Human cytomegalovirus infection and atherothrombosis

Journal of Thrombosis and Thrombolysis

Volumn 33, Issue 2, 2012, Pages 160-172

  Popović, Milan ^a   Smiljanić, Katarina ^a   Dobutović, Branislava ^a   Syrovets, Tatiana ^b   Simmet, Thomas ^b   Isenović, Esma R ^a  

^a UNIVERSITY OF BELGRADE   (Serbia)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

Atherosclerosis; Coagulation; HCMV; Vascular inflammation

Indexed keywords

ACICLOVIR; BENZIMIDAVIR; CIDOFOVIR; CIDOFOVIR 3 HEXADECYLOXYPROPYL ESTER; FOSCARNET; GANCICLOVIR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOSUPPRESSIVE AGENT; LEFLUNOMIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; TRANSCRIPTION FACTOR SP1; VALACICLOVIR; VALGANCICLOVIR; VIRUS VACCINE;

ACUTE KIDNEY FAILURE; ANTIBODY TITER; ATHEROSCLEROSIS; CELL MIGRATION; CELL PROLIFERATION; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTION; DISEASE ASSOCIATION; DRUG EFFICACY; DRUG MEGADOSE; ELECTROLYTE DISTURBANCE; ENCEPHALITIS; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEPATITIS; HUMAN; LIPID STORAGE; LUNG TRANSPLANTATION; MACROPHAGE; MONOCYTE; NEPHROTOXICITY; PANCREAS TRANSPLANTATION; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINITIS; REVIEW; SEROPREVALENCE; SMOOTH MUSCLE FIBER; THROMBOSIS;

ATHEROSCLEROSIS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; ENDOTHELIUM, VASCULAR; HUMANS; THROMBOSIS;

EID: 84858859627     PISSN: 09295305     EISSN: 1573742X     Source Type: Journal    
DOI: 10.1007/s11239-011-0662-x     Document Type: Review

References (160)

1. Bombeli T, Mueller M, Haeberli A (1997) Anticoagulant properties of the vascular endothelium. Thromb Haemost 77:408-423 (Pubitemid 27121001)
2. Cines DB, Pollak ES, Buck CA, Loscalzo J, Zimmerman GA, McEver RP, Pober JS, Wick TM, Konkle BA, Schwartz BS, Barnathan ES, McCrae KR, Hug BA, Schmidt AM, Stern DM (1998) Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 91:3527-3561 (Pubitemid 28225719)
3. Rosenberg RD, Rosenberg JS (1984) Natural anticoagulant mechanisms. J Clin Invest 76:1-5
4. Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898-1902 (Pubitemid 23026727)
5. Zimmerman GA, Whatley RE, Benson DE, Prescott SM (1990) Endothelial cells for studies of platelet-activating factor and arachidonate metabolites. Methods Enzymol 187:520-535 (Pubitemid 20309318)
6. Fantone CJ, Ward PA (1982) Role of oxygen-derived free radicals and metabolites in leukocyte-dependent inflammatory reactions. Am J Pathol 107:395-418
7. Touyz RM (2003) Reactive oxygen species in vascular biology: role in arterial hypertension. Expert Rev Cardiovasc Ther 1:91-106
8. Lubrano V, Di Cecco P, Zucchelli GC (2006) Role of superoxide dismutase in vascular inflammation and in coronary artery disease. Clin Exp Med 6:84-88
9. Coughlin SR (1999) How the protease thrombin talks to cells. Proc Natl Acad Sci USA 96:11023-11027
10. Roth GJ (1992) Platelets and blood vessels: the adhesion event. Immunol Today 13:100-105
11. Butcher EC (1991) Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67:1033-1036
12. Ebnet K, Vestweber D (1999) Molecular mechanism that control leukocyte extravasation: the selectins and chemokines. Histochem Cell Biol 112:1-23 (Pubitemid 29356300)
13. Nawroth PP, Stern DM (1985) An endothelial cell procogaulant pathway. J Cell Biochem 28:253-264
14. Stern DM, Carpenter B, Nawroth PP (1986) Endothelium and the regulation of coagulation. Pathol Immunopathol Res 5:29-36
15. Springer TA (1990) Adhesion receptors of the immune system. Nature 346:425-434
16. Bevilacqua MP, Nelson RM, Mannori G, Cecconi O (1994) Endothelial-leukocyte adhesion molecules in human disease. Annu Rev Med 45:361-378 (Pubitemid 24158168)
17. Reeves M, Sinclair J (2008) Aspects of human cytomegalovirus latency and reactivation. Curr Top Microbiol Immunol 325:297-313
18. Vanegas F, Montalvo RD, Alvarez OA, Donelson SS, Lee M (2000) Massive upper gastrointestinal hemorrhage due to cytomegalovirus infection in two patients with acquired immunodeficiency syndrome. South Med J 93:235-238
19. Martin DF, Sierra-Madero J, Walmsley S, Wolitz RA, Macey K, Georgiou P, Robinson CA, Stempien MJ (2002) A controlled trial of valganciclovir as induction therapy for cytomegalovirus retinitis; Valganciclovir Study Group. N Engl J Med 346:1119-1126 (Pubitemid 34984602)
20. Bissinger AL, Sinzger C, Kaiserling E, Jahn G (2002) Human cytomegalovirus as a direct pathogen: correlation of multiorgan involvement and cell distribution with clinical and pathological findings in a case of congenital inclusion disease. J Med Virol 67:200-206 (Pubitemid 34493433)
21. Snydman DR (2008) Persistent clinical impact of cytomegalovirus in organ transplantation. Clin Infect Dis 47:883-884
22. Kotton CN (2010) Management of cytomegalovirus infection in solid organ transplantation. Nat Rev Nephrol 6:711-721
23. Morris MI, Fischer SA, Ison MG (2010) Infections transmitted by transplantation. Infect Dis Clin North Am 24:497-514
24. Epstein SE, Zhu J, Burnett MS, Zhou YF, Vercellotti G, Hajjar D (2000) Infection and atherosclerosis: potential roles of pathogen burden and molecular mimicry. Arterioscler Thromb Vasc Biol 20:1417-1420 (Pubitemid 30353867)
25. Streblow DN, Orloff SL, Nelson JA (2001) Do pathogens accelerate atherosclerosis? J Nutr 131:2798S-2804S (Pubitemid 32947814)
26. Yi L, Wang DX, Feng ZJ (2008) Detection of human cytomegalovirus in atherosclerotic carotid arteries in humans. J Formos Med Assoc 107:774-781
27. Xenaki E, Hassoulas J, Apostolakis S, Sourvinos G, Spandidos DA (2009) Detection of cytomegalovirus in atherosclerotic plaques and nonatherosclerotic arteries. Angiology 60:504-508
28. Fish KN, Stenglein SG, Ibanez C, Nelson JA (1995) Cytomegalovirus persistence in macrophages and endothelial cells. Scand J Infect Dis Suppl 99:34-40
29. Fish KN, Soderberg-Naucler C, Mills LK, Stenglein S, Nelson JA (1998) Human cytomegalovirus persistently infects aortic endothelial cells. J Virol 72:5661-5668 (Pubitemid 28283351)
30. Jarvis MA, Nelson JA (2002) Human cytomegalovirus persistence and latency in endothelial cells and macrophages. Curr Opin Microbiol 5:403-407
31. Sinzger C, Grefte A, Plachter B, Gouw AS, The TH, Jahn G (1995) Fibroblasts, epithelial cells, endothelial cells and smooth muscle cells are major targets of human cytomegalovirus infection in lung and gastrointestinal tissues. J Gen Virol 76:741-750
32. Sinzger C, Digel M, Jahn G (2008) Cytomegalovirus cell tropism. Curr Top Microbiol Immunol 325:63-83
33. Stanton RJ, Baluchova K, Dargan DJ, Cunningham C, Sheehy O, Seirafian S, McSharry BP, Neale ML, Davies JA, Tomasec P, Davison AJ, Wilkinson GW (2010) Reconstruction of the complete human cytomegalovirus genome in a BAC reveals RL13 to be a potent inhibitor of replication. J Clin Invest 120:3191-3208
34. Compton T, Nepomuceno RR, Nowlin DM (1992) Human cytomegalovirus penetrates host cells by pH-independent fusion at the cell surface. Virology 191:387-395
35. Ryckman BJ, Jarvis MA, Drummond DD, Nelson JA, Johnson DC (2006) Human cytomegalovirus entry into epithelial and endothelial cells depends on genes UL128 to UL150 and occurs by endocytosis and low-pH fusion. J Virol 80:710-722 (Pubitemid 43062884)
36. Mach M, Kropff B, Dal Monte P, Britt W (2000) Complex formation by human cytomegalovirus glycoproteins M (gpUL100) and N (gpUL73). J Virol 74:11881-11892 (Pubitemid 32222338)
37. Varnum SM, Streblow DN, Monroe ME, Smith P, Auberry KJ, Pasa-Tolic L, Wang D, Camp DG II, Rodland K, Wiley S, Britt W, Shenk T, Smith RD, Nelson JA (2004) Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J Virol 78:10960-10966 (Pubitemid 39299636)
38. Wang D, Shenk T (2005) Human cytomegalovirus UL131 open reading frame is required for epithelial cell tropism. J Virol 79:10330-10338 (Pubitemid 41098573)
39. Dengler TJ, Raftery MJ, Werle M, Zimmermann R, Schönrich G (2000) Cytomegalovirus infection of vascular cells induces expression of pro-inflammatory adhesion molecules by paracrine action of secreted interleukin-1beta. Transplantation 69:1160-1168 (Pubitemid 30217601)
40. Maisch T, Kropff B, Sinzger C, Mach M (2002) Upregulation of CD40 expression on endothelial cells infected with human cytomegalovirus. J Virol 76:12803-12812 (Pubitemid 35386964)
41. Gerna G, Percivalle E, Baldanti F, Sozzani S, Lanzarini P, Genini E, Lilleri D, Revello MG (2000) Human cytomegalovirus replicates abortively in polymorphonuclear leukocytes after transfer from infected endothelial cells via transient microfusion events. J Virol 74:5629-5638 (Pubitemid 30346597)
42. Rahbar A, Söderberg-Nauclér C (2005) Human cytomegalovirus infection of endothelial cells triggers platelet adhesion and aggregation. J Virol 79:2211-2220 (Pubitemid 40204578)
43. Bentz GL, Yurochko AD (2008) Human CMV infection of endothelial cells induces an angiogenic response through viral binding to EGF receptor and beta1 and beta3 integrins. Proc Natl Acad Sci USA 105:5531-5536 (Pubitemid 351753897)
44. Wang X, Huong SM, Chiu ML, Raab-Traub N, Huang ES (2003) Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature 424:456-461 (Pubitemid 36917497)
45. Beutler T, Höflich C, Stevens PA, Krüger DH, Prösch S (2003) Downregulation of the epidermal growth factor receptor by human cytomegalovirus infection in human fetal lung fibroblasts. Am J Respir Cell Mol Biol 28:86-94 (Pubitemid 36017054)
46. Isaacson MK, Feire AL, Compton T (2007) Epidermal growth factor receptor is not required for human cytomegalovirus entry or signaling. J Virol 81:6241-6247 (Pubitemid 46878030)
47. Zhou YF, Yu ZX, Wanishsawad C, Shou M, Epstein SE (1999) 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 256:608-613 (Pubitemid 29301154)
48. Reinhardt B, Mertens T, Mayr-Beyrle U, Frank H, Lüske A, Schierling K, Waltenberger J (2005) HCMV infection of human vascular smooth muscle cells leads to enhanced expression of functionally intact PDGF beta-receptor. Cardiovasc Res 67:151-160 (Pubitemid 40798302)
49. Hajjar DP (1986) Herpesvirus infection prevents activation of cytoplasmic cholesteryl esterase in arterial smooth muscle cells. J Biol Chem 261:7611-7614
50. Zhou YF, Guetta E, Yu ZX, Finkel T, Epstein SE (1996) Human cytomegalovirus increases modified low density lipoprotein uptake and scavenger receptor mRNA expression in vascular smooth muscle cells. J Clin Invest 98:2129-2138 (Pubitemid 26376302)
51. Andreoni KA, Wang X, Huang SM, Huang ES (2002) Human cytomegalovirus hyperimmune globulin not only neutralizes HCMV infectivity, but also inhibits HCMV-induced intracellular NF-kappaB, Sp1, and PI3-K signaling pathways. J Med Virol 67:33-40 (Pubitemid 34260073)
52. Bentz GL, Jarquin-Pardo M, Chan G, Smith MS, Sinzger C, Yurochko AD (2006) Human cytomegalovirus (HCMV) infection of endothelial cells promotes naive monocyte extravasation and transfer of productive virus to enhance hematogenous dissemination of HCMV. J Virol 80:11539-11555 (Pubitemid 44788869)
53. Schäfer P, Tenschert W, Cremaschi L, Schröter M, Gutensohn K, Laufs R (2000) Cytomegalovirus cultured from different major leukocyte subpopulations: association with clinical features in CMV immunoglobulin G-positive renal allograft recipients. J Med Virol 61:488-496 (Pubitemid 30450691)
54. Dargan DJ, Douglas E, Cunningham C, Jamieson F, Stanton RJ, Baluchova K, McSharry BP, Tomasec P, Emery VC, Percivalle E, Sarasini A, Gerna G, Wilkinson GW, Davison AJ (2010) Sequential mutations associated with adaptation of human cytomegalovirus to growth in cell culture. J Gen Virol 91:1535-1546
55. Prichard MN, Penfold ME, Duke GM, Spaete RR, Kemble GW (2001) A review of genetic differences between limited and extensively passaged human cytomegalovirus strains. Rev Med Virol 11:191-200 (Pubitemid 32510202)
56. Bradley AJ, Lurain NS, Ghazal P, Trivedi U, Cunningham C, Baluchova K, Gatherer D, Wilkinson GW, Dargan DJ, Davison AJ (2009) High-throughput sequence analysis of variants of human cytomegalovirus strains Towne and AD169. J Gen Virol 90:2375-2380
57. van Dam-Mieras MC, Bruggeman CA, Muller AD, Debie WH, Zwaal RF (1987) Induction of endothelial cell procoagulant activity by cytomegalovirus infection. Thromb Res 47:69-75 (Pubitemid 17117448)
58. Visser MR, Tracy PB, Vercellotti GM, Goodman JL, White JG, Jacob HS (1988) Enhanced thrombin generation and platelet binding on herpes simplex virus-infected endothelium. Proc Natl Acad Sci USA 85:8227-8230
59. van Dam-Mieras MC, Muller AD, van Hinsbergh VW, Mullers WJ, Bomans PH, Bruggeman CA (1992) The procoagulant response of cytomegalovirus infected endothelial cells. Thromb Haemost 88:364-370
60. Sutherland MR, Raynor CM, Leenknegt H, Wright JF, Pryzdial ELG (1997) Coagulation initiated on herpesviruses. Proc Natl Acad Sci USA 94:13510-13514 (Pubitemid 28009613)
61. Livingston JR, Sutherland MR, Friedman HM, Pryzdial EL (2006) Herpes simplex virus type 1-encoded glycoprotein C contributes to direct coagulation factor X-virus binding. Biochem J 393:529-535 (Pubitemid 43099092)
62. Levi M, van der Poll T, Buller HR (2004) Bidirectional relation between inflammation and coagulation. Circulation 109:2698-2704 (Pubitemid 38737913)
63. Etingin OR, Silverstein RL, Friedman HM, Hajjar DP (1990) Viral activation of the coagulation cascade: molecular interactions at the surface of infected endothelial cells. Cell 61:657-662
64. Melnick JL, Adam E, DeBakey ME (1990) Possible role of cytomegalovirus in atherogenesis. JAMA 263:2204-2207 (Pubitemid 20144500)
65. McSorley J, Shapiro L, Brownstein MH, Hsu KC (1974) Herpes simplex and varicella-zoster: comparative histopathology of 77 cases. Int J Dermatol 13:69-75
66. Phinney PR, Fligiel S, Bryson YJ, Porter DD (1982) Necrotizing vasculitis in a case of disseminated neonatal herpes simplex infection. Arch Pathol Lab Med 106:64-67 (Pubitemid 12223185)
67. Hruban RH, Wu T-C, Beschomer WE, Cameron DE, Ambinder R, Baumgartner WA, Reitz BA, Hutchins GM (1990) Cytomegalovirus nucleic acids in allografted hearts. Hum Pathol 21:981-982 (Pubitemid 20308425)
68. Foegh ML (1990) Chronic rejection - graft arteriosclerosis. Transplant Proc 22:119-122
69. Wu TC, Hruban RH, Ambinder RF, Pizzomo M, Cameron DE, Baumgartner WA, Reitz BA, Hayward GS, Hutchins GM (1992) Demonstration of cytomegalovirus nucleic acids in the coronary arteries of transplanted hearts. Am J Pathol 140:739-747
70. Fabricant CG, Fabricant J, Litrenta MM, Minick CR (1978) Virus induced atherosclerosis. J Exp Med 148:335-340
71. Fabricant CG, Fabricant J, Minick CR, Litrenta MM (1983) Herpesvirus induced atherosclerosis in chickens. Fed Proc 42:2476-2479
72. Span AHM, Grauls G, Bosman F, Vanboven CPA, Bruggeman CA (1992) Cytomegalovirus infection induces vascular injury in the rat. Atherosclerosis 93:41-52
73. Pryzdial EL, Wright JF (1994) Prothrombinase assembly on an enveloped virus: evidence that the cytomegalovirus surface contains procoagulant phospholipid. Blood 84:3749-3757 (Pubitemid 24362472)
74. Rosenberg RD (1985) Role of heparin and heparinlike molecules in thrombosis and atherosclerosis. Biochemistry 24:6723-6729
75. Rux AH, Lou H, Lambris JD, Friedman HM, Eisenberg RJ, Cohen GH (2005) Kinetic analysis of glycoprotein C of herpes simplex virus types 1 and 2 binding to heparin, heparan sulfate, and complement component C3b. Virology 294:324-332 (Pubitemid 34920531)
76. Etingin OR, Silverstein RL, Hajjar DP (1991) Identification of a monocyte receptor on herpesvirus-infected endothelial cells. Proc Natl Acad Sci USA 88:7200-7203 (Pubitemid 21915117)
77. Popović M, Paskas S, Zivković M, Burysek L, Laumonnier Y (2010) Human cytomegalovirus increases HUVEC sensitivity to thrombin and modulates expression of thrombin receptors. J Thromb Thrombolysis 30:164-171
78. Inacio C, Hillaire S, Valla D, Denninger MH, Casadevall N, Erlinger S (1997) Case report: cytomegalovirus infection as a cause of acute portal vein thrombosis. J Gastroenterol Hepatol 12:287-288 (Pubitemid 27244519)
79. Squizzato A, Gerdes VE, Buller HR (2005) Effects of human cytomegalovirus infection on the coagulation system. Thromb Haemost 93:403-410 (Pubitemid 40392525)
80. Ofotokun I, Carlson C, Gitlin SD, Elta G, Singleton TP, Markovitz DM (2001) Acute cytomegalovirus infection complicated by vascular thrombosis: a case report. Clin Infect Dis 32:983-986 (Pubitemid 32524834)
81. Abgueguen P, Delbos V, Chennebault JM, Payan C, Pichard E (2003) Vascular thrombosis and acute cytomegalovirus infection in immunocompetent patients: report of 2 cases and literature review. Clin Infect Dis 36:E134-E139
82. Khater FJ, Myers JW, Moorman JP (2003) A 45-year-old woman with fever and splenic infarcts. Clin Infect Dis 37:1125-1126
83. Atzmony L, Halutz O, Avidor B, Finn T, Zimmerman O, Steinvil A, Zeltser D, Giladi M, Justo D (2010) Incidence of cytomegalovirus-associated thrombosis and its risk factors: a case-control study. Thromb Res 126:e439-e443
84. Rovery C, Granel B, Parola P, Foucault C, Brouqui P (2005) Acute cytomegalovirus infection complicated by venous thrombosis: a case report. Ann Clin Microbiol Antimicrob 12:4-11
85. Delbos V, Abgueguen P, Chennebault JM, Fanello S, Pichard E (2007) Acute cytomegalovirus infection and venous thrombosis: role of antiphospholipid antibodies. J Infect 54:47-50
86. Gharavi AE, Pierangeli SS, Espinola RG, Liu X, Colden-Stanfield M, Harris EN (2002) Antiphospholipid antibodies induced in mice by immunization with a cytomegalovirus-derived peptide cause thrombosis and activation of endothelial cells in vivo. 46:545-552
87. Benditt EP, Benditt JM (1973) Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci USA 70:1753-1756
88. Gattone M, Iacoviello L, Colombo M, Castelnuovo AD, Soffiantino F, Gramoni A, Picco D, Benedetta M, Giannuzzi P (2001) Chlamydia pneumoniae and cytomegalovirus seropositivity, inflammatory markers, and the risk of myocardial infarction at a young age. Am Heart J 142:633-640 (Pubitemid 32900489)
89. Epstein SE, Zhou YF, Zhu J (1999) Infection and atherosclerosis: emerging mechanistic paradigms. Circulation 100:e20-e28
90. Ross R (1999) Atherosclerosis: an inflammatory disease. N Engl J Med 340:115-126
91. Libby P, Ridker PM, Maseri A (2002) Inflammation and atherosclerosis. Circulation 105:1135-1143 (Pubitemid 34212626)
92. Hansson GK (2005) Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352:1685-1695
93. Melnick JL, Petrie BL, Dreesman GR, McCollum CH, Petrie BL, Burek J, DeBakey ME (1983) Cytomegalovirus antigen within human arterial smooth muscle cells. Lancet 2:644-647 (Pubitemid 13003484)
94. Hendrix MGR, Salimans MMM, van Boven CPA, Bruggeman CA (1990) High prevalence of latently present cytomegalovirus in arterial walls of patients suffering from grade III atherosclerosis. Am J Pathol 136:23-28 (Pubitemid 20034949)
95. Adam E, Melnick JL, Probtsfield JL, Petrie BL, Bailey KR, McCollum CH, DeBakey ME (1987) High level of cytomegalovirus antibody in patients requiring vascular surgery for atherosclerosis. Lancet 2:291-293
96. Speir E, Modali R, Huang ES, Leon MB, Shawl F, Finkel T, Epstein SE (1994) Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science 256:391-394 (Pubitemid 24259971)
97. Zhou YF, Leon MB, Waclawiw MA, Popma JJ, Yu ZX, Finkel T, Epstein SE (1996) Association between prior cytomegalovirus infection and the risk of restenosis after coronary atherectomy. N Engl J Med 335:624-630 (Pubitemid 26277952)
98. Nieto FJ, Adam E, Sorlie P, Farzadegan H, Melnick JL, Comstock GW, Szklo M (1996) Cohort study of cytomegalovirus infection as a risk factor for carotid intimal-medial thickening, a measure of subclinical atherosclerosis. Circulation 94:922-927 (Pubitemid 26292841)
99. Blum A, Giladi M, Weinberg M, Kaplan G, Pasternack H, Laniado S, Miller H (1998) High anti-cytomegalovirus (CMV) IgG antibody titer is associated with coronary artery disease and may predict post-coronary balloon angioplasty restenosis. Am J Cardiol 81:866-868
100. Smith MG (1956) Propagation in tissues cultures of cytopathogenic virus from human salivary gland virus (SGV) disease. Proc Soc Exp Biol Med 92:424-430
101. Bale JF Jr, O'Neil ME (1989) Detection of murine cytomegalovirus DNA in circulating leukocytes harvested during acute infection of mice. J Virol 63:2667-2673
102. Fish KN, Depto AS, Moses AV, Britt W, Nelson JA (1995) Growth kinetics of human cytomegalovirus are altered in monocyte-derived macrophages. J Virol 69:3737-3743
103. Grefte A, Harmsen MC, van der Giessen M, Knollema S, van Son WJ, The TH (1994) Presence of human cytomegalovirus (HCMV) immediate early mRNA but not ppUL83 (lower matrix protein pp65) mRNA in polymorphonuclear and mononuclear leukocytes during active HCMV infection. J Gen Virol 75:1989-1998 (Pubitemid 24243080)
104. Hassan-Walker AF, Mattes FM, Griffiths PD, Emery VC (2001) Quantity of cytomegalovirus DNA in different leukocyte populations during active infection in vivo and the presence of gB and UL18 transcripts. J Med Virol 64:283-289 (Pubitemid 32565124)
105. Sinclair J, Sissons P (1996) Latent and persistent infections of monocytes and macrophages. Intervirology 39:293-301 (Pubitemid 27174133)
106. Sinzger C, Jahn G (1996) Human cytomegalovirus cell tropism and pathogenesis. Intervirology 39:302-319 (Pubitemid 27174134)
107. Gnann JW Jr, Ahlmén J, Svalander C, Olding L, Oldstone MB, Nelson JA (1988) Inflammatory cells in transplanted kidneys are infected by human cytomegalovirus. Am J Pathol 132:239-248
108. Manez R, Kusne S, Rinaldo C, Aguado JM, St George K, Grossi P, Frye B, Fung JJ, Ehrlich GD (1996) Time to detection of cytomegalovirus (CMV) DNA in blood leukocytes is a predictor for the development of CMV disease in CMV-seronegative recipients of allografts from CMV-seropositive donors following liver transplantation. J Infect Dis 173:1072-1076 (Pubitemid 26251447)
109. Plachter B, Sinzger C, Jahn G (1996) Cell types involved in replication and distribution of human cytomegalovirus. Adv Virus Res 46:195-261 (Pubitemid 3027524)
110. Saederup N, Lin YC, Dairaghi DJ, Schall TJ, Mocarski ES (1999) Cytomegalovirus-encoded beta chemokine promotes monocyte-associated viremia in the host. Proc Natl Acad Sci USA 96:10881-10886 (Pubitemid 29442238)
111. van der Strate BW, Hillebrands JL, Lycklama à Nijeholt SS, Beljaars L, Bruggeman CA, Van Luyn MJ, Rozing J, The TH, Meijer DK, Molema G, Harmsen MC (2003) Dissemination of rat cytomegalovirus through infected granulocytes and monocytes in vitro and in vivo. J Virol 77:11274-11278
112. Gerna G, Zipeto D, Percivalle E, Parea M, Revello MG, Maccario R, Peri G, Milanesi G (1992) Human cytomegalovirus infection of the major leukocyte subpopulations and evidence for initial viral replication in polymorphonuclear leukocytes from viremic patients. J Infect Dis 166:1236-1244
113. Taylor-Wiedeman J, Sissons P, Sinclair J (1994) Induction of endogenous human cytomegalovirus gene expression after differentiation of mono-cytes from healthy carriers. J Virol 68: 1597-1604 (Pubitemid 24065725)
114. Smith MS, Bentz GL, Alexander JS, Yurochko AD (2004) Human cytomegalovirus induces monocyte differentiation and migration as a strategy for dissemination and persistence. J Virol 78:4444-4453 (Pubitemid 38501064)
115. Smith MS, Bentz GL, Smith PM, Bivins ER, Yurochko AD (2004) HCMV activates PI(3)K in monocytes and promotes monocyte motility and transendothelial migration in a PI(3)Kdependent manner. J Leukoc Biol 76:65-76 (Pubitemid 38857173)
116. Isaacson MK, Juckem LK, Compton T (2008) Virus entry and innate immune activation. Curr Top Microbiol Immunol 325:85-100
117. Soroceanu L, Akhavan A, Cobbs CS (2008) Platelet derived growth factor-alpha receptor activation is required for human cytomegalovirus infection. Nature 455:391-395
118. Eggers M, Radsak K, Enders G, Reschke M (2001) Use of recombinant antigens gB and gH for diagnosis of primary human cytomegalovirus infection during pregnancy. J Med Virol 63:135-142 (Pubitemid 32142270)
119. Pass RF (2009) Development and evidence for efficacy of CMV glycoprotein B vaccine with MF59 adjuvant. J Clin Virol 46(Suppl 4):S73-S76
120. Cui X, Meza BP, Adler SP, McVoy MA (2008) Cytomegalovirus vaccines fail to induce epithelial entry neutralizing antibodies comparable to natural infection. Vaccine 26:5760-5766
121. Hahn G, Revello MG, Patrone M, Percivalle E, Campanini G, Sarasini A, Wagner M, Gallina A, Milanesi G, Koszinowski U, Baldanti F, Gerna G (2004) Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J Virol 78:10023-10033 (Pubitemid 39187120)
122. Saccoccio FM, Sauer AL, Cui X, Armstrong AE, Habib el-SE, Johnson DC, Ryckman BJ, Klingelhutz AJ, Adler SP, McVoy MA (2011) Peptides from cytomegalovirus UL130 and UL131 proteins induce high titer antibodies that block viral entry into mucosal epithelial cells. Vaccine 29:2705-2711
123. Gerna G, Sarasini A, Patrone M, Percivalle E, Fiorina L, Campanini G, Gallina A, Baldanti F, Revello MG (2008) Human cytomegalovirus serum neutralizing antibodies block virus infection of endothelial/epithelial cells, but not fibroblasts, early during primary infection. J Gen Virol 89:853-865
124. Macagno A, Bernasconi NL, Vanzetta F, Dander E, Sarasini A, Revello MG, Gerna G, Sallusto F, Lanzavecchia A (2010) Isolation of human monoclonal antibodies that potently neutralize human cytomegalovirus infection by targeting different epitopes on the gH/gL/UL128-131A complex. J Virol 84:1005-1013
125. Oliver SE, Cloud GA, Sánchez PJ, Demmler GJ, Dankner W, Shelton M, Jacobs RF, Vaudry W, Pass RF, Soong SJ, Whitley RJ, Kimberlin DW (2009) Neurodevelopmental outcomes following ganciclovir therapy in symptomatic congenital cytomegalovirus infections involving the central nervous system; National Institute of Allergy, Infectious Diseases Collaborative Antiviral Study Group. J Clin Virol 46(Suppl 4):S22-S26
126. Jabs DA (2001) The ganciclovir implant plus oral ganciclovir versus parenteral cidofovir for the treatment of cytomegalovirus retinitis in patients with acquired immunodeficiency syndrome: the ganciclovir cidofovir cytomegalovirus retinitis trial. Am J Ophthalmol 131:457-467
127. Jabs DA, Van Natta ML, Holbrook JT, Kempen JH, Meinert CL, Davis MD (2007) Longitudinal study of the ocular complications of AIDS:1. Ocular diagnoses at enrollment. Ophthalmology 114:780-786
128. Martin DF, Sierra-Madero J, Walmsley S, Wolitz RA, Macey K, Georgiou P, Robinson CA, Stempien MJ (2002) A controlled trial of valganciclovir as induction therapy for cytomegalovirus retinitis. N Engl J Med 347:1119-1126 (Pubitemid 34984602)
129. Paya C, Humar A, Dominguez E, Washburn K, Blumberg E, Alexander B, Freeman R, Heaton N, Pescovitz MD (2004) Efficacy and safety of valganciclovir vs. oral ganciclovir for prevention of cytomegalovirus disease in solid organ transplant recipients; Valganciclovir Solid Organ Transplant Study Group. Am J Transplant 4:611-620 (Pubitemid 38523584)
130. Reusser P, Einsele H, Lee J, Volin L, Rovira M, Engelhard D, Finke J, Cordonnier C, Link H, Ljungman P (2002) Randomized multicenter trial of foscarnet versus ganciclovir for preemptive therapy of cytomegalovirus infection after allogeneic stemcell transplantation; Infectious Diseases Working Party of the European Group for Blood and Marrow Transplantation. Blood 99:1159-1164 (Pubitemid 34547067)
131. Boeckh M, Geballe AP (2011) Cytomegalovirus: pathogen, paradigm, and puzzle. J Clin Invest 121:1673-1680
132. Lowance D, Neumayer HH, Legendre CM, Squifflet JP, Kovarik J, Brennan PJ, Norman D, Mendez R, Keating MR, Coggon GL, Crisp A, Lee IC (1990) Valacyclovir for the prevention of cytomegalovirus disease after renal transplantation; International Valacyclovir Cytomegalovirus Prophylaxis Transplantation Study Group. N Engl J Med 340:1462-1470
133. Blumberg EA, Hauser IA, Stanisic S, Mueller E, Berenson K, Gahlemann CG, Humar A, Jardine AG (2010) Prolonged prophylaxis with valganciclovir is cost effective in reducing posttransplant cytomegalovirus disease within the United States. Transplantation 90:1420-1426
134. Riba Solé M, Farré Riba R, Badell Serra I, Mangues Bafalluy MA (2011) Acyclovir-induced acute renal failure in a paediatric oncology patient. Farm Hosp 35(5):281-282
135. Lurain NS, Chou S (2010) Antiviral drug resistance of human cytomegalovirus. Clin Microbiol Rev 23:689-712
136. Bidanset DJ, Beadle JR, Wan WB, Hostetler KY, Kern ER (2004) Oral activity of ether lipid ester prodrugs of cidofovir against experimental human cytomegalovirus infection. J Infect Dis 190:499-503 (Pubitemid 38982087)
137. Lischka P, Hewlett G, Wunberg T, Baumeister J, Paulsen D, Goldner T, Ruebsamen-Schaeff H, Zimmermann H (2010) In vitro and in vivo activities of the novel anticytomegalovirus compound AIC246. Antimicrob Agents Chemother 54:1290-1297
138. Winston DJ, Young JA, Pullarkat V, Papanicolaou GA, Vij R, Vance E, Alangaden GJ, Chemaly RF, Petersen F, Chao N, Klein J, Sprague K, Villano SA, Boeckh M (2008) Maribavir prophylaxis for prevention of cytomegalovirus infection in allogeneic stem cell transplant recipients: a multicenter, randomized, double-blind, placebo-controlled, doseranging study. Blood 111:5403-5410
139. Marty FM, Ljungman P, Papanicolaou GA, Winston DJ, Chemaly RF, Strasfeld L, Young JA, Rodriguez T, Maertens J, Schmitt M, Einsele H, Ferrant A, Lipton JH, Villano SA, Chen H, Boeckh M (2011) Maribavir prophylaxis for prevention of cytomegalovirus disease in recipients of allogeneic stem-cell transplants: a phase 3, double-blind, placebo-controlled, randomised trial; Maribavir 1263-300 Clinical Study Group. Lancet Infect Dis 11:284-292
140. Avery RK, Mossad SB, Poggio E, Lard M, Budev M, Bolwell B, Waldman WJ, Braun W, Mawhorter SD, Fatica R, Krishnamurthi V, Young JB, Shrestha R, Stephany B, Lurain N, Yen-Lieberman B (2010) Utility of leflunomide in the treatment of complex cytomegalovirus syndromes. Transplantation 90:419-426
141. Hodson EM, Jones CA, Strippoli GF, Webster AC, Craig JC (2007) Immunoglobulins, vaccines or interferon for preventing cytomegalovirus disease in solid organ transplant recipients. Cochrane Database Syst Rev 2:CD005129
142. Raanani P, Gafter-Gvili A, Paul M, Ben-Bassat I, Leibovici L, Shpilberg O (2009) Immunoglobulin prophylaxis in hematopoietic stem cell transplantation: systematic review and metaanalysis. J Clin Oncol 27:770-781
143. Nigro G, Adler SP, La Torre R, Best AM (2005) Passive immunization during pregnancy for congenital cytomegalovirus infection. N Engl J Med 353:1350-1362 (Pubitemid 41362703)
144. Bate SL, Dollard SC, Cannon MJ (2010) Cytomegalovirus seroprevalence in the United States: the national health and nutrition examination surveys, 1988-2004. J Infect Dis 50:1439-1447
145. Nichols WG, Price TH, Gooley T, Corey L, Boeckh M (2003) Transfusion-transmitted cytomegalovirus infection after receipt of leukoreduced blood products. Blood 101:4195-4200 (Pubitemid 36857904)
146. Cunha BA (2010) Cytomegalovirus pneumonia: community-acquired pneumonia in immunocompetent hosts. Infect Dis Clin North Am 24:147-158
147. Matsumura T, Narimatsu H, Kami M, Yuji K, Kusumi E, Hori A, Murashige N, Tanaka Y, Masuoka K, Wake A, Miyakoshi S, Kanda Y, Taniguchi S (2007) Cytomegalovirus infections following umbilical cord blood transplantation using reduced intensity conditioning regimens for adult patients. Biol Blood Marrow Transplant 13:577-583 (Pubitemid 46585928)
148. Ljungman P, Hakki M, Boeckh M (2010) Cytomegalovirus in hematopoietic stem cell transplant recipients. Infect Dis Clin North Am 24:319-337
149. Pollack M, Heugel J, Xie H, Leisenring W, Storek J, Young JA, Kukreja M, Gress R, Tomblyn M, Boeckh M (2011) An international comparison of current strategies to prevent herpesvirus and fungal infections in hematopoietic cell transplant recipients. Biol Blood Marrow Transplant 17:664-673
150. Fishman JA, Rubin RH (1998) Infection in organ-transplant recipients. N Engl J Med 338:1741-1751 (Pubitemid 28268592)
151. La Rosa C, Limaye AP, Krishnan A, Blumstein G, Longmate J, Diamond DJ (2011) Primary response against cytomegalovirus during antiviral prophylaxis with valganciclovir, in solid organ transplant recipients. Transpl Int. doi:10.1111/j.1432-2277.2011.01285.x
152. Guitard J, Rostaing L, Kamar N (2011) New-onset diabetes and nephropathy after renal transplantation. Contrib Nephrol 170:247-255
153. Maglione M, Biebl MO, Bonatti H, Göbel G, Ratschiller T, Schneeberger S, Brandacher G, Hengster P, Margreiter C, Berger N, Margreiter R, Pratschke J, Mark W (2010) Cytomegalovirus mismatch as major risk factor for delayed graft function after pancreas transplantation. Transplantation 90:666-671
154. Shlobin OA, West EE, Lechtzin N, Miller SM, Borja M, Orens JB, Dropulic LK, McDyer JF (2006) Persistent cytomegalovirus-specific memory responses in the lung allograft and blood following primary infection in lung transplant recipients. J Immunol 176:2625-2634 (Pubitemid 43201715)
155. Christie JD, Edwards LB, Aurora P, Dobbels F, Kirk R, Rahmel AO, Taylor DO, Kucheryavaya AY, Hertz MI (2008) Registry of the International Society for Heart and Lung Transplantation: twenty-fifth official adult lung and heart/lung transplantation report-2008. J Heart Lung Transplant 27:957-969
156. Sester U, Gärtner BC, Wilkens H, Schwaab B, Wössner R, Kindermann I, Girndt M, Meyerhans A, Mueller-Lantzsch N, Schäfers HJ, Sybrecht GW, Köhler H, Sester M (2005) Differences in CMV-specific T-cell levels and long-term susceptibility to CMV infection after kidney, heart and lung transplantation. Am J Transplant 5:1483-1489 (Pubitemid 40839442)
157. Costa C, Astegiano S, Terlizzi ME, Sidoti F, Curtoni A, Solidoro P, Baldi S, Bergallo M, Cavallo R (2011) Evaluation and significance of cytomegalovirus-specific cellular immune response in lung transplant recipients. Transplant Proc 43:1159-1161
158. Kwakkel-van Erp JM, Paantjens AW, van Kessel DA, Grutters JC, van den Bosch JM, van de Graaf EA, Otten HG (2011) Mannose-binding lectin deficiency linked to cytomegalovirus (CMV) reactivation and survival in lung transplantation. Clin Exp Immunol. doi:10.1111/j.1365-2249.2011.04436.x
159. da Cunha-Bang C, Sørensen SS, Iversen M, Sengeløv H, HillingsøJG, Rasmussen A, Mortensen SA, Fox ZV, Kirkby NS, Christiansen CB, Lundgren JD (2011) Factors associated with the development of cytomegalovirus infection following solid organ transplantation. Scand J Infect Dis 43:360-365
160. Lefeuvre S, Chevalier P, Charpentier C, Zekkour R, Havard L, Benammar M, Amrein C, Boussaud V, Lillo-Le Louët A, Guillemain R, Billaud EM (2010) Valganciclovir prophylaxis for cytomegalovirus infection in thoracic transplant patients: retrospective study of efficacy, safety, and drug exposure. Transpl Infect Dis 12:213-219