The Role of Viruses in Cardiac Allograft Vasculopathy

American Journal of Transplantation

Volumn 4, Issue 2, 2004, Pages 169-177

  Valantine, Hannah A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytomegalovirus; Endothelial dysfunction; Transplant vasculopathy

Indexed keywords

ANTIVIRUS AGENT; CHEMOKINE; CYTOKINE; GANCICLOVIR; IMMEDIATE EARLY PROTEIN; IMMEDIATE EARLY PROTEIN 1; IMMEDIATE EARLY PROTEIN 2; INTERCELLULAR ADHESION MOLECULE 1; NITRIC OXIDE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ADENOVIRUS; ADULT; ALLOGRAFT; ANIMAL MODEL; ARTERIOSCLEROSIS; CARDIOVASCULAR RISK; CELL MIGRATION; CELL PROLIFERATION; DISEASE COURSE; GRAFT REJECTION; HEART GRAFT; HEART MUSCLE BIOPSY; HUMAN; HUMAN CYTOMEGALOVIRUS; HUMAN TISSUE; MOUSE; NONHUMAN; PREDICTION; PRIORITY JOURNAL; PROPHYLAXIS; SHORT SURVEY; SMOOTH MUSCLE FIBER; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE; VIREMIA; VIRUS GENOME;

ANIMALS; ARTERIOSCLEROSIS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HEART TRANSPLANTATION; HUMANS; NITRIC OXIDE; POSTOPERATIVE COMPLICATIONS; TRANSPLANTATION, HOMOLOGOUS;

EID: 1342325544     PISSN: 16006135     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1600-6143.2003.00316.x     Document Type: Short Survey

References (72)

1. Yeung AC, Davis SF, Hauptman PJ et al. Incidence and progression of transplant coronary artery disease over 1 year: results of a multicenter trial with use of intravascular ultrasound. Multicenter Intravascular Ultrasound Transplant Study Group. J Heart Lung Transplant 1995; 14: (6 Pt 2): S215-S220.
2. Gao SZ, Schroeder JS, Alderman EL et al. Prevalence of accelerated coronary artery disease in heart transplant survivors. Comparison of cyclosporine and azathioprine regimens. Circulation 1989; 80: III100.
3. Yamani MH, Cook D, Starling RC et al. Myocardial ischemic injury following heart transplantation is associated with decreased risk of acute cellular rejection in the absence of humoral rejection. J Heart Lung Transplant 2001; 20: 238.
4. Yamani MHSR, Young JB, Cook D et al. Acute vascular rejection is associated with up-regulation of vitronectin receptor (alphav-beta3), increased expression of tissue factor, and activation of the extracellular matrix metalloproteinase induction system. J Heart Lung Transplant 2002; 21: 983.
5. Valantine H, Rickenbacker P, Kemna M et al. Metabolic abnormalities characteristic of dysmetabolic syndrome predict the development of transplant coronary artery disease: a prospective study. Circulation 2001; 103: 2144.
6. Fabricant CG, Fabricant J. Atherosclerosis induced by infection with Marek's disease herpesvirus in chickens. Am Heart J 1999; 138: S465.
7. Berencsi K, Endresz V, Klurfeld D, Kari L, Kritchevsky D, Gonozol E. Early atherosclerotic plaques in the aorta following cytomegalovirus infection of mice. Cell Adhes Commun 1998; 5: 39.
8. Bruggeman CA. Does Cytomegalovirus Play a Role in Atherosclerosis? Herpes 2000; 7: 51.
9. Kloover JS, Soots AP, Krogerus LA et al. Rat cytomegalovirus infection in kidney allograft recipients is associated with increased expression of intracellular adhesion molecule-1 vascular adhesion molecule-1, and their ligands leukocyte function antigen-1 and very late antigen-4 in the graft. Transplantation 2000; 69: 2641.
10. Hendrix MG, Salimans MM, van Boven CP, Bruggeman CA. High prevalence of latently present cytomegalovirus in arterial walls of patients suffering from grade III atherosclerosis. Am J Pathol 1990; 136: 23.
11. Gulizia JM, Kandolf R, Kendall TJ et al. Infrequency of cytomegalovirus genome in coronary arteriopathy of human heart allografts. Am J Pathol 1995; 147: 461.
12. Bruggeman CA, Marjorie HJ, Nelissen-Vrancken G. Cytomegalovirus and atherogenesis. Antiviral Res 1999; 43: 135.
13. Speir E, Yu ZX, Ferrans VJ, Huang ES, Epstein SE. Aspirin attenuates cytomegalovirus infectivity and gene expression mediated by cyclooxygenase-2 in coronary artery smooth muscle cells. Circ Res 1998; 83: 210.
14. van Dorp WT, Jonges E, Bruggeman CA, Daha MR, van Es LA, van Der Woude FJ. Direct induction of MHC class I, but not class II, expression on endothelial cells by cytomegalovirus infection. Transplantation 1989; 48: 469.
15. Martelius T, Salmi M, Wu H et al. Induction of vascular adhesion protein-1 during liver allograft rejection and concomitant cytomegalovirus infection in rats. Am J Pathol 2000; 157: 1229.
16. Streblow DN, Orloff SL, Nelson JA. The HCMV chemokine receptor US28 is a potential target in vascular disease. Curr Drug Targets Infect Disord 2001; 1: 151.
17. Zhou YF, Yu ZX, Wanishsawad C, Shou M, Epstein SE. The immediate early gene products of human cytomegalovirus increase vascular smooth muscle cell migration, proliferation, and expression of PDGF beta-receptor. Biochem Biophys Res Commun 1999; 256: 608.
18. Speir E, Modali R, Huang ES et al. Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science 1994; 265: 391.
19. Tanaka K, Zou JP, Takeda K et al. Effects of human cytomegalovirus immediate-early proteins on p53- mediated apoptosis in coronary artery smooth muscle cells. Circulation 1999; 99: 1656.
20. Zhu H, Shen Y, Shenk T. Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J Virol 1995; 69: 7960.
21. van Dam-Mieras MC, Muller AD, van Hinsbergh VW, Mullers WJ, Bomans PH, Bruggeman CA. The procoagulant response of cytomegalovirus infected endothelial cells. Thromb Haemost 1992; 68: 364.
22. Pryzdial EL, Wright JF. Prothrombinase assembly on an enveloped virus: evidence that the cytomegalovirus surface contains procoagulant phospholipid. Blood 1994; 84: 3749.
23. Danesh J. Coronary heart disease, Helicobacter pylori, dental disease, Chlamydia pneumoniae, and cytomegalovirus: meta-analyses of prospective studies. Am Heart J 1999; 138: S434.
24. Danesh J, Whincup P, Walker M et al. Chlamydia pneumoniae IgG titres and coronary heart disease: prospective study and meta-analysis. Br Med J 2000; 321: 208.
25. Anderson JL, Carlquist JF, Muhlestein JB, Horne BD, Elmer SP. Evaluation of C-reactive protein, an inflammatory marker, and infectious serology as risk factors for coronary artery disease and myocardial infarction. J Am Coll Cardiol 1998; 32: 35.
26. Nieto FJ. Viruses and atherosclerosis: a critical review of the epidemiologic evidence. Am Heart J 1999; 138: S453.
27. Muhlestein JB, Horne BD, Carlquist JF et al. Cytomegalovirus seropositivity and C-reactive protein have independent and combined predictive value for mortality in patients with angiographically demonstrated coronary artery disease. Circulation 2000; 102: 1917.
28. Blankenberg S, Rupprecht HJ, Bickel C et al. Cytomegalovirus infection with interleukin-6 response predicts cardiac mortality in patients with coronary artery disease. Circulation 2001; 103: 2915.
29. Smieja M, Gnarpe J, Lonn E et al. Multiple infections and subsequent cardiovascular events in the Heart Outcomes Prevention Evaluation (HOPE) Study. Circulation 2003; 107: 251.
30. Zhu J, Quyyumi AA, Norman JE et al. Effects of total pathogen burden on coronary artery disease risk and C-reactive protein levels. Am J Cardiol 2000; 85: 140.
31. Zhu J, Nieto FJ, Horne BD, Anderson JL, Muhlestein JB, Epstein SE. Prospective study of pathogen burden and risk of myocardial infarction or death. Circulation 2001; 103: 45.
32. Rupprecht HJ, Blankenberg S, Bickel C et al. Impact of viral and bacterial infectious burden on long-term prognosis in patients with coronary artery disease. Circulation 2001; 104: 25.
33. Ross R. Atherosclerosis is an inflammatory disease. Am Heart J 1999; 138: S419.
34. Liuzzo G, Biasucci LM, Gallimore JR et al. The prognostic value of C-reactive protein and serum amyloid a protein in severe unstable angina. N Engl J Med 1994; 331: 417.
35. Zhu J, Quyyumi AA, Norman JE, Csako G, Epstein SE. Cytomegalovirus in the pathogenesis of atherosclerosis: the role of inflammation as reflected by elevated C-reactive protein levels. J Am Coll Cardiol 1999; 34: 1738.
36. Visser MR, Tracy PB, Vercellotti GM, Goodman JL, White JG, Jacob HS. Enhanced thrombin generation and platelet binding on herpes simplex virus-infected endothelium. Proc Natl Acad Sci USA 1988; 85: 8227.
37. Kol A, Sukhova GK, Lichtman AH, Libby P. Chlamydial heat shock protein 60 localizes in human atheroma and regulates macrophage tumor necrosis factor-alpha and matrix metalloproteinase expression. Circulation 1998; 98: 300.
38. Etingin OR, Silverstein RL, Friedman HM, Hajjar DP. Viral activation of the coagulation cascade: molecular interactions at the surface of infected endothelial cells. Cell 1990; 61: 657.
39. Dechend R, Maass M, Gieffers J et al. Chlamydia pneumoniae infection of vascular smooth muscle and endothelial cells activates NF-kappaB and induces tissue factor and PAI-1 expression: a potential link to accelerated arteriosclerosis. Circulation 1999; 100: 1369.
40. Epstein SE, Zhou YF, Zhu J. Infection and atherosclerosis: emerging mechanistic paradigms. Circulation 1999; 100: e20.
41. Prasad A, Zhu J, Halcox JP, Waclawiw MA, Epstein SE, Quyyumi AA. Predisposition to atherosclerosis by infections: role of endothelial dysfunction. Circulation 2002; 106: 184.
42. Grattan MT, Moreno-Cabral CE, Starnes VA, Oyer PE, Stinson EB, Shumway NE. Cytomegalovirus infection is associated with cardiac allograft rejection and atherosclerosis. JAMA 1989; 261: 3561.
43. Everett JP, Hershberger RE, Norman DJ et al. Prolonged cytomegalovirus infection with viremia is associated with development of cardiac allograft vasculopathy. J Heart Lung Transplant 1992; 11: 8133.
44. Shirali GSNJ, Chinnock RE, Johnston JK, Rosenthal GL, Bowles NE, Towbin JA. Association of viral genome with graft loss in children after cardiac transplantation. N Engl J Med 2001; 334: 1498.
45. Persoons MC, van Stals FS, dam Mieras MC, Bruggeman CA. Multiple organ involvement during experimental cytomegalovirus infection is associated with disseminated vascular pathology. J Pathol 1998; 184: 103.
46. Wu TC, Hruban RH, Ambinder RF et al. Demonstration of cytomegalovirus nucleic acids in the coronary arteries of transplanted hearts. Am J Pathol 1992; 140: 739.
47. Koskinen P, Lemstrom K, Bruggeman C, Lautenschlager I, Hayry P. Acute cytomegalovirus infection induces a subendothelial inflammation (endothelialitis) in the allograft vascular wall. A possible linkage with enhanced allograft arteriosclerosis. Am J Pathol 1994; 144: 41.
48. Balk A, Linden M, Meeter K et al. Is there a relationship between transplant coronary artery disease and the occurrence of CMV infection. J Heart Lung Transplant 1991; 10: 188.
49. 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.
50. Valantine HA, Gao SZ, Menon SG et al. Impact of prophylactic immediate posttransplant ganciclovir on development of transplant atherosclerosis: a post hoc analysis of a randomized, placebo-controlled study. Circulation 1999; 100: 61.
51. Hengel H, Weber C. Driving cells into atherosclerotic lesions - a deleterious role for viral chemokine receptors? Trends Microbiol 2000; 8: 294.
52. Streblow DN, Soderberg-Naucler C, Vieira J et al. The human cytomegalovirus chemokine receptor US28 mediates vascular smooth muscle cell migration. Cell 1999; 99: 511.
53. Penfold ME, Dairaghi DJ, Duke GM et al. Cytomegalovirus encodes a potent alpha chemokine. Proc Natl Acad Sci USA 1999; 96: 9839.
54. Naruse K, Shimizu K, Muramatsu M et al. Long-term inhibition of NO synthesis promotes atherosclerosis in the hypercholesterolemic rabbit thoracic aorta. PGH2 does not contribute to impaired endothelium-dependent relaxation. Arterioscler Thromb Vasc Biol 1994; 14: 746.
55. Yoshimura M, Yasue H, Nakayama M et al. A missense Glu298Asp variant in the endothelial nitric oxide synthase gene is associated with coronary spasm in the Japanese. Hum Genet 1998; 103: 65.
56. Weis M, Cooke JP. Cardiac Allograft Vasculopathy and Dysregulation of the NO Synthase Pathway. Arterioscler Thromb Vasc Biol 2003; 23: 567.
57. Yeung AC, Anderson T, Meredith I et al. Endothelial dysfunction in the development and detection of transplant coronary artery disease. J Heart Lung Transplant 1992; 11: S69.
58. Drexler H, Fischell TA, Pinto FJ et al. Effect of 1-arginine on coronary endothelial function in cardiac transplant recipients. Relation to vessel wall morphology. Circulation 1994; 89: 1615.
59. Davis SF, Yeung AC, Meredith IT et al. Early endothelial dysfunction predicts the development of transplant coronary artery disease at 1 year posttransplant. Circulation 1996; 93: 457.
60. Hollenberg SM, Klein LW, Parrillo JE et al. Coronary endothelial dysfunction after heart transplantation predicts allograft vasculopathy and cardiac death. Circulation 2001; 104: 3091.
61. 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.
62. Lee PC, Wang ZL, Qian S et al. Endothelial nitric oxide synthase protects aortic allografts from the development of transplant arteriosclerosis. Transplantation 2000; 69: 1186.
63. Iwata A, Sai S, Nitta Y et al. Liposome-mediated gene transfection of endothelial nitric oxide synthase reduces endothelial activation and leukocyte infiltration in transplanted hearts. Circulation 2001; 103: 2753.
64. 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.
65. Shears LL, Kawaharada N, Tzeng E et al. Inducible nitric oxide synthase suppresses the development of allograft arteriosclerosis. J Clin Invest 1997; 100: 2035.
66. Koglin J, Glysing-Jensen T, Mudgett JS, Russell ME. Exacerbated transplant arteriosclerosis in inducible nitric oxide-deficient mice. Circulation 1998; 97: 2059.
67. Wildhirt SM, Weis M, Schulze C et al. Expression of endomyocardial nitric oxide synthase and coronary endothelial function in human cardiac allografts. Circulation 2001; 104 (Suppl. 1): S336.
68. Lou H, Kodama T, Wang YN, Katz N, Ramwell P, Foegh ML. 1-arginine prevents heart transplant arteriosclerosis by modulating the vascular cell proliferative response to insulin-like growth factor-I and interleukin-6. J Heart Lung Transplant 1996; 15: 1248.
69. Burns LJ, Pooley JC, Walsh DJ, Vercellotti GM, Weber ML, Kovacs A. Intercellular adhesion molecule-1 expression in endothelial cells is activated by cytomegalovirus immediate early proteins. Transplantation 1999; 67: 137.
70. Knight DA, Briggs BR, Bennett CF, Harindranath N, Waldman WJ, Sedmak DD. Attenuation of cytomegalovirus-induced endothelial intercellular adhesion molecule-1 mRNA/protein expression and T lymphocyte adhesion by a 2-O-methoxyethyl antisense oligonucleotide. Transplantation 2000; 69: 417.
71. Hingorani AD, Cross J, Kharbanda RK et al. Acute systemic inflammation impairs endothelium-dependent dilatation in humans. Circulation 2000; 102: 994.
72. Alber DG, Powell KL, Vallance P, Goodwin DA, Grahame-Clarke C. Herpesvirus infection accelerates atherosclerosis in the apolipoprotein E-deficient mouse. Circulation 2000; 102: 779.