Matrix metalloproteinase (MMP)-3 activates MMP-9 mediated vascular smooth muscle cell migration and neointima formation in mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 9, 2011, Pages

  Johnson, Jason L ^a   Dwivedi, Amrita ^a   Somerville, Michelle ^a   George, Sarah J ^a   Newby, Andrew C ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

genetically altered mice; metalloproteinases; restenosis; smooth muscle cells; vascular biology

Indexed keywords

GELATINASE B; SMALL INTERFERING RNA; STROMELYSIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAROTID ARTERY LIGATION; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEOINTIMA; NONHUMAN; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE; VASCULAR SMOOTH MUSCLE CELL;

ANIMALS; ATHEROSCLEROSIS; CAROTID ARTERIES; CELL MOVEMENT; MATRIX METALLOPROTEINASE 3; MATRIX METALLOPROTEINASE 9; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NEOINTIMA;

EID: 80052137568     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.225623     Document Type: Article

References (53)

1. Gerthoffer WT. Mechanisms of vascular smooth muscle cell migration. Circ Res. 2007;100:607-621. (Pubitemid 46594875)
2. Murry CE, Gipaya CT, Bartosek T, Benditt EP, Schwartz SM. Monoclonality of smooth muscle cells in human atherosclerosis. Am J Pathol. 1997;151:697-705.
3. Schwartz SM. Smooth muscle migration in atherosclerosis and restenosis. J Clin Invest. 1997;99:2814-2817. (Pubitemid 27278654)
4. Davies MJ, Richardson PD, Woolf N, Katz DR, Mann J. Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth-muscle cell content. Br Heart J. 1993;69: 377-381. (Pubitemid 23171108)
5. Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006;69:562-573. (Pubitemid 43139720)
6. Newby AC. Metalloproteinase expression in monocytes and macrophages and its relationship to atherosclerotic plaque instability. Arterioscler Thromb Vasc Biol. 2008;28:2108-2114.
7. Johnson JL. Matrix metalloproteinases: influence on smooth muscle cells and atherosclerotic plaque stability. Expert Rev Cardiovasc Ther. 2007; 5:265-282. (Pubitemid 46488141)
8. Newby AC. Matrix metalloproteinases regulate migration, proliferation, and death of vascular smooth muscle cells by degrading matrix and non-matrix substrates. Cardiovasc Res. 2006;69:614-624. (Pubitemid 43140745)
9. Kuzuya M, Kanda S, Sasaki T, Tamaya-Mori N, Cheng XW, Itoh T, Itohara S, Iguchi A. Deficiency of gelatinase a suppresses smooth muscle cell invasion and development of experimental intimal hyperplasia. Circulation. 2003;108:1375-1381. (Pubitemid 37174417)
10. Johnson C, Galis ZS. Matrix metalloproteinase-2 and-9 differentially regulate smooth muscle cell migration and cell-mediated collagen organization. Arterioscler Thromb Vasc Biol. 2004;24:54-60. (Pubitemid 38082411)
11. Cho A, Reidy MA. Matrix metalloproteinase-9 is necessary for the regulation of smooth muscle cell replication and migration after arterial injury. Circ Res. 2002;91:845-851. (Pubitemid 35285083)
12. Galis ZS, Johnson C, Godin D, Magid R, Shipley JM, Senior RM, Ivan E. Targeted disruption of the matrix metalloproteinase-9 gene impairs smooth muscle cell migration and geometrical arterial remodeling. Circ Res. 2002;91:852-859. (Pubitemid 35285084)
13. Kuzuya M, Nakamura K, Sasaki T, Cheng XW, Itohara S, Iguchi A. Effect of MMP-2 deficiency on atherosclerotic lesion formation in ApoEdeficient mice. Arterioscler Thromb Vasc Biol. 2006;26:1120-1125. (Pubitemid 43732121)
14. 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. (Pubitemid 41528098)
15. Ogata Y, Enghild JJ, Nagase H. Matrix metalloproteinase 3 (stromelysin) activates the precursor of the human matrix metalloproteinase 9. J Biol Chem. 1992;267:3581-3584.
16. Okada Y, Gonoji Y, Naka K, Tomita K, Nakanishi I, Iwata K, Yamashita K, Hayakawa T. Matrix metalloproteinase 9 (92-kDa gelatinase/type IV collagenase) from HT 1080 human fibrosarcoma cells: purification and activation of the precursor and enzymic properties. J Biol Chem. 1992; 267:21712-21719.
17. Shapiro SD, Fliszar CJ, Broekelmann TJ, Mecham RP, Senior RM, Welgus HG. Activation of the 92-kDa gelatinase by stromelysin and 4-aminophenylmercuric acetate: differential processing and stabilization of the carboxyl-terminal domain by tissue inhibitor of metalloproteinases (TIMP). J Biol Chem. 1995;270:6351-6356.
18. Webb KE, Henney AM, Anglin S, Humphries SE, McEwan JR. Expression of matrix metalloproteinases and their inhibitor TIMP-1 in the rat carotid artery after balloon injury. Arterioscler Thromb Vasc Biol. 1997;17:1837-1844. (Pubitemid 27424009)
19. Dwivedi A, Slater SC, George SJ. MMP-9 and-12 cause N-cadherin shedding and therebyα-catenin signalling and vascular smooth muscle cell proliferation. Cardiovasc Res. 2009;81:178-186.
20. Kumar A, Lindner V. Remodeling with neointima formation in the mouse carotid artery after cessation of blood flow. Arterioscler Thromb Vasc Biol. 1997;17:2238-2244. (Pubitemid 28057127)
21. Uglow EB, Slater S, Sala-Newby GB, Aguilera-Garcia CM, Angelini GD, Newby AC, George SJ. Dismantling of cadherin-mediated cell-cell contacts modulates smooth muscle cell proliferation. Circ Res. 2003;92: 1314-1321. (Pubitemid 36773473)
22. 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.
23. 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.
24. Jiang Z, Berceli SA, Pfahnl CL, Wu L, Killingsworth CD, Vieira FG, Ozaki CK. Impact of IL-1βon flow-induced outward arterial remodeling. Surgery. 2004;136:478-482. (Pubitemid 39037690)
25. 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.
26. Southgate KM, Davies M, Booth RFG, Newby AC. Involvement of extracellular-matrix-degrading metalloproteinases in rabbit aortic smooth-muscle cell proliferation. Biochem J. 1992;288:93-99.
27. Kenagy RD, Nikkari ST, Welgus HG, Clowes AW. Heparin inhibits the induction of three matrix metalloproteinases (stomelysin, 92-kD gelatinase, and collagenase) in primate arterial smooth muscle cells. J Clin Invest. 1994;93:1987-1993. (Pubitemid 24143077)
28. Lijnen HR, Van Hoef B, Lupu F, Moons L, Carmeliet P, Collen D. Function of the plasminogen/plasmin and matrix metalloproteinase systems after vascular injury in mice with targeted inactivation of fibrinolytic system genes. Arterioscler Thromb Vasc Biol. 1998;18: 1035-1045. (Pubitemid 28323587)
29. Bendeck MP, Zempo N, Clowes AW, Galardy RE, Reidy MA. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ Res. 1994;75:539-545. (Pubitemid 24256415)
30. Zempo N, Kenagy RD, Au T, Bendeck M, Clowes MM, Reidy MA, Clowes AW. Matrix metalloproteinases of vascular wall cells are increased in balloon-injured rat carotid. J Vasc Surg. 1994;20:209-217. (Pubitemid 24260589)
31. Southgate KM, Fisher M, Banning AP, Thurston VJ, Baker AH, Fabunmi RP, Groves PH, Davies M, Newby AC. Upregulation of basement membrane-degrading metalloproteinase secretion after balloon injury of pig carotid arteries. Circ Res. 1996;79:1177-1187. (Pubitemid 26404150)
32. Southgate KM, Mehta D, Izzat MB, Newby AC, Angelini GD. Increased secretion of basement membrane-degrading metalloproteinases in pig saphenous vein into carotid artery interposition grafts. Arterioscler Thromb Vasc Biol. 1999;19:1640-1649. (Pubitemid 29323822)
33. Bendeck MP, Irvin C, Reidy MA. Inhibition of matrix metalloproteinase activity inhibits smooth muscle cell migration but not neointimal thickening after arterial injury. Circ Res. 1996;78:38-43. (Pubitemid 26004118)
34. Zempo N, Koyama N, Kenagy RD, Lea HJ, Clowes AW. Regulation of vascular smooth muscle cell migration and proliferation in vitro and in injured rat arteries by a synthetic matrix metalloproteinase inhibitor. Arterioscler Thromb Vasc Biol. 1996;16:28-33. (Pubitemid 26026928)
35. Forough R, Koyama N, Hasenstab D, Lea H, Clowes M, Nikkari ST, Clowes AW. Overexpression of tissue inhibitor of matrix metalloprotienase-1 inhibits vascular smooth muscle cell functions in vitro and in vivo. Circ Res. 1996;79:812-820. (Pubitemid 26317829)
36. George SJ, Baker AH, Angelini GD, Newby AC. Gene transfer of tissue inhibitor of metalloproteinase-2 inhibits metalloproteinase activity and neointima formation in human saphenous veins. Gene Ther. 1998;5: 1552-1560. (Pubitemid 28517383)
37. George SJ, Johnson JL, Angelini GD, Newby AC, Baker AH. Adenovirus-mediated gene transfer of the human TIMP-1 gene inhibits SMC migration and neointima formation in human saphenous vein. Hum Gene Ther. 1998;9:867-877. (Pubitemid 28197373)
38. Cheng L, Mantile G, Pauly R, Nater C, Felici A, Monticone R, Bilato C, Gluzband YA, Crow MT, Stetler-Stevenson W, Capogrossi MC. Adenovirus-mediated gene transfer of the human tissue inhibitor of metalloproteinase-2 blocks vascular smooth muscle cell invasiveness in vitro and modulates neointimal development in vivo. Circulation. 1998; 98:2195-2201. (Pubitemid 28527480)
39. Dollery CM, Humphries SE, McClelland A, Latchman DS, McEwan JR. Expression of tissue inhibitor of matrix metalloproteinases 1 by use of an adenoviral vector inhibits smooth muscle cell migration and reduces neointimal hyperplasia in the rat model of vascular balloon injury. Circulation. 1999;99:3199-3205. (Pubitemid 29289087)
40. Furman C, Luo Z, Walsh K, Duverger N, Copin C, Fruchart JC, Rouis M. Systemic tissue inhibitor of metalloproteinase-1 gene delivery reduces neointimal hyperplasia in balloon-injured rat carotid artery. FEBS Lett. 2002;531:122-126. (Pubitemid 35341181)
41. Prescott MF, Sawyer WK, Von Linden-Reed J, Jeune M, Chou M, Caplan SL, Jeng AY. Effect of matrix metalloproteinase inhibition on progression of atherosclerosis and aneurysm in LDL receptor-deficient mice overexpressing MMP3, MMP-12, and MMP-13 and on restenosis in rats after balloon injury. Ann NY Acad Sci. 1999;878:179-190. (Pubitemid 29353569)
42. Filippov S, Koenig GC, Chun T-H, Hotary KB, Ota I, Bugge TH, Roberts JD, Fay WP, Birkedal-Hansen H, Holmbeck K, Sabeh F, Allen ED, Weiss SJ. MT1-matrix metalloproteinase directs arterial wall invasion and neointima formation by vascular smooth muscle cells. J Exp Med. 2005;5:663-671. (Pubitemid 41248417)
43. Mason DP, Kenagy RD, Hasenstab D, Bowen-Pope DF, Seifert RA, Coats S, Hawkins SM, Clowes AW. Matrix metalloproteinase-9 overexpression enhances vascular smooth muscle migration and alters remodeling in the injured rat carotid artery. Circ Res. 1999;85: 1179-1185. (Pubitemid 30430623)
44. Ramos-DeSimone N, Hahn-Dantona E, Sipley J, Nagase H, French DL, Quigley JP. Activation of matrix metalloproteinase-9 (MMP-9) via a converging plasmin/stromelysin-1 cascade enhances tumor cell invasion. J Biol Chem. 1999;274:13066-13076.
45. Legrand C, Polette M, Tournier J-M, de Bentzmann S, Huet E, Monteau M, Birembaut P. uPA/plasmin system-mediated MMP-9 activation is implicated in bronchial epithelial cell migration. Exp Cell Res. 2001;264: 326-336. (Pubitemid 32980237)
46. Devy L, Noël A, Baramova E, Bajou K, Trentesaux C, Jardillier J-C, Foidart J-M, Jeannesson P. Production and activation of matrix metalloprotease-9 (MMP-9) by HL-60 promyelocytic leukemia cells. Biochem Biophys Res Commun. 1997;238:842-846. (Pubitemid 27472663)
47. Hultgårdh-Nilsson A, Lovdahl C, Blomgren K, Kallin B, Thyberg J. Expression of phenotype-and proliferation-related genes in rat aortic smooth muscle cells in primary culture. Cardiovasc Res. 1997;34: 418-430. (Pubitemid 27241588)
48. Bond M, Chase AJ, Baker AH, Newby AC. Inhibition of transcription factor NF-B reduces matrix metalloproteinase-1,-3 and-9 production by vascular smooth muscle cells. Cardiovasc Res. 2001;50:556-565. (Pubitemid 32480249)
49. Janssens S, Lijnen HR. What has been learned about the cardiovascular effects of matrix metalloproteinases from mouse models? Cardiovasc Res. 2006;69:585-594. (Pubitemid 43139722)
50. Blindt R, Vogt F, Lamby D, Zeiffer U, Krott N, Hilger-Eversheim K, Hanrath P, vom Dahl J, Bosserhoff A-K. Characterization of differential gene expression in quiescent and invasive human arterial smooth muscle cells. J Vasc Res. 2002;39:340-352. (Pubitemid 34983865)
51. Castier Y, Ramkhelawon B, Riou S, Tedgui A, Lehoux S. Role of NF-B in flow-induced vascular remodelling. Antioxid Redox Sign. 2009;11: 1641-1649.
52. 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. (Pubitemid 26144227)
53. Luttun A, Lutgens E, Manderveld A, Maris K, Collen D, Carmeliet P, Moons L. Loss of matrix metalloproteinase-9 or matrix metalloproteinase-12 protects apolipoprotein E-deficient mice against atherosclerotic media destruction but differentially affects plaque growth. Circulation. 2004;109:1408-1414. (Pubitemid 38387828)