Plant-produced subunit vaccine candidates against yellow fever induce virus neutralizing antibodies and confer protection against viral challenge in animal models

American Journal of Tropical Medicine and Hygiene

Volumn 98, Issue 2, 2018, Pages 420-431

  Tottey, Stephen ^a   Shoji, Yoko ^a   Jones, R Mark ^a   Chichester, Jessica A ^a   Green, Brian J ^a   Musiychuk, Konstantin ^a   Si, Huaxin ^a   Manceva, Slobodanka D ^a   Rhee, Amy ^a   Shamloul, Moneim ^a   Norikane, Joey ^a   Guimarães, Rosane C ^b   Caride, Elena ^b   Silva, Andrea N M R ^b   Simões, Marisol ^b   Neves, Patricia C C ^b   Marchevsky, Renato ^b   Freire, Marcos S ^b   Streatfield, Stephen J ^a   Yusibov, Vidadi ^a  

^a Fraunhofer USA Inc   (United States)

^b Instituto de Technologia em Imunobiologicos   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; LICHENASE; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; YELLOW FEVER VACCINE; YELLOW FEVER VIRUS ENVELOPE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; IMMUNIZATION; IMMUNOGENICITY; INFECTION PREVENTION; MOUSE; NICOTIANA BENTHAMIANA; NONHUMAN; YELLOW FEVER; YELLOW FEVER VIRUS; ANIMAL; BIOSYNTHESIS; DISEASE MODEL; ENZYME LINKED IMMUNOSPOT ASSAY; HUMAN; IMMUNOLOGY; PROCEDURES; SERODIAGNOSIS;

ANIMALS; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSPOT ASSAY; HUMANS; MICE; NEUTRALIZATION TESTS; YELLOW FEVER; YELLOW FEVER VACCINE; YELLOW FEVER VIRUS;

EID: 85041516091     PISSN: 00029637     EISSN: None     Source Type: Journal    
DOI: 10.4269/ajtmh.16-0293     Document Type: Article

References (70)

1. WHO, 2016. Yellow Fever Fact Sheet. Updated May 2016. Available at: http://www.who.int/mediacentre/factsheets/fs100/en/. Accessed February 2017.
2. WHO, 2017. WHO Prequalified Vaccines. Available at: https:// extranet.who.int/gavi/PQ-Web/. Accessed February 2017.
3. Sanofi Pasteur, 2016. Yellow Fever Vaccine YF-VAX®. Available at: http://www.fda.gov/downloads/BiologicsBloodVaccines/ Vaccines/ApprovedProducts/UCM142831.pdf. Accessed February 2017.
4. Barrett ADT, 2016. Yellow fever in Angola and beyond-The problemof vaccine supply and demand. N Engl J Med 375: 301-303.
5. MartinsRMet al., 2013.17DDyellow fever vaccine: a double blind, randomized clinical trial of immunogenicity and safety on a dose-response study. Hum Vaccin Immunother 9: 879-888.
6. Camacho LA, 2008. Yellow fever and public health in Brazil. Cad Saude Publica 24: 482-483.
7. Campi-Azevedo AC et al., 2014. Subdoses of 17DD yellow fever vaccine elicit equivalent virological/immunological kinetics timeline. BMC Infect Dis 14: 391.
8. Martins RdeM et al., 2014. Adverse events following yellow fever immunization: report and analysis of 67 neurological cases in Brazil. Vaccine 32: 6676-6682.
9. Monath TP, 2012. Review of the risks and benefits of yellow fever vaccination including some new analyses. Expert Rev Vaccines 11: 427-448.
10. SeligmanSJ, 2014.Risk groups for yellowfever vaccine-associated viscerotropic disease (YEL-AVD). Vaccine 32: 5769-5775.
11. Gubler DJ, Kuno G, Markoff L, 2007. Flaviviruses. Knipe DM, HowleyPM, Griffin DE,LambRA, Martin MA, Roizman B, Straus SE, ed. Fields Virology. Philadelphia, PA: Lippincott Williams & Wilkins, 1153-1252.
12. Kaufmann B, Rossmann MG, 2011. Molecular mechanisms involved in the early steps of flavivirus cell entry. Microbes Infect 13: 1-9.
13. Smit JM, Moesker B, Rodenhuis-Zybert I, Wilschut J, 2011. Flavivirus cell entry and membrane fusion. Viruses 3: 160-171.
14. Stiasny K, Heinz FX, 2006. Flavivirus membrane fusion. J Gen Virol 87: 2755-2766.
15. StiasnyK, Fritz R, Pangerl K,Heinz FX, 2011.Molecularmechanisms of flavivirus membrane fusion. Amino Acids 41: 1159-1163.
16. Pierson TC, Diamond MS, 2008. Molecular mechanisms of antibody-mediated neutralisation of flavivirus infection. Expert Rev Mol Med 10: e12.
17. Pierson TC, Fremont DH, Kuhn RJ, Diamond MS, 2008. Structural insights into the mechanisms of antibody-mediated neutralization of flavivirus infection: implications for vaccine development. Cell Host Microbe 4: 229-238.
18. Desprès P, Cahour A, Wychowski C, Girard M, Bouloy M, 1988. Expression of the yellow fever virus envelope protein using hybrid SV40/yellow fever viruses. Ann Inst Pasteur Virol 139: 59-67.
19. Desprès P, Girard M, Bouloy M, 1991. Characterization of yellow fever virus proteins E and NS1 expressed in Vero and Spodoptera frugiperda cells. J Gen Virol 72: 1331-1342.
20. Ruiz-Linares A, Cahour A, Desprès P, Girard M, Bouloy M, 1989. Processing of yellow fever virus polyprotein: role of cellular proteases in maturation of the structural proteins. J Virol 63: 4199-4209.
21. Shiu SY, Morikawa S, Buckley A, Higgs S, Karunakarannair V, Blachere C, Gould EA, 1991. 17D yellow fever vaccine virus envelope protein expressed by recombinant baculovirus is antigenically indistinguishable from authentic viral protein. J Gen Virol 72: 1451-1454.
22. Barros MC, Galasso TG, Chaib AJ, Degallier N, Nagata T, Ribeiro BM, 2011. Yellow fever virus envelope protein expressed in insect cells is capable of syncytium formation in lepidopteran cells and could be used for immunodetection of YFV in human sera. Virol J 8: 261.
23. Mett V, Farrance CE, Green BJ, Yusibov V, 2008. Plants as biofactories. Biologicals 36: 354-358.
24. Rybicki EP, 2010. Plant-made vaccines for humans and animals. Plant Biotechnol J 8: 620-637.
25. Yusibov V, Streatfield SJ, Kushnir N, 2011. Clinical development of plant-produced recombinant pharmaceuticals: vaccines, antibodies and beyond. Hum Vaccin 7: 313-321.
26. Gomord V, Faye L, 2004. Posttranslational modification of therapeutic proteins in plants. Curr Opin Plant Biol 7: 171-181.
27. Bosch D, Castilho A, Loos A, Schots A, Steinkellner H, 2013. Nglycosylation of plant-produced recombinant proteins. Curr Pharm Des 19: 5503-5512.
28. Gomord V, Fitchette AC, Menu-Bouaouiche L, Saint-Jore-Dupas C, Plasson C, Michaud D, Faye L, 2010. Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol J 8: 564-587.
29. Webster DE, Thomas MC, 2012. Post-translational modification of plant-made foreign proteins; glycosylation and beyond. Biotechnol Adv 30: 410-418.
30. Mamedov T, Ghosh A, Jones RM, Mett V, Farrance CE, Musiychuk K, Horsey A, Yusibov V, 2012. Production of nonglycosylated recombinant proteins in Nicotiana benthamiana plants by co-expressing bacterial PNGase F. Plant Biotechnol J 10: 773-782.
31. Shaaltiel Y et al., 2007. Production of glucocerebrosidase with terminal mannose glycans for enzyme replacement therapy of Gaucher's disease using a plant cell system. Plant Biotechnol J 5: 579-590.
32. Traynor K, 2012. Taliglucerase alfa approved for Gaucher disease. Am J Health Syst Pharm 69: 1009.
33. Yusibov V, Streatfield SJ, Kushnir N, Roy G, Padmanaban A, 2013. Hybrid viral vectors for vaccine and antibody production in plants. Curr Pharm Des 19: 5574-5586.
34. Yusibov V, RabindranS, 2008. Recent progress in the development of plant derived vaccines. Expert Rev Vaccines 7: 1173-1183.
35. Musiychuk K et al., 2007. A launch vector for the production of vaccine antigens in plants. Influenza Other Respir Viruses 1: 19-25.
36. Shoji Y et al., 2011. Plant-based rapid production of recombinant subunit hemagglutinin vaccines targeting H1N1 and H5N1 influenza. Hum Vaccin 7 (Suppl): 41-50.
37. Chichester JA, Manceva SD, Rhee A, Coffin MV, Musiychuk K, Mett V, Shamloul M, Norikane J, Streatfield SJ, Yusibov V, 2013. A plant-produced protective antigen vaccine confers protection in rabbits against a lethal aerosolized challenge with Bacillus anthracis Ames spores. Hum Vaccin Immunother 9: 544-552.
38. Chichester JA, Musiychuk K, Farrance CE, Mett V, Lyons J, Yusibov V, 2009. A single component two-valent LcrV-F1 vaccine protects non-human primates against pneumonic plague. Vaccine 27: 3471-3474.
39. Mett V, Lyons J, Musiychuk K, Chichester JA, Brasil T, Couch R, Sherwood R, Palmer GA, Streatfield SJ, Yusibov V, 2007. A plant-produced plague vaccine candidate confers protection to monkeys. Vaccine 25: 3014-3017.
40. Farrance CE et al., 2011. Antibodies to plant-produced Plasmodium falciparum sexual stage protein Pfs25 exhibit transmission blocking activity. Hum Vaccin 7 (Suppl): 191-198.
41. Jones RM et al., 2015. A novel plant-produced Pfs25 fusion subunit vaccine induces long-lasting transmission blocking antibody responses. Hum Vaccin Immunother 11: 124-132.
42. Knapp EGL et al., 2010. Tubulin-based vaccine candidates to combat African animal trypanosomiasis.AmJ TropMedHyg 83 (Suppl): 206 (American Society of Tropical Medicine and Hygene 59th Annual Meeting. Abstract 691).
43. Chichester JA, JonesRM,GreenBJ,StowM,Miao F,Moonsammy G, StreatfieldSJ, Yusibov V, 2012. Safety and immunogenicity of a plant-produced recombinant hemagglutinin-based influenza vaccine (HAI-05) derived from A/Indonesia/05/2005 (H5N1) influenza virus: a phase 1 randomized, double-blind, placebocontrolled, dose-escalation study in healthy adults. Viruses 4: 3227-3244.
44. Cummings JF, Guerrero ML, Moon JE, Waterman P, Nielsen RK, Jefferson S, Gross FL, Hancock K, Katz JM, Yusibov V, 2014. Safety and immunogenicity of a plant-produced recombinant monomer hemagglutinin-based influenza vaccine derived from influenza A (H1N1)pdm09 virus: a Phase 1 dose-escalation study in healthy adults. Vaccine 32: 2251-2259.
45. Chichester JA, Musiychuk K, de la Rosa P, Horsey A, Stevenson N, Ugulava N, Rabindran S, Palmer GA, Mett V, Yusibov V, 2007. Immunogenicity of a subunit vaccine against Bacillus anthracis. Vaccine 25: 3111-3114.
46. Mett V et al., 2008. A plant-produced influenza subunit vaccine protects ferrets against virus challenge. Influenza Other Respir Viruses 2: 33-40.
47. Shoji Y et al., 2009. Plant-derived hemagglutinin protects ferrets against challenge infection with the A/Indonesia/05/05 strain of avian influenza. Vaccine 27: 1087-1092.
48. Shoji Y et al., 2008. Plant-expressed HA as a seasonal influenza vaccine candidate. Vaccine 26: 2930-2934.
49. Shoji Y et al., 2009. Immunogenicity of hemagglutinin from A/Barheaded Goose/Qinghai/1A/05 and A/Anhui/1/05 strains of H5N1 influenza viruses produced in Nicotiana benthamiana plants. Vaccine 27: 3467-3470.
50. Shamloul M, Trusa J, Mett V, Yusibov V, 2014. Optimization and utilization of Agrobacterium-mediated transient protein production in Nicotiana. J Vis Exp 86: e51204.
51. Pace CN, Vajdos F, Fee L, Grimsley G, Gray T, 1995. How to measure and predict the molar absorption coefficient of a protein. Protein Sci 4: 2411-2423.
52. Niedrig M, Lademann M, Emmerich P, Lafrenz M, 1999. Assessment of IgG antibodies against yellow fever virus after vaccination with 17D by different assays: neutralization test, haemagglutination inhibition test, immunofluorescence assay and ELISA. Trop Med Int Health 4: 867-871.
53. Simoes M, Camacho LA, Yamamura AM, Miranda EH, Cajaraville AC, da Silva Freire M, 2012. Evaluation of accuracy and reliability of the plaque reduction neutralization test (micro-PRNT) in detection of yellow fever virus antibodies. Biologicals 40: 399-404.
54. Caufour PS, Motta MC, Yamamura AM, Vazquez S, Ferreira II, Jabor AV, Bonaldo MC, Freire MS, Galler R, 2001. Construction, characterization and immunogenicity of recombinant yellow fever 17D-dengue type 2 viruses. Virus Res 79: 1-14.
55. Trindade GF, Marchevsky RS, Fillipis AM, Nogueira RM, Bonaldo MC, Acero PC, Caride E, Freire MS, Galler R, 2008. Limited replication of yellow fever 17DD and 17D-dengue recombinant viruses in rhesus monkeys. An Acad Bras Cienc 80: 311-321.
56. Matos DC, Silva AM, Neves PC, Martins RM, Homma A, Marcovistz R, 2009. Pattern of functional antibody activity against Haemophilus influenzae type B (Hib) in infants immunized with diphtheria-tetanus-pertussis/Hib Brazilian combination vaccine. Braz J Med Biol Res 42: 1242-1247.
57. Santos AP, Matos DC, Bertho AL, Mendonca SC, Marcovistz R, 2008. Detection of Th1/Th2 cytokine signatures in yellow fever 17DD first-time vaccinees through ELISpot assay. Cytokine 42: 152-155.
58. Dowd KA, Pierson TC, 2011. Antibody-mediated neutralization of flaviviruses: a reductionist view. Virology 411: 306-315.
59. Monath TP et al., 2010. Inactivated yellow fever 17D vaccine: development and nonclinical safety, immunogenicity and protective activity. Vaccine 28: 3827-3840.
60. Liu T, Matsuguchi T, Tsuboi N, Yajima T, Yoshikai Y, 2002. Differences in expression of toll-like receptors and their reactivities in dendritic cells in BALB/c and C57BL/6 mice. InfectImmun70: 6638-6645.
61. Schulte S, Sukhova GK, Libby P, 2008. Genetically programmed biases in Th1 and Th2 immune responses modulate atherogenesis. Am J Pathol 172: 1500-1508.
62. Stiasny K, Aberle JH, Keller M, Grubeck-Loebenstein B, Heinz FX, 2012. Age affects quantity but not quality of antibody responses after vaccination with an inactivated flavivirus vaccine against tick-borne encephalitis. PLoS One 7: e34145.
63. Puschnik A, Lau L, Cromwell EA, Balmaseda A, Zompi S, Harris E, 2013. Correlation between dengue-specific neutralizing antibodies and serum avidity in primary and secondary dengue virus 3 natural infections in humans. PLoS Negl Trop Dis 7: e2274.
64. Barba-Spaeth G, Longman RS, Albert ML, Rice CM, 2005. Live attenuated yellow fever 17D infects human DCs and allows for presentation of endogenous and recombinant T cell epitopes. J Exp Med 202: 1179-1184.
65. Luiza-Silva M et al., 2011. Cytokine signatures of innate and adaptive immunity in 17DD yellow fever vaccinated children and its association with the level of neutralizing antibody. J Infect Dis 204: 873-883.
66. Querec T, Bennouna S, Alkan S, Laouar Y, Gorden K, Flavell R, Akira S, Ahmed R, Pulendran B, 2006. Yellow fever vaccine YF-17D activates multiple dendritic cell subsets via TLR2, 7, 8, and 9 to stimulate polyvalent immunity. J Exp Med 203: 413-424.
67. Kohler S, Bethke N, Bothe M, Sommerick S, Frentsch M, Romagnani C, Niedrig M, Thiel A, 2012. The early cellular signatures of protective immunity induced by live viral vaccination. Eur J Immunol 42: 2363-2373.
68. Neves PC, Rudersdorf RA, Galler R, BonaldoMC,de SantanaMG, Mudd PA, Martins MA, Rakasz EG, Wilson NA, Watkins DI, 2010. CD8+ gamma-delta TCR+ and CD4+ T cells produce IFNgamma at 5-7 days after yellow fever vaccination in Indian rhesus macaques, before the induction of classical antigenspecific T cell responses. Vaccine 28: 8183-8188.
69. Neves PC, Santos JR, Tubarao LN, Bonaldo MC, Galler R, 2013. Early IFN-gamma production after YF 17D vaccine virus immunization in mice and its association with adaptive immune responses. PLoS One 8: e81953.
70. Liu T, Chambers TJ, 2001. Yellow fever virus encephalitis: properties of the brain-associated T-cell response during virus clearance in normal and gamma interferon-deficient mice and requirement for CD4+ lymphocytes. J Virol 75: 2107-2118.