1,326
Views
97
CrossRef citations to date
0
Altmetric
Review

Insect cell technology is a versatile and robust vaccine manufacturing platform

&
Pages 1063-1081 | Published online: 09 Jan 2014

References

  • Smith GE, Fraser MJ, Summers MD. Molecular engineering of the Autographa californica nuclear polyhedrosis virus genome: deletion mutations within the polyhedrin gene. J. Virol.46(2), 584–593 (1983).
  • Jarvis DL. Baculovirus-insect cell expression systems. Methods Enzymol.463, 191–222 (2009).
  • Chung Y-C, Ho M-S, Wu J-C et al. Immunization with virus-like particles of enterovirus 71 elicits potent immune responses and protects mice against lethal challenge. Vaccine26(15), 1855–1862 (2008).
  • Hofmann C, Sandig V, Jennings G, Rudolph M, Schlag P, Strauss M. Efficient gene transfer into human hepatocytes by baculovirus vectors. Proc. Natl Acad. Sci. USA92(22), 10099–10103 (1995).
  • Haynes JR. Influenza virus-like particle vaccines. Expert Rev. Vaccines8(4), 435–445 (2009).
  • van Oers MM. Vaccines for viral and parasitic diseases produced with baculovirus vectors. Adv. Virus Res.68, 193–253 (2006).
  • Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc. Natl Acad. Sci. USA89(24), 12180–12184 (1992).
  • Wickham TJ, Davis T, Granados RR, Shuler ML, Wood HA. Screening of insect cell lines for the production of recombinant proteins and infectious virus in the baculovirus expression system. Biotechnol. Prog.8(5), 391–396 (1992).
  • Maranga L, Brazao TF, Carrondo MJT. Virus-like particle production at low multiplicities of infection with the baculovirus insect cell system. Biotechnol. Bioeng.84(2), 245–253 (2003).
  • Mena JA, Aucoin MG, Montes J, Chahal PS, Kamen AA. Improving adeno-associated vector yield in high density insect cell cultures. J. Gene Med.12(2), 157–167 (2010).
  • Mena JA, Ramírez OT, Palomares LA. Population kinetics during simultaneous infection of insect cells with two different recombinant baculoviruses for the production of rotavirus-like particles. BMC Biotechnol.7, 39 (2007).
  • Roldão A, Vieira HLA, Alves PM, Oliveira R, Carrondo MJT. Intracellular dynamics in rotavirus-like particles production: evaluation of multigene and monocistronic infection strategies. Process Biochem.41(10), 2188–2199 (2006).
  • Maranga L, Rueda P, Antonis A et al. Large scale production and downstream processing of a recombinant porcine parvovirus vaccine. Appl. Microbiol. Biotechnol.59(1), 45–50 (2002).
  • de Boer M, Conroy L, Min HY, Kwekkeboom J. Generation of monoclonal antibodies to human lymphocyte cell surface antigens using insect cells expressing recombinant proteins. J. Immunol. Methods152(1), 15–23 (1992).
  • Licari P, Bailey JE. Modeling the population dynamics of baculovirus-infected insect cells: optimizing infection strategies for enhanced recombinant protein yields. Biotechnol. Bioeng.39(4), 432–441 (1992).
  • Yang DG, Chung YC, Lai YK, Lai CW, Liu HJ, Hu YC. Avian influenza virus hemagglutinin display on baculovirus envelope: cytoplasmic domain affects virus properties and vaccine potential. Mol. Ther.15(5), 989–996 (2007).
  • Meghrous J, Mahmoud W, Jacob D, Chubet R, Cox M, Kamen AA. Development of a simple and high-yielding fed-batch process for the production of influenza vaccines. Vaccine28(2), 309–316 (2009).
  • Redfield RR, Birx DL, Ketter N et al. A Phase I evaluation of the safety and immunogenicity of vaccination with recombinant gp160 in patients with early human immunodeficiency virus infection. N. Engl. J. Med.324(24), 1677–1684 (1991).
  • Ludvigsson J, Faresjö M, Hjorth M et al. GAD treatment and insulin secretion in recent-onset Type 1 diabetes. N. Engl. J. Med.359(18), 1909–1920 (2008).
  • King JC Jr, Cox MM, Reisinger K, Hedrick J, Graham I, Patriarca P. Evaluation of the safety, reactogenicity and immunogenicity of FluBlok® trivalent recombinant baculovirus-expressed hemagglutinin influenza vaccine administered intramuscularly to healthy children aged 6–59 months. Vaccine27(47), 6589–6594 (2009).
  • Keitel WA, Treanor JJ, El Sahly HM et al. Comparative immunogenicity of recombinant influenza hemagglutinin (rHA) and trivalent inactivated vaccine (TIV) among persons ≥65 years old. Vaccine28(2), 379–385 (2009).
  • Cox MMJ, Hollister JR. FluBlok, a next generation influenza vaccine manufactured in insect cells. Biologicals37(3), 182–189 (2009).
  • Agardh CD, Lynch KF, Palmér M, Link K, Lernmark Å. GAD65 vaccination: 5 years of follow-up in a randomised dose-escalating study in adult-onset autoimmune diabetes. Diabetologia52(7), 1363–1368 (2009).
  • Mauch L, Seissler J, Haubruck H et al. Baculovirus-mediated expression of human 65 kDa and 67 kDa glutamic acid decarboxylases in SF9 insect cells and their relevance in diagnosis of insulin-dependent diabetes mellitus. J. Biochem.113(6), 699–704 (1993).
  • Burch PA, Croghan GA, Gastineau DA et al. Immunotherapy (APC8015, provenge®) targeting prostatic acid phosphatase can induce durable remission of metastatic androgen-independent prostate cancer: a Phase 2 trial. Prostate60(3), 197–204 (2004).
  • Kantoff PW, Higano CS, Shore ND et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. N. Engl. J. Med.363(5), 411–422 (2010).
  • Small EJ, Schellhammer PF, Higano CS et al. Placebo-controlled Phase III trial of immunologic therapy with Sipuleucel-T (APC8015) in patients with metastatic, asymptomatic hormone refractory prostate cancer. J. Clin. Oncol.24(19), 3089–3094 (2006).
  • Robinson RA, Burgess WH, Emerson SU et al. Structural characterization of recombinant hepatitis E virus ORF2 proteins in baculovirus-infected insect cells. Protein Expr. Purif.12(1), 75–84 (1998).
  • Purcell RH, Nguyen H, Shapiro M et al. Pre-clinical immunogenicity and efficacy trial of a recombinant hepatitis E vaccine. Vaccine21(19–20), 2607–2615 (2003).
  • Shrestha MP, Scott RM, Joshi DM et al. Safety and efficacy of a recombinant hepatitis E vaccine. N. Engl. J. Med.356(9), 895–903 (2007).
  • Treanor JJ, Wilkinson BE, Masseoud F et al. Safety and immunogenicity of a recombinant hemagglutinin vaccine for H5 influenza in humans. Vaccine19(13–14), 1732–1737 (2001).
  • Wei CJ, Xu L, Kong WP et al. Comparative efficacy of neutralizing antibodies elicited by recombinant hemagglutinin proteins from avian H5N1 influenza virus. J. Virol.82(13), 6200–6208 (2008).
  • Bisht H, Roberts A, Vogel L, Subbarao K, Moss B. Neutralizing antibody and protective immunity to SARS coronavirus infection of mice induced by a soluble recombinant polypeptide containing an N-terminal segment of the spike glycoprotein. Virology334(2), 160–165 (2005).
  • He Y, Li J, Heck S, Lustigman S, Jiang S. Antigenic and immunogenic characterization of recombinant baculovirus-expressed severe acute respiratory syndrome coronavirus spike protein: implication for vaccine design. J. Virol.80(12), 5757–5767 (2006).
  • Zhou Z, Post P, Chubet R et al. A recombinant baculovirus-expressed S glycoprotein vaccine elicits high titers of SARS-associated coronavirus (SARS-CoV) neutralizing antibodies in mice. Vaccine24(17), 3624–3631 (2006).
  • Johansson BE, Brett IC. Recombinant influenza B virus HA and NA antigens administered in equivalent amounts are immunogenically equivalent and induce equivalent homotypic and broader heterovariant protection in mice than conventional and live influenza vaccines. Hum. Vaccin.4(6), 420–424 (2008).
  • Bonafé N, Rininger JA, Chubet RG et al. A recombinant West Nile virus envelope protein vaccine candidate produced in Spodoptera frugiperda expresSF+ cells. Vaccine27(2), 213–222 (2009).
  • Arefian E, Bamdad T, Soleimanjahi H, Akhoond MR, Parsania M, Ghaemi A. A kinetic study of gamma interferon production in herpes simplex virus-1 DNA prime-protein boost regimen comparing to DNA or subunit vaccination. Mol. Biol.43(3), 388–393 (2009).
  • Fotouhi F, Soleimanjahi H, Roostaee MH, Behzadian F. Enhancement of protective humoral immune responses against Herpes simplex virus-2 in DNA-immunized guinea-pigs using protein boosting. FEMS Immunol. Med. Microbiol.54(1), 18–26 (2008).
  • Kimura H, Straus SE, Williams RK. Varicella-zoster virus glycoproteins E and I expressed in insect cells form a heterodimer that requires the N-terminal domain of glycoprotein I. Virology233(2), 382–391 (1997).
  • Arnot DE, Cavanagh DR, Remarque EJ et al. Comparative testing of six antigen-based malaria vaccine candidates directed toward merozoite-stage Plasmodium falciparum. Clin. Vaccine Immunol.15(9), 1345–1355 (2008).
  • Collins WE, Galland GG, Barnwell JW et al. Preliminary observations on the efficacy of a recombinant multistage Plasmodium falciparum vaccine in Aotus nancymai monkeys. Am. J. Trop. Med. Hyg.73(4), 686–693 (2005).
  • Lyon JA, Angov E, Fay MP et al. Protection induced by Plasmodium falciparum MSP142 is strain-specific, antigen and adjuvant dependent, and correlates with antibody responses. PLoS ONE3(7), e2830 (2008).
  • Ahrens U, Kaden V, Drexler C, Visser N. Efficacy of the classical swine fever (CSF) marker vaccine Porcilis® Pesti in pregnant sows. Vet. Microbiol.77(1–2), 83–97 (2000).
  • Depner KR, Bouma A, Koenen F et al. Classical swine fever (CSF) marker vaccine: trial II. Challenge study in pregnant sows. Vet. Microbiol.83(2), 107–120 (2001).
  • Dong XN, Chen YH. Marker vaccine strategies and candidate CSFV marker vaccines. Vaccine25(2), 205–230 (2007).
  • Lipowski A, Drexler C, Pejsak Z. Safety and efficacy of a classical swine fever subunit vaccine in pregnant sows and their offspring. Vet. Microbiol.77(1–2), 99–108 (2000).
  • Wu CM, Hsuan SL, Chen ZW et al. Expression and immunological studies of classical swine fever virus glycoprotein E2 in the bi-cistronic baculovirus/larvae expression system. Biosci. Biotechnol. Biochem.74(7), 1343–1349 (2010).
  • Fachinger V, Bischoff R, Jedidia SB, Saalmüller A, Elbers K. The effect of vaccination against porcine circovirus type 2 in pigs suffering from porcine respiratory disease complex. Vaccine26(11), 1488–1499 (2008).
  • Gonzalez DD, Mozgovoj MV, Bellido D et al. Evaluation of a bovine rotavirus VP6 vaccine efficacy in the calf model of infection and disease. Vet. Immunol. Immunopathol.137(1–2), 155–160 (2010).
  • Thomas C, Young NJ, Heaney J, Collins ME, Brownlie J. Evaluation of efficacy of mammalian and baculovirus expressed E2 subunit vaccine candidates to bovine viral diarrhoea virus. Vaccine27(17), 2387–2393 (2009).
  • Lee YJ, Sung HW, Choi JG et al. Protection of chickens from Newcastle disease with a recombinant baculovirus subunit vaccine expressing the fusion and hemagglutinin- neuraminidase proteins. J. Vet. Sci.9(3), 301–308 (2008).
  • Yang DK, Kweon CH, Kim BH et al. Immunogenicity of baculovirus expressed recombinant proteins of Japanese encephalitis virus in mice. J. Vet. Sci.6(2), 125–133 (2005).
  • Lin YJ, Deng MC, Wu SH et al. Baculovirus-derived hemagglutinin vaccine protects chickens from lethal homologous virus H5N1 challenge. J. Vet. Med. Sci.70(11), 1147–1152 (2008).
  • Kaba SA, Musoke AJ, Schaap D et al. Novel baculovirus-derived p67 subunit vaccines efficacious against East Coast fever in cattle. Vaccine23(21), 2791–2800 (2005).
  • Poot J, Janssen LHM, van Kasteren-Westerneng TJ, van der Heijden-Liefkens KHA, Schijns VEJC, Heckeroth A. Vaccination of dogs with six different candidate leishmaniasis vaccines composed of a chimerical recombinant protein containing ribosomal and histone protein epitopes in combination with different adjuvants. Vaccine27(33), 4439–4446 (2009).
  • Palomares LA, Ramírez OT. Challenges for the production of virus-like particles in insect cells: the case of rotavirus-like particles. Biochemical Engineering Journal45(3), 158–167 (2009).
  • Aucoin MG, Mena JA, Kamen AA. Bioprocessing of baculovirus vectors: a review. Curr. Gene Ther.10(3), 174–186 (2010).
  • Krammer F, Schinko T, Palmberger D, Tauer C, Messner P, Grabherr R. Trichoplusia ni cells (High Five™) are highly efficient for the production of influenza A virus-like particles: a comparison of two insect cell lines as production platforms for influenza vaccines. Mol. Biotechnol.45(3), 226–234 (2010).
  • Krammer F, Nakowitsch S, Messner P, Palmberger D, Ferko B, Grabherr R. Swine-origin pandemic H1N1 influenza virus-like particles produced in insect cells induce hemagglutination inhibiting antibodies in BALB/c mice. Biotechnol. J.5(1), 17–23 (2010).
  • Deschuyteneer M, Elouahabi A, Plainchamp D et al. Molecular and structural characterization of the L1 virus-like particles that are used as vaccine antigens in Cervarix™, the AS04-adjuvanted HPV-16 and -18 cervical cancer vaccine. Hum. Vaccin.6(5), 407–419 (2010).
  • Marek M, van Oers MM, Devaraj FF, Vlak JM, Merten OW. Engineering of baculovirus vectors for the manufacture of virion-free biopharmaceuticals. Biotechnol. Bioeng.108(5), 1056–1067 (2010).
  • Pincus S, Boddapati S, Li J, Sadowski T. Release and stability testing programs for a novel virus-like particle vaccine. BioPharm. Int.23(10 Suppl.), 26–34 (2010).
  • Peixoto C, Sousa MFQ, Silva AC, Carrondo MJT, Alves PM. Downstream processing of triple layered rotavirus like particles. J. Biotechnol.127(3), 452–461 (2007).
  • Benavides J, Mena JA, Cisneros-Ruiz M, Ramirez OT, Palomares LA, Rito-Palomares M. Rotavirus-like particles primary recovery from insect cells in aqueous two-phase systems. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci.842(1), 48–57 (2006).
  • Monie A, Hung CF, Roden R, Wu TC. Cervarix: a vaccine for the prevention of HPV 16, 18-associated cervical cancer. Biologics2, 97–105 (2008).
  • Rose RC, Bonnez W, Reichman RC, Garcea RL. Expression of human papillomavirus type 11 L1 protein in insect cells: in vivo and in vitro assembly of viruslike particles. J. Virol.67(4), 1936–1944 (1993).
  • Bhatla N, Suri V, Basu P et al. Immunogenicity and safety of human papillomavirus-16/18 AS04-adjuvanted cervical cancer vaccine in healthy Indian women. J. Obstet. Gynaecol. Res.36(1), 123–132 (2010).
  • Paavonen J, Jenkins D, Bosch FX et al. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a Phase III double-blind, randomised controlled trial. Lancet369(9580), 2161–2170 (2007).
  • Einstein MH, Baron M, Levin MJ et al. Comparison of the immunogenicity and safety of Cervarix™ and Gardasil® human papillomavirus (HPV) cervical cancer vaccines in healthy women aged 18–45 years. Hum. Vaccin.5(10), 705–719 (2009).
  • Zhang T, Xu Y, Qiao L et al. Trivalent human papillomavirus (HPV) VLP vaccine covering HPV type 58 can elicit high level of humoral immunity but also induce immune interference among component types. Vaccine28(19), 3479–3487 (2010).
  • Xu Y, Wang Q, Han Y, Song G, Xu E. Type-specific and cross-reactive antibodies induced by human papillomavirus 31 L1/L2 virus-like particles. J. Med. Microbiol.56(7), 907–913 (2007).
  • Baek J-O, Seo J-W, Kim I-H, Kim CH. Production and purification of human papillomavirus type 33 L1 virus-like particles from Spodoptera frugiperda 9 cells using two-step column chromatography. Protein Expr. Purif.75(2), 211–217 (2011).
  • Bansal GP, Hatfield JA, Dunn FE et al. Candidate recombinant vaccine for human B19 parvovirus. J. Infect. Dis.167(5), 1034–1044 (1993).
  • Tsao EI, Mason MR, Cacciuttolo MA, Bowen SH, Folena-Wasserman G. Production of parvovirus B19 vaccine in insect cells co-infected with double baculoviruses. Biotechnol. Bioeng.49(2), 130–138 (1996).
  • Shelly D, Van Cleave V. Parvovirus B19 VLP vaccine manufacturing. Genetic Engineering and Biotechnology News29(16), 1–3 (2009).
  • Sico C, White S, Tsao E, Varma A. Enhanced kinetic extraction of parvovirus B19 structural proteins. Biotechnol. Bioeng.80(3), 250–256 (2002).
  • Ballou WR, Reed JL, Noble W, Young NS, Koenig S. Safety and immunogenicity of a recombinant parvovirus B19 vaccine formulated with MF59C.1. J. Infect. Dis.187(4), 675–678 (2003).
  • Jiang X, Wang M, Graham DY, Estes MK. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J. Virol.66(11), 6527–6532 (1992).
  • Ball JM, Hardy ME, Atmar RL, Conner ME, Estes MK. Oral immunization with recombinant Norwalk virus-like particles induces a systemic and mucosal immune response in mice. J. Virol.72(2), 1345–1353 (1998).
  • Ausar SF, Foubert TR, Hudson MH, Vedvick TS, Middaugh CR. conformational stability and disassembly of norwalk virus-like particles: effect of pH and temperature. J. Biol. Chem.281(28), 19478–19488 (2006).
  • Nicollier-Jamot B, Ogier A, Piroth L, Pothier P, Kohli E. Recombinant virus-like particles of a norovirus (genogroup II strain) administered intranasally and orally with mucosal adjuvants LT and LT(R192G) in BALB/c mice induce specific humoral and cellular Th1/Th2-like immune responses. Vaccine22(9–10), 1079–1086 (2004).
  • Tacket CO, Sztein MB, Losonsky GA, Wasserman SS, Estes MK. Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin. Immunol.108(3), 241–247 (2003).
  • Roy P, Noad R. Virus-like particles as a vaccine delivery system: myths and facts. Hum. Vaccin.4(1), 5–12 (2008).
  • Ward RL, McNeal MM, Steele AD. Why does the world need another rotavirus vaccine? Ther. Clin. Risk Manag.4(1), 49–63 (2008).
  • Agnello D, Hervé CA, Lavaux A et al. Intrarectal immunization with rotavirus 2/6 virus-like particles induces an antirotavirus immune response localized in the intestinal mucosa and protects against rotavirus infection in mice. J. Virol.80(8), 3823–3832 (2006).
  • Murphy TV, Gargiullo PM, Massoudi MS et al. Intussusception among infants given an oral rotavirus vaccine. N. Engl. J. Med.344(8), 564–572 (2001).
  • Mena JA, Ramírez OT, Palomares LA. Intracellular distribution of rotavirus structural proteins and virus-like particles expressed in the insect cell-baculovirus system. J. Biotechnol.122(4), 443–452 (2006).
  • Madore HP, Estes MK, Zarley CD et al. Biochemical and immunologic comparison of virus-like particles for a rotavirus subunit vaccine. Vaccine17(19), 2461–2471 (1999).
  • Kim Y, Chang K-O, Kim W-Y, Saif LJ. Production of hybrid double- or triple-layered virus-like particles of group A and C rotaviruses using a baculovirus expression system. Virology302(1), 1–8 (2002).
  • Bertolotti-Ciarlet A, Ciarlet M, Crawford SE, Conner ME, Estes MK. Immunogenicity and protective efficacy of rotavirus 2/6-virus-like particles produced by a dual baculovirus expression vector and administered intramuscularly, intranasally, or orally to mice. Vaccine21(25–26), 3885–3900 (2003).
  • Shuttleworth G, Eckery DC, Awram P. Oral and intraperitoneal immunization with rotavirus 2/6 virus-like particles stimulates a systemic and mucosal immune response in mice. Arch. Virol.150(2), 341–349 (2005).
  • Ogier A, Franco MA, Charpilienne A, Cohen J, Pothier P, Kohli E. Distribution and phenotype of murine rotavirus-specific B cells induced by intranasal immunization with 2/6 virus-like particles. Eur. J. Immunol.35(7), 2122–2130 (2005).
  • O’Neal CM, Crawford SE, Estes MK, Conner ME. Rotavirus virus-like particles administered mucosally induce protective immunity. J. Virol.71(11), 8707–8717 (1997).
  • Park JY, Kim H, Hwang HK et al. Large-scale production of rotavirus VLP as vaccine candidate using baculovirus expression vector system (BEVS). J. Microbiol. Biotechnol.14(1), 35–40 (2004).
  • Parez N, Fourgeux C, Mohamed A et al. Rectal immunization with rotavirus virus-like particles induces systemic and mucosal humoral immune responses and protects mice against rotavirus infection. J. Virol.80(4), 1752–1761 (2006).
  • Ciarlet M, Crawford SE, Barone C et al. Subunit rotavirus vaccine administered parenterally to rabbits induces active protective immunity. J. Virol.72(11), 9233–9246 (1998).
  • Istrate C, Hinkula J, Charpilienne A et al. Parenteral administration of RF 8–2/6/7 rotavirus-like particles in a one-dose regimen induce protective immunity in mice. Vaccine26(35), 4594–4601 (2008).
  • Palomares LA, López S, Ramírez OT. Strategies for manipulating the relative concentration of recombinant rotavirus structural proteins during simultaneous production by insect cells. Biotechnol. Bioeng.78(6), 635–644 (2002).
  • Vieira HLA, Estêvão C, Roldão A et al. Triple layered rotavirus VLP production: kinetics of vector replication, mRNA stability and recombinant protein production. J. Biotechnol.120(1), 72–82 (2005).
  • Li TC, Suzaki Y, Ami Y, Dhole TN, Miyamura T, Takeda N. Protection of cynomolgus monkeys against HEV infection by oral administration of recombinant hepatitis E virus-like particles. Vaccine22(3–4), 370–377 (2004).
  • Chung C-Y, Chen C-Y, Lin S-Y et al. Enterovirus 71 virus-like particle vaccine: improved production conditions for enhanced yield. Vaccine28(43), 6951–6957 (2010).
  • Goldmann C, Petry H, Frye S et al. Molecular cloning and expression of major structural protein VP1 of the human polyomavirus JC virus: formation of virus-like particles useful for immunological and therapeutic studies. J. Virol.73(5), 4465–4469 (1999).
  • Chung YC, Huang JH, Lai CW et al. Expression, purification and characterization of enterovirus-71 virus-like particles. World J. Gastroenterol.12(6), 921–927 (2006).
  • Pushko P, Tumpey TM, Bu F, Knell J, Robinson R, Smith G. Influenza virus-like particles comprised of the HA, NA, and M1 proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine23(50), 5751–5759 (2005).
  • Matassov D, Cupo A, Galarza JM. A novel intranasal virus-like particle (VLP) vaccine designed to protect against the pandemic 1918 influenza A virus (H1N1). Viral Immunol.20(3), 441–452 (2007).
  • Bright RA, Carter DM, Daniluk S et al. Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine25(19), 3871–3878 (2007).
  • Bright RA, Carter DM, Crevar CJ et al. Cross-clade protective immune responses to influenza viruses with H5N1 HA and NA elicited by an influenza virus-like particle. PLoS ONE3(1), e1501 (2008).
  • Mahmood K, Bright RA, Mytle N et al. H5N1 VLP vaccine induced protection in ferrets against lethal challenge with highly pathogenic H5N1 influenza viruses. Vaccine26(42), 5393–5399 (2008).
  • Kang SM, Yoo DG, Lipatov AS et al. Induction of long-term protective immune responses by influenza H5N1 virus-like particles. PLoS ONE4(3), e4667 (2009).
  • Pushko P, Kort T, Nathan M, Pearce MB, Smith G, Tumpey TM. Recombinant H1N1 virus-like particle vaccine elicits protective immunity in ferrets against the 2009 pandemic H1N1 influenza virus. Vaccine28(30), 4771–4776 (2010).
  • Galarza JM, Latham T, Cupo A. Virus-like particle vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol.18(2), 365–372 (2005).
  • Krammer F, Schinko T, Messner P, Palmberger D, Ferko B, Grabherr R. Influenza virus-like particles as an antigen-carrier platform for the ESAT-6 epitope of Mycobacterium tuberculosis. J. Virol. Methods167(1), 17–22 (2010).
  • Lu X, Chen Y, Bai B et al. Immune responses against severe acute respiratory syndrome coronavirus induced by virus-like particles in mice. Immunology122(4), 496–502 (2007).
  • Ho Y, Lin PH, Liu CYY, Lee SP, Chao YC. Assembly of human severe acute respiratory syndrome coronavirus-like particles. Biochem. Biophys. Res. Commun.318(4), 833–838 (2004).
  • Bai B, Hu Q, Hu H et al. Virus-like particles of SARS-like coronavirus formed by membrane proteins from different origins demonstrate stimulating activity in human dendritic cells. PLoS ONE3(7), e2685 (2008).
  • Lu B, Huang Y, Huang L et al. Effect of mucosal and systemic immunization with virus-like particles of severe acute respiratory syndrome coronavirus in mice. Immunology130(2), 254–261 (2010).
  • Ye L, Lin J, Sun Y et al. Ebola virus-like particles produced in insect cells exhibit dendritic cell stimulating activity and induce neutralizing antibodies. Virology351(2), 260–270 (2006).
  • Sun Y, Carrion R Jr, Ye L et al. Protection against lethal challenge by Ebola virus-like particles produced in insect cells. Virology383(1), 12–21 (2009).
  • Warfield KL, Posten NA, Swenson DL et al. Filovirus-like particles produced in insect cells: immunogenicity and protection in rodents. J. Infect. Dis.196(Suppl. 2), S421–S429 (2007).
  • Yang C, Ye L, Compans RW. Protection against filovirus infection: virus-like particle vaccines. Expert Rev. Vaccines7(3), 333–344 (2008).
  • Fort M, Sibila M, Allepuz A, Mateu E, Roerink F, Segalés J. Porcine circovirus type 2 (PCV2) vaccination of conventional pigs prevents viremia against PCV2 isolates of different genotypes and geographic origins. Vaccine26(8), 1063–1071 (2008).
  • Fort M, Sibila M, Pérez-Martín E, Nofrarías M, Mateu E, Segalés J. One dose of a porcine circovirus 2 (PCV2) sub-unit vaccine administered to 3-week-old conventional piglets elicits cell-mediated immunity and significantly reduces PCV2 viremia in an experimental model. Vaccine27(30), 4031–4037 (2009).
  • Fan H, Ju C, Tong T, Huang H, Lv J, Chen H. Immunogenicity of empty capsids of porcine circovius type 2 produced in insect cells. Vet. Res. Commun.31(4), 487–496 (2007).
  • Liu LJ, Suzuki T, Tsunemitsu H et al. Efficient production of type 2 porcine circovirus-like particles by a recombinant baculovirus. Arch. Virol.153(12), 2291–2295 (2008).
  • Pérez-Martín E, Gómez-Sebastián S, Argilaguet JM et al. Immunity conferred by an experimental vaccine based on the recombinant PCV2 Cap protein expressed in Trichoplusia ni-larvae. Vaccine28(11), 2340–2349 (2010).
  • Antonis AFG, Bruschke CJM, Rueda P et al. A novel recombinant virus-like particle vaccine for prevention of porcine parvovirus-induced reproductive failure. Vaccine24(26), 5481–5490 (2006).
  • Stewart M, Bhatia Y, Athmaran TN et al. Validation of a novel approach for the rapid production of immunogenic virus-like particles for Bluetongue virus. Vaccine28(17), 3047–3054 (2010).
  • Prel A, Le Gall-Reculé G, Cherbonnel M, Grasland B, Amelot M, Jestin V. Assessment of the protection afforded by triple baculovirus recombinant coexpressing H5, N3, M1 proteins against a homologous H5N3 low-pathogenicity avian influenza virus challenge in Muscovy ducks. Avian Dis.51(Suppl. 1), 484–489 (2007).
  • Prel A, Le Gall-Reculé G, Jestin V. Achievement of avian influenza virus-like particles that could be used as a subunit vaccine against low-pathogenic avian influenza strains in ducks. Avian Pathol.37(5), 513–520 (2008).
  • Cao Y, Lu Z, Sun J et al. Synthesis of empty capsid-like particles of Asia I foot-and-mouth disease virus in insect cells and their immunogenicity in guinea pigs. Vet. Microbiol.137(1–2), 10–17 (2009).
  • Martínez C, Dalsgaard K, López de Turiso J, Cortés E, Vela C, Casal J. Production of porcine parvovirus empty capsids with high immunogenic activity. Vaccine10(10), 684–690 (1992).
  • Madhan S, Prabakaran M, Kwang J. Baculovirus as vaccine vectors Curr. Gene Ther.10(3), 201–213 (2010).
  • Hu YC, Yao K, Wu TY. Baculovirus as an expression and/or delivery vehicle for vaccine antigens. Expert Rev. Vaccines7(3), 363–371 (2008).
  • He F, Madhan S, Kwang J. Baculovirus vector as a delivery vehicle for influenza vaccines. Expert Rev. Vaccines8(4), 455–467 (2009).
  • Barsoum J, Brown R, McKee M, Boyce FM. Efficient transduction of mammalian cells by a recombinant baculovirus having the vesicular stomatitis virus G glycoprotein. Hum. Gene Ther.8(17), 2011–2018 (1997).
  • Wang S, Fang L, Fan H et al. Construction and immunogenicity of pseudotype baculovirus expressing GP5 and M protein of porcine reproductive and respiratory syndrome virus. Vaccine25(49), 8220–8227 (2007).
  • Vicente T, Peixoto C, Carrondo MJT, Alves PM. Purification of recombinant baculoviruses for gene therapy using membrane processes. Gene Ther.16(6), 766–775 (2009).
  • Hu YC, Tsai CT, Chung YC, Lu JT, Hsu JTA. Generation of chimeric baculovirus with histidine-tags displayed on the envelope and its purification using immobilized metal affinity chromatography. Enzyme Microb. Technol.33(4), 445–452 (2003).
  • Transfiguracion J, Jorio H, Meghrous J, Jacob D, Kamen A. High yield purification of functional baculovirus vectors by size exclusion chromatography. J. Virol. Methods142(1–2), 21–28 (2007).
  • Wu C, Ker YS, Wang S. Ion-exchange membrane chromatography method for rapid and efficient purification of recombinant baculovirus and baculovirus gp64 protein. Hum. Gene Ther.18(7), 665–672 (2007).
  • Chen CY, Liu HJ, Tsai CP et al. Baculovirus as an avian influenza vaccine vector: differential immune responses elicited by different vector forms. Vaccine28(48), 7644–7651 (2010).
  • Yoshida S, Kawasaki M, Hariguchi N, Hirota K, Matsumoto M. A baculovirus dual expression system-based malaria vaccine induces strong protection against Plasmodium berghei sporozoite challenge in mice. Infect. Immun.77(5), 1782–1789 (2009).
  • Strauss R, Hüser A, Ni S et al. Baculovirus-based vaccination vectors allow for efficient induction of immune responses against Plasmodium falciparum circumsporozoite protein. Mol. Ther.15(1), 193–202 (2007).
  • Jin R, Lv Z, Chen Q et al. Safety and Immunogenicity of H5N1 influenza vaccine based on baculovirus surface display system of Bombyx mori. PLoS ONE3(12), e3933 (2008).
  • Peakman M, Tree TI, Endl J, Van Endert P, Atkinson MA, Roep BO. Characterization of preparations of GAD65, proinsulin, and the islet tyrosine phosphatase IA-2 for use in detection of autoreactive T-Cells in Type 1 Diabetes: report of Phase II of the Second International Immunology of Diabetes Society Workshop for Standardization of T-cell Assays in Type 1 Diabetes. Diabetes50(8), 1749–1754 (2001).
  • Burch PA, Breen JK, Buckner JC et al. Priming tissue-specific cellular immunity in a Phase I trial of autologous dendritic cells for prostate cancer. Clin. Cancer Res.6(6), 2175–2182 (2000).
  • Dosch SF, Mahajan SD, Collins AR. SARS coronavirus spike protein-induced innate immune response occurs via activation of the NF-κB pathway in human monocyte macrophages in vitro. Virus Res.142(1–2), 19–27 (2009).
  • Meeusen ENT, Walker J, Peters A, Pastoret PP, Jungersen G. Current status of veterinary vaccines. Clin. Microbiol. Rev.20(3), 489–510 (2007).
  • Bouma A, De Smit AJ, De Kluijver EP, Terpstra C, Moormann RJM. Efficacy and stability of a subunit vaccine based on glycoprotein E2 of classical swine fever virus. Vet. Microbiol.66(2), 101–114 (1999).
  • Kixmöller M, Ritzmann M, Eddicks M, Saalmüller A, Elbers K, Fachinger V. Reduction of PMWS-associated clinical signs and co-infections by vaccination against PCV2. Vaccine26(27–28), 3443–3451 (2008).
  • Opriessnig T, Patterson AR, Madson DM, Pal N, Halbur PG. Comparison of efficacy of commercial one dose and two dose PCV2 vaccines using a mixed PRRSV-PCV2-SIV clinical infection model 2–3-months post vaccination. Vaccine27(7), 1002–1007 (2009).
  • Senger T, Schädlich L, Gissmann L, Müller M. Enhanced papillomavirus-like particle production in insect cells. Virology388(2), 344–353 (2009).
  • Franssila R, Hedman K. T-helper cell-mediated interferon-γ, interleukin-10 and proliferation responses to a candidate recombinant vaccine for human parvovirus B19. Vaccine22(27–28), 3809–3815 (2004).
  • Kissmann J, Ausar SF, Foubert TR et al. Physical stabilization of norwalk virus-like particles. J. Pharma. Sci.97(10), 4208–4218 (2008).
  • El-Attar L, Oliver SL, Mackie A et al. Comparison of the efficacy of rotavirus VLP vaccines to a live homologous rotavirus vaccine in a pig model of rotavirus disease. Vaccine27(24), 3201–3208 (2009).
  • Azevedo MSP, Gonzalez AM, Yuan L et al. An oral versus intranasal prime/boost regimen using attenuated human rotavirus or VP2 and VP6 virus-like particles with immunostimulating complexes influences protection and antibody-secreting cell responses to rotavirus in a neonatal gnotobiotic pig model. Clin. Vaccine Immunol.17(3), 420–428 (2010).
  • Wen Z, Ye L, Gao Y et al. Immunization by influenza virus-like particles protects aged mice against lethal influenza virus challenge. Antiviral Res.84(3), 215–224 (2009).
  • Haynes JR, Dokken L, Wiley JA et al. Influenza-pseudotyped Gag virus-like particle vaccines provide broad protection against highly pathogenic avian influenza challenge. Vaccine27(4), 530–541 (2009).
  • Buonaguro L, Tornesello ML, Tagliamonte M et al. Baculovirus-derived human immunodeficiency virus type 1 virus-like particles activate dendritic cells and induce ex vivo T-cell responses. J. Virol.80(18), 9134–9143 (2006).
  • Buonaguro L, Visciano ML, Tornesello ML, Tagliamonte M, Biryahwaho B, Buonaguro FM. Induction of systemic and mucosal cross-clade neutralizing antibodies in BALB/c mice immunized with human immunodeficiency virus type 1 clade A virus-like particles administered by different routes of inoculation. J. Virol.79(11), 7059–7067 (2005).
  • Chege GK, Shephard EG, Meyers A et al. HIV-1 subtype C Pr55gag virus-like particle vaccine efficiently boosts baboons primed with a matched DNA vaccine. J. Gen. Virol.89(9), 2214–2227 (2008).
  • Speth C, Bredl S, Hagleitner M et al. Human immunodeficiency virus type-1 (HIV-1) Pr55gag virus-like particles are potent activators of human monocytes. Virology382(1), 46–58 (2008).
  • Bai B, Lu X, Meng J et al. Vaccination of mice with recombinant baculovirus expressing spike or nucleocapsid protein of SARS-like coronavirus generates humoral and cellular immune responses. Mol. Immunol.45(4), 868–875 (2008).
  • Qiao M, Ashok M, Bernard KA et al. Induction of sterilizing immunity against West Nile virus (WNV), by immunization with WNV-like particles produced in insect cells. J. Infect. Dis.190(12), 2104–2108 (2004).
  • Li Z, Yi Y, Yin X, Zhang Z, Liu J. Expression of foot-and-mouth disease virus capsid proteins in silkworm-baculovirus expression system and its utilization as a subunit vaccine. PLoS ONE3(5), e2273 (2008).
  • Prabakaran M, He F, Meng T et al. Neutralizing epitopes of influenza virus hemagglutinin: target for the development of a universal vaccine against H5N1 lineages. J. Virol.84(22), 11822–11830 (2010).
  • Prabakaran M, Madhan S, Prabhu N, Geng GY, New R, Kwang J. Reverse micelle-encapsulated recombinant baculovirus as an oral vaccine against H5N1 infection in mice. Antiviral Res.86(2), 180–187 (2010).
  • Prabakaran M, Madhan S, Prabhu N, Qiang J, Kwang J. Gastrointestinal delivery of baculovirus displaying influenza virus hemagglutinin protects mice against heterologous H5N1 infection. J. Virol.84(7), 3201–3209 (2010).
  • Tang X-C, Lu H-R, Ross TM. Hemagglutinin displayed baculovirus protects against highly pathogenic influenza. Vaccine28(42), 6821–6831 (2010).
  • Mlambo G, Kumar N, Yoshida S. Functional immunogenicity of baculovirus expressing Pfs25, a human malaria transmission-blocking vaccine candidate antigen. Vaccine28(43), 7025–7029 (2010).
  • Yoshida S, Araki H, Yokomine T. Baculovirus-based nasal drop vaccine confers complete protection against malaria by natural boosting of vaccine-induced antibodies in mice. Infect. Immun.78(2), 595–602 (2010).
  • Feng Q, Liu Y, Qu X et al. Baculovirus surface display of SARS coronavirus (SARS-CoV) spike protein and immunogenicity of the displayed protein in mice models. DNA Cell Biol.25(12), 668–673 (2006).
  • Peralta A, Molinari P, Conte-Grand D, Calamante G, Taboga O. A chimeric baculovirus displaying bovine herpesvirus-1 (BHV-1) glycoprotein D on its surface and their immunological properties. Appl. Microbiol. Biotechnol.75(2), 407–414 (2007).
  • Fang R, Feng H, Nie H et al. Construction and immunogenicity of pseudotype baculovirus expressing Toxoplasma gondii SAG1 protein in BALB/c mice model. Vaccine28(7), 1803–1807 (2010).
  • Li Y, Ye J, Cao S et al. Immunization with pseudotype baculovirus expressing envelope protein of Japanese encephalitis virus elicits protective immunity in mice. J. Gene Med.11(1), 57–65 (2009).
  • Molinari P, Bianco V, Peralta A et al. Recombinant baculoviruses as vehicles for presentation and adjuvancy of antigens for the development of new tuberculosis candidate vaccines. Procedia in Vaccinology1(1), 81–84 (2009).
  • Li M, Wang YF, Wang Y et al. Immune responses induced by a BacMam virus expressing the E2 protein of classical swine fever virus in mice. Immunol. Lett.125(2), 145–150 (2009).
  • Xu X-G, Chiou M-T, Zhang Y-M et al. Baculovirus surface display of Erns envelope glycoprotein of classical swine fever virus. J. Virol. Methods153(2), 149–155 (2008).
  • Xu X-G, Tong D-W, Chiou M-T et al. Baculovirus surface display of NS3 nonstructural protein of classical swine fever virus. J. Virol. Methods159(2), 259–264 (2009).
  • Wu Q, Fang L, Wu X et al. A pseudotype baculovirus-mediated vaccine confers protective immunity against lethal challenge with H5N1 avian influenza virus in mice and chickens. Mol. Immunol.46(11–12), 2210–2217 (2009).
  • Grabowska AK, Lipinska AD, Rohde J, Szewczyk B, Bienkowska-Szewczyk K, Rziha H-J. New baculovirus recombinants expressing Pseudorabies virus (PRV) glycoproteins protect mice against lethal challenge infection. Vaccine27(27), 3584–3591 (2009).
  • Fan H, Pan Y, Fang L et al. Construction and immunogenicity of recombinant pseudotype baculovirus expressing the capsid protein of porcine circovirus type 2 in mice. J. Virol. Methods150(1–2), 21–26 (2008).

Websites

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.