Allograft vasculopathy versus atherosclerosis

Circulation Research

Volumn 99, Issue 8, 2006, Pages 801-815

  Rahmani, Maziar ^b   Cruz, Rani P ^b   Granville, David J ^a   McManus, Bruce M ^a  

^a ST PAUL S HOSPITAL   (Canada)

^b NONE

Author keywords

Allograft vasculopathy; Atherosclerosis; Cardiac transplantation; Chronic transplant rejection; Pathogenesis; Risk factors

Indexed keywords

CYTOKINE; PROTEOGLYCAN; SCLEROPROTEIN;

ANGIOPLASTY; ARTERIOSCLEROSIS; ARTERY INTIMA PROLIFERATION; ARTERY OCCLUSION; BLOOD VESSEL PERMEABILITY; CARDIAC ALLOGRAFT VASCULOPATHY; CELL ACTIVATION; CELL MIGRATION; CELL PROLIFERATION; CORONARY ARTERY ATHEROSCLEROSIS; CYTOKINE PRODUCTION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM INJURY; EXTRACELLULAR MATRIX; GRAFT OCCLUSION; HEART TRANSPLANTATION; HUMAN; IMMUNOPATHOGENESIS; LIPID STORAGE; NONHUMAN; PATHOPHYSIOLOGY; POSTOPERATIVE COMPLICATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RESTENOSIS; REVIEW; RISK FACTOR; VEIN OCCLUSION;

ANIMALS; ARTERIOSCLEROSIS; CORONARY ARTERIOSCLEROSIS; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; HEART TRANSPLANTATION; HUMANS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; RISK FACTORS;

EID: 33749681864     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000246086.93555.f3     Document Type: Review

References (128)

1. Rahmani M, McDonald PC, Wong BW, McManus BM. Transplant vascular disease: role of lipids and proteoglycans. Can J Cardiol. 2004;20:58B-65B.
2. Lin H, Wilson JE, Roberts CR, Horley KJ, Winters GL, Costanzo MR, McManus BM. Biglycan, decorin, and versican protein expression patterns in coronary arteriopathy of human cardiac allograft: distinctness as compared to native atherosclerosis. J Heart Lung Transplant. 1996;15:1233-1247.
3. McManus BM, Malcolm G, Kendall TJ. Lipid overload and proteoglycan expression in chronic rejection of the human transplanted heart. Clin Transplant. 1994;8:336-340.
4. McManus BM, Horley KJ, Wilson JE, Malcom GT, Kendall TJ, Miles RR, Winters GL, Costanzo MR, Miller LL, Radio SJ. Prominence of coronary arterial wall lipids in human heart allografts. Implications for pathogenesis of allograft arteriopathy. Am J Pathol. 1995;147:293-308.
5. Mehra MR, Ventura HO, Chambers R, Collins TJ, Ramee SR, Kates MA, Smart FW, Stapleton DD. Predictive model to assess risk for cardiac allograft vasculopathy: an intravascular ultrasound study. J Am Coll Cardiol. 1995;26:1537-1544.
6. Weis M, von Scheidt W. Cardiac allograft vasculopathy: a review. Circulation. 1997;96:2069-2077.
7. Mehra MR, Uber PA, Uber WE, Scott RL, Park MH. Allosensitization in heart transplantation: implications and management strategies. Curr Opin Cardiol. 2003;18:153-158.
8. Kemna MS, Valantine HA, Hunt SA, Schroeder JS, Chen YD, Reaven GM. Metabolic risk factors for atherosclerosis in heart transplant recipients. Am Heart J. 1994;128:68-72.
9. Valantine HA. Cardiac allograft vasculopathy: central role of endothelial injury leading to transplant "atheroma." Transplantation. 2003;76:891-899.
10. Laskowski I, Pratschke J, Wilhelm MJ, Gasser M, Tilney NL. Molecular and cellular events associated with ischemia/reperfusion injury. Ann Transplant. 2000;5:29-35.
11. Land W, Messmer K. The impact of ischemia/reperfusion injury on specific and non-specific early and late chronic events after organ transplantation. Transplant Rev. 1996;10:108-127.
12. Gasser M, Waaga AM, Laskowski IA, Tilney NL. The influence of donor brain death on short and long-term outcome of solid organ allografts. Ann Transplant. 2000;5:61-67.
13. Slager CJ, Wentzel JJ, Gijsen FJ, Thury A, van der Wal AC, Schaar JA, Serruys PW. The role of shear stress in the destabilization of vulnerable plaques and related therapeutic implications. Nat Clin Pract Cardiovasc Med. 2005;2:456-464.
14. Choy JC, Podor TJ, Yanagawa B, Lai JC, Granville DJ, Walker DC, McManus BM. The regulation and consequences of immune-mediated cell death in atheromatous diseases. Cardiovasc Toxicol. 2003;3:269-282.
15. Miller LW, Granville DJ, Narula J, McManus BM. Apoptosis in cardiac transplant rejection. Cardiol Clin. 2001;19:141-154.
16. Hallenbeck JM, Hansson GK, Becker KJ. Immunology of ischemic vascular disease: plaque to attack. Trends Immunol. 2005;26:550-556.
17. McManus B Endothelial aspects of transplant atheromata. Can J Cardiol. 1998;14:17D-18D.
18. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
19. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-874.
20. Miyamoto T, Yumoto H, Takahashi Y, Davey M, Gibson FC 3rd, Genco CA. Pathogen-accelerated atherosclerosis occurs early after exposure and can be prevented via immunization. Infect Immun. 2006;74:1376-1380.
21. Madan M, Bishayi B, Hoge M, Messas E, Amar S. Doxycycline affects diet- and bacteria-associated atherosclerosis in an ApoE heterozygote murine model: cytokine profiling implications. Atherosclerosis. In press.
22. Benditt EP, Benditt JM. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci U S A. 1973;70:1753-1756.
23. Bobryshev YV, Lord RS, Tran D. Chlamydia pneumoniae in foci of "early" calcification of the tunica media in arteriosclerotic arteries: an incidental presence? Am J Physiol Heart Circ Physiol. 2006;290:H1510-H1519.
24. Simmons RL, Weil R, Tallent MB, Kjellstrand CM, Najaran JS. Do mild infections trigger the rejection of renal allograft? Transplant Proc. 1970;2:419-423.
25. Subramanian AK, Quinn TC, Kickler TS, Kasper EK, Tucker PC. Correlation of chlamydia pneumoniae infection and severity of accelerated graft arteriosclerosis after cardiac transplantation. Transplantation. 2002;73:761-764.
26. Nieto FJ. Infective agents and cardiovascular disease. Semin Vasc Med. 2002;2:401-415.
27. Petrakopoulou P, Kubrich M, Pehlivanli S, Meiser B, Reichart B, von Scheidt W, Weis M. Cytomegalovirus infection in heart transplant recipients is associated with impaired endothelial function. Circulation. 2004;110(suppl II):II-207-II-212.
28. Weis M, Kledal TN, Lin KY, Panchal SN, Gao SZ, Valantine HA, Mocarski ES, Cooke JP. Cytomegalovirus infection impairs the nitric oxide synthase pathway: role of asymmetric dimethylarginine in transplant arteriosclerosis. Circulation. 2004;109:500-505.
29. Esper E, Glagov S, Karp RB, Simonsen KK, Filer SR, Scanu AM, Sand ME. Role of hypercholesterolemia in accelerated transplant coronary vasculopathy: results of surgical therapy with partial ileal bypass in rabbits undergoing heterotopic heart transplantation. J Heart Lung Transplant. 1997;16:420-435.
30. Chan JC, Cheung JC, Stehouwer CD, Emeis JJ, Tong PC, Ko GT, Yudkin JS. The central roles of obesity-associated dyslipidaemia, endothelial activation and cytokines in the metabolic syndrome - an analysis by structural equation modelling. Int J Obes Relat Metab Disord. 2002;26:994-1008.
31. Johnson MR. Transplant coronary disease: nonimmunologic risk factors. J Heart Lung Transplant. 1992;11:S124-S132.
32. Cantin B, Wen P, Zhu D, Dai M, Panchal SN, Billingham ME, Gwathmey JK, Valantine HA. Transplant coronary artery disease: a novel model independent of cellular alloimmune response. Circulation. 2001;104:2615-2619.
33. Kobashigawa JA, Katznelson S, Laks H, Johnson JA, Yeatman L, Wang XM, Chia D, Terasaki PI, Sabad A, Cogert GA, Trosian K, Hamilton MA, Moriguchi JD, Kawata N, Hage A, Drinkwater DC, Stevenson LW. Effect of pravastatin on outcomes after cardiac transplantation. N Engl J Med. 1995;333:621-627.
34. Rickenbacher PR, Kemna MS, Pinto FJ, Hunt SA, Alderman EL, Schroeder JS, Stinson EB, Popp RL, Chen I, Reaven G, Valantine HA. Coronary artery intimal thickening in the transplanted heart. An in vivo intracoronary untrasound study of immunologic and metabolic risk factors. Transplantation. 1996;61:46-53.
35. Valantine H, Rickenbacker P, Kemna M, Hunt S, Chen YD, Reaven G, Stinson EB. Metabolic abnormalities characteristic of dysmetabolic syndrome predict the development of transplant coronary artery disease: a prospective study. Circulation. 2001;103:2144-2152.
36. Wenke K, Meiser B, Thiery J, Nagel D, von Scheidt W, Krobot K, Steinbeck G, Seidel D, Reichart B. Simvastatin initiated early after heart transplantation: 8-year prospective experience. Circulation. 2003;107:93-97.
37. Kobashigawa JA. Statins as immunosuppressive agents. Liver Transpl. 2001;7:559-561.
38. Cook RC, Tupper JK, Parker S, Kingsbury K, Frohlich JJ, Abel JG, Gao M, Ignaszewski AP. Effect of immunosuppressive therapy, serum creatinine, and time after transplant on plasma total homocysteine in patients following heart transplantation. J Heart Lung Transplant. 1999;18:420-424.
39. Chambers JC, Ueland PM, Wright M, Dore CJ, Refsum H, Kooner JS. Investigation of relationship between reduced, oxidized, and protein-bound homocysteine and vascular endothelial function in healthy human subjects. Circ Res. 2001;89:187-192.
40. Gupta A, Moustapha A, Jacobsen DW, Goormastic M, Tuzcu EM, Hobbs R, Young J, James K, McCarthy P, van Lente F, Green R, Robinson K. High homocysteine, low folate, and low vitamin B6 concentrations: prevalent risk factors for vascular disease in heart transplant recipients. Transplantation. 1998;65:544-550.
41. Potena L, Grigioni F, Magnani G, Ortolani P, Coccolo F, Sassi S, Koessels K, Marrozzini C, Marzocchi A, Carigi S, Musuraca AC, Russo A, Magelli C, Branzi A. Homocysteine-lowering therapy and early progression of transplant vasculopathy: a prospective, randomized, IVUS-based study. Am J Transplant. 2005;5:2258-2264.
42. Boushey CJ, Beresford SA, Omenn GS, Motulsky AG. A quantitative assessment of plasma homocysteine as a risk factor for vascular disease. Probable benefits of increasing folic acid intakes. JAMA. 1995;274:1049-1057.
43. Lonn E, Yusuf S, Arnold MJ, Sheridan P, Pogue J, Micks M, McQueen MJ, Probstfield J, Fodor G, Held C, Genest J Jr. Homocysteine lowering with folic acid and B vitamins in vascular disease. N Engl J Med. 2006;354:1567-1577.
44. Bonaa KH, Njolstad I, Ueland PM, Schirmer H, Tverdal A, Steigen T, Wang H, Nordrehaug JE, Arnesen E, Rasmussen K. Homocysteine lowering and cardiovascular events after acute myocardial infarction. N Engl J Med. 2006;354:1578-1588.
45. Botas J, Pinto FJ, Chenzbraun A, Liang D, Schroeder JS, Oesterle SN, Alderman EL, Popp RL, Yeung AC. Influence of preexistent donor coronary artery disease on the progression of transplant vasculopathy. An intravascular ultrasound study. Circulation. 1995;92:1126-1132.
46. Pasceri V, Willerson JT, Yeh ET. Direct proinflammatory effect of C-reactive protein on human endothelial cells. Circulation. 2000;102:2165-2168.
47. Venugopal SK, Devaraj S, Yuhanna I, Shaul P, Jialal I. Demonstration that C-reactive protein decreases eNOS expression and bioactivity in human aortic endothelial cells. Circulation. 2002;106:1439-1441.
48. Wang CH, Li SH, Weisel RD, Fedak PW, Dumont AS, Szmitko P, Li RK, Mickle DA, Verma S. C-reactive protein upregulates angiotensin type 1 receptors in vascular smooth muscle. Circulation. 2003;107:1783-1790.
49. Torzewski M, Rist C, Mortensen RF, Zwaka TP, Bienek M, Waltenberger J, Koenig W, Schmitz G, Hombach V, Torzewski J. C-reactive protein in the arterial intima: role of C-reactive protein receptor-dependent monocyte recruitment in atherogenesis. Arterioscler Thromb Vasc Biol. 2000;20:2094-2099.
50. Liuzzo G, Biasucci LM, Gallimore JR, Grillo RL, Rebuzzi AG, Pepys MB, Maseri A. The prognostic value of C-reactive protein and serum amyloid a protein in severe unstable angina. N Engl J Med. 1994;331:417-424.
51. Verma S, Szmitko PE, Yeh ET. C-reactive protein: structure affects function. Circulation. 2004;109:1914-1917.
52. Hognestad A, Endresen K, Wergeland R, Stokke O, Geiran O, Holm T, Simonsen S, Kjekshus JK, Andreassen AK. Plasma C-reactive protein as a marker of cardiac allograft vasculopathy in heart transplant recipients. J Am Coll Cardiol. 2003;42:477-482.
53. Labarrere CA, Lee JB, Nelson DR, Al-Hassani M, Miller SJ, Pitts DE. C-reactive protein, arterial endothelial activation, and development of transplant coronary artery disease: a prospective study. Lancet. 2002;360:1462-1467.
54. Pethig K, Heublein B, Kutschka I, Haverich A. Systemic inflammatory response in cardiac allograft vasculopathy: high-sensitive C-reactive protein is associated with progressive luminal obstruction. Circulation. 2000;102(suppl III):III-233-III-236.
55. Billingham ME. Histopathology of graft coronary disease. J Heart Lung Transplant. 1992;11:S38-S44.
56. Johnson DE, Gao SZ, Schroeder JS, DeCampli WM, Billingham ME. The spectrum of coronary artery pathologic findings in human cardiac allografts. J Heart Transplant. 1989;8:349-359.
57. Lin H, Wilson JE, Kendall TJ, Radio SJ, Cornhill FJ, Herderick E, Winters GL, Costanzo MR, Porter T, Thieszen SL, McManus BM. Comparable proximal and distal severity of intimal thickening and size of epicardial coronary arteries in transplant arteriopathy of human cardiac allografts. J Heart Lung Transplant. 1994;13:824-833.
58. Stary HC. Evolution and progression of atherosclerotic lesions in coronary arteries of children and young adults. Arteriosclerosis. 1989;9:I19-I32.
59. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr, Rosenfeld ME, Schwartz CJ, Wagner WD, Wissler RW. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation. 1995;92:1355-1374.
60. Virmani R, Kolodgie FD, Burke AP, Farb A, Schwartz SM. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler Thromb Vasc Biol. 2000;20:1262-1275.
61. Brousseau ME, Hoeg JM. Transgenic rabbits as models for atherosclerosis research. J Lipid Res. 1999;40:365-375.
62. Shi W, Pei H, Fischer JJ, James JC, Angle JF, Matsumoto AH, Helm GA, Sarembock IJ. Neointimal formation in two apolipoprotein E-deficient mouse strains with different atherosclerosis susceptibility. J Lipid Res. 2004;45:2008-2014.
63. Zhang SH, Reddick RL, Piedrahita JA, Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science. 1992;258:468-471.
64. Plump AS, Smith JD, Hayek T, Aalto-Setala K, Walsh A, Verstuyft JG, Rubin EM, Breslow JL. Severe hypercholesterolemia and atherosclerosis in apolipoprotein E-deficient mice created by homologous recombination in ES cells. Cell. 1992;71:343-353.
65. Ishibashi S, Brown MS, Goldstein JL, Gerard RD, Hammer RE, Herz J. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest. 1993;92:883-893.
66. Wouters K, Shiri-Sverdlov R, van Gorp PJ, van Bilsen M, Hofker MH. Understanding hyperlipidemia and atherosclerosis: lessons from genetically modified apoE and LDLR mice. Clin Chem Lab Med. 2005;43:470-479.
67. Bonthu S, Heistad DD, Chappell DA, Lamping KG, Faraci FM. Atherosclerosis, vascular remodeling, and impairment of endothelium-dependent relaxation in genetically altered hyperlipidemic mice. Arterioscler Thromb Vasc Biol. 1997;17:2333-2340.
68. Sanan DA, Newland DL, Tao R, Marcovina S, Wang J, Mooser V, Hammer RE, Hobbs HH. Low density lipoprotein receptor-negative mice expressing human apolipoprotein B-100 develop complex atherosclerotic lesions on a chow diet: no accentuation by apolipoprotein(a). Proc Natl Acad Sci U S A. 1998;95:4544-4549.
69. Malek RL, Wang HY, Kwitek AE, Greene AS, Bhagabati N, Borchardt G, Cahill L, Currier T, Frank B, Fu X, Hasinoff M, Howe E, Letwin N, Luu TV, Saeed A, Sajadi H, Salzberg SL, Sultana R, Thiagarajan M, Tsai J, Veratti K, White J, Quackenbush J, Jacob HJ, Lee NH. Physiogenomic resources for rat models of heart, lung and blood disorders. Nat Genet. 2006;38:234-239.
70. Lee S, Willoughby WF, Smallwood CJ, Dawson A, Orloff MJ. Heterotopic heart and lung transplantation in the rat. Am J Pathol. 1970;59:279-298.
71. Wilhelm MJ, Pratschke J, Beato F, Taal M, Laskowski IA, Paz DM, Schmid C, Hancock WW, Scheld HH, Tilney NL. Activation of proinflammatory mediators in heart transplants from brain-dead donors: evidence from a model of chronic rat cardiac allograft rejection. Transplant Proc. 2002;34:2359-2360.
72. Lemstrom K, Sihvola R, Bruggeman C, Hayry P, Koskinen P. Cytomegalovirus infection-enhanced cardiac allograft vasculopathy is abolished by DHPG prophylaxis in the rat. Circulation. 1997;95:2614-2616.
73. Skarsgard PL, Wang X, McDonald P, Lui AH, Lam EK, McManus BM, van Breemen C, Laher I. Profound inhibition of myogenic tone in rat cardiac allografts is due to eNOS- and iNOS-based nitric oxide and an intrinsic defect in vascular smooth muscle contraction. Circulation. 2000;101:1303-1310.
74. Choy JC, Cruz RP, Kerjner A, Geisbrecht J, Sawchuk T, Fraser SA, Hudig D, Bleackley RC, Jirik FR, McManus BM, Granville DJ. Granzyme B induces endothelial cell apoptosis and contributes to the development of transplant vascular disease. Am J Transplant. 2005;5:494-499.
75. Russell PS, Chase CM, Colvin RB. Accelerated atheromatous lesions in mouse hearts transplanted to apolipoprotein-E-deficient recipients. Am J Pathol. 1996;149:91-99.
76. Isik FF, McDonald TO, Ferguson M, Yamanaka E, Gordon D. Transplant arteriosclerosis in a rat aortic model. Am J Pathol. 1992;141:1139-1149.
77. Shi C, Lee WS, He Q, Zhang D, Fletcher DL Jr, Newell JB, Haber E. Immunologic basis of transplant-associated arteriosclerosis. Proc Natl Acad Sci U S A. 1996;93:4051-4056.
78. Wagoner LE, Zhao L, Bishop DK, Chan S, Xu S, Barry WH. Lysis of adult ventricular myocytes by cells infiltrating rejecting murine cardiac allografts. Circulation. 1996;93:111-119.
79. Kawahara K, Sutherland DE, Rynasiewicz JJ, Najarian JS. Prolongation of heterotopic cardiac allografts in rats by cyclosporin A. Surgery. 1980;88:594-600.
80. Behrendt D, Ganz P. Endothelial function. From vascular biology to clinical applications. Am J Cardiol. 2002;90:40L-48L.
81. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 1999;399:601-605.
82. Patel RP, Levonen A, Crawford JH, Darley-Usmar VM. Mechanisms of the pro- and anti-oxidant actions of nitric oxide in atherosclerosis. Cardiovasc Res. 2000;47:465-474.
83. Chehal MK, Granville DJ. Cytochrome p450 2C (CYP2C) in ischemic heart injury and vascular dysfunction. Can J Physiol Pharmacol. 2006;84:15-20.
84. Ross R. Atherosclerosis - an inflammatory disease. N Engl J Med. 1999;340:115-126.
85. Weis M, Cooke JP. Cardiac allograft vasculopathy and dysregulation of the NO synthase pathway. Arterioscler Thromb Vasc Biol. 2003;23:567-575.
86. Lai JC, Tranfield EM, Walker DC, Dyck J, Kerjner A, Loo S, English D, Wong D, McDonald PC, Moghadasian MH, Wilson JE, McManus BM. Ultrastructural evidence of early endothelial damage in coronary arteries of rat cardiac allografts. J Heart Lung Transplant. 2003;22:993-1004.
87. Fish RD, Nabel EG, Selwyn AP, Ludmer PL, Mudge GH, Kirshenbaum JM, Schoen FJ, Alexander RW, Ganz P. Responses of coronary arteries of cardiac transplant patients to acetylcholine. J Clin Invest. 1988;81:21-31.
88. Davis SF, Yeung AC, Meredith IT, Charbonneau F, Ganz P, Selwyn AP, Anderson TJ. Early endothelial dysfunction predicts the development of transplant coronary artery disease at 1 year posttransplant. Circulation. 1996;93:457-462.
89. Weis M, Peter-Wolf W, Mazzilli N, Olbrich HG, Schacherer C, Wiemer J, Burger W, Hartmann A. Variations of segmental endothelium-dependent and endothelium-independent vasomotor tone after cardiac transplantation (qualitative changes in endothelial function). Am Heart J. 1997;134:306-315.
90. Drexler H, Fischell TA, Pinto FJ, Chenzbraun A, Botas J, Cooke JP, Alderman EL. Effect of L-arginine on coronary endothelial function in cardiac transplant recipients. Relation to vessel wall morphology. Circulation. 1994;89:1615-1623.
91. Cooke JP, Dzau VJ. Nitric oxide synthase: role in the genesis of vascular disease. Annu Rev Med. 1997;48:489-509.
92. Hasdai D, Gibbons RJ, Holmes DR Jr, Higano ST, Lerman A. Coronary endothelial dysfunction in humans is associated with myocardial perfusion defects. Circulation. 1997;96:3390-3395.
93. Weis M, Hartmann A, Olbrich HG, Hor G, Zeiher AM. Prognostic significance of coronary flow reserve on left ventricular ejection fraction in cardiac transplant recipients. Transplantation. 1998;65:103-108.
94. Hollenberg SM, Klein LW, Parrillo JE, Scherer M, Burns D, Tamburro P, Oberoi M, Johnson MR, Costanzo MR. Coronary endothelial dysfunction after heart transplantation predicts allograft vasculopathy and cardiac death. Circulation. 2001;104:3091-3096.
95. Cooke JP, Singer AH, Tsao P, Zera P, Rowan RA, Billingham ME. Antiatherogenic effects of L-arginine in the hypercholesterolemic rabbit. J Clin Invest. 1992;90:1168-1172.
96. von der Leyen HE, Gibbons GH, Morishita R, Lewis NP, Zhang L, Nakajima M, Kaneda Y, Cooke JP, Dzau VJ. Gene therapy inhibiting neointimal vascular lesion: in vivo transfer of endothelial cell nitric oxide synthase gene. Proc Natl Acad Sci U S A. 1995;92:1137-1141.
97. Shears LL, Kawaharada N, Tzeng E, Billiar TR, Watkins SC, Kovesdi I, Lizonova A, Pham SM. Inducible nitric oxide synthase suppresses the development of allograft arteriosclerosis. J Clin Invest. 1997;100:2035-2042.
98. Lee PC, Wang ZL, Qian S, Watkins SC, Lizonova A, Kovesdi I, Tzeng E, Simmons RL, Billiar TR, Shears LL 2nd. Endothelial nitric oxide synthase protects aortic allografts from the development of transplant arteriosclerosis. Transplantation. 2000;69:1186-1192.
99. Iwata A, Sai S, Nitta Y, Chen M, de Fries-Hallstrand R, Dalesandro J, Thomas R, Allen MD. Liposome-mediated gene transfection of endothelial nitric oxide synthase reduces endothelial activation and leukocyte infiltration in transplanted hearts. Circulation. 2001;103:2753-2759.
100. Vejlstrup NG, Andersen CB, Boesgaard S, Mortensen SA, Aldershvile J. Temporal changes in myocardial endothelial nitric oxide synthase expression following human heart transplantation. J Heart Lung Transplant. 2002;21:211-216.
101. Weis M, Wildhirt SM, Schulze C, Pehlivanli S, Rieder G, Wolf WP, Wilbert-Lampen U, Meiser BM, Enders G, von Scheidt W. Coronary vasomotor dysfunction in the cardiac allograft: impact of different immunosuppressive regimens. J Cardiovasc Pharmacol. 2000;36:776-784.
102. Dzau VJ, Braun-Dullaeus RC, Sedding DG. Vascular proliferation and atherosclerosis: new perspectives and therapeutic strategies. Nat Med. 2002;8:1249-1256.
103. Schwartz SM, deBlois D, O'Brien ER. The intima. Soil for atherosclerosis and restenosis. Circ Res. 1995;77:445-465.
104. Fuster V. Lewis A. Conner Memorial Lecture. Mechanisms leading to myocardial infarction: insights from studies of vascular biology. Circulation. 1994;90:2126-2146.
105. Campbell GR, Campbell JH, Manderson JA, Horrigan S, Rennick RE. Arterial smooth muscle. A multifunctional mesenchymal cell. Arch Pathol Lab Med. 1988;112:977-986.
106. Scott NA, Cipolla GD, Ross CE, Dunn B, Martin FH, Simonet L, Wilcox JN. Identification of a potential role for the adventitia in vascular lesion formation after balloon overstretch injury of porcine coronary arteries. Circulation. 1996;93:2178-2187.
107. Schwartz SM, Murry CE. Proliferation and the monoclonal origins of atherosclerotic lesions. Annu Rev Med. 1998;49:437-460.
108. Religa P, Bojakowski K, Maksymowicz M, Bojakowska M, Sirsjo A, Gaciong Z, Olszewski W, Hedin U, Thyberg J. Smooth-muscle progenitor cells of bone marrow origin contribute to the development of neointimal thickenings in rat aortic allografts and injured rat carotid arteries. Transplantation. 2002;74:1310-1315.
109. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362:801-809.
110. Autieri MV. Allograft-induced proliferation of vascular smooth muscle cells: potential targets for treating transplant vasculopathy. Curr Vasc Pharmacol. 2003;1:1-9.
111. Hedin U, Roy J, Tran PK. Control of smooth muscle cell proliferation in vascular disease. Curr Opin Lipidol. 2004;15:559-565.
112. Eisen H, Kobashigawa J, Starling RC, Valantine H, Mancini D. Improving outcomes in heart transplantation: the potential of proliferation signal inhibitors. Transplant Proc. 2005;37:4S-17S.
113. Gordon D, Reidy MA, Benditt EP, Schwartz SM. Cell proliferation in human coronary arteries. Proc Natl Acad Sci U S A. 1990;87:4600-4604.
114. Libby P, Salomon RN, Payne DD, Schoen FJ, Pober JS. Functions of vascular wall cells related to development of transplantation-associated coronary arteriosclerosis. Transplant Proc. 1989;21:3677-3684.
115. Isoda K, Sawada S, Ishigami N, Matsuki T, Miyazaki K, Kusuhara M, Iwakura Y, Ohsuzu F. Lack of interleukin-1 receptor antagonist modulates plaque composition in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2004;24:1068-1073.
116. Lattmann T, Hein M, Horber S, Ortmann J, Teixeira MM, Souza DG, Haas E, Tornillo L, Munter K, Vetter W, Barton M. Activation of pro-inflammatory and anti-inflammatory cytokines in host organs during chronic allograft rejection: role of endothelin receptor signaling. Am J Transplant. 2005;5:1042-1049.
117. Isoda K, Shiigai M, Ishigami N, Matsuki T, Horai R, Nishikawa K, Kusuhara M, Nishida Y, Iwakura Y, Ohsuzu F. Deficiency of interleukin-1 receptor antagonist promotes neointimal formation after injury. Circulation. 2003;108:516-518.
118. Hillebrands JL, Onuta G, Rozing J. Role of progenitor cells in transplant arteriosclerosis. Trends Cardiovasc Med. 2005;15:1-8.
119. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. 2002;8:403-409.
120. Rahmani M, Wong BW, Ang L, Cheung CC, Carthy JM, Walinski H, McManus BM. Versican: signaling to transcriptional control pathways. Can J Physiol Pharmacol. 2006;84:77-92.
121. Williams KJ. Arterial wall chondroitin sulfate proteoglycans: diverse molecules with distinct roles in lipoprotein retention and atherogenesis. Curr Opin Lipidol. 2001;12:477-487.
122. Williams KJ, Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol. 1995;15:551-561.
123. Kolset SO, Salmivirta M. Cell surface heparan sulfate proteoglycans and lipoprotein metabolism. Cell Mol Life Sci. 1999;56:857-870.
124. el-Sawy T, Fahmy NM, Fairchild RL. Chemokines: directing leukocyte infiltration into allografts. Curr Opin Immunol. 2002;14:562-568.
125. Bingley JA, Hayward IP, Campbell JH, Campbell GR. 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.
126. Weiser MC, Belknap JK, Grieshaber SS, Kinsella MG, Majack RA. Developmental regulation of perlecan gene expression in aortic smooth muscle cells. Matrix Biol. 1996;15:331-340.
127. Vikramadithyan RK, Kako Y, Chen G, Hu Y, Arikawa-Hirasawa E, Yamada Y, Goldberg IJ. Atherosclerosis in perlecan heterozygous mice. J Lipid Res. 2004;45:1806-1812.
128. Costell M, Gustafsson E, Aszodi A, Morgelin M, Bloch W, Hunziker E, Addicks K, Timpl R, Fassler R. Perlecan maintains the integrity of cartilage and some basement membranes. J Cell Biol. 1999;147:1109-1122.