubatz JW, Ballantyne CM, Wasserman BA, et al. Association of circulating matrix metalloproteinases with carotid artery characteristics: The atherosclerosis risk in communities carotid mri study. Arterioscler Thromb. Vasc Biol. 2010;30:1034–1042. doi: 10.1161/ATVBAHA.109.195370.10.1161/ATVBAHA.109.195370286038320167662Search in Google Scholar

41. Sasaki T, Nakamura K, Sasada K, et al. Matrix metalloproteinase-2 deficiency impairs aortic atherosclerotic calcification in apoE-deficient mice. Atherosclerosis. 2013;227:43–50. doi: 10.1016/j.atherosclerosis.2012.12.008.10.1016/j.atherosclerosis.2012.12.00823312504Search in Google Scholar

42. Purroy A, Roncal C, Orbe J, et al. Matrix metalloproteinase-10 deficiency delays atherosclerosis progression and plaque calcification. Atherosclerosis. 2018;278:124–134. doi: 10.1016/j. atherosclerosis.2018.09.022.Search in Google Scholar

43. Loftus IM, Naylor AR, Bell PR, Thompson MM. Matrix metalloproteinases and atherosclerotic plaque instability. Br. J. Surg. 2002;89:680-694. doi: 10.1046/j.1365-2168.2002.02099.x.10.1046/j.1365-2168.2002.02099.x12027977Search in Google Scholar

44. Myasoedova VA, Chistiakov DA, Grechko AV, Orekhov AN. Matrix metalloproteinases in pro-atherosclerotic arterial remodeling. J. Mol. Cell Cardiol. 2018;123:159–167. doi: 10.1016/j.yjmcc.2018.08.026.10.1016/j.yjmcc.2018.08.02630172754Search in Google Scholar

45. Lahdentausta L, Leskelä J, Winkelmann A, et al. Serum MMP-9 Diagnostics, Prognostics, and Activation in Acute Coronary Syndrome and Its Recurrence. J Cardiovasc Transl Res. 2018;11:210-220. doi: 10.1007/s12265-018-9789-x.10.1007/s12265-018-9789-x597400129349668Search in Google Scholar

46. Li T, Li X, Feng Y, Dong G, Wang Y, Yang J. The Role of Matrix Metalloproteinase-9 in Atherosclerotic Plaque Instability. Mediators Inflamm. 2020;2020:3872367. doi: 10.1155/2020/3872367.10.1155/2020/3872367755789633082709Search in Google Scholar

47. Galis ZS, Sukhova GK, Lark MW, Libby P. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest. 1994;94:2493-2503. doi: 10.1172/JCI117619.10.1172/JCI1176193300837989608Search in Google Scholar

48. Bayes-Genis A, Conover CA, Overgaard MT, et al. Pregnancy-associated plasma protein A as a marker of acute coronary syndromes. N Engl J Med. 2001;345:1022-1029. doi: 10.1056/NEJMoa003147.10.1056/NEJMoa00314711586954Search in Google Scholar

49. Noji Y, Kajinami K, Kawashiri MA, et al. Circulating matrix metalloproteinases and their inhibitors in premature coronary atherosclerosis. Clin Chem Lab Med. 2001;39:380-384. doi: 10.1515/CCLM.2001.060.10.1515/CCLM.2001.06011434385Search in Google Scholar

50. Pleva L, Kusnierova P, Plevova P, et al. Increased levels of MMP-3, MMP-9 and MPO represent predictors of in-stent restenosis, while increased levels of ADMA, LCAT, ApoE and ApoD predict bare metal stent patency. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2015;159:586-594. doi: 10.5507/bp.2015.037.10.5507/bp.2015.037Search in Google Scholar

51. Katsaros K, Kastl SP, Zorn G, et al. Increased Restenosis Rate After Implantation of Drug-Eluting Stents in Patients With Elevated Serum Activity of Matrix Metalloproteinase-2 and -9. JACC: Cardiovascular Interventions. 2010;3:90-97. doi: 10.1016/j.jcin.2009.10.023.10.1016/j.jcin.2009.10.023Search in Google Scholar

52. Orbe J, Fernandez L, Rodríguez JA, et al. Different expression of MMPs/TIMP-1 in human atherosclerotic lesions. Relation to plaque features and vascular bed. Atherosclerosis. 2003;170:269-276. doi: 10.1016/s0021-9150(03)00251-x.10.1016/S0021-9150(03)00251-XSearch in Google Scholar

53. Knox JB, Sukhova GK, Whittemore AD, Libby P. Evidence for altered balance between matrix metalloproteinases and their inhibitors in human aortic diseases. Circulation. 1997;95:205-212. doi: 10.1161/01.cir.95.1.205.10.1161/01.CIR.95.1.205Search in Google Scholar

54. Ruddy JM, Ikonomidis JS, Jones JA. Multidimensional Contribution of Matrix Metalloproteinases to Atherosclerotic Plaque Vulnerability: Multiple Mechanisms of Inhibition to Promote Stability. J Vasc Res. 2016;53:1-16. doi. org/10.1159/000446703.10.1159/000446703719692627327039Search in Google Scholar

55. Johnson J, Jenkins N, Huang W et al. Relationship of MMP-14 and TIMP-3 Expression with Macrophage Activation and Human Atherosclerotic Plaque Vulnerability. Mediators of Inflammation. 2014;2014;1-17. doi: 10.1155/2014/276457.10.1155/2014/276457416318625301980Search in Google Scholar

56. Lee JK, Zaidi SH, Liu P, Dawood F, Cheah AY, Wen WH, Saiki Y, Rabinovitch M. A serine elastase inhibitor reduces inflammation and fibrosis and preserves cardiac function after experimentally-induced murine myocarditis. Nat Med. 1998;4:1383-1391. doi: 10.1038/3973.10.1038/39739846575Search in Google Scholar

57. Fukuda D, Shimada K, Tanaka A, et al. Comparison of levels of serum matrix metalloproteinase-9 in patients with acute myocardial infarction versus unstable angina pectoris versus stable angina pectoris. Am J Cardiol. 2006;97:175-180. doi: 10.1016/j.amjcard.2005.08.020.10.1016/j.amjcard.2005.08.02016442358Search in Google Scholar

58. Kobayashi N, Hata N, Kume N, et al. Matrix metalloproteinase-9 for the earliest stage acute coronary syndrome. Circ J. 2011;75:2853-2861. doi: 10.1253/circj.cj-11-0640.10.1253/circj.CJ-11-0640Search in Google Scholar

59. Tyagi SC, Campbell SE, Reddy HK, Tjahja E, Voelker DJ. Matrix metalloproteinase activity expression in infarcted, noninfarcted and dilated cardiomyopathic human hearts. Mol Cell Biochem. 1996;155:13-21. doi: 10.1007/BF00714328.10.1007/BF007143288717434Search in Google Scholar

60. Sun M, Dawood F, Wen WH, et al. Excessive tumor necrosis factor activation after infarction contributes to susceptibility of myocardial rupture and left ventricular dysfunction. Circulation. 2004;110:3221-3228. doi: 10.1161/01. CIR.0000147233.10318.23.Search in Google Scholar

61. Kelly D, Khan SQ, Thompson M, et al. Plasma tissue inhibitor of metalloproteinase-1 and matrix metalloproteinase-9: novel indicators of left ventricular remodeling and prognosis after acute myocardial infarction. Eur Heart J. 2008;29:2116-2124. doi: 10.1093/eurheartj/ehn315.10.1093/eurheartj/ehn315294171718614523Search in Google Scholar

62. Van Doren SR. Matrix metalloproteinase interactions with collagen and elastin. Matrix Biol. 2015;44-46:224-231. doi: 10.1016/j.matbio.2015.01.005.10.1016/j.matbio.2015.01.005446614325599938Search in Google Scholar

63. Zhou ZX, Qiang H, Ma AQ, Chen H, Zhou P. Measurement peripheral blood index related to inflammation and ox-LDL, ox-LDLAb in patients with coronary heart disease and its clinical significance. Zhong Nan Da Xue Xue Bao Yi Xue Ban. 2006;31:258-262.Search in Google Scholar

64. Inokubo Y, Hanada H, Ishizaka H, Fukushi T, Kamada T, Okumura K. Plasma levels of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 are increased in the coronary circulation in patients with acute coronary syndrome. Am Heart J. 2001;141:211-217. doi: 10.1067/mhj.2001.112238.10.1067/mhj.2001.11223811174334Search in Google Scholar

65. Kumpatla S, Karuppiah K, Immaneni S, et al. Comparison of plasma adiponectin & certain inflammatory markers in angiographically proven coronary artery disease patients with & without diabetes – a study from India. Indian J Med Res. 2014;139:841-850.Search in Google Scholar

66. Hamed GM, Fattah MF. Clinical Relevance of matrix metalloproteinase 9 in patients with acute coronary syndrome. Clin Appl Thromb Hemost. 2015;21:705-711. doi: 10.1177/1076029614567309.10.1177/107602961456730925616488Search in Google Scholar

67. Owolabi US, Amraotkar AR, Coulter AR, et al. Change in matrix metalloproteinase 2, 3, and 9 levels at the time of and after acute atherothrombotic myocardial infarction. J Thromb Thrombolysis. 2020;49:235-244. doi: 10.1007/s11239-019-02004-7.10.1007/s11239-019-02004-7901298231808123Search in Google Scholar

68. Opstad TB, Seljeflot I, Bøhmer E, Arnesen H, Halvorsen S. MMP-9 and Its Regulators TIMP-1 and EMMPRIN in Patients with Acute ST-Elevation Myocardial Infarction: A NORDISTEMI Substudy. Cardiology. 2018;139:17-24. doi: 10.1159/000481684.10.1159/00048168429141241Search in Google Scholar

69. Zhu JJ, Zhao Q, Qu HJ, et al. Usefulness of plasma matrix metalloproteinase-9 levels in prediction of in-hospital mortality in patients who received emergent percutaneous coronary artery intervention following myocardial infarction. Oncotarget. 2017;8:105809-105818. doi: 10.18632/oncotarget.22401.10.18632/oncotarget.22401573968129285294Search in Google Scholar

70. Dhillon OS, Khan SQ, Narayan HK, et al. Matrix metalloproteinase-2 predicts mortality in patients with acute coronary syndrome. Clin Sci (Lond). 2009;118:249-257. doi: 10.1042/CS20090226.10.1042/CS2009022619583569Search in Google Scholar

71. Wu TC, Leu HB, Lin WT, Lin CP, Lin SJ, Chen JW. Plasma matrix metalloproteinase-3 level is an independent prognostic factor in stable coronary artery disease. Eur J Clin Invest. 2005;35:537-545. doi: 10.1111/j.1365-2362.2005.01548.x.10.1111/j.1365-2362.2005.01548.x16128859Search in Google Scholar