Using the nonhuman primate model of HCMV to guide vaccine development

Viruses

Volumn 6, Issue 4, 2014, Pages 1483-1501

  Deere, Jesse D ^a   Barry, Peter A ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cytomegalovirus; Immune modulation; Nonhuman primate; Persistence; Reinfection; RhCMV; Vaccine

Indexed keywords

ALPHA CHEMOKINE; CD34 ANTIGEN; CYTOMEGALOVIRUS ANTIGEN PP65; IMMUNOGLOBULIN G; CYTOMEGALOVIRUS VACCINE;

CYTOMEGALOVIRUS INFECTION; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CYTOMEGALOVIRUS; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSUPPRESSIVE TREATMENT; MORBIDITY; MORTALITY; NONHUMAN; POLYMERASE CHAIN REACTION; REVIEW; SEROPREVALENCE; SEXUALLY TRANSMITTED DISEASE; SIMIAN IMMUNODEFICIENCY VIRUS; T LYMPHOCYTE; VACCINE PRODUCTION; VERTICAL TRANSMISSION; ANIMAL; CYTOMEGALOVIRUS INFECTIONS; DISEASE MODEL; DRUG DEVELOPMENT; HOST PATHOGEN INTERACTION; IMMUNOLOGY; ISOLATION AND PURIFICATION; PRIMATE; PROCEDURES;

ANIMALS; CYTOMEGALOVIRUS INFECTIONS; CYTOMEGALOVIRUS VACCINES; DISEASE MODELS, ANIMAL; DRUG DISCOVERY; HOST-PATHOGEN INTERACTIONS; HUMANS; PRIMATES;

EID: 84897147013     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v6041483     Document Type: Review

References (95)

1. McGeoch, D. J.; Gatherer, D. Integrating reptilian herpesviruses into the family herpesviridae. J. Virol. 2005, 79, 725-731.
2. Kolb, A. W.; Ane, C.; Brandt, C. R. Using HSV-1 Genome Phylogenetics to Track Past Human Migrations. PLoS One 2013, 8, e76267.
3. Cannon, M. J.; Schmid, D. S.; Hyde, T. B. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev. Med. Virol. 2010, 20, 202-213.
4. Cannon, M. J.; Hyde, T. B.; Schmid, D. S. Review of cytomegalovirus shedding in bodily fluids and relevance to congenital cytomegalovirus infection. Rev. Med. Virol. 2011, 21, 240-255.
5. Noyola, D. E.; Valdez-Lopez, B. H.; Hernandez-Salinas, A. E.; Santos-Diaz, M. A.; Noyola-Frias, M. A.; Reyes-Macias, J. F.; Martinez-Martinez, L. G. Cytomegalovirus excretion in children attending day-care centers. Arch. Med. Res. 2005, 36, 590-593.
6. Berntsson, M.; Dubicanac, L.; Tunback, P.; Ellstrom, A.; Lowhagen, G. B.; Bergstrom, T. Frequent detection of cytomegalovirus and Epstein-Barr virus in cervical secretions from healthy young women. Acta Obstet. Gynecol. Scand. 2013, 92, 706-710.
7. de Franca, T. R.; de Albuquerque Tavares Carvalho, A.; Gomes, V. B.; Gueiros, L. A.; Porter, S. R.; Leao, J. C. Salivary shedding of Epstein-Barr virus and cytomegalovirus in people infected or not by human immunodeficiency virus 1. Clin. Oral Investig. 2012, 16, 659-664.
8. Arora, N.; Novak, Z.; Fowler, K. B.; Boppana, S. B.; Ross, S. A. Cytomegalovirus viruria and DNAemia in healthy seropositive women. J. Infect. Dis. 2010, 202, 1800-1803.
9. Gautheret-Dejean, A.; Aubin, J. T.; Poirel, L.; Huraux, J. M.; Nicolas, J. C.; Rozenbaum, W.; Agut, H. Detection of human Betaherpesvirinae in saliva and urine from immunocompromised and immunocompetent subjects. J. Clin. Microbiol. 1997, 35, 1600-1603.
10. Hayashi, S.; Kimura, H.; Oshiro, M.; Kato, Y.; Yasuda, A.; Suzuki, C.; Watanabe, Y.; Morishima, T.; Hayakawa, M. Transmission of cytomegalovirus via breast milk in extremely premature infants. J. Perinatol. 2011, 31, 440-445.
11. Hamprecht, K.; Maschmann, J.; Vochem, M.; Dietz, K.; Speer, C. P.; Jahn, G. Epidemiology of transmission of cytomegalovirus from mother to preterm infant by breastfeeding. Lancet 2001, 357, 513-518.
12. Jim, W. T.; Shu, C. H.; Chiu, N. C.; Chang, J. H.; Hung, H. Y.; Peng, C. C.; Kao, H. A.; Wei, T. Y.; Chiang, C. L.; Huang, F. Y. High cytomegalovirus load and prolonged virus excretion in breast milk increase risk for viral acquisition by very low birth weight infants. Pediatr. Infect. Dis. J. 2009, 28, 891-894.
13. Maciejewski, J. P.; Bruening, E. E.; Donahue, R. E.; Mocarski, E. S.; Young, N. S.; St Jeor, S. C. Infection of hematopoietic progenitor cells by human cytomegalovirus. Blood 1992, 80, 170-178.
14. 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.
15. Kondo, K.; Kaneshima, H.; Mocarski, E. S. Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proc. Natl. Acad. Sci. USA 1994, 91, 11879-11883.
16. Kondo, K.; Xu, J.; Mocarski, E. S. Human cytomegalovirus latent gene expression in granulocyte-macrophage progenitors in culture and in seropositive individuals. Proc. Natl. Acad. Sci. USA 1996, 93, 11137-11142.
17. Goodrum, F.; Reeves, M.; Sinclair, J.; High, K.; Shenk, T. Human cytomegalovirus sequences expressed in latently infected individuals promote a latent infection in vitro. Blood 2007, 110, 937-945.
18. Cheung, A. K.; Abendroth, A.; Cunningham, A. L.; Slobedman, B. Viral gene expression during the establishment of human cytomegalovirus latent infection in myeloid progenitor cells. Blood 2006, 108, 3691-3699.
19. Fowler, K. B.; Stagno, S.; Pass, R. F.; Britt, W. J.; Boll, T. J.; Alford, C. A. The outcome of congenital cytomegalovirus infection in relation to maternal antibody status. N. Engl. J. Med. 1992, 326, 663-667.
20. Rasmussen, L.; Matkin, C.; Spaete, R.; Pachl, C.; Merigan, T. C. Antibody response to human cytomegalovirus glycoproteins gB and gH after natural infection in humans. J. Infect. Dis. 1991, 164, 835-842.
21. Boppana, S. B.; Rivera, L. B.; Fowler, K. B.; Mach, M.; Britt, W. J., Intrauterine transmission of cytomegalovirus to infants of women with preconceptional immunity. N. Engl. J. Med. 2001, 344, 1366-1371.
22. Hansen, S. G.; Powers, C. J.; Richards, R.; Ventura, A. B.; Ford, J. C.; Siess, D.; Axthelm, M. K.; Nelson, J. A.; Jarvis, M. A.; Picker, L. J.; et al. Evasion of CD8+ T cells is critical for superinfection by cytomegalovirus. Science 2010, 328, 102-106.
23. Sylwester, A. W.; Mitchell, B. L.; Edgar, J. B.; Taormina, C.; Pelte, C.; Ruchti, F.; Sleath, P. R.; Grabstein, K. H.; Hosken, N. A.; Kern, F.; et al. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J. Exp. Med. 2005, 202, 673-685.
24. Griffiths, P. D. Burden of disease associated with human cytomegalovirus and prospects for elimination by universal immunisation. Lancet Infect. Dis. 2012, 12, 790-798.
25. Crough, T.; Khanna, R. Immunobiology of human cytomegalovirus: From bench to bedside. Clin. Microbiol. Rev. 2009, 22, 76-98.
26. Elek, S. D.; Stern, H. Development of a vaccine against mental retardation caused by cytomegalovirus infection in utero. Lancet 1974, 1, 1-5.
27. Hanshaw, J. B. Congenital cytomegalovirus infection: A fifteen year perspective. J. Infect. Dis. 1971, 123, 555-561.
28. Plotkin, S. A. Vaccines for varicella-zoster virus and cytomegalovirus: Recent progress. Science 1994, 265, 1383-1385.
29. Pass, R. F.; Zhang, C.; Evans, A.; Simpson, T.; Andrews, W.; Huang, M. L.; Corey, L.; Hill, J.; Davis, E.; Flanigan, C.; et al. Vaccine prevention of maternal cytomegalovirus infection. N. Engl. J. Med. 2009, 360, 1191-1199.
30. Stratton, K. R.; Durch, J. S.; Lawrence, R. S. Vaccines for the 21st Century: A Tool for Decision Making; National Academy Press: Washington, DC, USA, 2000; p. Appendix 4: 165-172.
31. Saccoccio, F. M.; Gallagher, M. K.; Adler, S. P.; McVoy, M. A. Neutralizing activity of saliva against cytomegalovirus. Clin. Vaccine Immunol. 2011, 18, 1536-1542.
32. Tamura, T.; Chiba, S.; Chiba, Y.; Nakao, T. Virus excretion and neutralizing antibody response in saliva in human cytomegalovirus infection. Infect. Immun. 1980, 29, 842-845.
33. Wang, J. B.; Adler, S. P.; Hempfling, S.; Burke, R. L.; Duliege, A. M.; Starr, S. E.; Plotkin, S. A. Mucosal antibodies to human cytomegalovirus glycoprotein B occur following both natural infection and immunization with human cytomegalovirus vaccines. J. Infect. Dis. 1996, 174, 387-392.
34. Simanek, A. M.; Dowd, J. B.; Pawelec, G.; Melzer, D.; Dutta, A.; Aiello, A. E. Seropositivity to cytomegalovirus, inflammation, all-cause and cardiovascular disease-related mortality in the United States. PLoS One 2011, 6, e16103.
35. Bale, J. F., Jr.; Petheram, S. J.; Souza, I. E.; Murph, J. R. Cytomegalovirus reinfection in young children. J. Pediatr. 1996, 128, 347-352.
36. Chandler, S. H.; Handsfield, H. H.; McDougall, J. K. Isolation of multiple strains of cytomegalovirus from women attending a clinic for sexually transmitted disease. J. Infect. Dis. 1987, 155, 655-660.
37. Sohn, Y. M.; Park, K. I.; Lee, C.; Han, D. G.; Lee, W. Y. Congenital cytomegalovirus infection in Korean population with very high prevalence of maternal immunity. J. Korean Med. Sci. 1992, 7, 47-51.
38. Gaytant, M. A.; Rours, G. I.; Steegers, E. A.; Galama, J. M.; Semmekrot, B. A. Congenital cytomegalovirus infection after recurrent infection: Case reports and review of the literature. Eur. J. Pediatr. 2003, 162, 248-253.
39. Gaytant, M. A.; Steegers, E. A.; Semmekrot, B. A.; Merkus, H. M.; Galama, J. M. Congenital cytomegalovirus infection: Review of the epidemiology and outcome. Obstet. Gynecol. Surv. 2002, 57, 245-256.
40. Gandhoke, I.; Aggarwal, R.; Lal, S.; Khare, S. Congenital CMV infection in symptomatic infants in Delhi and surrounding areas. Indian J. Pediatr. 2006, 73, 1095-1097.
41. Yamamoto, A. Y.; Mussi-Pinhata, M. M.; Boppana, S. B.; Novak, Z.; Wagatsuma, V. M.; Oliveira Pde, F.; Duarte, G.; Britt, W. J. Human cytomegalovirus reinfection is associated with intrauterine transmission in a highly cytomegalovirus-immune maternal population. Am. J. Obstet. Gynecol. 2010, 202, 297. e1-297. e8.
42. Ross, S. A.; Fowler, K. B.; Ashrith, G.; Stagno, S.; Britt, W. J.; Pass, R. F.; Boppana, S. B. Hearing loss in children with congenital cytomegalovirus infection born to mothers with preexisting immunity. J. Pediatr. 2006, 148, 332-336.
43. Wang, C.; Zhang, X.; Bialek, S.; Cannon, M. J. Attribution of congenital cytomegalovirus infection to primary versus non-primary maternal infection. Clin. Infect. Dis. 2011, 52, e11-e13.
44. Britt, W. J.; Mach, M. Human cytomegalovirus glycoproteins. Intervirology 1996, 39, 401-412.
45. Revello, M. G.; Gerna, G. Human cytomegalovirus tropism for endothelial/epithelial cells: Scientific background and clinical implications. Rev. Med. Virol. 2010, 20, 136-155.
46. Cui, X.; Meza, B. P.; Adler, S. P.; McVoy, M. A. Cytomegalovirus vaccines fail to induce epithelial entry neutralizing antibodies comparable to natural infection. Vaccine 2008, 26, 5760-5766.
47. Macagno, A.; Bernasconi, N. L.; Vanzetta, F.; Dander, E.; Sarasini, A.; Revello, M. G.; Gerna, G.; Sallusto, F.; Lanzavecchia, A. Isolation of human monoclonal antibodies that potently neutralize human cytomegalovirus infection by targeting different epitopes on the gH/gL/UL128-131A complex. J. Virol. 2010, 84, 1005-1013.
48. Britt, W. J. Neutralizing antibodies detect a disulfide-linked glycoprotein complex within the envelope of human cytomegalovirus. Virology 1984, 135, 369-378.
49. Ross, S. A.; Arora, N.; Novak, Z.; Fowler, K. B.; Britt, W. J.; Boppana, S. B. Cytomegalovirus reinfections in healthy seroimmune women. J. Infect. Dis. 2010, 201, 386-389.
50. Dunn, W.; Chou, C.; Li, H.; Hai, R.; Patterson, D.; Stolc, V.; Zhu, H.; Liu, F. Functional profiling of a human cytomegalovirus genome. Proc. Natl. Acad. Sci. USA 2003, 100, 14223-14228.
51. Yu, D.; Silva, M. C.; Shenk, T. Functional map of human cytomegalovirus AD169 defined by global mutational analysis. Proc. Natl. Acad. Sci. USA 2003, 100, 12396-12401.
52. Hakki, M.; Chou, S. The biology of cytomegalovirus drug resistance. Curr. Opin. Infect. Dis. 2011, 24, 605-611.
53. Renzette, N.; Gibson, L.; Bhattacharjee, B.; Fisher, D.; Schleiss, M. R.; Jensen, J. D.; Kowalik, T. F. Rapid intrahost evolution of human cytomegalovirus is shaped by demography and positive selection. PLoS Genet. 2013, 9, e1003735.
54. Vogel, P.; Weigler, B. J.; Kerr, H.; Hendrickx, A.; Barry, P. A. Seroepidemiologic studies of cytomegalovirus infection in a breeding population of rhesus macaques. Lab. Anim. Sci. 1994, 44, 25-30.
55. Andrade, M. R.; Yee, J.; Barry, P.; Spinner, A.; Roberts, J. A.; Cabello, P. H.; Leite, J. P.; Lerche, N. W. Prevalence of antibodies to selected viruses in a long-term closed breeding colony of rhesus macaques (Macaca mulatta) in Brazil. Am. J. Primatol. 2003, 59, 123-128.
56. Früh, K.; Malouli, D.; Oxford, K.; Barry, P. Non-Human-Primate Models of Cytomegalovirus Infection, Prevention, and Therapy. In CYTOMEGALOVIRUSES: From Molecular Pathogenesis to Therapy; Reddehase, M., Ed.; Caister Academic Press/Horizon: Norfolk, UK, 2013; Volume 2.
57. Jones-Engel, L.; Engel, G. A.; Heidrich, J.; Chalise, M.; Poudel, N.; Viscidi, R.; Barry, P. A.; Allan, J. S.; Grant, R.; Kyes, R. Temple monkeys and health implications of commensalism, Kathmandu, Nepal. Emerg. Infect. Dis. 2006, 12, 900-906.
58. Baskin, G. B. Disseminated cytomegalovirus infection in immunodeficient rhesus monkeys. Am. J. Pathol. 1987, 129, 345-352.
59. Kaur, A.; Kassis, N.; Hale, C. L.; Simon, M.; Elliott, M.; Gomez-Yafal, A.; Lifson, J. D.; Desrosiers, R. C.; Wang, F.; Barry, P.; et al. Direct relationship between suppression of virus-specific immunity and emergence of cytomegalovirus disease in simian AIDS. J. Virol. 2003, 77, 5749-5758.
60. Assaf, B. T.; Mansfield, K. G.; Westmoreland, S. V.; Kaur, A.; Oxford, K. L.; Diamond, D. J.; Barry, P. A. Patterns of acute rhesus cytomegalovirus (RhCMV) infection predict long-term RhCMV infection. J. Virol. 2012, 86, 6354-6357.
61. Oxford, K. L.; Strelow, L.; Yue, Y.; Chang, W. L.; Schmidt, K. A.; Diamond, D. J.; Barry, P. A. Open reading frames carried on UL/b' are implicated in shedding and horizontal transmission of rhesus cytomegalovirus in rhesus monkeys. J. Virol. 2011, 85, 5105-5114.
62. Wussow, F.; Yue, Y.; Martinez, J.; Deere, J. D.; Longmate, J.; Herrmann, A.; Barry, P. A.; Diamond, D. J. A Vaccine Based on the Rhesus Cytomegalovirus UL128 Complex Induces Broadly Neutralizing Antibodies in Rhesus Macaques. J. Virol. 2013, 87, 1322-1332.
63. Yue, Y.; Zhou, S. S.; Barry, P. A. Antibody responses to rhesus cytomegalovirus glycoprotein B in naturally infected rhesus macaques. J. Gen. Virol. 2003, 84, 3371-3379.
64. Yue, Y.; Kaur, A.; Zhou, S. S.; Barry, P. A. Characterization and immunological analysis of the rhesus cytomegalovirus homologue (Rh112) of the human cytomegalovirus UL83 lower matrix phosphoprotein (pp65). J. Gen. Virol. 2006, 87, 777-787.
65. Pitcher, C. J.; Hagen, S. I.; Walker, J. M.; Lum, R.; Mitchell, B. L.; Maino, V. C.; Axthelm, M. K.; Picker, L. J. Development and homeostasis of T cell memory in rhesus macaque. J. Immunol. 2002, 168, 29-43.
66. Asher, D. M.; Gibbs, C. J., Jr.; Lang, D. J. Rhesus monkey cytomegaloviruses: Persistent asymptomatic viruses. Bacteriol. Proc. 1969, 69, 191.
67. Asher, D. M.; Gibbs, C. J., Jr.; Lang, D. J.; Gajdusek, D. C.; Chanock, R. M. Persistent shedding of cytomegalovirus in the urine of healthy Rhesus monkeys. Proc. Soc. Exp. Biol. Med. 1974, 145, 794-801.
68. Huff, J. L.; Eberle, R.; Capitanio, J.; Zhou, S. S.; Barry, P. A. Differential detection of B virus and rhesus cytomegalovirus in rhesus macaques. J. Gen. Virol. 2003, 84, 83-92.
69. Oxford, K. L.; Eberhardt, M. K.; Yang, K. W.; Strelow, L.; Kelly, S.; Zhou, S. S.; Barry, P. A. Protein coding content of the UL)b' region of wild-type rhesus cytomegalovirus. Virology 2008, 373, 181-188.
70. Alcendor, D. J.; Barry, P. A.; Pratt-Lowe, E.; Luciw, P. A. Analysis of the rhesus cytomegalovirus immediate-early gene promoter. Virology 1993, 194, 815-821.
71. Barry, P. A.; Alcendor, D. J.; Power, M. D.; Kerr, H.; Luciw, P. A. Nucleotide sequence and molecular analysis of the rhesus cytomegalovirus immediate-early gene and the UL121-117 open reading frames. Virology 1996, 215, 61-72.
72. Hansen, S. G.; Strelow, L. I.; Franchi, D. C.; Anders, D. G.; Wong, S. W. Complete sequence and genomic analysis of rhesus cytomegalovirus. J. Virol. 2003, 77, 6620-6636.
73. 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.
74. Ryckman, B. J.; Rainish, B. L.; Chase, M. C.; Borton, J. A.; Nelson, J. A.; Jarvis, M. A.; Johnson, D. C. Characterization of the human cytomegalovirus gH/gL/UL128-131 complex that mediates entry into epithelial and endothelial cells. J. Virol. 2008, 82, 60-70.
75. Lilja, A. E.; Shenk, T. Efficient Replication of Rhesus Cytomegalovirus Variants in Multiple Rhesus and Human Cell Types. Proc. Natl. Acad. Sci. USA 2008, 105, 19950-19955.
76. Carlson, J. R.; Chang, W. L.; Zhou, S. S.; Tarantal, A. F.; Barry, P. A. Rhesus brain microvascular endothelial cells are permissive for rhesus cytomegalovirus infection. J. Gen. Virol. 2005, 86, 545-549.
77. Abel, K.; Martinez, J.; Yue, Y.; Lacey, S. F.; Wang, Z.; Strelow, L.; Dasgupta, A.; Li, Z.; Schmidt, K. A.; Oxford, K. L.; et al. Vaccine-induced control of viral shedding following rhesus cytomegalovirus challenge in rhesus macaques. J. Virol. 2011, 85, 2878-2890.
78. Assaf, B. T.; Mansfield, K. G.; Westmoreland, S. V.; Strelow, L.; Barry, P. A.; Kaur, A. Limited Dissemination and Shedding of the UL128-Complex-Intact, UL/b'-Defective Rhesus Cytomegalovirus Strain 180. 92. J. Virol., submitted.
79. Rivailler, P.; Kaur, A.; Johnson, R. P.; Wang, F. Genomic sequence of rhesus cytomegalovirus 180.92: Insights into the coding potential of rhesus cytomegalovirus. J. Virol. 2006, 80, 4179-4182.
80. Yue, Y.; Kaur, A.; Eberhardt, M. K.; Kassis, N.; Zhou, S. S.; Tarantal, A. F.; Barry, P. A. Immunogenicity and protective efficacy of DNA vaccines expressing rhesus cytomegalovirus glycoprotein B, phosphoprotein 65-2, and viral interleukin-10 in rhesus macaques. J. Virol. 2007, 81, 1095-1109.
81. Chang, W. L.; Barry, P. A. Attenuation of innate immunity by cytomegalovirus IL-10 establishes a long-term deficit of adaptive antiviral immunity. Proc. Natl. Acad. Sci. USA 2010, 107, 22647-22652.
82. Abel, K.; Strelow, L.; Yue, Y.; Eberhardt, M. K.; Schmidt, K. A.; Barry, P. A. A heterologous DNA prime/protein boost immunization strategy for rhesus cytomegalovirus. Vaccine 2008, 26, 6013-6025.
83. Lockridge, K. M.; Sequar, G.; Zhou, S. S.; Yue, Y.; Mandell, C. P.; Barry, P. A. Pathogenesis of experimental rhesus cytomegalovirus infection. J. Virol. 1999, 73, 9576-9583.
84. Hansen, S. G.; Vieville, C.; Whizin, N.; Coyne-Johnson, L.; Siess, D. C.; Drummond, D. D.; Legasse, A. W.; Axthelm, M. K.; Oswald, K.; Trubey, C. M.; et al. Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat. Med. 2009, 15, 293-299.
85. Pulendran, B.; Ahmed, R. Immunological mechanisms of vaccination. Nat. Immunol. 2011, 12, 509-517.
86. Lockridge, K. M.; Zhou, S. S.; Kravitz, R. H.; Johnson, J. L.; Sawai, E. T.; Blewett, E. L.; Barry, P. A. Primate cytomegaloviruses encode and express an IL-10-like protein. Virology 2000, 268, 272-280.
87. Slobedman, B.; Barry, P. A.; Spencer, J. V.; Avdic, S.; Abendroth, A. Virus-encoded homologs of cellular interleukin-10 and their control of host immune function. J. Virol. 2009, 83, 9618-9629.
88. Eberhardt, M. K.; Chang, W. L.; Logsdon, N. J.; Yue, Y.; Walter, M. R.; Barry, P. A. Host immune responses to a viral immune modulating protein: Immunogenicity of viral interleukin-10 in rhesus cytomegalovirus-infected rhesus macaques. PLoS One 2012, 7, e37931.
89. de Lemos Rieper, C.; Galle, P.; Pedersen, B. K.; Hansen, M. B. Characterization of specific antibodies against cytomegalovirus (CMV)-encoded interleukin 10 produced by 28% of CMV-seropositive blood donors. J. Gen. Virol. 2011, 92, 1508-1518.
90. Logsdon, N. J.; Eberhardt, M. K.; Allen, C. E.; Barry, P. A.; Walter, M. R. Design and analysis of rhesus cytomegalovirus IL-10 mutants as a model for novel vaccines against human cytomegalovirus. PLoS One 2011, 6, e28127.
91. Eberhardt, M.; Deshpande, A.; Chang, W.-L.; Barthold, S.; Walter, M.; Barry, P. Vaccination Against a Virally-Encoded Cytokine Significantly Restricts Viral Challenge. J. Virol. 2013, 87, 11323-11331.
92. Fu, T. M.; Wang, D.; Freed, D. C.; Tang, A.; Li, F.; He, X.; Cole, S.; Dubey, S.; Finnefrock, A. C.; ter Meulen, J.; Shiver, J. W.; Casimiro, D. R. Restoration of viral epithelial tropism improves immunogenicity in rabbits and rhesus macaques for a whole virion vaccine of human cytomegalovirus. Vaccine 2012, 30, 7469-7474.
93. Freed, D. C.; Tang, Q.; Tang, A.; Li, F.; He, X.; Huang, Z.; Meng, W.; Xia, L.; Finnefrock, A. C.; Durr, E.; et al. Pentameric complex of viral glycoprotein H is the primary target for potent neutralization by a human cytomegalovirus vaccine. Proc. Natl. Acad. Sci. USA 2013, 110, E4997-E5005.
94. Plotkin, S. A.; Furukawa, T.; Zygraich, N.; Huygelen, C. Candidate cytomegalovirus strain for human vaccination. Infect. Immun. 1975, 12, 521-527.
95. Plotkin, S. A.; Starr, S. E.; Friedman, H. M.; Gonczol, E.; Brayman, K. Vaccines for the prevention of human cytomegalovirus infection. Rev. Infect. Dis. 1990, 12, S827-S838.