Enhanced Cytomegalovirus Infection in Atherosclerotic Human Blood Vessels

American Journal of Pathology

Volumn 164, Issue 2, 2004, Pages 589-600

  Nerheim, Pamela L ^a   Meier, Jeffery L ^a,b   Vasef, Mohammad A ^a   Li, Wei Gen ^a   Hu, Ling ^a   Rice, James B ^a   Gavrila, Daniel ^a   Richenbacher, Wayne E ^a   Weintraub, Neal L ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN;

ADVENTITIA; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BLOOD VESSEL OCCLUSION; CONTROLLED STUDY; CORONARY ARTERY; CYTOMEGALOVIRUS INFECTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMEDIATE EARLY GENE; INTERNAL MAMMARY ARTERY; INTIMA; PRIORITY JOURNAL; SAPHENOUS VEIN; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE; ANIMAL; ARTERIOSCLEROSIS; ARTERY; COMPARATIVE STUDY; CYTOMEGALIC INCLUSION BODY DISEASE; CYTOMEGALOVIRUS; IMMUNOHISTOCHEMISTRY; METABOLISM; ORGAN CULTURE TECHNIQUE; PATHOGENICITY; VIROLOGY;

ANIMALS; ANTIGENS, CD31; ARTERIES; ARTERIOSCLEROSIS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; HUMANS; IMMUNOHISTOCHEMISTRY; ORGAN CULTURE TECHNIQUES; SAPHENOUS VEIN; TUNICA INTIMA;

EID: 1542379712     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)63148-3     Document Type: Article

References (72)

1. Levi M: CMV endothelitis as a factor in the pathogenesis of atherosclerosis. Cardiovasc Res 2001, 50:432-433
2. Bruggeman CA, Marjorie HJ, Nelissen-Vrancken G: Cytomegalovirus and atherosclerosis. Antiviral Res 1999, 43:191-200
3. Epstein SE, Speir E, Zhou YF, Guetta E, Leon M, Finkel T: The role of infection in restenosis and atherosclerosis: focus on cytomegalovirus. Lancet 1996, 348:13-17
4. Nieto FJ, Adam E, Farzadegan H, Melnick JL, Comstock GW, Szklo M: Cohort study of cytomegalovirus infection as a risk factor for carotid intimal-medial thickening, a measure of subclinical atherosclerosis. Circulation 1996, 94:922-927
5. Zhou YF, Leon MB, Waclawiw MA, Popma JJ, Yu ZX, Finkel T, Epstein SE: Association between prior cytomegalovirus infection and the risk of restenosis after coronary atherectomy. N Engl J Med 1996, 335: 624-630
6. Zhu J, Nieto J, Horne BD, Anderson JL, Muhlestein JB, Epstein SE: Prospective study of pathogen burden and risk of myocardial infarction or death. Circulation 2001, 103:45-51
7. Smieja M, Gnarpe J, Lonn E, Gnarpe H, Olsson G, Yi Q, Dzavik V, McQueen M, Yusuf S: Multiple infections and subsequent cardiovascular events in the heart outcomes prevention evaluation (HOPE) study. Circulation 2003, 107:251-257
8. Muhlestein J, Horne B, Carlquist J, Madsen T, Bair T, Egger M, Morris M, Peterson C, Habashi J, Anderson J: Cytomegalovirus seropositivity and c-reactive protein have independent and combined predictive value for mortality in patients with angiographically-demonstrated coronary artery disease. Circulation 2000, 102:1917-1923
9. Gratten MT, Moreno-Cabral CE, Starnes VA, Oyer PE, Stinson EB, Shumway NE: Cytomegalovirus infection is associated with cardiac allograft rejection and atherosclerosis. JAMA 1989, 261:3561-3566
10. Bruning JH, Persoons MCJ, Lemstrom KB, Stals FS, De Clerq E, Bruggeman CA: Enhancement of transplantation associated atherosclerosis by CMV, which can be prevented by antiviral therapy in the form of HPMPC. Tranplant Int 1994, 7:365-370
11. Libby P, Ergan D, Skarlatos S: Roles of infectious agents in atherosclerosis and restenosis. An assessment of evidence and need for future research. Circulation 1997, 96:4095-4103
12. Fong IW: Emerging relations between infectious diseases and coronary artery disease and atherosclerosis. Canadian Med Assoc J 2000, 163:49-56
13. de Boer OJ, van der Wal AC, Becker AE: Atherosclerosis, inflammation, and infection. J Pathol 2000, 190:237-243
14. Wu TC, Hruban RH, Ambinder RF, Pizzorno M, Cameron DE, Baumgartner WA, Reitz BA, Hayward GS, Hutchins GM: Demonstration of cytomegalovirus nucleic acids in the coronary arteries of transplanted hearts. Am J Pathol 1992, 140:739-747
15. Yamashiroya HM, Ghosh L, Yang R, Robertson AL: Herpesviridae in the coronary arteries and aorta of trauma victims. Am J Pathol 1988, 130:71-79
16. Speir E, Modali R, Huang E, Leon MB, Shawl F, Finkel T, Epstein SE: Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science 1994, 265:391-394
17. Melnick JL, Burek J, Adam E, DeBakey ME: Cytomegalovirus DNA in arterial walls of patients with atherosclerosis. J Med Virol 1994, 42: 170-174
18. Matthews-Geer JM, Eggerstedt JM, Gonzalez E, Jamison RM, Washington CD: Investigation of the prevalence of cardiovascular-associated cytomegalovirus among patients with coronary artery disease at Louisiana State University Medical Center at Shreveport. J Infect Dis 1998, 177:1860-1861
19. Hendrix MGR, Dormans PHR, Kitslaar P, Bosman F, Bruggeman CA: The presence of CMV nucleic acids in arterial walls of atherosclerotic and non-atherosclerotic patients. Am J Pathol 1989, 134:1151-1157
20. Sinzger C, Grefte A, Plachter B, Gouw ASH, Hauw The T, Jahn G: Fibroblasts, epithelial cells, endothelial cells, and smooth muscle cells are the major targets of human cytomegalovirus infection in lung and gastrointestinal tissues. J Gen Virol 1995, 76:741-750
21. Persoons MCJ, Daemen MJAP, Bruning JH, Bruggeman CA: Active cytomegalovirus infection of the arterial smooth muscle cells in immunocompromised rats. A clue to herpesvirus associated atherosclerosis? Circ Res 1994, 25:214-220
22. Tumilowicz JJ, Gawlik ME, Pwell BB, Tretin JJ: Replication of cytomegalovirus in human smooth muscle cells. J Virol 1985, 56:839-845
23. Kahl M, Siegel-Axel D, Stenglein S, Jahn G, Szinger C: Efficient lytic infection of human arterial endothelial cells by human cytomegalovirus strains. J Virol 2000, 74:7628-7635
24. Murphy EA, Streblow DN, Nelson JA, Stinski MS: The human cytomegalovirus IE86 protein can block cell cycle progression after inducing transition into the S phase of permissive cells. J Virol 2000, 74:7108-7118
25. van Dam-Miers MCE, Muller AD, van Hinsbergh VWM, Mullers WJ, Bomans PH, Bruggerman CA: The procoagulant response of cytomegalovirus infected endothelial cells. Thromb Haemost 1992, 68: 364-370
26. Shibutani T, Johnson TM, Yu Z-X, Ferrans VJ, Moss J, Epstein SE: Pertussis toxin-sensitive G protein as mediators of the signal pathways activated by cytomegalovirus infection of smooth muscle cells. J Clin Invest 1997, 100:2054-2061
27. Speir E, Yu Z-X, Ferrans VJ, Huang E-S, Epstein SE: Aspirin attenuates cytomegalovirus infectivity and gene expression mediated by cyclooxygenase-2 in coronary artery smooth muscle cells. Circ Res 1998, 83:210-216
28. Speir E, Shibutani T, Yu Z-X, Ferrans V, Epstein SE: Role of reactive oxygen intermediates in cytomegalovirus gene expression and in the response of human smooth muscle cells to viral infection. Circ Res 1996, 79:1143-1152
29. Sindre H, Haraldsen G, Beck S, Hestdal K, Kvale D, Brandtzaeg P, Degre M, Rollag H: Human intestinal endothelium shows high susceptibility to cytomegalovirus and altered expression of adhesion molecules after infection. Scand J Immunol 2000, 51:354-360
30. Sedmak DD, Knight DA, Vook NC, Waldman JW: Divergent patterns of ELAM-1, ICAM-1, and VCAM-1 expression on cytomegalovirus infected endothelial cells. Transplantation 1994, 58:1379-1385
31. Shahgasempour S, Woodroffe SB, Garnett HM: Alterations in the expression of ELAM-1, ICAM-1 and VCAM-1 after in vitro infection of endothelial cells with a clinical isolate of human cytomegalovirus. Microbiol Immunol 1997, 41:121-129
32. Guetta E, Scarpati EM, DiCorleto PE: Effect of cytomegalovirus immediate early gene products on endothelial cell gene activity. Cardiovasc Res 2001, 50:538-546
33. Zhou YF, Guetta E, Yu ZX, Finkel T, Epstein S: Human cytomegalovirus increases modified low density lipoprotein uptake and scavenger receptor mRNA expression in vascular smooth muscle cells. J Clin Invest 1996, 98:2129-2138
34. Streblow DN, Soderberg-Naucler C, Vieira J, Smith P, Wakabayashi E, Ruchti F, Mattison K, Altschuler Y, Nelson JA: The human cytomegalovirus chemokine receptor US28 mediates vascular smooth muscle cell migration. Cell 1999, 99:511-520
35. Ricotta D, Alessandri G, Pollara C, Fiorentini S, Favilli F, Tosetti M, Mantovani A, Grassi M, Garrafa E, Dei Cas L, Muneretto C, Caruso A: Adult human heart microvascular endothelial cells are permissive for non-lytic infection by human cytomegalovirus. Cardiovasc Res 2001, 49:440-448
36. Grundy JE, Lawson KM, MacCormac LP, Fletcher JM, Yong KL: Cytomegalovirus-infected endothelial cells recruit neutrophils by the secretion of C-X-C chemokines and transmit virus by direct neutrophil-endothelial cell contact and during neutrophil transendothelial migration. J Infect Dis 1998, 177:1465-1474
37. Schroeder MB, Worthen GS: Viral regulation of RANTES expression during human cytomegalovirus infection of endothelial cells. J Virol 2001, 75:3383-3390
38. Mocarski ES, Courcelle CT. Cytomegalovirus and its replication. Fields Virology, ed 4. Edited by DM Knipe, PM Howley. Philadelphia, Lippincott-Raven Publishers, 2001, pp 2629-2673
39. Fang X, Kaduce TL, Weintraub NL, VanRollins M, Spector AA: Functional implications of a newly-characterized pathway of 11,12-epoxyeicosatrienoic acid metabolism in arterial smooth muscle. Circ Res 1996, 79:784-793
40. Weintraub NL, Fang X, Kaduce TL, VanRollins M, Chatterjee P, Spector AA. Potentiation of endothelium-dependent relaxation by epoxyeicosatrienoic acids. Circ Res 1997;81:258-267
41. Meier JL, Stinski MF: Effect of a modulator deletion on transcription of the human cytomegalovirus major immediate-early genes in infected undifferentiated and differentiated cells. J Virol 1997, 71:1246-1255
42. Meier JL, Pruessner J: The human cytomegalovirus major immediate-early distal enhancer region is required for efficient viral replication and immediate-early gene expression. J Virol 2000, 74:1602-1613
43. Meier JL: Reactivation of the human cytomegalovirus major immediate-early regulatory region and viral replication in embryonal NTera2 cells: role of trichostatin A, retinoic acid, and deletion of the 21-base-pair repeats and modulator. J Virol 2001, 75:1581-1593
44. Holt CM, Francis SE, Roger S, Gadson PA, Taylor T, Celland C, Soyombo A, Newby AC: Intimal proliferation in an organ culture of human internal mammary artery. Cardiovasc Res 1992, 26:1189-1194
45. Kranzhoefer A, Baker AH, George SJ, Newby AC: Expression of tissue inhibitor of metalloproteinase-1, -2, and -3 during neointima formation in organ cultures of human saphenous vein. Arterioscler Thromb Vasc Biol 1999, 19:225-265
46. Soyombo AA, Angelini GD, Bryan AJ, Jasani B, Newby AC: Intimal proliferation in an organ culture of saphenous vein. Am J Pathol 1990, 137:1401-1410
47. Sheibani K, Tubbs RR: Enzyme immunohistochemistry: technical aspects. Semin Diag Pathol 1984, 1:235-250
48. Fish KN, Soderberg-Naucler C, Mills LK, Stenglein S, Nelson JA: Human cytomegalovirus persistently infects aortic endothelial cells. J Virol 1998, 72:5661-5668
49. Sinzger C, Jahn G: Human cytomegalovirus cell tropism and pathogenesis. Intervirology 1996, 39:302-319
50. Min KW, Wickemeyer WJ, Chandran P, Shadur CA, Gervich D, Phillips SJ, Zeff RH, Song J: Fatal cytomegalovirus infection and coronary arterial thromboses after heart transplantation: a case report. J Heart Transplant 1987, 6:100-105
51. Muldoon J, O'Riordan K, Rao S, Abecassis M: Ischemic colitis secondary to venous thrombosis. Transplantation 1996, 61:1651-1653
52. Ofotokun I, Carlson C, Gitlin SD, Elta G, Singleton TP, Markovitz DM: Acute cytomegalovirus infection complicated by vascular thrombosis. J Infect Dis 2001, 32:983-986
53. Rey FE, Pagano PJ: The reactive adventitia: fibroblast oxidase in vascular function. Arterscler Thromb Vasc Biol 2002, 22:1962-1971
54. Schwartz CJ, Mitchell JRA: Cellular infiltration of the human arterial adventitia associated with atheromatous plaques. Circulation 1962, 26:73-78
55. Azevedo LCP, Pedro MA, Souza LC, Souza HP, Janiszwski M, Protasio LL, Laurindo FRM: Oxidative stress as a signaling mechanism of the vascular response to injury: the redox hypothesis of restenosis. Cardiovasc Res 2000, 47:436-445
56. Miller FJ, Gutterman DD, Rios CD, Heistad DD, Davidson BL: Superoxide production in vascular smooth muscle contributes to oxidative stress and impaired relaxation in atherosclerosis. Circ Res 1998, 82:1298-1305
57. Ohara Y, Peterson TE, Harrison DG: Hypercholestolemia increases endothelial superoxide anion production. J Clin Invest 1993, 91: 2546-2551
58. Souza HP, Souza LC, Anastacio VM, Pereira AC, Junqueira DLM, Krieger JE, da Luz PL, Augusto O, Lauindo FRM: Vascular oxidant stress early after balloon injury: evidence for increased NAD(P)H oxidoreductase activity. Free Radic Biol Med 2000, 28:1232-1242
59. Lund DD, Faraci FM, Ooboshi H, Davidson BL, Heistad DD: Adenovirus-mediated gene transfer is augmented in basilar and carotid arteries of heritable hyperlipidemic rabbits. Stroke 1998, 29:120-125
60. Pauly RR, Pasaniti A, Crow M, Kinsella JL, Papadopoulos N, Monticone R, Lakatta EG, Martin GR: Experimental models that mimic the differentiation and dedifferentiation of vascular cells. Circulation 1992, 86(suppl III):III-68-III-73
61. Yoshikazu Y, Nakagawa K, Tanaka S, Mori R, Sugimachi K, Sueishi K: In situ detection of frequent and active infection of human cytomegalovirus in inflammatory abdominal aortic aneursyms: possible pathogenic role in sustained chronic inflammatory reaction. Lab Invest 1996, 74:723-736
62. Taylor-Wiedeman J, Sissons JG, Borysiewicz LK, Sinclair JH: Monocytes are a major site of persistence of human cytomegalovirus in peripheral blood mononuclear cells. J Gen Virol 1991, 72:2059-2064
63. Soderberg-Naucler NC, Fish KN, Nelson JA: Reactivation of latent human cytomegalovirus from by allogenic stimulation of blood cells from healthy donors. Cell 1997, 91:119-126
64. Hahn G, Jores R, Mocarski ES: Cytomegalovirus remains latent in a common precursor of dendritic and myeloid cells. Proc Natl Acad Sci USA 1998, 95:3937-3942
65. Mendelson M, Monard S, Sissons P, Sinclair J: Detection of endogenous human cytomegalovirus in CD34+ bone marrow progenitors. J Gen Virol 1996, 77:3099-3102
66. Bolvovan-Fritts C, Wiedeman JA: Human cytomegalovirus strain Toledo lacks a virus-encoded tropism factor required for infection of aortic endothelial cells. J Infect Dis 2001, 184:1252-1261
67. Sinzger C, Kahl M, Laib K, Klingel K, Reiger P, Plachter B, Jahn G: Tropism of human cytomegalovirus for endothelial cells is determined by a post-entry step dependent on efficient translocation to the nucleus. J Gen Virol 2000, 81:3021-3035
68. Waldman WJ, Sneddon JM, Stephens RE, Roberts WH: Enhanced endothelial cytopathogenicity induced by a cytomegalovirus strain propagated in endothelial cells. J Med Virol 1989, 28:223-300
69. Gerna G, Percivalle E, Baldanti F, Sozzani S, Lanzarini P, Genini E, Lilleri D, Revello MG: Human cytomegalovirus replicates abortively in polymorphonuclear leukocytes after transfer from infected endothelial cells via transient microfusion events. J Virol 2000, 74:5629-5638
70. Guetta E, Guetta V, Shibutani T, Epstein SE: Monocytes harboring cytomegalovirus: interactions with endothelial cells, smooth muscle cells, and oxidized low-density lipoprotein. Circulation Research 1997, 81:8-16
71. Waldman WJ, Knight DA, Huang EH, Sedmak DD: Bidirectional transmission of infectious cytomegalovirus between monocytes and vascular endothelial cells: an in vitro model. J Infect Dis 1995, 171:263-272
72. Schaarschnudt P, Reinhardt B, Michel D, Vaida B, Mayr K, Luske A, Baur R, Gschwend J, Klieinschmidt K, Kountidis M, Wenderoth U, Voisard R, Mertens T: Altered expression of extracellular matrix in human cytomegalovirus-infected cells and a human artery organ culture model to study its biological relevance. Intervirology 1999, 42:357-364