The pathogenesis of human cytomegalovirus

Journal of Pathology

Volumn 235, Issue 2, 2015, Pages 288-297

  Griffiths, Paul ^a   Baraniak, Ilona ^a   Reeves, Matt ^a  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

Congenital; Human cytomegalovirus; Pre emptive therapy; Threshold; Transplantation; Viraemia

Indexed keywords

ANTIVIRUS AGENT; VIRUS VACCINE; CYTOMEGALOVIRUS VACCINE;

ARTICLE; ASYMPTOMATIC INFECTION; HUMAN; HUMAN CYTOMEGALOVIRUS; IMMUNE RESPONSE; IMMUNE SYSTEM; INFECTION PREVENTION; NONHUMAN; VIRUS LOAD; VIRUS PATHOGENESIS; ANIMAL; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; DRUG EFFECTS; GENETICS; GENOTYPE; HOST PATHOGEN INTERACTION; IMMUNOLOGY; PATHOGENICITY; PATHOLOGY; PROGNOSIS; RISK FACTOR; TRANSMISSION; VIROLOGY; VIRULENCE;

ANIMALS; ANTIVIRAL AGENTS; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; CYTOMEGALOVIRUS VACCINES; GENOTYPE; HOST-PATHOGEN INTERACTIONS; HUMANS; PROGNOSIS; RISK FACTORS; VIRULENCE;

EID: 84917705498     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4437     Document Type: Article

References (93)

1. Smith AJ, Weidman F. Infection of a stillborn infant by an amebiform protozoön (Entamœba mortinatalium, N.S.). Univ Penn Med Bull 1910; 23: 285-298.
2. Hill RB Jr, Rowlands DT Jr, Rifkind D. Infectious pulmonary disease in patients receiving immunosuppressive therapy for organ transplantation. N Engl J Med 1964; 271: 1021-1027.
3. Rubin RH. The indirect effects of cytomegalovirus infection on the outcome of organ transplantation. J Am Med Assoc 1989; 261: 3607-3609.
4. Simanek AM, Dowd JB, Pawelec G, et al. Seropositivity to cytomegalovirus, infammation, all-cause and cardiovascular disease-related mortality in the United States. PLoS One 2011; 6: e16103.
5. Staras SA, Flanders WD, Dollard SC, et al. Cytomegalovirus sero-prevalence and childhood sources of infection: a population-based study among pre-adolescents in the United States. J Clin Virol 2008; 43: 266-271.
6. Cannon MJ, Hyde TB, Schmid DS. Review of cytomegalovirus shedding in bodily fuids and relevance to congenital cytomegalovirus infection. Rev Med Virol 2011; 21: 240-255.
7. Kenneson A, Cannon MJ. Review and meta-analysis of the epidemiology of congenital cytomegalovirus (CMV) infection. Rev Med Virol 2007; 17: 253-276.
8. Revello MG, Fabbri E, Furione M, et al. Role of prenatal diagnosis and counseling in the management of 735 pregnancies complicated by primary human cytomegalovirus infection: a 20-year experience. J Clin Virol 2011; 50: 303-307.
9. Revello MG, Sarasini A, Zavattoni M, et al. Improved prenatal diagnosis of congenital human cytomegalovirus infection by a modifed nested polymerase chain reaction. J Med Virol 1998; 56: 99-103.
10. Dollard SC, Grosse SD, Ross DS. New estimates of the prevalence of neurological and sensory sequelae and mortality associated with congenital cytomegalovirus infection. Rev Med Virol 2007; 17: 355-363.
11. Guerra B, Simonazzi G, Banf A, et al. Impact of diagnostic and con-frmatory tests and prenatal counseling on the rate of pregnancy termination among women with positive cytomegalovirus immunoglob-ulin M antibody titers. Am J Obstet Gynecol 2007; 196: 221-226.
12. Huang ES, Alford CA, Reynolds DW, et al. Molecular epidemiology of cytomegalovirus infections in women and their infants. N Engl J Med 1980; 303: 958-962.
13. Boppana SB, Rivera LB, Fowler KB, et al. Intrauterine transmission of cytomegalovirus to infants of women with preconceptional immunity. N Engl J Med 2001; 344: 1366-1371.
14. de Vries JJ, van Zwet EW, Dekker FW, et al. The apparent paradox of maternal seropositivity as a risk factor for congenital cytomegalovirus infection: a population-based prediction model. Rev Med Virol 2013; 23: 241-249.
15. Atabani SF, Smith C, Atkinson C, et al. Cytomegalovirus replication kinetics in solid organ transplant recipients managed by preemptive therapy. Am J Transpl 2012; 12: 2457-2464.
16. Grundy JE, Lui SF, Super M, et al. Symptomatic cytomegalovirus infection in seropositive kidney recipients: reinfection with donor virus rather than reactivation of recipient virus. Lancet 1988; 2: 132-135.
17. Fryer JF, WHO Expert Committee on Biological Standardization. Collaborative study to evaluate the proposed frst WHO international standard for human cytomegalovirus (HCMV) for nucleic acid ampli-fcation (NAT)-based assays. Publication No. WHO/BS/10.2138. Geneva: World Health Organization, 2010.
18. Owers DS, Webster AC, Strippoli GF, et al. Pre-emptive treatment for cytomegalovirus viraemia to prevent cytomegalovirus disease in solid organ transplant recipients. Cochrane Database Syst Rev 2013; 2: CD005133.
19. Singh N. Antiviral drugs for cytomegalovirus in transplant recipients: advantages ofpreemptive therapy. Rev Med Virol 2006; 16: 281-287.
20. Boeckh M, Nichols WG. The impact of cytomegalovirus serostatus of donor and recipient before hematopoietic stem cell transplantation in the era of antiviral prophylaxis and preemptive therapy. Blood 2004; 103: 2003-2008.
21. Wimperis JZ, Brenner MK, Prentice HG, et al. Transfer of a functioning humoral immune system in transplantation of T lymphocyte-depleted bone marrow. Lancet 1986; 1: 339-343.
22. Webster A, Lee CA, Cook DG, et al. Cytomegalovirus infection and progression towards AIDS in haemophiliacs with human immunod-efciency virus infection. Lancet 1989; 2: 63-66.
23. Deayton JR, Sabin CA, Johnson MA, et al. Importance of cytomegalovirus viraemia in risk of disease progression and death in HIV-infected patients receiving highly active antiretroviral therapy. Lancet 2004; 363: 2116-2121.
24. Limaye AP, Boeckh M. CMV in critically ill patients: pathogen or bystander? Rev Med Virol 2010; 20: 372-379.
25. Pawelec G, Derhovanessian E, Larbi A, et al. Cytomegalovirus and human immunosenescence. Rev Med Virol 2009; 19: 47-56.
26. Murphy E, Yu D, Grimwood J, et al. Coding potential of laboratory and clinical strains of human cytomegalovirus. Proc Natl Acad Sci USA2003; 100: 14976-14981.
27. Cha TA, Tom E, Kemble GW, et al. Human cytomegalovirus clinical isolates carry at least 19 genes not found in laboratory strains. J Virol 1996; 70: 78-83.
28. Varnum SM, Streblow DN, Monroe ME, et al. Identifcation of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J Virol 2004; 78: 10960-10966.
29. Vanarsdall AL, Johnson DC. Human cytomegalovirus entry into cells. Curr Opin Virol 2012; 2: 37-42.
30. Isaacson MK, Compton T. Human cytomegalovirus glycoprotein B is required for virus entry and cell-to-cell spread but not for virion attachment, assembly, or egress. J Virol 2009; 83: 3891-3903.
31. Compton T, Nowlin DM, Cooper NR. Initiation of human cytomegalovirus infection requires initial interaction with cell surface heparan sulfate. Virology 1993; 193: 834-841.
32. Carlson C, Britt WJ, Compton T. Expression, purifcation, and characterization of a soluble form of human cytomegalovirus glycoprotein B. Virology 1997; 239: 198-205.
33. Wang X, Huong SM, Chiu ML, et al. Epidermal growth factor receptor is a cellular receptor for human cytomegalovirus. Nature 2003; 424: 456-461.
34. Hahn G, Revello MG, Patrone M, et al. Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J Virol 2004; 78:10023-10033.
35. Soroceanu L, Akhavan A, Cobbs CS. Platelet-derived growth factor-oc receptor activation is required for human cytomegalovirus infection. Nature 2008; 455: 391-395.
36. Viswanathan K, Smith MS, Malouli D, et al. BST2/Tetherin enhances entry of human cytomegalovirus. PLoS Pathog 2011; 7: e1002332.
37. Wang X, Huang DY, Huong SM, et al. Integrin aß3 is a coreceptor for human cytomegalovirus. Nat Med 2005; 11: 515-521.
38. Feire AL, Koss H, Compton T. Cellular integrins function as entry receptors for human cytomegalovirus via a highly conserved disintegrin-like domain. Proc Natl Acad Sci USA 2004; 101: 15470-15475.
39. Isaacson MK, Feire AL, Compton T. Epidermal growth factor receptor is not required for human cytomegalovirus entry or signaling. J Virol 2007; 81: 6241-6247.
40. Wang D, Shenk T. Human cytomegalovirus virion protein complex required for epithelial and endothelial cell tropism. Proc Natl Acad Sci USA 2005; 102: 18153-18158.
41. Ryckman BJ, Rainish BL, Chase MC, et al. Characterization of the human cytomegalovirus gH/gL/UL128-131 complex that mediates entry into epithelial and endothelial cells. J Virol 2008; 82: 60-70.
42. Straschewski S, Patrone M, Walther P, et al. Protein pUL128 of human cytomegalovirus is necessary for monocyte infection and blocking of migration. J Virol 2011; 85: 5150-5158.
43. Reeves M, Sinclair J. Aspects of human cytomegalovirus latency and reactivation. Curr Top Microbiol Immunol 2008; 325: 297-313.
44. Reeves MB, MacAry PA, Lehner PJ, et al. Latency, chromatin remodeling, and reactivation of human cytomegalovirus in the dendritic cells of healthy carriers. Proc Natl Acad Sci USA 2005; 102: 4140-4145.
45. + cells. J Virol 2010; 84: 5594-5604.
46. Kew VG, Yuan J, Meier J, et al. Mitogen and stress activated kinases act co-operatively with CREB during the induction of human cytomegalovirus immediate-early gene expression from latency. PLoS Pathog 2014; 10: e1004195.
47. Jackson SE, Mason GM, Wills MR. Human cytomegalovirus immunity and immune evasion. Viru s Res 2011; 157: 151-160.
48. Engel P, Angulo A. Viral immunomodulatory proteins: usurping host genes as a survival strategy. Adv Exp Med Biol 2012; 738: 256-276.
49. Miller-Kittrell M, Sparer TE. Feeling manipulated: cytomegalovirus immune manipulation. Vi ro l J 2009; 6: 4; DOI: 10.1186/1743-422X-6-4.
50. Boeckh M, Geballe AP. Cytomegalovirus: pathogen, paradigm, and puzzle. J Clin Invest 2011; 121: 1673-1680.
51. Benz C, Reusch U, Muranyi W, et al. Effcient downregulation of major histocompatibility complex class I molecules in human epithelial cells infected with cytomegalovirus. J Gen Virol 2001; 82: 2061-2070.
52. Hewitt EW, Gupta SS, Lehner PJ. The human cytomegalovirus gene product US6 inhibits ATP binding by TAP. EMBO J 2001; 20: 387-396.
53. Kikkert M, Hassink G, Barel M, et al. Ubiquitination is essential for human cytomegalovirus US11-mediated dislocation of MHC class I molecules from the endoplasmic reticulum to the cytosol. Biochem J 2001; 358: 369-377.
54. + T cells. Nat Med 1999; 5: 1039-1043.
55. McSharry BP, Avdic S, Slobedman B. Human cytomegalovirus encoded homologs of cytokines, chemokines and their receptors: roles in immunomodulation. Viruses 2012; 4: 2448-2470.
56. Moutaftsi M, Mehl AM, Borysiewicz LK, et al. Human cytomegalovirus inhibits maturation and impairs function of monocyte-derived dendritic cells. Blood 2002; 99: 2913-2921.
57. Moutaftsi M, Brennan P, Spector SA, et al. Impaired lymphoid chemokine-mediated migration due to a block on the chemokine receptor switch in human cytomegalovirus-infected dendritic cells. J Virol 2004; 78: 3046-3054.
58. Grigoleit U, Riegler S, Einsele H, et al. Human cytomegalovirus induces a direct inhibitory effect on antigen presentation by monocyte-derived immature dendritic cells. Br J Haematol 2002; 119: 189-198.
59. Tomasec P, Braud VM, Rickards C, et al. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 2000; 287: 1031.
60. Hill GR, Tey SK, Beagley L, et al. Successful immunotherapy of HCMV disease using virus-specifc T cells expanded from an allogeneic stem cell transplant recipient. Am J Transpl 2010; 10: 173-179.
61. Kapp M, Tan SM, Einsele H, et al. Adoptive immunotherapy of HCMV infection. Cytotherapy 2007; 9: 699-711.
62. Stagno S, Reynolds DW, Tsiantos A, et al. Comparative Serial Viro-logic and Serologic Studies of Symptomatic and Subclinical Congen-itally and Natally Acquired Cytomegalovirus Infections. J Infect Dis 1975; 132: 568-577.
63. Schleiss MR. Cytomegalovirus in the neonate: immune correlates of infection and protection. Clin Dev Immunol 2013; 2013: 14 p.
64. Cope AV, Sweny P, Sabin C, et al. Quantity of cytomegalovirus viruria is a major risk factor for cytomegalovirus disease after renal transplantation. J Med Virol 1997; 52: 200-205.
65. Cope AV, Sabin C, Burroughs A, et al. Interrelationships among quantity of human cytomegalovirus (HCMV) DNA in blood, donor-recipient serostatus, and administration of methylprednisolone as risk factors for HCMV disease following liver transplantation. J Infect Dis 1997; 176: 1484-1490.
66. Emery VC, Griffths PD. Prediction of cytomegalovirus load and resistance patterns after antiviral chemotherapy. Proc Natl Acad Sci USA 2000; 97: 8039-8044.
67. Emery VC, Cope AV, Bowen EF, et al. The dynamics of human cytomegalovirus replication in vivo. J Exp Med 1999; 190: 177-182.
68. Schleiss MR. Congenital cytomegalovirus infection: molecular mechanisms mediating viral pathogenesis. Infect Disord Drug Targets 2011; 11: 449-465.
69. Emery VC, Hassan-Walker AF, Burroughs AK, et al. Human cytomegalovirus (HCMV) replication dynamics in HCMV-naive and-experienced immunocompromised hosts. J Infect Dis 2002; 185: 1723-1728.
70. Plotkin SA, Starr SE, Friedman HM, et al. Protective effects of Towne cytomegalovirus vaccine against low-passage cytomegalovirus administered as a challenge. J Infect Dis 1989; 159: 860-865.
71. National Institutes of Health (NIH), USA. Clinical Trials Gov. No. NCT01335932.
72. Wald A, Selke S, Magaret A, et al. Impact of human cytomegalovirus (CMV) infection on immune response to pandemic 2009 H1N1 infuenza vaccine in healthy adults. J Med Virol 2013; 85: 1557-1560.
73. Gkrania-Klotsas E, Langenberg C, Sharp SJ, et al. Seropositivity and higher immunoglobulin g antibody levels against cytomegalovirus are associated with mortality in the population-based European prospective investigation of Cancer-Norfolk cohort. Clin Infect Dis 2013; 56: 1421-1427.
74. Griffths PD. Burden of disease associated with human cytome-galovirus and prospects for elimination by universal immunisation. Lancet Infect Dis 2012; 12: 790-798.
75. Whitley RJ, Cloud G, Gruber W, et al. Ganciclovir treatment of symptomatic congenital cytomegalovirus infection: results of a phase II study. National Institute of Allergy and Infectious Diseases Collaborative Antiviral Study Group. J Infect Dis 1997; 175: 1080-1086.
76. Oliver SE, Cloud GA, Sanchez PJ, et al. Neurodevelopmental outcomes following ganciclovir therapy in symptomatic congenital cytomegalovirus infections involving the central nervous system. J Clin Virol 2009; 46(suppl 4): S22-26.
77. Kimberlin DW, Lin CY, Sanchez PJ, et al. Effect of ganciclovir therapy on hearing in symptomatic congenital cytomegalovirus disease involving the central nervous system: a randomized, controlled trial. J Pediatr 2003; 143: 16-25.
78. Acosta EP, Brundage RC, King JR, et al. Ganciclovir population pharmacokinetics in neonates following intravenous administration of ganciclovir and oral administration of a liquid valganciclovir formulation. Clin Pharmacol Ther 2007; 81: 867-872.
79. Kimberlin DW. Six months versus six weeks of oral valganciclovir for infants with symptomatic congenital cytomegalovirus (CMV) disease with and without central nervous system (CNS) involvement: Results of a Phase III, randomized, double-blind, placebo-controlled, multinational study. ID Week 2014 (abstract).
80. Winston DJ, Young JA, Pullarkat V, et al. Maribavir prophylaxis for prevention of cytomegalovirus infection in allogeneic stem-cell transplant recipients: a multicenter, randomized, double-blind, placebo-controlled, dose-ranging study. Blood 2008; 111: 5403-5410.
81. Marty FM, Ljungman P, Papanicolaou GA, et al. Maribavir prophylaxis for prevention of cytomegalovirus disease in recipients of allogeneic stem-cell transplants: a phase 3, double-blind, placebo-controlled, randomised trial. Lancet Infect Dis 2011; 11: 284-292.
82. Marty FM, Boeckh M. Maribavir and human cytomegalovirus-what happened in the clinical trials and why might the drug have failed? Curr Opin Virol 2011; 1: 555-562.
83. Marty FM, Winston DJ, Rowley SD, et al. CMX001 to prevent cytomegalovirus disease in hematopoietic cell transplantation. N Engl J Med 2013; 369: 1227-1236.
84. Chemaly RF, Ullmann AJ, Stoelben S, et al. Letermovir for cytomegalovirus prophylaxis in hematopoietic cell transplantation. N Engl J Med 2014; 370: 1781-1789.
85. Weekes MP, Tan SY, Poole E, et al. Latency-associated degradation of the MRP1 drug transporter during latent human cytomegalovirus infection. Science 2013; 340: 199-202.
86. Plotkin SA, Smiley ML, Friedman HM, et al. Towne-vaccine-induced prevention of cytomegalovirus disease after renal transplants. Lancet 1984; 1: 528-530.
87. Kharfan-Dabaja MA, Boeckh M, Wilck MB, et al. A novel therapeutic cytomegalovirus DNA vaccine in allogeneic haemopoietic stem cell transplantation: a randomised, double-blind, placebo-controlled, phase 2 trial. Lancet Infect Dis 2012; 12: 290-299.
88. Griffths PD, Stanton A, McCarrell E, et al. Cytomegalovirus glycoprotein-B vaccine with MF59 adjuvant in transplant recipients: a phase 2 randomised placebo-controlled trial. Lancet 2011; 377: 1256-1263.
89. Pass RF, Zhang C, Evans A, et al. Vaccine prevention of maternal cytomegalovirus infection. N Engl J Med 2009; 360: 1191-1199.
90. National Institutes of Health (NIH), USA. Clinical Trials Gov. No. NCT01753167.
91. Revello MG, Lazzarotto T, Guerra B, et al. A randomized trial of hyperimmune globulin to prevent congenital cytomegalovirus. N Engl J Med 2014; 370: 1316-1326.
92. Griffths PD. Cytomegalovirus. In Infections of the Central Nervous System, Scheld WM, Whitley RJ, Marra CM (eds). Wolters Kluwer Health: Philadelphia, 2014; 168-182.
93. Griffths PD. Cytomegalovirus. In Principles and Practice of Clinical Virology, 6th edn. Wiley: Chichester, 2009; 161-197.