Endothelial cell injury in cardiovascular surgery: The intimal hyperplastic response

Annals of Thoracic Surgery

Volumn 63, Issue 2, 1997, Pages 582-591

  Allaire, Eric ^a   Clowes, Alexander W ^a  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD FLOW; CARDIOVASCULAR SURGERY; CELL PROLIFERATION; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; HYPERPLASIA; PRIORITY JOURNAL; REVIEW;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BLOOD VESSEL PROSTHESIS; CELL DIVISION; ENDOTHELIUM, VASCULAR; HUMANS; HYPERPLASIA; REGIONAL BLOOD FLOW; TUNICA INTIMA;

EID: 0031057769     PISSN: 00034975     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0003-4975(96)01045-4     Document Type: Review

References (112)

1. Grondin CM, Campeau L, Lesperance J, Enjalbert M, Bourassa MG. Comparison of late changes in internal mammary artery and saphenous vein grafts in two consecutive series of patients 10 years after operation. Circulation 1984;70(Suppl 1):208-12.
2. Gurlek A, Dagalp Z, Oral D, et al. Restenosis after transluminal coronary angioplasty: a risk factor analysis. J Cardiovasc Risk 1995;2:51-5.
3. Echave V, Koornick AR, Haimov M, Jacobson JH. Intimal hyperplasia as a complication of the use of the polytetrafluoroethylene graft for femoral-popliteal bypass. Surgery 1979;86:791-8.
4. Becquemin JP, Cavillon A, Haiduc F. Surgical transluminal femoropopliteal angioplasty: multivariate analysis outcome. J Vasc Surg 1994;19:495-502.
5. Davies MG, Hagen PO. The vascular endothelium. A new horizon. Ann Surg 1993;218:593-609.
6. Busse R, Mulsch A, Fleming I, Hecker M. Mechanisms of nitric oxide release from the vascular endothelium. Circulation 1993;87(Suppl 5):18-25.
7. Springer TA. Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu Rev Physiol 1995;57:827-72.
8. Baumgartner HR, Haudenschild C. Adhesion of platelets to subendothelium. Ann NY Acad Sci 1972;201:22-36.
9. Langille BL, O'Donnell F. Reduction in arterial diameter produced by chronic decreases in flow are endothelium-dependent. Science 1986;231:405-7.
10. Schwartz SM, Heimark RL, Majesky MW. Developmental mechanisms underlying pathology of arteries. Physiol Rev 1990;70:1177-209.
11. Scott-Burden T, Vanhoutte PM. The endothelium as a regulator of vascular smooth muscle proliferation. Circulation 1993;87(Suppl 5):51-5.
12. Noris M, Morigi M, Donadelli R, et al. Nitric oxide synthesis by cultured endothelial cells is modulated by flow conditions. Circ Res 1995;76:536-43.
13. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature 1993;362:801-9.
14. Nakahashi T, Fukuo K, Inoue T, et al. Endothelin-1 enhances nitric oxide-induced cytotoxicity in vascular smooth muscle. Hypertension 1995;25:744-7.
15. Risau W. Differentiation of endothelium. FASEB J 1995;9: 926-33.
16. Shalaby F, Rossant J, Yamaguchi TP, et al. Failure of blood-island formation and vasculogenesis in FIk-1-deficient mice. Nature 1995;376:62-6.
17. Sterpetti AV, Hunter WJ, Schultz RD, Farina C. Healing of high-porosity polytetrafluoroethylene arterial grafts is influenced by the nature of the surrounding tissue. Surgery 1992;111:677-82.
18. Clowes AW, Gown AM, Hanson SR, Reidy MA. Mechanisms of arterial graft failure. I. Role of cellular proliferation in early healing of PTFE prostheses. Am J Pathol 1985;118: 43-54.
19. Sottiurai VS, Yao JTS, Flinn WR, Batson RC. Intimal hyperplasia and neointima: an ultrastructural analysis of thrombosed grafts in humans. Surgery 1983;93:809-17.
20. Snow AD, Bolender RP, Wight TN, Clowes AW. Heparin modulates the composition of the extracellular matrix domain surrounding arterial smooth muscle cells. Am J Pathol 1990;137:313-30.
21. Campeau L, Lesperance J, Cordobe F, et al. Aortocoronary saphenous vein bypass graft changes 5 to 7 years after surgery. Circulation 1978;58(Suppl 1):170-5.
22. Cox JL, Chiasson DA, Gotlieb AI. Stranger in a strange land: the pathogenesis of saphenous vein graft stenosis with emphasis on structural and functional differences between veins and arteries. Prog Cardiovasc Dis 1991;34: 45-68.
23. Nikkari ST, Jarvelainen HT, Wight TN, Ferguson M, Clowes AW. Smooth muscle cell expression of extracellular matrix genes after arterial injury. Am J Pathol 1994;144:1348-56.
24. Fingerle J, Au YP, Clowes AW, Reidy MA. Intimal lesion formation in rat carotid arteries after endothelial denudation in absence of medial injury. Arteriosclerosis 1990;10: 1082-7.
25. Clowes AW, Clowes MM, Reidy MA. Kinetics of cellular proliferation after arterial injury. III. Endothelial and smooth muscle growth in chronically denuded vessels. Lab Invest 1986;54:295-303.
26. 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 USA 1991; 88:3739-43.
27. Garg UC, Hassid A. Nitric oxide-generating vasodilatators and 8-bromo-cyclic GMP inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J Clin Invest 1989;83:1774-7.
28. Jawien A, Bowen-Pope DF, Lindner 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;89:507-11.
29. Koyama N, Hart CE, Clowes AW. Different functions of the platelet-derived growth factor-α and -β receptors for the migration and proliferation of cultured baboon smooth muscle cells. Circ Res 1994;75:682-91.
30. Bennett MR, Evan GI, Schwarte SM. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest 1995;95: 2266-74.
31. Lindner V, Giachelli CM, Schwartz SM, Reidy M. A subpopulation of smooth muscle cells in injured rat arteries expresses platelet-derived growth factor-B chain mRNA. Circ Res 1995;76:951-7.
32. Ferns GA, 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;253:1129-31.
33. 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 USA 1989;86:8412-6.
34. Majesky MW, Lindner V, Twardzik DR, Schwartz SM, Reidy MA. Production of transforming growth factor β-1 during repair of arterial injury. J Clin Invest 1991;88:904-10.
35. Prescott M, Webb R, Reidy MA. Angiotensin-converting enzyme inhibitor versus angiotensin II, AT receptor antagonist: effects on smooth muscle cell migration and proliferation after balloon catheter injury. Am J Pathol 1991;139: 1291-302.
36. 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: 1017-23.
37. Clowes AW, Clowes MM, Au YPT, Reidy MA. Smooth muscle cells express urokinase during mitogenesis and tissue-type plasminogen activator during migration in injured rat carotid artery. Circ Res 1990;67:61-7.
38. Kenagy RD, Clowes AW. Regulation of baboon arterial smooth muscle cell plasminogen activators by heparin and growth factors. Thromb Res 1995;77:55-61.
39. Jackson CL, Raines EW, Ross R, Reidy MA. Role of endogenous platelet-derived growth factor in arterial smooth muscle cell migration after balloon catheter injury. Arterioscler Thromb 1993;13:1218-26.
40. 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;75:539-45.
41. Manashi S, Lu H, Soria C, Legrand Y. Endothelial cell proteases: physiological role and regulation. Baillieres Clin 1993;6:559-76.
42. Schwartz SM, deBlois D, O'Brien ERM. The intima. Soil for atherosclerosis and restenosis. Circ Res 1995;77:445-65.
43. Majesky MW, Reidy MA, Bowen-Pope DF, Wilcox JN, Schwartz SM. PDGF ligand and receptor gene expression during repair of arterial injury. J Cell Biol 1990;111:2149-58.
44. 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: 1755-60.
45. Viswanathan M, Stromberg C, Seltzer A, Saavedra JM. Balloon angioplasty enhances the expression of angiotensin II AT1 receptors in the neointima of rat aorta. J Clin Invest 1992;90:1707-12.
46. 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: 450-6.
47. Hansson GK, Jonasson L, Holm J, Clowes M, Clowes AW. γ-Interferon regulates vascular smooth muscle proliferation and Ia antigen expression in vivo and in vitro. Circ Res 1995;63:712-9.
48. Nunokawa Y, Tanaka S. Interferon gamma inhibits proliferation of rat vascular smooth muscle cells by nitric oxide generation. Biochem Biophys Res Commun 1992;188: 409-15.
49. Castellot JJ, Addonizio ML, Rosenberg R, Karnovsky MJ. Cultured endothelial cells produce a heparin-like inhibitor of smooth muscle cell growth. J Cell Biol 1981;90:372-9.
50. Niimi YA, Hirakawa K. Repeated endothelial removal augments intimal thickening and attenuates EDRF release. Am J Physiol 1994;266:H-1348-56.
51. Bush HL, Jakubowski JA, Curl GR, Deykin D, Nabseth DC. The natural history of endothelial structure and function in arterialized vein grafts. J Vasc Surg 1986;3:204-15.
52. Luscher TF. Vascular biology of coronary bypass grafts. Coronary Artery Dis 1992;3:157-65.
53. Brody WR, Angel WW, Kosek JC. Histological fate of the venous coronary bypass in dogs. Am J Pathol 1972;66: 111-29.
54. Carrel A, Guthrie CC. Results of biterminal transplantation of veins. Am J Med Sci 1906;132:415-22.
55. Carrel A, Guthrie CC. Uniterminal and biterminal venous transplantations. Surg Gynecol Obstet 1906;2:266-86.
56. Davies MG, Klyachkin ML, Dalen H, Svendsen E, Hagen PO. Regression of intimal hyperplasia with restoration of endothelium-dependent relaxing factor-mediated relaxation in experimental vein grafts. Surgery 1993;114:258-71.
57. Zwolak RM, Adams MC, Clowes AW. Kinetics of vein graft hyperplasia: association with tangential stress. J Vasc Surg 1987;5:126-36.
58. Kohler T, Kirkman TR, Clowes AW. The effect of rigid external support on vein graft adaptation to arterial circulation. J Vasc Surg 1989;9:277-85.
59. Clowes AW, Kirkman TR, Clowes MM. Mechanisms of arterial graft failure. II. Chronic endothelial and smooth muscle cell proliferation in healing polytetrafluoroethylene prostheses. J Vasc Surg 1986;3:877-84.
60. Kaufman BR, Fox PL, Graham LM. Platelet-derived growth factor production by canine aortic grafts seeded with endothelial cells. J Vasc Surg 1992;15:699-707.
61. Golden MA, Au YPT, Kenagy RD, Clowes AW. Growth factor gene expression by intimal cells in healing polytetrafluoroethylene grafts. J Vasc Surg 1990;11:580-5.
62. Golden MA, Au YPT, Kirkman TR, et al. Platelet-derived growth factor activity and mRNA expression in healing vascular grafts in baboons. Association in vivo of platelet-derived growth factor mRNA and protein with cellular proliferation. J Clin Invest 1991;87:406-14.
63. Zwolak RM, Kirkman TR, Clowes AW. Atherosclerosis in rabbit vein grafts. Arteriosclerosis 1989;9:374-9.
64. Batellier J, Wassef M, Merval R, Duriez M, Tedgui A. Protection from atherosclerosis in vein grafts by a rigid external support. Arteriosclerosis Thromb 1993;13:379-84.
65. Clowes AW, Kirkman TR, Reidy MA. Mechanisms of arterial graft healing. Rapid transmural capillary ingrowth provides a source of intimal endothelium and smooth muscle in porous PTFE prostheses. Am J Pathol 1986;123: 220-30.
66. Geary RL, Kohler TR, Vergel S, Kirkman TR, Clowes AW. Time course of flow-induced smooth muscle cell proliferation and intimal thickening in endothelialized baboon vascular grafts. Circ Res 1993;74:14-23.
67. Golden MA, Hanson SR, Kirkman TR, Schneider PA, Clowes AW. Healing of polytetrafluoroethylene arterial grafts is influenced by graft porosity. J Vasc Surg 1990;11: 838-45.
68. Kraiss LW, Kirkman TR, Kohler TR, et al. Shear stress regulates smooth muscle proliferation and neointimal thickening in porous polytetraethylene grafts. Arteriosclerosis Thromb 1991;11:1844-52.
69. Kraiss LW, Raines EW, Wilcox JN, et al. Regional expression of the platelet-derived growth factor and its receptors in a primate graft model of vessel wall assembly. J Clin Invest 1993;92:338-48.
70. Joannides R, Haefeli WE, Linder L, et al. Nitric oxide is responsible for flow-dependent dilation of human peripheral conduit arteries in vivo. Circulation 1995;91:1314-9.
71. Arnal JF, Schott C, Stoclet JC, Michel JB. Vascular relaxation and cyclic guanidine monophosphate in a rat model of high output heart failure. Cardiovasc Res 1993;27:1651-6.
72. Blanco FJ, Ochs RL, Schwarz H, Lotz M. Chondrocyte apoptosis induced by nitric oxide. Am J Pathol 1995;146: 75-85.
73. De Caterina R, Libby P, Peng H-B, et al. Nitric oxide decreases cytokine-induced endothelial activation. Nitric oxide selectively reduces endothelial expression of adhesion molecules and proinflammatory cytokines. J Clin Invest 1995;96:60-8.
74. Zeiher AM, Fisslthaler B, Schray-Utz B, Busse R. Nitric oxide modulates the expression of monocyte chemoattractant protein 1 in cultured human endothelial cells. Circ Res 1995;76:980-6.
75. Arnal JF, Yamin J, Dockery S, Harrison DG. Regulation of endothelial nitric oxide synthase mRNA, protein, and activity during cell growth. Am J Physiol 1994;267:C1381-8.
76. Kolpakov V, Gordon D, Kulik TJ. Nitric oxide-generating compounds inhibit total protein and collagen synthesis in cultured vascular smooth muscle cells. Circ Res 1995;76: 305-9.
77. Bassiouni HS, White S, Glagov S, Choi E, Giddens DP, Zarins CK. Anastomotic intimal hyperplasia: mechanical injury or flow induced. J Vasc Surg 1992;15:708-17.
78. Berger K, Sauvage LR, Roa AM, Wood SJ. Healing of arterial prosthesis in man: its incompleteness. Ann Surg 1972;175:118-27.
79. DeBakey ME, Jordan GL, Abbott JP, et al. The fate of the Dacron vascular graft. Arch Surg 1964;80:754-82.
80. Pomerantz KB, Hajjar DP. Eicosanoids in regulation of arterial smooth muscle cell phenotype, proliferative capacity, and cholesterol metabolism. Arteriosclerosis 1989;9: 413-29.
81. Cross KS, El-Sanadiki MN, Murray JJ, Mikat EM, McCann RL, Hagen PO. Functional abnormalities of experimental autogenous vein graft neoendothelium. Ann Surg 1988;208: 631-8.
82. Miller VM, Reigel MM, Hollier LH, Vanhoutte PM. Endothelium-dependent responses in autogenous femoral veins grafted into the arterial circulation of the dog. J Clin Invest 1987;80:1350-7.
83. Luscher TJ, Diederich D, Siebenmann R, et al. Difference between endothelium-dependent relaxation in arterial and in venous coronary bypass grafts. N Engl J Med 1988;319: 462-7.
84. Sterpetti AV, Schultz RD, Bailey RI. Endothelial cell seeding after carotid endarterectomy in a canine model reduces platelet uptake. Eur J Vasc Surg 1992;6:390-4.
85. Zilla P, Deutsch M, Meinhart J, et al. Clinical in vitro endothelialization of femoropopliteal bypass grafts: follow-up over three years. J Vasc Surg 1994;19:540-8.
86. Conte MS, Choudhry RP, Shirakowa M, Fallon JT, Birinyi LK. Endothelial cell seeding fails to attenuate intimal thickening in balloon-injured rabbit arteries. J Vasc Surg 1995;21: 413-21.
87. Clowes MM, Lynch CM, Miller AD, Miller DG, Osborne WRA, Clowes AW. Long-term biological expression of injured rat carotid artery seeded with smooth muscle cells expressing retrovirally introduced human genes. J Clin Invest 1994;93:644-51.
88. Peiro C, Redondo J, Rodriguez-Martinez MA, Angulo J, Marin J, Sanchez-Ferrer CF. Influence of endothelium on cultured vascular smooth muscle cell proliferation. Hypertension 1995;25:748-51.
89. Gimbrone MA. Vascular endothelium: an integrator of pathologic stimuli in atherosclerosis. Am J Cardiol 1995;75: 67B-70B.
90. Pietersma A, Kofflard M, de Wit LEA, et al. Late lumen loss after coronary angioplasty is associated with the activation status of circulating phagocytes before treatment. Circulation 1995;91:1320-5.
91. Herring M, Smith J, Dalsing M, et al. Endothelial seeding of polytetrafluoroethylene femoral popliteal bypasses: the failure of low-density seeding to improve patency. J Vasc Surg 1994;20:650-5.
92. Cambria RA, Lowell RC, Gloviczki P, Miller VM. Chronic changes in blood flow alter endothelium-dependent responses in autogenous vein grafts in dog. J Vasc Surg 1994; 20:765-73.
93. Komori K, Ishii T, Mawatari K, et al. Endothelium-dependent relaxation in response to adenosine diphosphate is impaired under poor runoff conditions in the canine femoral artery. J Surg Res 1995;58:302-6.
94. Nicosia RF, Bonanno E, Villaschi S. Large-vessel endothelium switches to a microvascular phenotype during angiogenesis in collagen gel culture of rat aorta. Atherosclerosis 1992;95:191-9.
95. Canfield AE, Schor AM. Evidence that tenascin and thrombospondin-1 modulate sprouting of endothelial cells. J Cell Sci 1995;108:797-809.
96. Ott MJ, Ballermann BJ. Shear stress-conditioned, endothelial cell-seeded vascular grafts: improved cell adherence in response to in vitro shear stress. Surgery 1995;117:334-9.
97. Bauters C, Asahara T, Zheng LP, et al. Recovery of disturbed endothelium-dependent flow in the collateral-perfused rabbit ischemic hindlimb after administration of vascular endothelial growth factor. Circulation 1995;91: 2802-9.
98. Geary RL, Clowes AW, Lau S, Vergel S, Dale DC, Osborne WRA. Gene transfer in baboons using prosthetic vascular grafts seeded with retrovirally transduced smooth muscle cells: a model for local and systemic gene therapy. Hum Gene Ther 1994;5:1211-6.
99. Von der Leyen HE, Gibbons GH, Morishita R, et al. Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. Proc Natl Acad Sci USA 1995;92:1137-41.
100. Lee SW, Trapnell BC, Rade JJ, Virmani R, Dichek DA. In vivo adenoviral vector-mediated gene transfer into balloon-injured rat carotid arteries. Circ Res 1993;73:797-807.
101. Schulick AH, Newman KD, Virmani R, Dichek DA. In vivo gene transfer into injured carotid arteries. Optimization and evaluation of acute toxicity. Circulation 1995;91: 2407-14.
102. Herrman JPR, Hermans WRM, Vos J, Serruys PW. Pharmacological approaches to the prevention of restenosis following angioplasty. The search of the Holy Grail? (Part I). Drugs 1993;46:18-52.
103. Herrman JPR, Hermans WRM, Vos J, Serruys PW. Pharmacological approaches to the prevention of restenosis following angioplasty. The search of the Holy Grail? (Part II). Drugs 1993;46:249-62.
104. Clowes AW, Karnovsky MJ. Suppression by heparin of smooth muscle cell proliferation in injured arteries. Nature 1977;265:625-6.
105. Clowes AW, Clowes MM. Kinetics of cellular proliferation after arterial injury. II. Inhibition of smooth muscle growth by heparin. Lab Invest 1985;52:611-6.
106. Reilly CF, Kindy MS, Brown KE, Rosenberg RD, Sonenshein GE. Heparin prevents vascular smooth muscle cell progression through the G1 phase of the cell cycle. J Biol Chem 1989;264:6990-5.
107. Au YPT, Kenagy RD, Clowes MM, Clowes AW. Mechanisms of inhibition by heparin of vascular smooth muscle cell proliferation and migration. Haemostasis 1993;23: 177-82.
108. Kenagy RD, Nikkari ST, Welgus HG, Clowes AW. Heparin inhibits the induction of three matrix metalloproteinases (stromelysin, 92-kD gelatinase, and collagenase) in primate arterial smooth muscle cells. J Clin Invest 1994;93:1987-93.
109. Au YPT, Montgomery KF, Clowes AW. Heparin inhibits collagenase gene expression mediated by phorbol esterresponsive element in primate arterial smooth muscle cells. Circ Res 1992;70:1062-9.
110. Clowes AW, Clowes MM, Kirkman TR, Jackson CL, Au YPT, Kenagy R. Heparin inhibits the expression of tissue-type plasminogen activator by smooth muscle cells in injured rat carotid artery. Circ Res 1992;70:1128-36.
111. Mutoh S, Clowes MM, Clowes AW. Heparin increases cell membrane-associated heparan sulfate proteoglycan in balloon-injured rat carotid artery. J Vasc Res 1993;30:161-8.
112. Geary RL, Koyama N, Wang TW, Vergel S, Clowes AW. Failure of heparin to inhibit intimal hyperplasia in injured baboon arteries: the role of heparin-sensitive and -insensitive pathways in the stimulation of smooth muscle cell migration and proliferation. Circulation 1995;91:2972-81.