Cytomegalovirus-based vaccine expressing Ebola virus glycoprotein protects nonhuman primates from Ebola virus infection

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Marzi, Andrea ^a   Murphy, Aisling A ^b   Feldmann, Friederike ^a   Parkins, Christopher J ^c   Haddock, Elaine ^a   Hanley, Patrick W ^a   Emery, Matthew J ^b   Engelmann, Flora ^d   Messaoudi, Ilhem ^d   Feldmann, Heinz ^a   Jarvis, Michael A ^b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF PLYMOUTH   (United Kingdom)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DRUG CARRIER; EBOLA VACCINE; ENVELOPE GLYCOPROTEIN, EBOLA VIRUS; RECOMBINANT VACCINE; VIRUS ANTIBODY; VIRUS ENVELOPE PROTEIN;

ANIMAL; BLOOD; CYTOMEGALOVIRUS; DISEASE MODEL; FEMALE; GENETICS; HEMORRHAGIC FEVER, EBOLA; IMMUNOLOGY; MALE; RHESUS MONKEY; SURVIVAL ANALYSIS;

ANIMALS; ANTIBODIES, VIRAL; CYTOMEGALOVIRUS; DISEASE MODELS, ANIMAL; DRUG CARRIERS; EBOLA VACCINES; FEMALE; HEMORRHAGIC FEVER, EBOLA; MACACA MULATTA; MALE; SURVIVAL ANALYSIS; VACCINES, SYNTHETIC; VIRAL ENVELOPE PROTEINS;

EID: 84958213109     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep21674     Document Type: Article

References (59)

1. Feldmann, H. & Geisbert, T. W. Ebola haemorrhagic fever. Lancet 377, 849-862, doi: 10.1016/S0140-6736(10)60667-8 (2011).
2. Pigott, D. M. et al. Mapping the zoonotic niche of Ebola virus disease in Africa. eLife 3, e04395, doi: doi: 10.7554/eLife.04395 (2014).
3. WHO. Ebola situation report, http://apps.who.int/ebola/current-situation/ebola-situation-report-15-july-2015 (2015). [Accessed 08/12/2015]
4. Bermejo, M. et al. Ebola outbreak killed 5000 gorillas. Science 314, 1564, doi: 314/5805/1564 10.1126/science.1133105 (2006).
5. Genton, C. et al. Recovery potential of a western lowland gorilla population following a major Ebola outbreak: results from a ten year study. PLoS One 7, e37106, doi: 10.1371/journal.pone.0037106 (2012).
6. Mahl, P. et al. Twenty year experience of the oral rabies vaccine SAG2 in wildlife: a global review. Vet Res 45, 77, doi: 10.1186/s13567-014-0077-8 s13567-014-0077-8 (2014).
7. Swayne, D. E. Impact of vaccines and vaccination on global control of avian influenza. Avian Dis 56, 818-828 (2013).
8. Marzi, A. & Feldmann, H. Ebola virus vaccines: an overview of current approaches. Expert Rev Vaccines 13, 521-531, doi: 10.1586/14760584.2014.885841 (2014).
9. Henao-Restrepo, A. M. et al. Efficacy and effectiveness of an rVSV-vectored vaccine expressing Ebola surface glycoprotein: interim results from the Guinea ring vaccination cluster-randomised trial. Lancet (2015).
10. Rizvanov, A. A. et al. Generation of a recombinant cytomegalovirus for expression of a hantavirus glycoprotein. J Virol 77, 12203-12210 (2003).
11. Hansen, S. G. et al. Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nature Med 15, 293-299, doi: 10.1038/nm.1935 (2009).
12. Jarvis, M. A., Hansen, S. G., Nelson, J. A., Picker, L. J. & Frueh, K. In Cytomegaloviruses: From Molecular Pathogenesis to Intervention Vol. II (ed M. J., Reddehase) (Caister Academic Press, 2013).
13. Redwood, A. J. et al. Viral vectored immunocontraception: screening of multiple fertility antigens using murine cytomegalovirus as a vaccine vector. Vaccine 25, 698-708, doi: 10.1016/j.vaccine.2006.08.021 (2007).
14. Hansen, S. G. et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 473, 523-527, doi: 10.1038/nature10003 (2011).
15. Tsuda, Y. et al. A replicating cytomegalovirus-based vaccine encoding a single Ebola virus nucleoprotein CTL epitope confers protection against Ebola virus. PLoS Negl Trop Dis 5, e1275, doi: 10.1371/journal.pntd.0001275 (2011).
16. Tsuda, Y. et al. A cytomegalovirus-based vaccine provides long-lasting protection against lethal Ebola virus challenge after a single dose. Vaccine 33, 2261-2266, doi: 10.1016/j.vaccine.2015.03.029 (2015).
17. Kaech, S. M. & Wherry, E. J. Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity 27, 393-405, doi: 10.1016/j.immuni.2007.08.007 (2007).
18. Hansen, S. G. et al. Immune clearance of highly pathogenic SIV infection. Nature 502, 100-104, doi: 10.1038/nature12519 (2013).
19. Sequar, G. et al. Experimental coinfection of rhesus macaques with rhesus cytomegalovirus and simian immunodeficiency virus: pathogenesis. J Virol 76, 7661-7671 (2002).
20. 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 344, 1366-1371 (2001).
21. Hansen, S. G. et al. Evasion of CD8+ T cells is critical for superinfection by cytomegalovirus. Science 328, 102-106, doi: 10.1126/science.1185350 (2010).
22. Murthy, S. et al. Absence of frequent herpesvirus transmission in a nonhuman primate predator-prey system in the wild. J Virol 87, 10651-10659, doi: 10.1128/JVI.01104-13 (2013).
23. Moro, D., Lloyd, M. L., Smith, A. L., Shellam, G. R. & Lawson, M. A. Murine viruses in an island population of introduced house mice and endemic short-tailed mice in Western Australia. J Wildl Dis 35, 301-310 (1999).
24. Anoh, A. E. et al. Genetic identification of cytomegaloviruses in a rural population of Cote d'Ivoire. Virol J 12, 155, doi: 10.1186/s12985-015-0394-1 (2015).
25. Reed, D. S. & Mohamadzadeh, M. Status and challenges of filovirus vaccines. Vaccine 25, 1923-1934, doi: 10.1016/j.vaccine.2006.11.037 (2007).
26. Geisbert, T. W. et al. Evaluation in nonhuman primates of vaccines against Ebola virus. Emerg Infect Dis 8, 503-507 (2002).
27. Shurtleff, A. C. & Bavari, S. Animal models for ebolavirus countermeasures discovery: what defines a useful model? Expert Opin Drug Discov 10, 685-702, doi: 10.1517/17460441.2015.1035252 (2015).
28. Richardson, J. S. et al. Enhanced protection against Ebola virus mediated by an improved adenovirus-based vaccine. PLoS One 4, e5308, doi: 10.1371/journal.pone.0005308 (2009).
29. Malouli, D. et al. Cytomegalovirus pp65 limits dissemination but is dispensable for persistence. J Clin Invest 124, 1928-1944, doi: 10.1172/JCI67420 (2014).
30. Chang, W. L. & Barry, P. A. Cloning of the full-length rhesus cytomegalovirus genome as an infectious and self-excisable bacterial artificial chromosome for analysis of viral pathogenesis. J Virol 77, 5073-5083 (2003).
31. Hansen, S. G. et al. Corrigendum: Immune clearance of highly pathogenic SIV infection. Nature 514, 654, doi: 10.1038/nature13840 (2014).
32. Bilello, J. P. et al. Vaccine protection against simian immunodeficiency virus in monkeys using recombinant gamma-2 herpesvirus. J Virol 85, 12708-12720, doi: 10.1128/JVI.00865-11 (2011).
33. Marzi, A. et al. Antibodies are necessary for rVSV/ZEBOV-GP-mediated protection against lethal Ebola virus challenge in nonhuman primates. Proc Nat Acad Sci USA 110, 1893-1898, doi: 10.1073/pnas.1209591110 (2013).
34. Qiu, X. et al. Sustained protection against Ebola virus infection following treatment of infected nonhuman primates with ZMAb. Sci Rep 3, 3365, doi: 10.1038/srep03365 (2013).
35. Jones, S. M. et al. Live attenuated recombinant vaccine protects nonhuman primates against Ebola and Marburg viruses. Nature Med 11, 786-790, doi: nm1258 10.1038/nm1258 (2005).
36. Falzarano, D., Geisbert, T. W. & Feldmann, H. Progress in filovirus vaccine development: evaluating the potential for clinical use. Expert Rev Vaccines 10, 63-77, doi: 10.1586/erv.10.152 (2011).
37. Sullivan, N. J. et al. CD8+ cellular immunity mediates rAd5 vaccine protection against Ebola virus infection of nonhuman primates. Nature Med 17, 1128-1131, doi: 10.1038/nm.2447 (2011).
38. Sullivan, N. J., Martin, J. E., Graham, B. S. & Nabel, G. J. Correlates of protective immunity for Ebola vaccines: implications for regulatory approval by the animal rule. Nature Rev Microbiol 7, 393-400, doi: 10.1038/nrmicro2129 (2009).
39. Sullivan, N. J., Sanchez, A., Rollin, P. E., Yang, Z. Y. & Nabel, G. J. Development of a preventive vaccine for Ebola virus infection in primates. Nature 408, 605-609, doi: 10.1038/35046108 (2000).
40. Wong, G. et al. Immune parameters correlate with protection against ebola virus infection in rodents and nonhuman primates. Sci Transl Med 4, 158ra146, doi: 10.1126/scitranslmed.3004582 (2012).
41. Agnandji, S. T. et al. Phase 1 Trials of rVSV Ebola Vaccine in Africa and Europe - Preliminary Report. N Engl J Med, doi: 10.1056/NEJMoa1502924 (2015).
42. Tapia, M. D. et al. Use of ChAd3-EBO-Z Ebola virus vaccine in Malian and US adults, and boosting of Malian adults with MVA-BN-Filo: a phase 1, single-blind, randomised trial, a phase 1b, open-label and double-blind, dose-escalation trial, and a nested, randomised, double-blind, placebo-controlled trial. Lancet Infect Dis, doi: 10.1016/S1473-3099(15)00362-X (2015).
43. Xu, G., Smith, T., Grey, F. & Hill, A. B. Cytomegalovirus-based cancer vaccines expressing TRP2 induce rejection of melanoma in mice. Biochem Biophys Res Comm 437, 287-291, doi: 10.1016/j.bbrc.2013.06.068 (2013).
44. Stanley, D. A. et al. Chimpanzee adenovirus vaccine generates acute and durable protective immunity against ebolavirus challenge. Nature Med 20, 1126-1129, doi: 10.1038/nm.3702 (2014).
45. Pande, N. T., Powers, C., Ahn, K. & Fruh, K. Rhesus Cytomegalovirus Contains Functional Homologues of US2, US3, US6, and US11. J Virol 79, 5786-5798 (2005).
46. + T-cell immune responses and enhances vaccine potency. Mol Ther 15, 1211-1219, doi: 10.1038/sj.mt.6300121 (2007).
47. + T cell help in the tumor microenvironment. PloS One 9, e115711, doi: 10.1371/journal.pone.0115711 (2014).
48. Alexander, J. et al. Development of high potency universal DR-restricted helper epitopes by modification of high affinity DR-blocking peptides. Immunity 1, 751-761 (1994).
49. Delrieu, J., Ousset, P. J., Caillaud, C. & Vellas, B. 'Clinical trials in Alzheimer's disease': immunotherapy approaches. J Neurochem 120 Suppl 1, 186-193, doi: 10.1111/j.1471-4159.2011.07458.x (2012).
50. Ross, S. A. et al. Cytomegalovirus reinfections in healthy seroimmune women. J Infect Dis 201, 386-389, doi: 10.1086/649903 (2010).
51. Farroway, L. N. et al. Transmission of two Australian strains of murine cytomegalovirus (MCMV) in enclosure populations of house mice (Mus domesticus). Epidemiol Infect 133, 701-710 (2005).
52. Murphy, A. A., Redwood, A. J. & Jarvis, M. A. Self-disseminating vaccines for emerging infectious diseases. Expert Rev Vaccines, 15, 31-9, doi: 10.1586/14760584.2016.1106942 (2016).
53. Groseth, A., Feldmann, H. & Strong, J. E. The ecology of Ebola virus. Trends in Microbiol 15, 408-416, doi: 10.1016/j.tim.2007.08.001 (2007).
54. Leroy, E. M. et al. Fruit bats as reservoirs of Ebola virus. Nature 438, 575-576, doi: 10.1038/438575a (2005).
55. Volchkov, V. E., Feldmann, H., Volchkova, V. A. & Klenk, H. D. Processing of the Ebola virus glycoprotein by the proprotein convertase furin. Proc Nat Acad Sci USA 95, 5762-5767 (1998).
56. 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 77, 6620-6636 (2003).
57. Reed, L. J. & Muench, H. A simple method of estimating fifty percent endpoints. Am J Hygeine 27, 493-497 (1938).
58. Nakayama, E. et al. Enzyme-linked immunosorbent assay for detection of filovirus species-specific antibodies. Clin Vacc Immunol 17, 1723-1728, doi: 10.1128/CVI.00170-10 (2010).
59. Qiu, X. et al. Mucosal immunization of cynomolgus macaques with the VSVDeltaG/ZEBOVGP vaccine stimulates strong ebola GP-specific immune responses. PLoS One 4, e5547, doi: 10.1371/journal.pone.0005547 (2009).