Plant-made vaccines against West Nile virus are potent, safe, and economically feasible

Biotechnology Journal

Volumn 10, Issue 5, 2015, Pages 671-680

  Chen, Qiang ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Nicotiana benthamiana; Plant biotechnology; Plant made vaccines; Vaccine; West Nile virus (WNV)

Indexed keywords

COST BENEFIT ANALYSIS; DISEASE CONTROL; PLANTS (BOTANY); VIRUSES;

CLINICAL INVESTIGATION; DOWNSTREAM-PROCESSING; ECONOMIC CHALLENGES; NICOTIANA BENTHAMIANA; PLANT BIOTECHNOLOGY; PLANT-MADE VACCINES; TRANSIENT EXPRESSION; WEST NILE VIRUS;

VACCINES;

EPITOPE; HERBACEOUS AGENT; IMMUNOGLOBULIN G; INACTIVATED VACCINE; LIVE VACCINE; NEUTRALIZING ANTIBODY; SUBUNIT VACCINE; VIRUS DNA; VIRUS VECTOR; WEST NILE VACCINE; VIRUS ENVELOPE PROTEIN;

ANTIBODY RESPONSE; DENGUE VIRUS; DOWNSTREAM PROCESSING; DRUG COST; DRUG POTENCY; DRUG SAFETY; FOOD AND DRUG ADMINISTRATION; HUMAN; HUMORAL IMMUNITY; IMMUNOGENICITY; NONHUMAN; PLANT BIOTECHNOLOGY; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SUBUNIT; REVIEW; TRANSIENT EXPRESSION; VACCINATION; VACCINE PRODUCTION; VIRUS LIKE AGENT; WEST NILE FEVER; WEST NILE VIRUS; ANIMAL; BIOSYNTHESIS; ECONOMICS; GENETICS; IMMUNOLOGY; METABOLISM; PLANT; VIROLOGY;

ANIMALIA; NICOTIANA BENTHAMIANA; WEST NILE VIRUS;

ANIMALS; HUMANS; PLANTS; VIRAL ENVELOPE PROTEINS; WEST NILE FEVER; WEST NILE VIRUS; WEST NILE VIRUS VACCINES;

EID: 84928825678     PISSN: 18606768     EISSN: 18607314     Source Type: Journal    
DOI: 10.1002/biot.201400428     Document Type: Review

References (79)

1. Petersen, L. R., Brault, A. C., Nasci, R. S., West Nile virus: review of the literature. Jama 2013, 310, 308-315.
2. Brinton, M. A., The molecular biology of West Nile Virus: a new invader of the western hemisphere. Annu. Rev. Microbiol. 2002, 56, 371-402.
3. Chambers, T. J., Hahn, C. S., Galler, R., Rice, C. M., Flavivirus genome organization, expression, and replication. Annu. Rev. Microbiol. 1990, 44, 649-688.
4. Mukhopadhyay, S., Kim, B. S., Chipman, P. R., Rossmann, M. G., Kuhn, R. J., Structure of West Nile virus. Science 2003, 302, 248.
5. May, F. J., Davis, C. T., Tesh, R. B., Barrett, A. D., Phylogeography of West Nile virus: from the cradle of evolution in Africa to Eurasia, Australia, and the Americas. J. Virol. 2011, 85, 2964-2974.
6. Lanciotti, R. S., Ebel, G. D., Deubel, V., Kerst, A. J. et al., Complete genome sequences and phylogenetic analysis of West Nile virus strains isolated from the United States, Europe, and the Middle East. Virology 2002, 298, 96-105.
7. Rudolf, I., Bakonyi, T., Sebesta, O., Mendel, J. et al., West Nile virus lineage 2 isolated from Culex modestus mosquitoes in the Czech Republic, 2013: expansion of the European WNV endemic area to the North? Euro Surveill. 2014, 19, 2-5.
8. Bakonyi, T., Hubalek, Z., Rudolf, I., Nowotny, N., Novel flavivirus or new lineage of West Nile virus, central Europe. Emerg. Infect. Dis. 2005, 11, 225-231.
9. Hinckley, A. F., O'Leary, D. R., Hayes, E. B., Transmission of West Nile virus through human breast milk seems to be rare. Pediatrics 2007, 119, e666-671.
10. Heinz, F. X., Stiasny, K., Flaviviruses and flavivirus vaccines. Vaccine 2012, 30, 4301-4306.
11. Seino, K. K., Long, M. T., Gibbs, E. P., Bowen, R. A. et al., Comparative efficacies of three commercially available vaccines against West Nile Virus (WNV) in a short-duration challenge trial involving an equine WNV encephalitis model. Clin. Vaccine Immunol. 2007, 14, 1465-1471.
12. Ng, T., Hathaway, D., Jennings, N., Champ, D. et al., Equine vaccine for West Nile virus. Dev. Biol. (Basel) 2003, 114, 221-227.
13. Wolf, R. F., Papin, J. F., Hines-Boykin, R., Chavez-Suarez, M. et al., Baboon model for West Nile virus infection and vaccine evaluation. Virology 2006, 355, 44-51.
14. Samina, I., Khinich, Y., Simanov, M., Malkinson, M., An inactivated West Nile virus vaccine for domestic geese-efficacy study and a summary of 4 years of field application. Vaccine 2005, 23, 4955-4958.
15. Pinto, A. K., A Hydrogen Peroxide-Inactivated Virus Vaccine Elicits Humoral and Cellular Immunity and Protects against Lethal West Nile Virus Infection in Aged Mice. J. Virol. 2013, 87, 1926.
16. Orlinger, K. K., Holzer, G. W., Schwaiger, J., Mayrhofer, J. et al., An inactivated West Nile Virus vaccine derived from a chemically synthesized cDNA system. Vaccine 2010, 28, 3318-3324.
17. Hall, R. A., Nisbet, D. J., Pham, K. B., Pyke, A. T. 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. USA 2003, 100, 10460-10464.
18. Yamshchikov, G., Borisevich, V., Seregin, A., Chaporgina, E. et al., An attenuated West Nile prototype virus is highly immunogenic and protects against the deadly NY99 strain: a candidate for live WN vaccine development. Virology 2004, 330, 304-312.
19. Yu, L., Robert Putnak, J., Pletnev, A. G., Markoff, L., Attenuated West Nile viruses bearing 3'SL and envelope gene substitution mutations. Vaccine 2008, 26, 5981-5988.
20. Whiteman, M. C., Li, L., Wicker, J. A., Kinney, R. M. et al., Development and characterization of non-glycosylated E and NS1 mutant viruses as a potential candidate vaccine for West Nile virus. Vaccine 2010, 28, 1075-1083.
21. Dayan, G. H., Pugachev, K., Bevilacqua, J., Lang, J., Monath, T. P., Preclinical and Clinical Development of a YFV 17 D-Based Chimeric Vaccine against West Nile Virus. Viruses-Basel 2013, 5, 3048-3070.
22. Monath, T. P., Liu, J., Kanesa-Thasan, N., Myers, G. A. et al., A live, attenuated recombinant West Nile virus vaccine. Proc. Natl. Acad. Sci. USA 2006.
23. Biedenbender, R., Bevilacqua, J., Gregg, A. M., Watson, M., Dayan, G., Phase II, randomized, double-blind, placebo-controlled, multicenter study to investigate the immunogenicity and safety of a West Nile virus vaccine in healthy adults. J. Infect Dis. 2011, 203, 75-84.
24. Dayan, G. H., Bevilacqua, J., Coleman, D., Buldo, A., Risi, G., Phase II, dose ranging study of the safety and immunogenicity of single dose West Nile vaccine in healthy adults >/= 50 years of age. Vaccine 2012, 30, 6656-6664.
25. Pletnev, A. G., Swayne, D. E., Speicher, J., Rumyantsev, A. A., Murphy, B. R., Chimeric West Nile/dengue virus vaccine candidate: preclinical evaluation in mice, geese and monkeys for safety and immunogenicity. Vaccine 2006, 24, 6392-6404.
26. Durbin, A. P., Wright, P. F., Cox, A., Kagucia, W. et al., The live attenuated chimeric vaccine rWN/DEN4Delta30 is well-tolerated and immunogenic in healthy flavivirus-naive adult volunteers. Vaccine 2013, 31, 5772-5777.
27. Hanley, K. A., Goddard, L. B., Gilmore, L. E., Scott, T. W. et al., Infectivity of West Nile/dengue chimeric viruses for West Nile and dengue mosquito vectors. Vector Borne Zoonotic Dis. 2005, 5, 1-10.
28. Iyer, A. V., Pahar, B., Boudreaux, M. J., Wakamatsu, N. et al., Recombinant vesicular stomatitis virus-based west Nile vaccine elicits strong humoral and cellular immune responses and protects mice against lethal challenge with the virulent west Nile virus strain LSU-AR01. Vaccine 2009, 27, 893-903.
29. Coutant, F., Frenkiel, M. P., Despres, P., Charneau, P., Protective antiviral immunity conferred by a nonintegrative lentiviral vector-based vaccine. PLoS One 2008, 3, e3973.
30. Davis, B. S., Chang, G-J. J., Cropp, B., Roehrig, J.T., Martin, D.A., Mitchell, C.J., Bowen, R., Bunning, M.L., West Nile Virus Recombinant DNA Vaccine Protects Mouse and Horse from Virus Challenge and Expresses In Vitro a Noninfectious Recombinant Antigen That Can Be Used in Enzyme-Linked Immunosorbent Assays. J. Virol. 2001, 75, 4040-4047.
31. Ledgerwood, J. E., Pierson, T. C., Hubka, S. A., Desai, N. et al., A West Nile virus DNA vaccine utilizing a modified promoter induces neutralizing antibody in younger and older healthy adults in a phase I clinical trial. Infect Dis 2011, 203, 1396-1404.
32. Ramanathan, M. P., Kutzler, M. A., Kuo, Y. C., Yan, J. et al., Coimmunization with an optimized IL15 plasmid adjuvant enhances humoral immunity via stimulating B cells induced by genetically engineered DNA vaccines expressing consensus JEV and WNV E DIII. Vaccine 2009, 27, 4370-4380.
33. Chang, D. C., Liu, W. J., Anraku, I., Clark, D. C. et al., Single-round infectious particles enhance immunogenicity of a DNA vaccine against West Nile virus. Nature biotechnology 2008, 26, 571-577.
34. Vogt, M. R., Moesker, B., Goudsmit, J., Jongeneelen, M. et al., Human monoclonal antibodies against West Nile virus induced by natural infection neutralize at a postattachment step. J. Virol. 2009, 83, 6494-6507.
35. Nelson, S., Jost, C. A., Xu, Q., Ess, J. et al., Maturation of West Nile Virus Modulates Sensitivity to Antibody-Mediated Neutralization. PLoS Pathog 2008, 4, e1000060.
36. Nybakken, G., Oliphant, T., Johnson, S., Burke, S. et al., Structural basis for neutralization of a therapeutic antibody against West Nile virus. Nature 2005, 437, 764-769.
37. Coller, B. A., Pai, V., Weeks-Levy, C., Ogata, S., Recombinant subunit West Nile virus vaccine for protection of human subjects. United States patent application No. US20120141520 A1 2012.
38. Magnusson, S. E., Matrix-M adjuvanted envelope protein vaccine protects against lethal lineage 1 and 2 West Nile virus infection in mice. Vaccine 2014, 32, 800.
39. Chu, J.-H. J., Chiang, C.-C. S., Ng, M.-L., Immunization of Flavivirus West Nile Recombinant Envelope Domain III Protein Induced Specific Immune Response and Protection against West Nile Virus Infection. J. Immunol. 2007, 178, 2699-2705.
40. Ohtaki, N., Takahashi, H., Kaneko, K., Gomi, Y. et al., Immunogenicity and efficacy of two types of West Nile virus-like particles different in size and maturation as a second-generation vaccine candidate. Vaccine 2010, 28, 6588-6596.
41. Qiao, M., Ashok, M., Bernard, K. A., Palacios, G. et al., Induction of sterilizing immunity against West Nile Virus (WNV), by immunization with WNV-like particles produced in insect cells. J. Infect Dis. 2004, 190, 2104-2108.
42. Merino-Ramos, T., Blázquez, A.-B., Escribano-Romero, E., Cañas-Arranz, R. et al., Protection of a Single Dose West Nile Virus Recombinant Subviral Particle Vaccine against Lineage 1 or 2 Strains and Analysis of the Cross-Reactivity with Usutu Virus. PLoS ONE 2014, 9, e108056.
43. Zohrabian, A., Hayes, E. B., Petersen, L. R., Cost-effectiveness of West Nile virus vaccination. Emerg. Infect. Dis. 2006, 12, 375-380.
44. Martina, B. E., Koraka, P., Osterhaus, A. D., West Nile Virus: is a vaccine needed? Curr. Opin. Investig. Drugs 2010, 11, 139-146.
45. Chen, Q., Expression and manufacture of pharmaceutical proteins in genetically engineered horticultural plants, in: Mou, B., Scorza, R. (Eds.), Transgenic Horticultural Crops: Challenges and Opportunities - Essays by Experts, Taylor & Francis Boca Raton 2011, pp. 83-124.
46. Chen, Q., Expression and Purification of Pharmaceutical Proteins in Plants. Biological Engineering 2008, 1, 291-321.
47. Chen, Q., Zhang, C., Santi, L., Plant-Made Biologics. Biomed. Res. Int. 2014, 2014, 3.
48. Tuse, D., Tu, T., McDonald, K., Manufacturing Economics of Plant-Made Biologics: Case Studies in Therapeutic and Industrial Enzymes. Biomed. Res. Int. 2014, 2014, 10.
49. Wang, Y., Deng, H., Zhang, X., Xiao, H. et al., Generation and immunogenicity of Japanese encephalitis virus envelope protein expressed in transgenic rice. Biochem. Biophys. Res. Commun. 2009, 380, 292-297.
50. Chen, Q., Mason, H., Mor, T., Cardineau, G. A. et al., Subunit vaccines produced using plant biotechnology, in: Levine, M. M. (Ed.), New Generation Vaccines, Informa Healthcare USA, Inc., New York 2009, pp. 306-315.
51. Lico, C., Chen, Q., Santi, L., Viral vectors for production of recombinant proteins in plants. J. Cell. Physiol. 2008, 216, 366-377.
52. Santi, L., Batchelor, L., Huang, Z., Hjelm, B. et al., An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles. Vaccine 2008, 26, 1846-1854.
53. Phoolcharoen, W., Bhoo, S. H., Lai, H., Ma, J. et al., Expression of an immunogenic Ebola immune complex in Nicotiana benthamiana. Plant Biotechnology Journal 2011, 9, 807-816.
54. Phoolcharoen, W., Dye, J. M., Kilbourne, J., Piensook, K. et al., A nonreplicating subunit vaccine protects mice against lethal Ebola virus challenge. Proc. Natl. Acad. Sci. USA 2011, 108, 20695-20700.
55. Lai, H., He, J., Engle, M., Diamond, M. S., Chen, Q., Robust production of virus-like particles and monoclonal antibodies with geminiviral replicon vectors in lettuce. Plant Biotechnology Journal 2012, 10, 95-104.
56. Huang, Z., Chen, Q., Hjelm, B., Arntzen, C., Mason, H., A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnol Bioeng 2009, 103, 706-714.
57. Huang, Z., Phoolcharoen, W., Lai, H., Piensook, K. et al., High-level rapid production of full-size monoclonal antibodies in plants by a single-vector DNA replicon system. Biotechnol. Bioeng. 2010, 106, 9-17.
58. Chen, Q., He, J., Phoolcharoen, W., Mason, H. S., Geminiviral vectors based on bean yellow dwarf virus for production of vaccine antigens and monoclonal antibodies in plants. Hum. Vaccin 2011, 7, 331-338.
59. He, J., Peng, L., Lai, H., Hurtado, J. et al., A Plant-Produced Antigen Elicits Potent Immune Responses against West Nile Virus in Mice. Biomed. Res. Int. 2014, 2014, 10.
60. He, J., Lai, H., Brock, C., Chen, Q., A Novel System for Rapid and Cost-Effective Production of Detection and Diagnostic Reagents of West Nile Virus in Plants. Journal of Biomedicine and Biotechnology 2012, 2012, 1-10.
61. Leuzinger, K., Dent, M., Hurtado, J., Stahnke, J. et al., Efficient Agroinfiltration of Plants for High-level Transient Expression of Recombinant Proteins. Journal of Visualized Experiments 2013, doi:10.3791/50521.
62. Chen, Q., Lai, H., Gene delivery into plant cells for recombinant protein production. Biomed. Res. Int. 2014, 2014, 10.
63. Saejung, W., Fujiyama, K., Takasaki, T., Ito, M. et al., Production of dengue 2 envelope domain III in plant using TMV-based vector system. Vaccine 2007, 25, 6646-6654.
64. Lai, H., Engle, M., Fuchs, A., Keller, T. et al., Monoclonal antibody produced in plants efficiently treats West Nile virus infection in mice. Proc. Natl. Acad. Sci. USA 2010, 107, 2419-2424.
65. He, J., Lai, H., Engle, M., Gorlatov, S. et al., Generation and Analysis of Novel Plant-Derived Antibody-Based Therapeutic Molecules against West Nile Virus. PLoS ONE 2014, 9, e93541 DOI:93510.91371/journal.pone.0093541.
66. Lai, H., He, J., Hurtado, J., Stahnke, J. et al., Structural and functional characterization of an anti-West Nile virus monoclonal antibody and its single-chain variant produced in glycoengineered plants. Plant Biotechnology Journal 2014, 12, 1098-1107.
67. Demento, S. L., Bonafe, N., Cui, W., Kaech, S. M. et al., TLR9-Targeted Biodegradable Nanoparticles as Immunization Vectors Protect against West Nile Encephalitis. The Journal of Immunology 2010, 185, 2989-2997.
68. Appaiahgari, M. B., Abdin, M. Z., Bansal, K. C., Vrati, S., Expression of Japanese encephalitis virus envelope protein in transgenic tobacco plants. J. Virol. Methods 2009, 162, 22-29.
69. Chen, Q., Lai, H., Plant-derived virus-like particles as vaccines. Human Vaccines & Immunotherapeutics 2013, 9, 26-49.
70. Davis, B. S., Chang, G. J., Cropp, B., Roehrig, J. T. et al., West Nile virus recombinant DNA vaccine protects mouse and horse from virus challenge and expresses in vitro a noninfectious recombinant antigen that can be used in enzyme-linked immunosorbent assays. J. Virol. 2001, 75, 4040-4047.
71. Roldao, A., Mellado, M. C., Castilho, L. R., Carrondo, M. J., Alves, P. M., Virus-like particles in vaccine development. Expert Rev Vaccines 2010, 9, 1149-1176.
72. Fehr, T., Skrastina, D., Pumpens, P., Zinkernagel, R. M., T cell-independent type I antibody response against B cell epitopes expressed repetitively on recombinant virus particles. Proc. Natl. Acad. Sci. USA 1998, 95, 9477-9481.
73. Faye, L., Gomord, V., Success stories in molecular farming - a brief overview. Plant Biotechnology Journal 2010, 8, 525-528.
74. Lai, H., Chen, Q., Bioprocessing of plant-derived virus-like particles of Norwalk virus capsid protein under current Good Manufacture Practice regulations. Plant Cell Reports 2012, 31, 573-584.
75. Landry, N., Ward, B. J., Trepanier, S., Montomoli, E. et al., Preclinical and clinical development of plant-made virus-like particle vaccine against avian H5N1 influenza. PLoS One 2010, 5, e15559.
76. Castilho, A., Steinkellner, H., Glyco-engineering in plants to produce human-like N-glycan structures. Biotechnology Journal 2012, 7, 1088-1098.
77. Chen, Q., Turning a new leaf. European Biopharm. Rev. 2011, 2, 64-68.
78. Check Hayden, E., Reardon, S., Should experimental drugs be used in the Ebola outbreak? Nature (London) 2014, http://dx.doi.org/10.1038/nature.2014.1569.
79. Martin, J. E., Pierson, T. C., Hubka, S., Rucker, S. et al., A West Nile virus DNA vaccine induces neutralizing antibody in healthy adults during a phase 1 clinical trial. J. Infect. Dis. 2007, 196, 1732-1740.