- Introduction
- Materials and Methods
- Results
- Evaluation of DENV-4 E gene expression in P. pastoris.
- Purification and characterization of recombinant DENV-4 E protein.
- DENV-4 E VLPs have conformational display of critical epitopes on its surface.
- DENV-4 E VLPs are immunogenic in mice and elicit EDIII-focused serotype-specific neutralizing antibody response.
- Discussion
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
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Swaminathan S, Khanna N, Herring B, Mahalingam S, 2013. Dengue vaccine efficacy trial: does interference cause failure? Lancet Infect Dis 13: 191–192.
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Chackerian B, 2007. Virus-like particles: flexible platforms for vaccine development. Expert Rev Vaccines 6: 381–390.
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Tang YX, Jiang LF, Zhou JM, Yin Y, Yang XM, Liu WQ, Fang DY, 2012. Induction of virus-neutralizing antibodies and T cell responses by dengue virus type 1 virus-like particles prepared from Pichia pastoris. Chin Med J (Engl) 125: 1986–1992.
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Akahata W, Yang ZY, Andersen H, Sun S, Holdaway HA, Kong WP, Lewis MG, Higgs S, Rossmann MG, Rao S, Nabel GJ, 2010. A virus-like particle vaccine for epidemic Chikungunya virus protects nonhuman primates against infection. Nat Med 16: 334–338.
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Recombinant Dengue Virus 4 Envelope Glycoprotein Virus-Like Particles Derived from Pichia pastoris are Capable of Eliciting Homotypic Domain III-Directed Neutralizing Antibodies
Niyati Khetarpal
Niyati Khetarpal
Recombinant Gene Products Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India.
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Rahul Shukla
Rahul Shukla
Recombinant Gene Products Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India.
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Ravi Kant Rajpoot
Ravi Kant Rajpoot
Recombinant Gene Products Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India.
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Ankur Poddar
Ankur Poddar
Recombinant Gene Products Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India.
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Meena Pal
Meena Pal
Recombinant Gene Products Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India.
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Sathyamangalam Swaminathan
Sathyamangalam Swaminathan
Department of Biological Sciences, Birla Institute of Technology and Sciences, Hyderabad, India.
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Upasana Arora
Upasana Arora
Recombinant Gene Products Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India.
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Navin Khanna
Navin Khanna
Recombinant Gene Products Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India.
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Dengue is a viral pandemic caused by four dengue virus serotypes (DENV-1, 2, 3, and 4) transmitted by Aedes mosquitoes. Reportedly, there has been a 2-fold increase in dengue cases every decade. An efficacious tetravalent vaccine, which can provide long-term immunity against all four serotypes in all target populations, is still unavailable. Despite the progress being made in the live virus-based dengue vaccines, the World Health Organization strongly recommends the development of alternative approaches for safe, affordable, and efficacious dengue vaccine candidates. We have explored virus-like particles (VLPs)-based nonreplicating subunit vaccine approach and have developed recombinant envelope ectodomains of DENV-1, 2, and 3 expressed in Pichia pastoris. These self-assembled into VLPs without pre-membrane (prM) protein, which limits the generation of enhancing antibodies, and elicited type-specific neutralizing antibodies against the respective serotype. Encouraged by these results, we have extended this work further by developing P. pastoris–expressed DENV-4 ectodomain (DENV-4 E) in this study, which was found to be glycosylated and assembled into spherical VLPs without prM, and displayed critical neutralizing epitopes on its surface. These VLPs were found to be immunogenic in mice and elicited DENV-4-specific neutralizing antibodies, which were predominantly directed against envelope domain III, implicated in host-receptor recognition and virus entry. These observations underscore the potential of VLP-based nonreplicative vaccine approach as a means to develop a safe, efficacious, and tetravalent dengue subunit vaccine. This work paves the way for the evaluation of a DENV E-based tetravalent dengue vaccine candidate, as an alternative to live virus-based dengue vaccines.
Author Notes
Financial support: The funding for this work was received from Department of Biotechnology, Government of India (Grant no. BT/PR11807/MED/29/871/2014) to Navin Khanna.
Authors' addresses: Niyati Khetarpal, Rahul Shukla, Ravi Kant Rajpoot, Ankur Poddar, Meena Pal, Upasana Arora, and Navin Khanna, Recombinant Gene Products Group, International Centre for Genetic Engineering and Biotechnology, New Delhi, India, E-mails: 27.niyati@gmail.com, rahulshukla.2802@gmail.com, rajpootravikant@gmail.com, ankurgemini29@gmail.com, maina2u@gmail.com, upasanaaro@gmail.com, and navinkhanna5@gmail.com. Sathyamangalam Swaminathan, Department of Biological Sciences, Birla Institute of Technology and Sciences, Hyderabad, India, E-mail: ssn225@gmail.com.
- Introduction
- Materials and Methods
- Results
- Evaluation of DENV-4 E gene expression in P. pastoris.
- Purification and characterization of recombinant DENV-4 E protein.
- DENV-4 E VLPs have conformational display of critical epitopes on its surface.
- DENV-4 E VLPs are immunogenic in mice and elicit EDIII-focused serotype-specific neutralizing antibody response.
- Discussion
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, Myers MF, George DB, Jaenisch T, Wint GR, Simmons CP, Scott TW, Farrar JJ, Hay SI, 2013. The global distribution and burden of dengue. Nature 496: 504–507.
-
2.
Stanaway JD, Shepard DS, Undurraga EA, Halasa YA, Coffeng LE, Brady OJ, Hay SI, Bedi N, Bensenor IM, Castaneda-Orjuela CA, Chuang TW, Gibney KB, Memish ZA, Rafay A, Ukwaja KN, Yonemoto N, Murray CJ, 2016. The global burden of dengue: an analysis from the Global Burden of Disease Study 2013. Lancet Infect Dis 16: 712–723.
-
3.
Gubler DJ, Kuno G, Markoff L, 2007. Flaviviruses. Knipe DM, Howley PM, eds. Fields Virology, 5th edition. Philadelphia, PA: Wolters Kluwer and Lippincott Williams and Wilkins, 1153–1252.
-
4.
Swaminathan S, Khanna N, 2009. Dengue: recent advances in biology and current status of translational research. Curr Mol Med 9: 152–173.
-
5.
WHO, 2016. Fact Sheet on Dengue and Severe Dengue. Available at: http://www.who.int/mediacentre/factsheets/fs117/en/. Accessed June 20, 2016.
-
6.
Halstead SB, 2014. Dengue antibody-dependent enhancement: knowns and unknowns. Microbiol Spectr 2. doi:10.1128/microbiolspec.AID-0022-2014.
-
7.
Swaminathan S, Batra G, Khanna N, 2010. Dengue vaccines: state of the art. Expert Opin Ther Pat 20: 819–835.
-
8.
Schmitz J, Roehrig J, Barrett A, Hombach J, 2011. Next generation dengue vaccines: a review of candidates in preclinical development. Vaccine 29: 7276–7284.
-
9.
Coller BA, Clements DE, 2011. Dengue vaccines: progress and challenges. Curr Opin Immunol 23: 391–398.
-
10.
Thomas SJ, Endy TP, 2011. Vaccines for the prevention of dengue: development update. Hum Vaccin 7: 674–684.
-
11.
Guy B, Briand O, Lang J, Saville M, Jackson N, 2015. Development of the Sanofi Pasteur tetravalent dengue vaccine: one more step forward. Vaccine 33: 7100–7111.
-
12.
Hadinegoro SR, Arredondo-Garcia JL, Capeding MR, Deseda C, Chotpitayasunondh T, Dietze R, Muhammad Ismail HI, Reynales H, Limkittikul K, Rivera-Medina DM, Tran HN, Bouckenooghe A, Chansinghakul D, Cortes M, Fanouillere K, Forrat R, Frago C, Gailhardou S, Jackson N, Noriega F, Plennevaux E, Wartel TA, Zambrano B, Saville M; CYD-TDV Dengue Vaccine Working Group, 2015. Efficacy and long-term safety of a dengue vaccine in regions of endemic disease. N Engl J Med 373: 1195–1206.
-
13.
Halstead SB, Russell PK, 2016. Protective and immunological behavior of chimeric yellow fever dengue vaccine. Vaccine 34: 1643–1647.
-
14.
Edelman R, 2011. Unique challenges faced by the clinical evaluation of dengue vaccines. Expert Rev Vaccines 10: 133–136.
-
15.
Thomas SJ, 2011. The necessity and quandaries of dengue vaccine development. J Infect Dis 203: 299–303.
-
16.
Swaminathan S, Khanna N, Herring B, Mahalingam S, 2013. Dengue vaccine efficacy trial: does interference cause failure? Lancet Infect Dis 13: 191–192.
-
17.
Chackerian B, 2007. Virus-like particles: flexible platforms for vaccine development. Expert Rev Vaccines 6: 381–390.
-
18.
Wang PG, Kudelko M, Lo J, Siu LY, Kwok KT, Sachse M, Nicholls JM, Bruzzone R, Altmeyer RM, Nal B, 2009. Efficient assembly and secretion of recombinant subviral particles of the four dengue serotypes using native prM and E proteins. PLoS One 4: e8325.
-
19.
Liu W, Jiang H, Zhou J, Yang X, Tang Y, Fang D, Jiang L, 2010. Recombinant dengue virus-like particles from Pichia pastoris: efficient production and immunological properties. Virus Genes 40: 53–59.
-
20.
Kuwahara M, Konishi E, 2010. Evaluation of extracellular subviral particles of dengue virus type 2 and Japanese encephalitis virus produced by Spodoptera frugiperda cells for use as vaccine and diagnostic antigens. Clin Vaccine Immunol 17: 1560–1566.
-
21.
Tang YX, Jiang LF, Zhou JM, Yin Y, Yang XM, Liu WQ, Fang DY, 2012. Induction of virus-neutralizing antibodies and T cell responses by dengue virus type 1 virus-like particles prepared from Pichia pastoris. Chin Med J (Engl) 125: 1986–1992.
-
22.
Bachmann MF, Jennings GT, 2010. Vaccine delivery: a matter of size, geometry, kinetics and molecular patterns. Nat Rev Immunol 10: 787–796.
-
23.
Yildiz I, Shukla S, Steinmetz NF, 2011. Applications of viral nanoparticles in medicine. Curr Opin Biotechnol 22: 901–908.
-
24.
Perrone LA, Ahmad A, Veguilla V, Lu X, Smith G, Katz JM, Pushko P, Tumpey TM, 2009. Intranasal vaccination with 1918 influenza virus-like particles protects mice and ferrets from lethal 1918 and H5N1 influenza virus challenge. J Virol 83: 5726–5734.
-
25.
Akahata W, Yang ZY, Andersen H, Sun S, Holdaway HA, Kong WP, Lewis MG, Higgs S, Rossmann MG, Rao S, Nabel GJ, 2010. A virus-like particle vaccine for epidemic Chikungunya virus protects nonhuman primates against infection. Nat Med 16: 334–338.
-
26.
Lindenbach BD, Thiel HJ, Rice CM, 2007. Flaviviridae: The viruses and their replication. Knipe DM, Howley PM, eds. Fields Virology, 5th edition. Philadelphia, PA: Wolters Kluwer and Lippincott Williams and Wilkins, 1101–1152.
-
27.
Gromowski GD, Barrett AD, 2007. Characterization of an antigenic site that contains a dominant, type-specific neutralization determinant on the envelope protein domain III (ED3) of dengue 2 virus. Virology 366: 349–360.
-
28.
Shrestha B, Brien JD, Sukupolvi-Petty S, Austin SK, Edeling MA, Kim T, O'Brien KM, Nelson CA, Johnson S, Fremont DH, Diamond MS, 2010. The development of therapeutic antibodies that neutralize homologous and heterologous genotypes of dengue virus type 1. PLoS Pathog 6: e1000823.
-
29.
Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S, Limpitikul W, Puttikhunt C, Edwards C, Duangchinda T, Supasa S, Chawansuntati K, Malasit P, Mongkolsapaya J, Screaton G, 2010. Cross-reacting antibodies enhance dengue virus infection in humans. Science 328: 745–748.
-
30.
Rodenhuis-Zybert IA, van der Schaar HM, da Silva Voorham JM, van der Ende-Metselaar H, Lei HY, Wilschut J, Smit JM, 2010. Immature dengue virus: a veiled pathogen? PLoS Pathog 6: e1000718.
-
31.
Mani S, Tripathi L, Raut R, Tyagi P, Arora U, Barman T, Sood R, Galav A, Wahala W, de Silva A, Swaminathan S, Khanna N, 2013. Pichia pastoris-expressed dengue 2 envelope forms virus-like particles without pre-membrane protein and induces high titer neutralizing antibodies. PLoS One 8: e64595.
-
32.
Poddar A, Ramasamy V, Shukla R, Rajpoot RK, Arora U, Jain SK, Swaminathan S, Khanna N, 2016. Virus-like particles derived from Pichia pastoris-expressed dengue virus type 1 glycoprotein elicit homotypic virus-neutralizing envelope domain III-directed antibodies. BMC Biotechnol 16: 50.
-
33.
Tripathi L, Mani S, Raut R, Poddar A, Tyagi P, Arora U, de Silva A, Swaminathan S, Khanna N, 2015. Pichia pastoris-expressed dengue 3 envelope-based virus-like particles elicit predominantly domain III-focused high titer neutralizing antibodies. Front Microbiol 6: 1005.
-
34.
Macauley-Patrick S, Fazenda ML, McNeil B, Harvey LM, 2005. Heterologous protein production using the Pichia pastoris expression system. Yeast 22: 249–270.
-
35.
Kraus AA, Messer W, Haymore LB, de Silva AM, 2007. Comparison of plaque- and flow cytometry-based methods for measuring dengue virus neutralization. J Clin Microbiol 45: 3777–3780.
-
36.
Henchal EA, Gentry MK, McCown JM, Brandt WE, 1982. Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am J Trop Med Hyg 31: 830–836.
-
37.
Brien JD, Austin SK, Sukupolvi-Petty S, O'Brien KM, Johnson S, Fremont DH, Diamond MS, 2010. Genotype-specific neutralization and protection by antibodies against dengue virus type 3. J Virol 84: 10630–10643.
-
38.
Sukupolvi-Petty S, Austin SK, Engle M, Brien JD, Dowd KA, Williams KL, Johnson S, Rico-Hesse R, Harris E, Pierson TC, Fremont DH, Diamond MS, 2010. Structure and function analysis of therapeutic monoclonal antibodies against dengue virus type 2. J Virol 84: 9227–9239.
-
39.
Sukupolvi-Petty S, Brien JD, Austin SK, Shrestha B, Swayne S, Kahle K, Doranz BJ, Johnson S, Pierson TC, Fremont DH, Diamond MS, 2013. Functional analysis of antibodies against dengue virus type 4 reveals strain-dependent epitope exposure that impacts neutralization and protection. J Virol 87: 8826–8842.
-
40.
Wahala WM, Donaldson EF, de Alwis R, Accavitti-Loper MA, Baric RS, de Silva AM, 2010. Natural strain variation and antibody neutralization of dengue serotype 3 viruses. PLoS Pathog 6: e1000821.
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