DNA-launched live-attenuated vaccines for biodefense applications

Expert Review of Vaccines

Volumn 15, Issue 9, 2016, Pages 1223-1234

  Pushko, Peter ^a   Lukashevich, Igor S ^b   Weaver, Scott C ^c   Tretyakova, Irina ^a  

^a Medigen Inc   (United States)

^b University of Louisville School of Medicine   (United States)

^c University of Texas Medical Branch School of Medicine   (United States)

Author keywords

alphavirus; chikungunya; DNA vaccine; flavivirus; live attenuated vaccine; Venezuelan equine encephalitis; yellow fever

Indexed keywords

CHIKUNGUNYA VACCINE; DNA VACCINE; GENOMIC RNA; JAPANESE ENCEPHALITIS VACCINE; LIVE VACCINE; UNCLASSIFIED DRUG; VENEZUELAN EQUINE ENCEPHALITIS VACCINE; VIRUS VACCINE; WEST NILE VACCINE; YELLOW FEVER VACCINE; VIRUS RNA;

ALPHAVIRUS; CHIKUNGUNYA VIRUS; DNA IMMUNIZATION; FLAVIVIRUS; HUMAN; IMMUNE RESPONSE; JAPANESE ENCEPHALITIS VIRUS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RECIPIENT; RECOMBINANT PLASMID; REVERSE GENETICS; REVERTANT; REVIEW; VENEZUELAN EQUINE ENCEPHALITIS VIRUS; WEST NILE VIRUS; YELLOW FEVER VIRUS; ANIMAL; GENETICS; IMMUNOLOGY; PLASMID; RNA VIRUS; RNA VIRUS INFECTIONS;

ANIMALS; HUMANS; PLASMIDS; RNA VIRUS INFECTIONS; RNA VIRUSES; RNA, VIRAL; VACCINES, ATTENUATED; VACCINES, DNA; VIRAL VACCINES;

EID: 84964547398     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1080/14760584.2016.1175943     Document Type: Review

References (112)

1. B.Ferraro, M.P.Morrow, N.A.Hutnick, et al. Clinical applications of DNA vaccines:current progress. Clin Infect Dis. 2011 Aug 1;53(3):296–302.
2. M.A.Kutzler, D.B.Weiner DNA vaccines:ready for prime time? Nat Rev Genet. 2008 Oct;9(10):776–788.
3. M.A.Liu. DNA vaccines:an historical perspective and view to the future. Immunol Rev. 2011 Jan;239(1):62–84.
4. M.Sällberg, L.Frelin, G.Ahlén, et al. Electroporation for therapeutic DNA vaccination in patients. Med Microbiol Immunol. 2015 Feb;204(1):131–135.
5. L.C.Dupuy, C.S.Schmaljohn. DNA vaccines for biodefense. Expert Rev Vaccines. 2009 Dec;8(12):1739–1754.
6. J.T.Schiller, D.R.Lowy. Raising expectations for subunit vaccine. J Infect Dis. 2015 May 1;211(9):1373–1375.
7. P.Pushko, L.M.Pujanauski, X.Sun, et al. Recombinant H7 hemagglutinin forms subviral particles that protect mice and ferrets from challenge with H7N9 influenza virus. Vaccine. 2015 Jul 21;33:4975–4982.
8. P.Pushko, P.Pumpens, E.Grens. Development of virus-like particle technology from small highly symmetric to large complex virus-like particle structures. Intervirology. 2013;56(3):141–165.
9. K.M.Holtz, P.S.Robinson, E.E.Matthews, et al. Modifications of cysteine residues in the transmembrane and cytoplasmic domains of a recombinant hemagglutinin protein prevent cross-linked multimer formation and potency loss. BMC Biotechnol. 2014 Dec 24;14(1):1.
10. I.A.Ramshaw, A.J.Ramsay. The prime-boost strategy:exciting prospects for improved vaccination. Immunol Today. 2000 Apr;21(4):163–165.
11. D.O.Villarreal, K.T.Talbott, D.K.Choo, et al. Synthetic DNA vaccine strategies against persistent viral infections. Expert Rev Vaccines. 2013 May;12(5):537–554.
12. K.E.Broderick, L.M.Humeau. Electroporation-enhanced delivery of nucleic acid vaccines. Expert Rev Vaccines. 2015 Feb;14(2):195–204.
13. L.Lambricht, A.Lopes, S.Kos, et al. Clinical potential of electroporation for gene therapy and DNA vaccine delivery. Expert Opin Drug Deliv. 2016 Feb;13(2):295–310.
14. L.C.Dupuy, M.J.Richards, B.Ellefsen, et al. A DNA vaccine for venezuelan equine encephalitis virus delivered by intramuscular electroporation elicits high levels of neutralizing antibodies in multiple animal models and provides protective immunity to mice and nonhuman primates. Clin Vaccine Immunol. 2011 May;18(5):707–716.
15. J.M.Luke, G.G.Simon, J.Söderholm, et al. Coexpressed RIG-I agonist enhances humoral immune response to influenza virus DNA vaccine. J Virol. 2011 Feb;85(3):1370–1383.
16. J.A.Williams. Improving DNA vaccine performance through vector design. Curr Gene Ther. 2014;14(3):170–189.
17. J.Mairhofer, A.R.Lara. Advances in host and vector development for the production of plasmid DNA vaccines. Methods Mol Biol. 2014;1139:505–541.
18. A.Xenopoulos, P.Pattnaik. Production and purification of plasmid DNA vaccines:is there scope for further innovation? Expert Rev Vaccines. 2014 Dec;13(12):1537–1551.
19. I.Tretyakova, J.Hearn, E.Wang, et al. DNA vaccine initiates replication of live attenuated chikungunya virus in vitro and elicits protective immune response in mice. J Infect Dis. 2014 Jun 15;209(12):1882–1890.• Describes DNA-launched live-attenuated vaccine for CHIKV alphavirus.
20. I.Tretyakova, I.S.Lukashevich, P.Glass, et al. Novel vaccine against Venezuelan equine encephalitis combines advantages of DNA immunization and a live attenuated vaccine. Vaccine. 2013 Feb 4;31(7):1019–1025.•• Describes proof-of-concept DNA-launched live-attenuated vaccine for VEEV alphavirus.
21. I.Tretyakova, B.Nickols, R.Hidajat, et al. Plasmid DNA initiates replication of yellow fever vaccine in vitro and elicits virus-specific immune response in mice. Virology. 2014 Nov;468-470:28–35.• Describes DNA-launched live-attenuated vaccine for YFV flavivirus.
22. R.A.Hall, D.J.Nisbet, K.B.Pham, et al. DNA vaccine coding for the full-length infectious Kunjin virus RNA protects mice against the New York strain of West Nile virus. Proc Natl Acad Sci U S A. 2003 Sep 2;100(18):10460–10464.
23. V.P.Mishin, F.Cominelli, V.F.Yamshchikov. A ‘minimal’ approach in design of flavivirus infectious DNA. Virus Res. 2001 Dec 4;81(1–2):113–123.
24. V.Yamshchikov. Development of a human live attenuated West Nile infectious DNA vaccine:conceptual design of the vaccine candidate. Virology. 2015 Oct;484:59–68.• Describes DNA-launched live-attenuated vaccine approach for WNV flavivirus.
25. P.Pushko, P.B.Bredenbeek, I.S.Lukashevich. Experimental DNA-launched live-attenuated vaccines against infections caused by Flavi-and alphaviruses. In:S.Igor, H.S.Lukashevich, editor. Novel technologies for vaccine development. Vienna:Springer Vienna; 2014.
26. P.D.Minor. Live attenuated vaccines:historical successes and current challenges. Virology. 2015 May;479-480:379–392.
27. L.L.Coffey, Y.Beeharry, A.V.Bordería, et al. Arbovirus high fidelity variant loses fitness in mosquitoes and mice. Proc Natl Acad Sci U S A. 2011 Sep 20;108(38):16038–16043.
28. S.C.Weaver, L.A.Bellew, L.Gousset, et al. Diversity within natural populations of eastern equine encephalomyelitis virus. Virology. 1993 Aug;195(2):700–709.
29. S.A.Plotkin. Vaccines:past, present and future. Nat Med. 2005 Apr;11(4 Suppl):S5–11.
30. WHO. Standard operating procedure. Mutant analysis by PCR and restriction enzyme cleavage (MAPREC) for oral poliovirus (Sabin) vaccine types 1, 2 or 3. 2012 [cited 2015 May27]. Available from:http://www.who.int/biologicals/vaccines/MAPREC_SOP_Final_09112012.pdf.
31. X.Jiang, T.J.Dalebout, I.S.Lukashevich, et al. Molecular and immunological characterization of a DNA-launched yellow fever virus 17D infectious clone. J Gen Virol. 2015 Apr;96(Pt 4):804–814.• Describes DNA-launched live attenuated vaccine for YFV flavivirus.
32. R.Hidajat, B.Nickols, N.Forrester, et al. Next generation sequencing of DNA-launched chikungunya vaccine virus. Virology. 2016 Mar;490:83–90.•• Presents evidence that DNA-launched live-attenuated CHIKV vaccine has lower probability of reversion mutations as compared to classic live-attenuated vaccine.
33. C.Kilchert, S.Wittmann, L.Vasiljeva. The regulation and functions of the nuclear RNA exosome complex. Nat Rev Mol Cell Biol. 2016 Jan 4;17:227–239.
34. D.S.Mansur, G.L.Smith, B.J.Ferguson. Intracellular sensing of viral DNA by the innate immune system. Microbes Infect. 2014 Dec;16(12):1002–1012.
35. A.D.Barrett, D.W.Beasley. Development pathway for biodefense vaccines. Vaccine. 2009 Nov 5;27(Suppl 4):D2–7.
36. S.C.Weaver, A.D.Barrett. Transmission cycles, host range, evolution and emergence of arboviral disease. Nat Rev Microbiol. 2004 Oct;2(10):789–801.
37. S.R.Walsh, R.Dolin. Vaccinia viruses:vaccines against smallpox and vectors against infectious diseases and tumors. Expert Rev Vaccines. 2011 Aug;10(8):1221–1240.
38. K.Ljungberg, A.C.Whitmore, M.E.Fluet, et al. Increased immunogenicity of a DNA-launched Venezuelan equine encephalitis virus-based replicon DNA vaccine. J Virol. 2007 Dec;81(24):13412–13423.
39. N.Bhat, K.A.Fitzgerald. Recognition of cytosolic DNA by cGAS and other STING-dependent sensors. Eur J Immunol. 2014 Mar;44(3):634–640.
40. C.Coban, K.Kobiyama, N.Jounai, et al. DNA vaccines:a simple DNA sensing matter? Hum Vaccin Immunother. 2013 Oct;9(10):2216–2221.
41. S.Wicker, H.Seale, L.Von Gierke, et al. Vaccination of healthcare personnel:spotlight on groups with underlying conditions. Vaccine. 2014 Jul;32(32):4025–4031.
42. P.Haber, P.L.Moro, M.Cano, et al. Post-licensure surveillance of quadrivalent live attenuated influenza vaccine United States, Vaccine Adverse Event Reporting System (VAERS), July 2013-June 2014. Vaccine. 2015 Apr 15;33(16):1987–1992.
43. P.J.Turner, J.Southern, N.J.Andrews, et al. Safety of live attenuated influenza vaccine in young people with egg allergy:multicentre prospective cohort study. Bmj. 2015;351:h6291.
44. F.Franceschini, P.Bottau, S.Caimmi, et al. Vaccination in children with allergy to non active vaccine components. Clin Transl Med. 2015;4:3.
45. Yamshchikov. Inventor infectious DNA as a vaccine against West Nile and other flaviviruses USA. US Patent 7459163 B2. 2008.
46. V.Yamshchikov, M.Manuvakhova, E.Rodriguez. Development of a human live attenuated West Nile infectious DNA vaccine:suitability of attenuating mutations found in SA14-14-2 for WN vaccine design. Virology. 2016 Nov 3;487:198–206.
47. V.Yamshchikov, V.Mishin, F.Cominelli. A new strategy in design of +RNA virus infectious clones enabling their stable propagation in E. coli. Virology. 2001 Mar 15;281(2):272–280.
48. O.Schwartz, M.L.Albert. Biology and pathogenesis of chikungunya virus. Nat Rev. 2010 Jul;8(7):491–500.
49. J.H.Strauss, E.G.Strauss. The alphaviruses:gene expression, replication, and evolution. Microbiol Rev. 1994 Sep;58(3):491–562.
50. V.A.Arankalle, S.Shrivastava, S.Cherian, et al. Genetic divergence of chikungunya viruses in India (1963-2006) with special reference to the 2005-2006 explosive epidemic. J Gen Virol. 2007 Jul;88(Pt 7):1967–1976.
51. S.C.Weaver, W.K.Reisen. Present and future arboviral threats. Antiviral Res. 2010 Feb;85(2):328–345.
52. T.Couderc, N.Khandoudi, M.Grandadam, et al. Prophylaxis and therapy for chikungunya virus infection. J Infect Dis. 2009 Aug 15;200(4):516–523.
53. B.Queyriaux, F.Simon, M.Grandadam, et al. Clinical burden of chikungunya virus infection. Lancet Infect Dis. 2008 Jan;8(1):2–3.
54. F.J.Burt, M.S.Rolph, N.E.Rulli, et al. Chikungunya:a re-emerging virus. Lancet. 2012 Feb 18;379(9816):662–671.
55. B.Queyriaux, A.Armengaud, C.Jeannin, et al. Chikungunya in Europe. Lancet. 2008 Mar 1;371(9614):723–724.
56. M.Enserink. ENTOMOLOGY:A Mosquito Goes Global. Science (New York, NY). 2008 May 16;320(5878):864–866.
57. S.C.Weaver, J.E.Osorio, J.A.Livengood, et al. Chikungunya virus and prospects for a vaccine. Expert Rev Vaccines. 2012 Sep;11(9):1087–1101.
58. R.C.Dhiman, S.Pahwa, G.P.Dhillon, et al. Climate change and threat of vector-borne diseases in India:are we prepared? Parasitol Res. 2010 Mar;106(4):763–773.
59. T.Pistone, K.Ezzedine, I.Schuffenecker, et al. An imported case of chikungunya fever from Madagascar:use of the sentinel traveller for detecting emerging arboviral infections in tropical and European countries. Travel Med Infect Dis. 2009 Jan;7(1):52–54.
60. S.E.Randolph, D.J.Rogers. The arrival, establishment and spread of exotic diseases:patterns and predictions. Nat Rev Microbiol. 2010 May;8(5):361–371.
61. S.C.Weaver. Urbanization and geographic expansion of zoonotic arboviral diseases:mechanisms and potential strategies for prevention. Trends Microbiol. 2013 Aug;21(8):360–363.
62. M.M.Thiboutot, S.Kannan, O.U.Kawalekar, et al. Chikungunya:a potentially emerging epidemic? PLoS Negl Trop Dis. 2010;4(4):e623.
63. L.R.Petersen, S.L.Stramer, A.M.Powers. Chikungunya virus:possible impact on transfusion medicine. Transfus Med Rev. 2010 Jan;24(1):15–21.
64. M.Schwameis, N.Buchtele, P.P.Wadowski, et al. Chikungunya vaccines in development. Hum Vaccin Immunother. 2015 Nov;10:0.
65. R.Gorchakov, E.Wang, G.Leal, et al. Attenuation of chikungunya virus vaccine strain 181/clone 25 is determined by two amino acid substitutions in the E2 envelope glycoprotein. J Virol. 2012;86(11):6084–6096.• Describes attenuating mutations in CHIKV alphavirus.
66. K.S.Plante, S.L.Rossi, N.A.Bergren, et al. Extended preclinical safety, efficacy and stability testing of a live-attenuated chikungunya vaccine candidate. PLoS Negl Trop Dis. 2015 Sep;9(9):e0004007.
67. R.Edelman, C.O.Tacket, S.S.Wasserman, et al. Phase II safety and immunogenicity study of live chikungunya virus vaccine TSI-GSD-218. Am J Trop Med Hyg. 2000 Jun;62(6):681–685.
68. Inovio. Inovio pharmaceuticals breakthrough DNA-based monoclonal antibody therapy completely protects animals from lethal viral challenge. 2014 [cited March19, 2016]. Available from:http://ir.inovio.com/news/news-releases/news-releases-details/2014/Inovio-Pharmaceuticals-Breakthrough-DNA-Based-Monoclonal-Antibody-Therapy-Completely-Protects-Animals-From-Lethal-Viral-Challenge/.
69. D.Hallengärd, M.Kakoulidou, A.Lulla, et al. Novel attenuated chikungunya vaccine candidates elicit protective immunity in C57BL/6 mice. J Virol. 2014;88(5):2858–2866.• Describes DNA-launched live-attenuated vaccine for CHIKV alphavirus.
70. W.F.Scherer, E.W.Cupp, G.M.Dziem, et al. Mesenteronal infection threshold of an epizootic strain of Venezuelan encephalitis virus in Culex (Melanoconion) taeniopus mosquitoes and its implication to the apparent disappearance of this virus strain from an enzootic habitat in Guatemala. Am J Trop Med Hyg. 1982 Sep;31(5):1030–1037.
71. A.C.Brault, A.M.Powers, D.Ortiz, et al. Venezuelan equine encephalitis emergence:enhanced vector infection from a single amino acid substitution in the envelope glycoprotein. Proc Natl Acad Sci U S A. 2004 Aug 3;101(31):11344–11349.
72. E.R.Deardorff, S.C.Weaver. Vector competence of Culex (Melanoconion) taeniopus for equine-virulent subtype IE strains of Venezuelan equine encephalitis virus. Am J Trop Med Hyg. 2010 Jun;82(6):1047–1052.
73. S.C.Weaver, C.Ferro, R.Barrera, et al. Venezuelan equine encephalitis. Annu Rev Entomol. 2004;49:141–174.
74. W.F.Scherer, S.C.Weaver, C.A.Taylor, et al. Vector competence of Culex (Melanoconion) taeniopus for allopatric and epizootic Venezuelan equine encephalomyelitis viruses. Am J Trop Med Hyg. 1987 Jan;36(1):194–197.
75. D.L.Smart, D.O.Trainer. Serologic evidence of Venezuelan equine encephalitis in some wild and domestic populations of southern Texas. J Wildl Dis. 1975 Apr;11(2):195–200.
76. S.C.Weaver, M.Pfeffer, K.Marriott, et al. Genetic evidence for the origins of Venezuelan equine encephalitis virus subtype IAB outbreaks. Am J Trop Med Hyg. 1999 Mar;60(3):441–448.
77. L.W.Kitchen, D.W.Vaughn. Role of U.S. military research programs in the development of U.S.-licensed vaccines for naturally occurring infectious diseases. Vaccine. 2007 Oct;25(41):7017–7030.
78. S.M.Lemon, Thaul S, Fisseha S, et al., editors. Protecting our forces:improving vaccine acquisition and availability in the U.S. military. Institute of Medicine (U.S.). Committee on a strategy for minimizing the impact of naturally occurring infectious diseases of military importance. 1st ed. Washington (DC):National Academies Press; 2002.
79. S.Paessler, S.C.Weaver. Vaccines for Venezuelan equine encephalitis. Vaccine. 2009 Nov 5;27 Suppl 4:D80–5.
80. R.M.Kinney, G.J.Chang, K.R.Tsuchiya, et al. Attenuation of Venezuelan equine encephalitis virus strain TC-83 is encoded by the 5ʹ-noncoding region and the E2 envelope glycoprotein. J Virol. 1993 Mar;67(3):1269–1277.
81. R.J.Phillpotts, A.J.Wright. TC-83 vaccine protects against airborne or subcutaneous challenge with heterologous mouse-virulent strains of Venezuelan equine encephalitis virus. Vaccine. 1999 Feb 26;17(7–8):982–988.
82. P.R.Pittman, R.S.Makuch, J.A.Mangiafico, et al. Long-term duration of detectable neutralizing antibodies after administration of live-attenuated VEE vaccine and following booster vaccination with inactivated VEE vaccine. Vaccine. 1996 Mar;14(4):337–343.
83. J.L.Kenney, S.M.Volk, J.Pandya, et al. Stability of RNA virus attenuation approaches. Vaccine. 2011 Mar 9;29(12):2230–2234.
84. R.Zhang, C.F.Hryc, Y.Cong, et al. 4.4 A cryo-EM structure of an enveloped alphavirus Venezuelan equine encephalitis virus. Embo J. 2011 Sep 14;30(18):3854–3863.
85. S.Perri, C.E.Greer, K.Thudium, et al. An alphavirus replicon particle chimera derived from venezuelan equine encephalitis and sindbis viruses is a potent gene-based vaccine delivery vector. J Virol. 2003 Oct;77(19):10394–10403.
86. J.M.Polo, J.P.Gardner, Y.Ji, et al. Alphavirus DNA and particle replicons for vaccines and gene therapy. Dev Biol (Basel). 2000;104:181–185.
87. V.Riabov, I.Tretyakova, R.B.Alexander, et al. Anti-tumor effect of the alphavirus-based virus-like particle vector expressing prostate-specific antigen in a HLA-DR transgenic mouse model of prostate cancer. Vaccine. 2015 Aug 26;33:5386–5395.
88. E.L.Nelson, D.Prieto, T.G.Alexander, et al. Venezuelan equine encephalitis replicon immunization overcomes intrinsic tolerance and elicits effective anti-tumor immunity to the ‘self’ tumor-associated antigen, neu in a rat mammary tumor model. Breast Cancer Res Treat. 2003 Dec;82(3):169–183.
89. P.Pushko, I.Tretyakova. Alphavirus replicon vectors for prophylactic applications and cancer interventions. In:I.S.Lukashevich, H.Shirwan, editors. Novel technologies for vaccine development. Vienna:Springer; 2014. p. 61–87. 2014 edition.
90. P.Pushko, M.Parker, G.V.Ludwig, et al. Replicon-helper systems from attenuated Venezuelan equine encephalitis virus:expression of heterologous genes in vitro and immunization against heterologous pathogens in vivo. Virology. 1997 Dec 22;239(2):389–401.
91. T.W.Geisbert, P.Pushko, K.Anderson, et al. Evaluation in nonhuman primates of vaccines against Ebola virus. Emerg Infect Dis. 2002 May;8(5):503–507.
92. P.Pushko, J.Geisbert, M.Parker, et al. Individual and bivalent vaccines based on alphavirus replicons protect guinea pigs against infection with Lassa and Ebola viruses. J Virol. 2001 Dec;75(23):11677–11685.
93. P.Pushko, M.Bray, G.V.Ludwig, et al. Recombinant RNA replicons derived from attenuated Venezuelan equine encephalitis virus protect guinea pigs and mice from Ebola hemorrhagic fever virus. Vaccine. 2000 Aug 15;19(1):142–153.
94. T.O.Berge, I.S.Banks, W.D.Tigertt. Attenuation of Venezuelan equine encephalomyelitis virus by in vitro cultivation in guinea-pig heart cells. Am J Trop Med Hyg. 1961;73:209–218.
95. J.D.Grabenstein, P.R.Pittman, J.T.Greenwood, et al. Immunization to protect the US Armed Forces:heritage, current practice, and prospects. Epidemiol Rev. 2006;28:3–26.
96. C.H.HokeJr. History of U.S. military contributions to the study of viral encephalitis. Mil Med. 2005 Apr;170(4 Suppl):92–105.
97. B.Y.Cheng, E.Ortiz-Riano, J.C.De La Torre, et al. Arenavirus genome rearrangement for the development of live attenuated vaccines. J Virol. 2015 Jul;89(14):7373–7384.
98. A.C.Lowen, A.Boyd, J.K.Fazakerley, et al. Attenuation of bunyavirus replication by rearrangement of viral coding and noncoding sequences. J Virol. 2005 Jun;79(11):6940–6946.
99. P.Pushko, M.D.Parker, J.F.Smith, et al. Inventor Live attenuated venezuelan equine encephalitis vaccine. US Patent 6296854 B1. 2001.
100. W.K.Reisen. Ecology of West Nile virus in North America. Viruses. 2013 Sep;5(9):2079–2105.
101. L.R.Petersen, A.C.Brault, R.S.Nasci. West Nile virus:review of the literature. Jama. 2013 Jul 17;310(3):308–315.
102. M.J.Frost, J.Zhang, J.H.Edmonds, et al. Characterization of virulent West Nile virus Kunjin strain, Australia, 2011. Emerg Infect Dis. 2012 May;18(5):792–800.
103. S.B.Halstead, S.J.Thomas. New Japanese encephalitis vaccines:alternatives to production in mouse brain. Expert Rev Vaccines. 2011 Mar;10(3):355–364.
104. C.M.Rice, A.Grakoui, R.Galler, et al. Transcription of infectious yellow fever RNA from full-length cDNA templates produced by in vitro ligation. New Biol. 1989 Dec;1(3):285–296.
105. J.Cohen. Unfilled vials. Science. 2016 Jan 1;351(6268):16–19.
106. I.S.Lukashevich, R.CarrionJr., M.S.Salvato, et al. Safety, immunogenicity, and efficacy of the ML29 reassortant vaccine for Lassa fever in small non-human primates. Vaccine. 2008 Sep 26;26(41):5246–5254.
107. N.J.Sullivan, L.Hensley, C.Asiedu, et al. CD8+ cellular immunity mediates rAd5 vaccine protection against Ebola virus infection of nonhuman primates. Nat Med. 2011 Sep;17(9):1128–1131.
108. D.Safronetz, C.Mire, K.Rosenke, et al. A recombinant vesicular stomatitis virus-based Lassa fever vaccine protects guinea pigs and macaques against challenge with geographically and genetically distinct Lassa viruses. PLoS Negl Trop Dis. 2015 Apr;9(4):e0003736.
109. S.M.Kang, P.Pushko, R.A.Bright, et al. Influenza virus-like particles as pandemic vaccines. Curr Top Microbiol Immunol. 2009;333:269–289.
110. I.Tretyakova, R.Hidajat, G.Hamilton, et al. Preparation of quadri-subtype influenza virus-like particles using bovine immunodeficiency virus gag protein. Virology. 2016;487:163–171.
111. W.Akahata, Z.Y.Yang, H.Andersen, et al. A virus-like particle vaccine for epidemic chikungunya virus protects nonhuman primates against infection. Nat Med. 2010 Mar;16(3):334–338.
112. M.Carrillo-Tripp, C.M.Shepherd, I.A.Borelli, et al. VIPERdb2:an enhanced and web API enabled relational database for structural virology. Nucleic Acids Res. 2009 Jan;37(Databaseissue):D436–D442.