Using the Nonhuman Primate Model of HCMV to Guide Vaccine Development
Abstract
:1. Introduction
2. HCMV Natural History
2.1. HCMV Shedding in Bodily Fluids
2.2. HCMV Immune Responses
2.3. HCMV Persistence
2.4. HCMV Reinfection
2.5. HCMV Immune Modulation
2.6. Future Directions for HCMV Vaccine Development
3. RhCMV Natural History
3.1. Endemic RhCMV Infectious Cycle in Rhesus Macaques (Macaca mulatta)
3.2. Early Virus-Host Interactions during Experimental Infection
3.3. Rapid Emergence of RhCMV Variants with Complete UL/b’ Coding Capacity during Experimental Infection
3.4. Long-term Parameters of RhCMV Infection during Experimental Infection
3.5. RhCMV Immune Modulation
3.6. RhCMV Reinfection
4. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References and Notes
- McGeoch, D.J.; Gatherer, D. Integrating reptilian herpesviruses into the family herpesviridae. J. Virol. 2005, 79, 725–731. [Google Scholar] [CrossRef]
- Kolb, A.W.; Ane, C.; Brandt, C.R. Using HSV-1 Genome Phylogenetics to Track Past Human Migrations. PLoS One 2013, 8, e76267. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Kondo, K.; Kaneshima, H.; Mocarski, E.S. Human cytomegalovirus latent infection of granulocyte-macrophage progenitors. Proc. Natl. Acad. Sci. USA 1994, 91, 11879–11883. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Griffiths, P.D. Burden of disease associated with human cytomegalovirus and prospects for elimination by universal immunisation. Lancet Infect. Dis. 2012, 12, 790–798. [Google Scholar] [CrossRef]
- Crough, T.; Khanna, R. Immunobiology of human cytomegalovirus: From bench to bedside. Clin. Microbiol. Rev. 2009, 22, 76–98. [Google Scholar] [CrossRef]
- Elek, S.D.; Stern, H. Development of a vaccine against mental retardation caused by cytomegalovirus infection in utero. Lancet 1974, 1, 1–5. [Google Scholar] [CrossRef]
- Hanshaw, J.B. Congenital cytomegalovirus infection: A fifteen year perspective. J. Infect. Dis. 1971, 123, 555–561. [Google Scholar] [CrossRef]
- Plotkin, S.A. Vaccines for varicella-zoster virus and cytomegalovirus: Recent progress. Science 1994, 265, 1383–1385. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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; pp. Appendix 4:165–172. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- Bale, J.F., Jr.; Petheram, S.J.; Souza, I.E.; Murph, J.R. Cytomegalovirus reinfection in young children. J. Pediatr. 1996, 128, 347–352. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Britt, W.J.; Mach, M. Human cytomegalovirus glycoproteins. Intervirology 1996, 39, 401–412. [Google Scholar]
- Revello, M.G.; Gerna, G. Human cytomegalovirus tropism for endothelial/epithelial cells: Scientific background and clinical implications. Rev. Med. Virol. 2010, 20, 136–155. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Britt, W.J. Neutralizing antibodies detect a disulfide-linked glycoprotein complex within the envelope of human cytomegalovirus. Virology 1984, 135, 369–378. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Hakki, M.; Chou, S. The biology of cytomegalovirus drug resistance. Curr. Opin. Infect. Dis. 2011, 24, 605–611. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Baskin, G.B. Disseminated cytomegalovirus infection in immunodeficient rhesus monkeys. Am. J. Pathol. 1987, 129, 345–352. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- Asher, D.M.; Gibbs, C.J., Jr.; Lang, D.J. Rhesus monkey cytomegaloviruses: Persistent asymptomatic viruses. Bacteriol. Proc. 1969, 69, 191. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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.
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- Pulendran, B.; Ahmed, R. Immunological mechanisms of vaccination. Nat. Immunol. 2011, 12, 509–517. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Plotkin, S.A.; Furukawa, T.; Zygraich, N.; Huygelen, C. Candidate cytomegalovirus strain for human vaccination. Infect. Immun. 1975, 12, 521–527. [Google Scholar]
- 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. [Google Scholar] [CrossRef]
© 2014 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Deere, J.D.; Barry, P.A. Using the Nonhuman Primate Model of HCMV to Guide Vaccine Development. Viruses 2014, 6, 1483-1501. https://doi.org/10.3390/v6041483
Deere JD, Barry PA. Using the Nonhuman Primate Model of HCMV to Guide Vaccine Development. Viruses. 2014; 6(4):1483-1501. https://doi.org/10.3390/v6041483
Chicago/Turabian StyleDeere, Jesse D., and Peter A. Barry. 2014. "Using the Nonhuman Primate Model of HCMV to Guide Vaccine Development" Viruses 6, no. 4: 1483-1501. https://doi.org/10.3390/v6041483