Differential effects of tissue inhibitor of metalloproteinase (TIMP)-1 and TIMP-2 on atherosclerosis and monocyte/macrophage invasion

Cardiovascular Research

Volumn 109, Issue 2, 2016, Pages 318-330

  Di Gregoli, Karina ^a   George, Sarah J ^a   Jackson, Christopher L ^a   Newby, Andrew C ^a   Johnson, Jason L ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Atherosclerosis; Macrophage; Matrix metalloproteinases; Monocyte; Plaque progression

Indexed keywords

COLLAGEN; MATRIX METALLOPROTEINASE 14; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2; TIMP1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BIOACCUMULATION; BRACHIOCEPHALIC TRUNK; CELL INFILTRATION; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; EXPERIMENTAL INFLAMMATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; MONOCYTE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CYTOLOGY; GENETICS; KNOCKOUT MOUSE; METABOLISM; NECROSIS; PATHOLOGY; SMOOTH MUSCLE CELL; VASCULAR SMOOTH MUSCLE;

ANIMALS; FEMALE; MACROPHAGES; MALE; MICE, KNOCKOUT; MONOCYTES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NECROSIS; PLAQUE, ATHEROSCLEROTIC; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TISSUE INHIBITOR OF METALLOPROTEINASE-2;

EID: 84959920448     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv268     Document Type: Article

References (54)

1. Falk E, Nakano M, Bentzon JF, Finn AV, Virmani R. Update on acute coronary syndromes: The pathologists view. Eur Heart J 2013;34:719-728.
2. Bentzon JF, Otsuka F, Virmani R, Falk E. Mechanisms of plaque formation and rupture. Circ Res 2014;114:1852-1866.
3. 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.
4. Fabunmi RP, Sukhova GK, Sugiyama S, Libby P. Expression of tissue inhibitor of metalloproteinases-3 in human atheroma and regulation in lesion-Associated cells. Circ Res 1998;83:270-278.
5. Robbins CS, Hilgendorf I, Weber GF, Theurl I, Iwamoto Y, Figueiredo J-L, Gorbatov R, Sukhova GK, Gerhardt LMS, Smyth D, Zavitz CCJ, Shikatani EA, Parsons M, van Rooijen N, Lin HY, Husain M, Libby P, Nahrendorf M, Weissleder R, Swirski FK. Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat Med 2013;19:1166-1172.
6. Nahrendorf M, Swirski FK. Monocyte and macrophage heterogeneity in the heart. Circ Res 2013;112:1624-1633.
7. Libby P, Nahrendorf M, Pittet MJ, Swirski FK. Diversity of denizens of the atherosclerotic plaque-not all monocytes are created equal. Circulation 2008;117:3168-3170.
8. Shipley JM, Wesselschmidt RL, Kobayashi DK, Ley TJ, Shapiro SD. Metalloelastase is required for macrophage-mediated proteolysis and matrix invasion in mice. Proc Natl Acad Sci USA 1996;93:3942-3946.
9. Johnson JL, Devel L, Czarny B, George SJ, Jackson CL, Rogakos V, Beau F, Yiotakis A, Newby AC, Dive V. A selective matrix metalloproteinase-12 inhibitor retards atherosclerotic plaque development in apolipoprotein E-knockout mice. Arterioscler Thromb Vasc Biol 2011;31:528-535.
10. Matias-Roman S, Galvez BG, Genis L, Yanez-Mo M, de la Rosa G, Sanchez-Mateos P, Sanchez-Madrid F, Arroyo AG. Membrane type 1-matrix metalloproteinase is involved in migration of human monocytes and is regulated through their interaction with fibronectin or endothelium. Blood 2005;105:3956-3964.
11. Sithu SD, English WR, Olson P, Krubasik D, Baker AH, Murphy G, DSouza SE. Membrane-Type 1-matrix metalloproteinase regulates intracellular adhesion molecule-1 (ICAM-1)-mediated monocyte transmigration. J Biol Chem 2007;282: 25010-9.
12. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, Stack MS, Friedl P. Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 2007;9:893-904.
13. Rajavashisth TB, Xu X-P, Jovinge S, Meisel S, Xu X-O, Chai N-N, Fishbein C, Kaul S, Cercek B, Sharifi BG, Shah PD. Membrane type 1 matrix metalloproteinase expression in human atherosclerotic plaques. Circ Res 1999;99:3101-3109.
14. Schmidt R, Bultmann A, Ungerer M, Joghetaei N, Bulbul O, Thieme S, Chavakis T, Toole BP, Gawaz M, Schomig A, May AE. Extracellular matrix metalloproteinase inducer regulates matrix metalloproteinase activity in cardiovascular cells. Circulation 2006;113:834-841.
15. Schneider F, Sukhova GK, Aikawa M, Canner J, Gerdes N, Tang SMT, Shi GP, Apte SS, Libby P. Matrix metalloproteinase-14 deficiency in bone marrow-derived cells promotes collagen accumulation in mouse atherosclerotic plaques. Circulation 2008;117: 931-939.
16. Di Gregoli K, Jenkins N, Salter R, White S, Newby AC, Johnson JL. MicroRNA-24 regulates macrophage behavior and retards atherosclerosis. Arterioscler Thromb Vasc Biol 2014;34:1990-2000.
17. Newby AC. Matrix metalloproteinase inhibition therapy for vascular diseases. Vasc Pharmacol 2012;56:232-244.
18. Galis ZS, Sukhova GK, Libby P. Microscopic localisation of active proteases by in situ zymography: detection of matrix metalloproteinase activity in vascular tissue. Faseb J 1995;9:974-980.
19. Johnson JL, Jackson CL, Angelini GD, George SJ. Activation of matrix-degrading metalloproteinases by mast cell proteases in atherosclerotic plaques. Arterioscler Thromb Vasc Biol 1998;18:1707-1715.
20. Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Science 2002;115:3719-3727.
21. Johnson JL, Baker AH, Oka K, Chan L, Newby AC, Jackson CL, George SJ. Suppression of atherosclerotic plaque progression and instability by tissue inhibitor of metalloproteinase-2: involvement of macrophage migration and apoptosis. Circulation 2006;113:2435-2444.
22. Soloway P, Alexander CM, Werb Z, Jaenisch R. Targeted mutagenesis of TIMP-1 reveals that lung tumour invasion is influenced by TIMP-1 genotype of the tumour but not by that of the host. Oncogene 1996;13:2307-2314.
23. Wang Z, Juttermann R, Soloway PD. TIMP-2 is required for efficient activation of proMP-2 in vivo. J Biol Chem 2000;275:26411-26415.
24. Johnson J, Carson K, Williams H, Karanam S, Newby A, Angelini G, George S, Jackson C. plaque rupture after short periods of fat-feeding in the apolipoprotein E knockout mouse: model characterisation, and effects of pravastatin treatment. Circulation 2005;111:1422-1430.
25. Johnson JL, Sala-Newby GB, Ismail Y, Aguilera CNM, Newby AC. Low tissue inhibitor of metalloproteinases 3 and high matrix metalloproteinase 14 levels defines a subpopulation of highly invasive foam-cell macrophages. Arterioscler Thromb Vasc Biol 2008;28: 1647-1653.
26. Thorp E, Cui D, Schrijvers DM, Kuriakose G, Tabas I. Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of Apoe-/-mice. Arterioscler Thromb Vasc Biol 2008;28: 1421-1428.
27. Shiomi M, Ito T, Hirouchi Y, Enomoto M. Fibromuscular cap composition is important for the stability of established atherosclerotic plaques in mature WHHL rabbits treated with statins. Atherosclerosis 2001;157:75-84.
28. Burke AP, Kolodgie FD, Farb A, Weber DK, Malcom GT, Smialek J, Virmani R. Healed plaque ruptures and sudden coronary death-evidence that subclinical rupture has a role in plaque progression. Circulation 2001;103:934-940.
29. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, Sarnacki S, Cumano A, Lauvau G, Geissmann F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 2007;317:666-670.
30. Nahrendorf M, Swirski FK, Aikawa E, Stangenberg L, Wurdinger T, Figueiredo J-L, Libby P, Weissleder R, Pittet MJ. The healing myocardium sequentially mobilizes two monocyte subsets with divergent and complementary functions. J Exp Med 2007; 204:3037-3047.
31. WongCW, Christen T, Roth I, Chadjichristos CE, Derouette J-P, Foglia BF, Chanson M, Goodenough DA, Kwak BR. Connexin37 protects against atherosclerosis by regulating monocyte adhesion. Nat Med 2006;12:950-954.
32. Lyon CA, Johnson JL, Williams H, Sala-Newby GB, George SJ. Soluble N-cadherin overexpression reduces features of atherosclerotic plaque instability. Arterioscler Thromb Vasc Biol 2009;29:195-201.
33. Koppisetti RK, Fulcher YG, Jurkevich A, Prior SH, Xu J, Lenoir M, Overduin M, Van Doren SR. Ambidextrous binding of cell and membrane bilayers by soluble matrix metalloproteinase-12. Nat Commun 2014;5:5552.
34. Newby AC. Metalloproteinase expression in monocytes and macrophages and its relationship to atherosclerotic plaque instability. Arterioscler Thromb Vasc Biol 2008;28: 2108-2114.
35. Moore Kathryn J, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell 2011;145:341-355.
36. Lemaître V, Soloway PD, DArmiento J. Increased medial degradation with pseudo-Aneurysm formation in apolipoprotein E-knockout mice deficient in tissue inhibitor of metalloproteinases-1. Circulation 2003;107:333-338.
37. Cuaz-Perolin C, Jguirim I, Larigauderie G, Jlassi A, Furman C, Moreau M, Chapman MJ, Fruchart JC, Slimane MN, Mezdour H, Rouis M. Apolipoprotein E knockout mice overexpressing human tissue inhibitor of metalloproteinase 1 are protected against aneurysm formation but not against atherosclerotic plaque development. J Vasc Res 2006;43: 493-501.
38. Silence J, Collen D, Lijnen HR. Reduced atherosclerotic plaque but enhanced aneurysm formation in mice with inactivation of the tissue inhibitor of metalloproteinase-1 (TIMP-1) gene. Circ Res 2002;90:897-903.
39. Rouis M, Adamy C, Duverger N, Lesnik P, Horellou P, Moreau M, Emmanuel F, Caillaud JM, Laplaud PM, Dachet C, Chapman MJ. Adenovirus-mediated overexpression of tissue inhibitor of metalloproteinase-1 reduces atherosclerotic lesions in apolipoprotein E-deficient mice. Circulation 1999;100:533-540.
40. Gogly B, Fournier B, Couty L, Naveau A, Brasselet C, Durand E, Coulomb B, Lafont A. Gingival fibroblast inhibits MMP-7: evaluation in an ex vivo aorta model. J Mol Cell Cardiol 2009;47:296-303.
41. Imanishi T, Han DKM, Hofstra L, Hano T, Nishio I, Liles WC, Gorden AM, Schwartz SA. Apoptosis of vascular smooth muscle cells is induced by Fas ligand derived from monocytes/macrophage. Atherosclerosis 2002;161:143-151.
42. Williams H, Johnson JL, Jackson CL, White SJ, George SJ. MMP-7 mediates cleavage of N-cadherin and promotes smooth muscle cell apoptosis. Cardiovasc Res 2010;87: 137-146.
43. Johnson JL, George SJ, Newby AC, Jackson CL. Divergent effects of matrix metalloproteinases-3,-7,-9 and-12 on atherosclerotic plaque stability in mouse brachiocephalic arteries. Proc Natl Acad Sci USA 2005;102:15575-15580.
44. Wang ZP, Soloway PD. TIMP-1 and TIMP-2 perform different functions in vivo. Ann NY Acad Sci 1999;878:519-521.
45. Johnson JL. Matrix metalloproteinases and their inhibitors in cardiovascular pathologies: current knowledge and clinical potential. Metalloproteinases Med 2014;1: 21-36.
46. Johnson JL, Jenkins NP, Huang W-C, Di Gregoli K, Sala-Newby GB, Scholtes VPW, Moll FL, Pasterkamp G, Newby AC. Relationship of MMP-14 and TIMP-3 expression with macrophage activation and human atherosclerotic plaque vulnerability. Mediat Inflamm 2014;2014:17.
47. Faveeuw C, Preece G, Ager A. Transendothelial migration of lymphocytes across high endothelial venules into lymph nodes is affected by metalloproteinases. Blood 2001;98: 688-695.
48. Kandalam V, Basu R, Abraham T, Wang X, Soloway PD, Jaworski DM, Oudit GY, Kassiri Z. TIMP2 deficiency accelerates adverse post-myocardial infarction remodeling because of enhanced MT1-MMP activity despite lack of MMP2 activation. Circ Res 2010; 106:796-808.
49. Gautier EL, Huby T, Witztum JL, Ouzilleau B, Miller ER, Saint-Charles F, Aucouturier P, Chapman MJ, Lesnik P. Macrophage apoptosis exerts divergent effects on atherogenesis as a function of lesion stage. Circulation 2009;119:1795-1804.
50. Uzui H, Harpf A, Liu M, Doherty TM, Shukla A, Chai N-N, Tripathi PV, Jovinge S, Wilkin DJ, Asotra K, Shah PK, Rajavashisth TB. Increased expression of membrane type 3-matrix metalloproteinase in human atherosclerotic plaque. Role of activated macrophages and inflammatory cytokines. Circ Res 2002;106:3024-3030.
51. Horozoglu C, Ozdes T, Erginel T, Unaltuna N. Expression of MMP-15 and MMP-24 in atherosclerotic and nonatherosclerotic coronary arteries. Metalloproteinases Med 2014;1:15-20.
52. Huang W-C, Sala-Newby GB, Susana A, Johnson JL, Newby AC. Classical macrophage activation up-regulates several matrix metalloproteinases through mitogen activated protein kinases and nuclear factor-kB. PLoS ONE 2012;7:e42507.
53. Ray BK, Shakya A, Turk JR, Apte SS, Ray A. Induction of the MMP-14 gene in macrophages of the atherosclerotic plaque. Circ Res 2004;95:1082-1090.
54. Sithu SD, English WR, Olson P, Krubasik D, Baker AH, Murphy G, DSouza SE. Membrane-Type 1-matrix metalloproteinase regulates intracellular adhesion molecule-1 (ICAM-1)-mediated monocyte transmigration. J Biol Chem 2007;282: 25010-25019.