Molecular mechanisms in intimal hyperplasia

Journal of Pathology

Volumn 190, Issue 3, 2000, Pages 300-309

  Newby, Andrew C ^a   Zaltsman, Alla B ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Growth factors; Metalloproteinases; Migration; Proliferation; Vascular smooth muscle

Indexed keywords

GROWTH FACTOR; MATRIX METALLOPROTEINASE; SCLEROPROTEIN;

ANGIOPLASTY; ARTERY INTIMA PROLIFERATION; ARTERY WALL; ATHEROSCLEROSIS; CELL MIGRATION; CELL PROLIFERATION; DUCTUS ARTERIOSUS; PRIORITY JOURNAL; PULMONARY HYPERTENSION; REVIEW; VASCULAR SMOOTH MUSCLE; VEIN GRAFT;

CELL DIVISION; CELL MOVEMENT; ENDOTHELIAL GROWTH FACTORS; HUMANS; HYPERPLASIA; METALLOENDOPEPTIDASES; MUSCLE, SMOOTH, VASCULAR; TUNICA INTIMA;

EID: 0034007969     PISSN: 00223417     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9896(200002)190:3<300::AID-PATH596>3.0.CO;2-I     Document Type: Review

References (159)

1. Timpl R. Macromolecular organization of basement membrane. Curr Opin Cell Biol 1996; 8: 618-624.
2. Woods A, Oh ES, Couchman JR Syndecan proteoglycans and cell adhesion. Matrix Biol 1998; 17: 477-483.
3. Stary HC. The sequence of cell and matrix changes in atherosclerotic lesions of coronary arteries in the first forty years of life. Eur Heart J 1990; 11 (Suppl E): 3-19.
4. Wight T. The extracellular matrix and atherosclerosis. Curr Opin Lipidol 1995; 6: 326-334.
5. Wight TN. The vascular extracellular matrix. In Atherosclerosis and Coronary Artery Disease, Faster V, Ross R, Topol EJ (eds). Lippincolt-Raven: Philadelphia, 1996; 421-440.
6. Slomp J, van Munsteren JC, Poelman RE, de Reeder EG, Bogers AJJC, Gittenberger-deGroot AC. Formation of intimal cushions in the ductus arteriosus as a model for vascular intimal thickening. An immunohistochemical study of changes in extracellular matrix components. Atherosclerosis 1992; 93: 25-39.
7. Orekhov AN, Karpova II, Tertov VV, et al. Cellular composition of atherosclerotic and uninvolved human aortic subendothelial intima: light microscopic study of dissociated aortic cells. Am J Pathol 1984; 115: 17-24.
8. Weiser MCM, Majack RA, Tucker A, Orton EC. Static tension is associated with increased smooth muscle cell DNA synthesis in rat pulmonary arteries. Am J Physiol 1995; 268: H1133-H1138.
9. Ip JH, Fuster V, Badimon L, Badimon J, Taubman MB, Chesebro JH. Syndromes of accelerated atherosclerosis: role of vascular injury and smooth muscle cell proliferation. J Am Coll Cardiol 1990; 15: 1667-1687.
10. Salomon RN, Hughes CCW, Schoen FJ, Payne DB, Pober JS, Libby P. Human transplant coronary arteriosclerosis: evidence for a chronic immune reaction to activated graft endothelium. Am J Pathol 1991; 138: 791-798.
11. Dilley RJ, McGeachie JK, Prendergast FJ. A review of the histological changes in vein to artery grafts, with particular reference to intimal hyperplasia. Arch Surg 1988; 123: 691-696.
12. Angelini GD, Newby AC. The future of saphenous vein as a coronary artery bypass conduit. Eur Heart J 1989; 10: 273-280.
13. Davies MJ, Woolf N. Atherosclerosis in Ischaemic Heart Disease. The Mechanism. Science Press: London, 1990.
14. Ross R. Mechanisms of disease - atherosclerosis - an inflammatory disease. N Engl J Med 1999; 340: 115-126.
15. Schwartz S, Campbell G, Campbell J. Replication of smooth muscle cells in vascular disease. Circ Res 1986; 58: 427-444.
16. O'Brien ER, Alpers CE, Stewart DK, et al. Proliferation in primary and restenotic coronary atherectomy tissue: implications for antiproliferative therapy. Circ Res 1993; 73: 223-231.
17. Bjorkerud S, Bjorkerud B. Apoptosis is abundant in human atherosclerotic lesions, especially in inflammatory cells (macrophages and T cells), and may contribute to the accumulation of gruel and plaque instability. Pathology 1996; 149: 369-380.
18. Geng Y-J, Libby P. Evidence for apoptosis in advanced human atheroma. Colocalization with interleukin-1β-coverting enzyme. Am J Pathol 1995; 147: 251-266.
19. Clowes AW, Reidy MA, Clowes MM. Kinetics of cellular proliferation after arterial injury. Smooth muscle growth in the absence of endothelium. Lab Invest 1983; 49: 327-333.
20. Campbell GR, Campbell JH. Smooth muscle phenotypic changes in arterial wall hemostasis: implications for the pathogenesis of atherosclerosis. Exp Mol Pathol 1985; 42: 139-162.
21. Chamley-Campbell JH, Campbell GR. What controls smooth muscle phenotype? Atherosclerosis 1981; 40: 347-357.
22. Thyberg J. Phenotypic modulation of smooth muscle cells during formation of neointimal thickenings following vascular injury. Histol Histopathol 1998; 13: 871-891.
23. Ang AH, Tachas G, Campbell JH, Bateman JF, Campbell GR. Collagen synthesis by cultured rabbit aortic smooth muscle cells. Biochem J 1990; 265: 461-469.
24. Thyberg J. Differentiated properties and proliferation of arterial smooth muscle cells in culture. Int Rev Cytol 1996; 169: 183-265.
25. Savani R, Wang C, Yang B, et al. Migration of bovine aortic smooth muscle cells after wounding injury the role of hyaluronan and rhamm. J Clin Invest 1995; 95: 1158-1168.
26. Thyberg J, Blomgren K, Roy J, Tran PK, Hedin U. Phenotypic modulation of smooth muscle cells after arterial injury is associated with changes in the distribution of laminin and fibronectin. J Histochem Cytochem 1997; 45: 837-846.
27. Koyama H, Raines EW, Bornfeldt KE, Roberts JM. Ross R. Fibrillar collagen inhibits arterial smooth muscle cell proliferation through regulation of Cdk2 inhibitors. Cell 1996; 87: 1069-1078.
28. Grainger DJ, Hesketh TR, Metcalfe JC, Weissberg PL. A large accumulation of nonmuscle myosin occurs at first entry into M-phase in rat vascular smooth-muscle cells. Biochem J 1991; 277: 145-151.
29. Pines J. Cyclins and cyclin-dependent kinases: a biochemical view. Biochem J 1995; 308: 697-711.
30. Sherr CJ, Roberts JM. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 1995; 9: 1149-1163.
31. Li JM, Brooks G. Cell cycle regulatory molecules (cyclins, cyclin-dependent kinases and cyclin-dependent kinase inhibitors) and the cardiovascular system potential targets for therapy? Eur Heart J 1999; 20: 406-420.
32. Ullrich A, Schlessinger J. Signal transduction by receptors with tyrosine kinase activity. Cell 1990; 61: 203-212.
33. Cadena DL, Gill GN. Receptor tyrosine kinases. FASEB J 1992; 6: 2332-2337.
34. Davis RJ. MAPKs: new JNK expands the group. Trends Biochem Sci 1994; 19: 470-473.
35. Seger R, Krebs EG. The MAPK signalling cascade. FASEB J 1995; 9: 726-735.
36. Marte BM, Downward J. PKB/Akt: connecting phosphoinositide 3-kinase to cell survival and beyond. Trends Biochem Sci 1997; 22: 355-358.
37. Coffer PJ, Jin J, Woodgett JR Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem J 1998; 335: 1-13.
38. Chan TO, Rittenhouse SE, Tsichlis PN. AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide-dependent phosphorylation. Annu Rev Biochem 1999; 68: 965-1014.
39. Berra E, DiazMeco MT, Dominguez I, et al. Protein kinase C zeta isoform is critical for mitogenic signal transduction. Cell 1993; 74: 555-563.
40. Newby AC, Lim K, Evans MA, Booth RFG. Inhibition of rabbit aortic smooth muscle cell proliferation by selective inhibitors of protein kinase C. Br J Pharmacol 1995; 114: 1652-1656.
41. Leszczynski D, Joenvaara S, Foegh ML. Protein kinase c-alpha regulates proliferation but not apoptosis in rat coronary vascular smooth muscle cells. Life Sci 1996; 58: 599-606.
42. Liao DF, Monia B, Dean N, Berk BC. Protein kinase C-zeta mediates angiotensin II activation of ERK1/2 in vascular smooth muscle cells. J Biol Chem 1997; 272: 6146-6150.
43. Nakajima T, Kitajima I, Shin H, et al. Involvement of NF-κB activation in thrombin-induced human vascular smooth muscle cell proliferation. Biochem Biophys Res Commun 1994; 204: 950-955.
44. Autieri MV, Yue TL, Fernstein GZ, Ohlstein E. Antisense oligonucleotides to the p65 subunit of NF-kappaB inhibit human vascular smooth muscle cell adherence and proliferation and prevent neointima formation in rat carotid arteries. Biochem Biophys Res Commun 1995; 213: 827-836.
45. Bellas RE, Lee JS, Sonenshein GE. Expression of a constitutive NF-κB-like activity is essential for proliferation of cultured bovine vascular smooth muscle cells. J Clin Invest 1995; 96: 2521-2527.
46. Selzman CH, Shames BD, McIntyre RC, Banerjee A, Harken AH. The NF kappa B inhibitory peptide, I kappa B alpha, prevents human vascular smooth muscle proliferation. Ann Thorac Surg 1999; 67: 1227-1231.
47. Barone MV, Courtneidge SA. Myc but not Fos rescue of PDGF signalling block caused by kinase-inactive Src. Nature 1995; 378: 509-512.
48. Duff JL, Marrero MB, Paxton WG, Schieffer B, Bernstein KE, Berk BD. Angiotensin II signal transduction and the mitogen-activated protein kinase pathway. Cardiovasc Res 1995; 30: 511-517.
49. Malarkey K, Belham CM, Paul A, Graham A, McLees A, Scott PH. The regulation of tyrosine kinase signalling pathways by growth factor and G-protein-coupled receptors. Biochem J 1995; 309: 361-375.
50. Liao DF, Duff JL, Daum G, Pelech SL, Berk BC. Angiotensin-II stimulates MAP kinase activity in vascular smooth-muscle cells role of raf. Circ Res 1996; 79: 1007-1014.
51. Post GR, Brown JH. G protein-coupled receptors and signalling pathways regulating growth responses. FASEB J 1996; 10: 741-749.
52. Newby AC, George SJ. Proposed roles for growth factors in mediating smooth muscle proliferation in vascular pathologies. Cardiovasc Res 1993; 27: 1173-1183.
53. Lavoie JN, Lallemain G, Brunet A, Muller R, Pouyssegur J. Cyclin D1 expression is regulated positively by the p42/ p44(MAPK) and negatively by the p38/HOG(MAPK) pathway. J Biol Chem 1996; 271: 20608-20616.
54. Assoian RK, Marcantonio EE. The extracellular matrix as a cell cycle control element in atherosclerosis and restenosis. J Clin Invest 1996; 98: 2436-2439.
55. Assoian RK. Anchorage-dependent cell cycle progression. J Cell Biol 1997; 136: 1-4.
56. Assoian RK, Zhu X. Cell anchorage and the cytoskeleton as partners in growth factor dependent cell cycle progression. Curr Opin Cell Biol 1997; 9: 93-98.
57. Hedin U, Bottger BA, Forsberg E, Johansson S, Thyberg J. Diverse effects of fibronectin and laminin on phenotypic properties of cultured smooth muscle cells. J Cell Biol 1988; 107: 307-319.
58. Au YPT, Dobrowolska G, Morris DR, Clowes AW. Heparin decreases activator protein-1 binding to DNA in part by posttranslational modification of Jun B. Circ Res 1994; 75: 15-22.
59. Wang Y, Kovanen P. Heparin proteoglycans released from rat serosal mast cells inhibit proliferation of rat aortic smooth muscle cells in culture. Circ Res 1999; 84: 74-83.
60. Newby AC, Southgate KM, Assender JW. Inhibition of vascular smooth muscle cell proliferation by endothelium-dependent vasodilators. Herz 1992; 17: 291-299.
61. Jeremy JY, Rowe D, Emsley AM, Newby AC. Nitric oxide and the proliferation of vascular smooth muscle cells. Cardiovasc Res 1999; 43: 580-594.
62. Cospedal R, Lobo M, Zachary I. Differential regulation of extracellular signal-regulated protein kinases (ERKs) 1 and 2 by cAMP and dissociation of ERK inhibition from anti-mitogenic effects in rabbit vascular smooth muscle cells. Biochem J 1999; 342: 407-414.
63. 1. Exp Cell Res 1985; 160: 117-125.
64. Kahan C, Seuwen K, Meloche S, Pouyssegur J. Coordinate biphasic activation of p44 mitogen-activated protein kinase and S6 kinase by growth factors in hamster fibroblasts. Evidence for thrombin-induced signals different from phosphoinositide turn-over and adenylylcyclase inhibition. J Biol Chem 1992; 267: 13369-13375.
65. Lallemain G, Lavoie JN, Rivard N, Baldin V, Pouyssegur J. Cyclin D1 expression is a major target of the cAMP-induced inhibition of cell cycle entry in fibroblasts. Oncogene 1997; 14: 1981-1990.
66. Bennett MR, Littlewood TD, Hancock DC, Evan GI, Newby AC. Down-regulation of the c-myc proto-oncogene in arrest of rat aortic vascular smooth muscle cell proliferation different effects of mitogen withdrawal, heparin, interferon-gamma and cyclic nucleotide analogues. Biochem J 1994; 302: 701-708.
67. McCaffrey TA, Consigli S, Du B, et al. Decreased type II/type I TGF-β receptor ratio in cells derived from human atherosclerotic lesions. Conversion from an antiproliferative to profibrotic response to TGF-β. J Clin Invest 1995; 96: 2667-2675.
68. Abedi H, Zachary I. Signalling mechanisms in the regulation of vascular cell migration. Cardiovasc Res 1995; 30: 544-556.
69. Bilato C, Pauly RR, Melillo G, et al. Intracellular signalling pathways required for rat vascular smooth muscle cell migration. J Clin Invest 1995; 96: 1905-1915.
70. Lundberg MS, Curto KA, Bilato C, Monticone RE, Crow MT. Regulation of vascular smooth muscle migration by mitogen-activated protein kinase and calcium/calmodulin-dependent protein kinase II signalling pathways. J Mol Cell Cardiol 1998; 30: 2377-2389.
71. Bilato C, Curto KA, Monticone RE, Pauly RR, White AJ, Crow MT. Inhibition of vascular smooth muscle cell migration by peptide and antibody antagonists of the alpha(v)beta(3) integrin complex is reversed by activated calcium/calmodulin-dependent protein kinase II. J Clin Invest 1997; 100: 693-704.
72. Pauly RR, Bilato C, Sollott SJ, et al. The role of calcium/ calmodulin-dependent protein kinase II in the regulation of vascular smooth muscle cell migration. Circulation 1995; 91: 1107-1115.
73. Aspenstrom P. The Rho GTPases have multiple effects on the actin cytoskeleton. Exp Cell Res 1999; 246: 20-25.
74. Denhardt DT. Signal-transducing protein phosphorylation cascades mediated by Ras/Rho proteins in the mammalian cell: the potential for multiplex signalling. Biochem J 1996; 318: 729-747.
75. Mackay DJG, Hall A. Rho GTPases. J Biol Chem 1998; 273: 20685-20688.
76. Symons M. Rho family GTPases: the cytoskeleton and beyond. Trends Biochem Sci 1996; 21: 178-181.
77. Jockusch BM, Bubeck P, Giehl K, et al. The molecular architecture of focal adhesions. Annu Rev Cell Dev Biol 1995; 11: 379-416.
78. Craig SW, Johnson RP. Assembly of focal adhesions: progress, paradigms, and portents. Curr Opin Cell Biol 1996; 8: 74-85.
79. Zwolak RM, Adams MC, Clowes AW. Kinetics of vein graft hyperplasia: association with tangential stress. J Vasc Surg 1987; 5: 126-136.
80. Booth R, Martin JF, Honey AC, Hassel DG, Beesley JE, Moncada S. Rapid development of atherosclerotic lesions in the rabbit carotid artery induced by perivascular manipulation. Atherosclerosis 1989; 76: 257-268.
81. Soyombo AA, Angelini GD, Bryan AJ, Jasani B, Newby AC. Intimal proliferation in an organ culture of human saphenous vein. Am J Pathol 1990; 137: 1401-1410.
82. Reidy MA, Silver M. Endothelial regeneration - lack of intimal proliferation after defined injury to rat aortas. Am J Pathol 1985; 118: 173-177.
83. Fingerle J, Au YPT, Clowes AW, Reidy MA. Intimal lesion formation in rat carotid arteries after endothelial denudation in absence of medial injury. Arteriosclerosis 1990; 10: 1082-1087.
84. Clowes AW, Clowes MM, Fingerle J, Reidy MA. Kinetics of cellular proliferation after arterial injury role of acute distension in the induction of smooth muscle proliferation. Lab Invest 1989; 60: 360-364.
85. Jackson CL. Animal models of restenosis. Trends Cardiovasc Mcd 1994; 4: 122-130.
86. Shi Y, Obrien JE, Fard A, Mannion JD, Wang D, Zalewski A. Adventitial myofibroblasts contribute to neointimal formation in injured porcine coronary arteries. Circulation 1996; 94: 1655-1664.
87. Fager G. Thrombin and proliferation of vascular smooth muscle cells. Circ Res 1995; 77: 645-650.
88. Fingerle J, Johnson R, Clowes AW, Majesky MW, Reidy MA. Role of platelets in smooth muscle cell proliferation and migration after vascular injury in rat carotid artery. Proc Natl Acad Sci U S A 1989; 86: 8412-8416.
89. Ferns GAA, Raines EW, Sprugel KH, Motani AS, Reidy MA, Ross R. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science 1991; 253: 1129-1132.
90. George SJ, Williams AW, Newby AC. An essential role for platelet-derived growth factor in neointima formation in human saphenous vein in vitro. Atherosclerosis 1996; 120: 227-240.
91. Lindner V, Reidy MA. Proliferation of smooth muscle cells after vascular injury is inhibited by an antibody against basic fibroblast growth factor. Proc Natl Acad Sci U S A 1991; 88: 3739-3743.
92. Olson NE, Chao S, Lindner V, Reidy MA. Intimal smooth muscle cell proliferation after balloon catheter injury: the role of basic fibroblast growth factor. Am J Pathol 1992; 140: 1017-1023.
93. Cercek B, Fishbein MC, Forrester JS, Helfant RH, Fagin JA. Induction of insulin-like growth factor I messenger RNA in rat aorta after balloon denudation. Circ Res 1990; 66: 1755-1760.
94. Bornfeldt KE, Arnqvist HJ, Capron L. In vivo proliferation of rat vascular smooth muscle in relation to diabetes mellitus insulin-like growth factor I and insulin. Diabetologia 1992; 35: 104-108.
95. Kanthou C, Benzahour O, Patel G, Deadman J, Kakkar VV, Lupu F. Thrombin receptor activating peptide (TRAP) stimulates mitogenesis, c-fos and PDGF-A gene expression in human vascular smooth muscle cells. Thromb Haemostas 1995; 74: 1340-1347.
96. Malloy CJ, Pawlowski JE, Taylor DS, et al. Thrombin receptor activation elicits rapid protein tyrosine phosphorylation and stimulation of the Raf-1/MAP kinase pathway preceding delayed mitogenesis in cultured rat aortic smooth muscle cells. Evidence for an obligate autocrine mechanism promoting cell proliferation induced by G protein-coupled receptor agonists. J Clin Invest 1996; 97: 1173-1183.
97. Weissberg PL, Witchell C, Davenport AP, Hesketh TR, Metcalfe JC. The endothelin peptides ET-1, ET-2, ET-3 and sarafotoxin S6b are co-mitogenic with platelet-derived growth factor for vascular smooth muscle cells. Atherosclerosis 1990; 85: 257-262.
98. Powell JS, Clozel J-P, Müller RKM, et al. Inhibitors of angiotensin-converting enzyme prevent myointimal proliferation after vascular injury. Science 1989; 245: 186-188.
99. Daemen MJAP, Lombardi DM, Bosman FT, Schwartz SM. Angiotensin II induces smooth muscle cell proliferation in the normal and injured rat arterial wall. Circ Res 1991; 68: 450-456.
100. Davies M, Woolf N, Rowles P. Morphology of the endothelium over atherosclerotic plaques in human coronary arteries. Br Heart J 1988; 60: 459-464.
101. Falk E, Fuster V. Angina pectoris and disease progression. Circulation 1995; 92: 2033-2035.
102. Geng Y-J, Wu Q, Muszynski M, Hansson GK, Libby P. Apoptosis of vascular smooth muscle cells induced by in vitro stimulation with interferon-γ, tumor necrosis factor-α, and interleukin-1β. Arterioscler Thromb Vasc Biol 1996; 16: 19-27.
103. Jawien A, Bowen-Pope DF, Linder V, Schwartz SM, Clowes AW. Platelet-derived growth factor promotes smooth muscle migration and intimal thickening in a rat model of balloon angioplasty. J Clin Invest 1992; 89: 507-511.
104. Lindner V, Majack RA, Reidy MA. Basic fibroblast growth factor stimulates endothelial regrowth and proliferation in denuded arteries. J Clin Invest 1990; 85: 2004-2008.
105. Fingerle J, Kraft T. The induction of smooth muscle cell proliferation in vitro using an organ culture system. Int Angiol 1987; 6: 65-72.
106. Soyombo AA, Angelini GD, Bryan AJ, Newby AC. Surgical preparation induces injury and promotes smooth muscle cell proliferation in a culture of human saphenous vein. Cardiovasc Res 1993; 27: 1961-1967.
107. Fitzgerald M, Hayward IP, Thomas AC, Campbell GR, Campbell JH. Matrix metalloproteinases can facilitate the heparanase-induced promotion of phenotypic change in vascular smooth muscle cells. Atherosclerosis 1999; 145: 97-106.
108. Bingley J, Hayward I, Campbell J, Campbell G. Arterial heparan sulfate proteoglycans inhibit vascular smooth muscle cell proliferation and phenotype change in vitro and neointimal formation in vivo. J Vasc Surg 1998; 28: 308-318.
109. Reidy MA, Irvin C, Lindner V. Migration of arterial wall cells: expression of plasminogen activators and inhibitors in injured rat arteries. Circ Res 1996; 78: 405-414.
110. Bendeck MP, Zempo N, Clowes AW, Gelardy RE, Reidy MA. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ Res 1994; 75: 539-545.
111. Zempo N, Kenagy RD, Au T, et al. Matrix metalloproteinases of vascular wall cells are increased in balloon-injured rat carotid artery. J Vasc Surg 1994; 20: 209-217.
112. Southgate KM, Fisher M, Banning AP, et al. Upregulation of basement-membrane-degrading metalloproteinase secretion following balloon angioplasty of pig carotid arteries. Circ Res 1996; 79: 1177-1187.
113. Jackson CL, Reidy MA. The role of plasminogen activation in smooth muscle cell migration after arterial injury. Ann N Y Acad Sci 1992; 667: 141-150.
114. 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.
115. 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 metalloproteinases inhibitor. Arterioscler Thromb Vasc Biol 1996; 16: 28-33.
116. George SJ, Angelini GD, Newby AC, Baker AH. Adenovirus mediated gene transfer of the human TIMP-1 gene inhibits smooth muscle cell migration and neointima formation in human saphenous vein. Hum Gene Ther 1998; 9: 867-877.
117. 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.
118. Galis ZS. Muszynski M, Sukhova GK, et al. Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of extracellular enzymes required for extracellular matrix degradation. Circ Res 1994; 75: 181-189.
119. Kishi J-I, Hayakawa T. Synthesis of latent collagenase and collagenase inhibitor by bovine aortic medial explants and cultured medial smooth muscle cells. Connective Tissue Res 1989; 19: 63-76.
120. Fabunmi RP, Baker AH, Murray EJ, Booth RFG, Newby AC. Divergent regulation by growth factors and cytokines of 95-kDa and 72-kDa gelatinases and tissue inhibitors of metalloproteinases-1, -2 and -3 in rabbit aortic smooth muscle cells. Biochem J 1996; 315: 335-342.
121. Sukhova GK, Shi GP, Simon DI, Chapman HA, Libby P. Expression of the elastolytic cathepsins S and K in human atheroma and regulation of their production in smooth muscle cells. J Clin Invest 1998; 102: 576-583.
122. Blobel C. Metalloprotease-disintegritis: links to cell adhesion and cleavage of TNFα and Notch. Cell 1997; 90: 589-592.
123. Herren B, Coats S, BowenPope DF, Raines EW, Ross R. Overexpression of a metalloproteinase-disintegrin, MDC15, in NIH3T3 cells inhibits cell migration of fibronectin, but not cell-matrix attachment. Mol Biol Cell 1997; 8: 1052-1052.
124. Ross R, Masuda J, Raines EW, et al. Localization of PDGF-B protein in macrophages in all phases of atherogenesis. Science 1990; 248: 1009-1012.
125. Rouis M, Nigon F, Lafuma C, Hornebeck W, Chapman MJ. Expression of elastase activity by human monocyte-macrophages is modulated by cellular cholesterol content, inflammatory mediators, and phorbol myristate acetate. Arteriosclerosis 1990; 10: 246-255.
126. Galis ZS, Sukhova GK, Kranzhöfer R, Clark S, Libby P. Macrophage foam cells from experimental atheroma constitutively express matrix-degrading proteases. Proc Natl Acad Sci USA 1995; 92: 402-406.
127. Brown D, Hibbs M, Kearney M, Loushin C, Isner JM. Identification of 92-kDa gelatinase in human coronary atherosclerotic lesions. Association of active enzyme synthesis with unstable angina. Circulation 1995; 91: 2125-2131.
128. Mach F, Schonbeck U, Sukhova GK, Bonnefoy JY, Libby P. Ligation of CD40 on macrophage induces matrix metalloproteinases and tissue factor expression. Atherosclerosis 1997; 134: 280-281.
129. Mach F, Schonbeck U, Bonnefoy J-Y, 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: 393-399.
130. Aikawa M, Voglic SJ, Rabkin E, Shiomi M, Libby P. An HMG-CoA reductase inhibitor (cerivastatin) suppresses accumulation of macrophages expressing matrix metalloproteinases and tissue factor in atheroma of WHHL rabbits. Circulation 1998; 98: 231
131. Hansson GK, Jonasson L, Lojsthed B. Stemme S, Koche O, Gabbiani G. Localisation of T lymphocytes and macrophages in fibrous and complicated human atherosclerotic plaques. Atherosclerosis 1988; 72: 135-141.
132. Cybulsky MI, Gimbrone MA. Endothelial expression of a mononuclear leukocyte adhesion molecule during atherogenesis. Science 1991; 251: 788-791.
133. Anitschkow N, Chalatow S. Uber experimentelle cholesterinsteatose und ihre bendeutung fur die enstehung einiger. Pathologischer prozess. Allg Pathol Anat 1913; 24: 1-13.
134. Newby A, Zaltsman AB. Fibrous cap formation or destruction - the critical importance of vascular smooth muscle cell proliferation, migration and matrix formation. Cardiovasc Res 1999; 41: 345-360.
135. Aikawa M, Rabkin E, Voglic SJ, et al. Lipid lowering promotes accumulation of mature smooth muscle cells expressing smooth muscle myosin heavy chain isoforms in rabbit atheroma. Circ Res 1998; 83: 1015-1026.
136. Faggiotto A, Ross R, Harker L. Studies of hypercholesterolaemia in the non-human primate. 1. Changes that lead to fatty streak formation. Arteriosclerosis 1984; 4: 323-340.
137. Faggiotto A, Ross R. Studies of hypercholesterolaemia in the non-human primate. 2. Fatty streak conversion to fibrous plaque. Arteriosclerosis 1984; 4: 341-356.
138. Masuda J, Ross R. Atherogenesis during low level hypercholesterolemia in the nonhuman primate. 1. Fatty streak formation. Arteriosclerosis 1990; 10: 164-177.
139. Masuda J, Ross R. Atherogenesis during low level hypercholesterolemia in the nonhuman primate. 2. Fatty streak conversion to fibrous plaque. Arteriosclerosis 1990; 10: 178-187.
140. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoE-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb 1994; 14: 133-140.
141. Wilcox JN, Smith KM, Williams LT, Schwartz SM, Gordon D. Platelet-derived growth factor mRNA detection in human atherosclerotic plaques by in situ hybridization. J Clin Invest 1988; 82: 1134-1143.
142. 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.
143. Sarén P, Welgus HG, Kovanen PT. TNF-α and IL-1β selectively induce expression of 92-kDa gelatinase by human macrophages. J Immunol 1996; 157: 4159-4165.
144. Mach F, Schonbeck U, Sukhova GK, Atkinson E, Libby P. Reduction of atherosclerosis in mice by inhibition of CD40 signalling. Nature 1998; 394: 200-203.
145. Hansson GK, Jonasson L, Holm J, Clowes MM, Clowes AW. γ Interferon regulates vascular smooth muscle proliferation and Ia antigen expression in vivo and in vitro. Circ Res 1988; 63: 712-719.
146. Amento EP, Ehsani N, Palmer H, Libby P. Cytokines and growth factors positively and negatively regulate interstitial collagen gene expression in human vascular smooth muscle cells. Arterioscler Thromb 1991; 11: 1223-1230.
147. Francis SE, Hunter S. Holt CM, et al. Release of platelet derived growth factor activity from arteriovenous by-pass grafts. J Thorac Cardiovasc Surg 1994; 108: 540-548.
148. 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.
149. Mehta D, George SJ, Jeremy JY, et al. External stenting reduces long term medial and neointimal thickening and platelet derived growth factor expression in a pig model of arteriovenous bypass grafting. Nature Med 1998; 4: 235-239.
150. Zhou Y, Dietrich H, Yanhua H, Metzler B, Wick G, Xu Q. Mouse model of vein bypass graft arteriosclerosis. Am J Pathol 1998; 153: 1301-1310.
151. Leung DYM, Glagov S, Mathews MB. Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro. Science 1976; 191: 475-477.
152. Banes AJ, Baird CW, Dorofi D, et al. Cyclic mechanical load and growth factors stimulate endothelial and smooth muscle cell DNA synthesis. Eur Respir Rev 1993; 3: 618-622.
153. Angelini GD, Passani SL, Breckenridge IM, Newby AC. Nature and pressure dependence of damage induced by distension of human saphenous vein coronary artery bypass grafts. Cardiovasc Res 1987; 21: 902-907.
154. Shi Y, O'Brien JE, Mannion JD, et al. Remodeling of autologous saphenous vein grafts. The role of perivascular myofibroblasts. Circulation 1997; 95: 2684-2693.
155. Koyama N, Koshikawa T, Morisaki N, Saito Y, Yoshida S. Secretion of a potent new migration factor for smooth muscle cells (SMC) by cultured SMC. Atherosclerosis 1991; 86: 219-226.
156. DiMilla P, Stone J, Quinn J, Albelda S, Lauffenburger D. Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J Cell Biol 1993; 122: 729-737.
157. Liaw L, Skinner MP, Raines EW, et al. Adhesive and migratory effects of osteopontin are mediated via distinct cell-surface integrins role of alpha(V)beta(3) in smooth-muscle cell-migration to osteopontin in-vitro. J Clin Invest 1995; 95: 713-724.
158. Naito M, Hayasi T, Funaki C, Kuzuya M, Asai K, Kuzuya F. Vitronectin-induced haptotaxis of vascular smooth muscle cells in vitro. Exp Cell Res 1991; 194: 154-156.
159. Brown E, Landgren C, Nordt T, Fujii S. Stimulation of migration of human aortic smooth muscle cells by vitronectin: implications for atherosclerosis. Cardiovasc Res 1994; 28: 1815-1820.