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Virus-Like Particles as a Vaccine Delivery System: Myths and Facts

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 655)

Abstract

Vaccines against viral disease have traditionally relied on attenuated virus strains or inactivation of infectious virus. Subunit vaccines based on viral proteins expressed in heterologous systems have been effective for some pathogens, but have often suffered from poor immunogenicity due to incorrect protein folding or modification. In this chapter we focus on a specific class of viral subunit vaccine that mimics the overall structure of virus particles and thus preserves the native antigenic conformation of the immunogenic proteins. These virus-like particles (VLPs) have been produced for a wide range of taxonomically and structurally distinct viruses, and have unique advantages in terms of safety and immunogenicity over previous approaches. With new VLP vaccines for papillomavirus beginning to reach the market place we argue that this technology has now ‘come-of-age’ and must be considered a viable vaccine strategy.

Keywords

Insect Cell Newcastle Disease Virus Bovine Leukemia Virus Subunit Vaccine Infectious Bursal Disease Virus 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. 1.
    Miyanohara A, Imamura T, Araki M. et al. Expression of hepatitis B virus core antigen gene in Saccharomyces cerevisiae: synthesis of two polypeptides translated from different initiation codons. J Virol 1986; 59(1):176–80.PubMedGoogle Scholar
  2. 2.
    Delchambre M, Gheysen D, Thines D. et al. The GAG precursor of simian immunodeficiency virus assembles into virus-like particles. EMBO J 1989; 8(9):2653–60.PubMedGoogle Scholar
  3. 3.
    Gheysen D, Jacobs E, de Foresta F et al. Assembly and release of HIV-1 precursor Pr55gag virus-like particles from recombinant baculovirus-infected insect cells. Cell 1989; 59(1):103–12.CrossRefPubMedGoogle Scholar
  4. 4.
    French TJ, Marshall JJ, Roy P. Assembly of double-shelled, virus-like particles of bluetongue virus by the simultaneous expression of four structural proteins. J Virol 1990; 64(12):5695–700.PubMedGoogle Scholar
  5. 5.
    Schirmbeck R, Bohm W, Reimann J. Virus-like particles induce MHC class I-restricted T-cell responses. Lessons learned from the hepatitis B small surface antigen. Intervirology 1996; 39(1–2):111–9.PubMedGoogle Scholar
  6. 6.
    Paliard X, Liu Y, Wagner R, et al. Priming of strong, broad and long-lived HIV type 1 p55gag-specific CD8+ cytotoxic T-cells after administration of a virus-like particle vaccine in rhesus macaques. AIDS Res Hum Retroviruses 2000; 16(3):273–82.CrossRefPubMedGoogle Scholar
  7. 7.
    Murata K, Lechmann M, Qiao M, et al. Immunization with hepatitis C virus-like particles protects mice from recombinant hepatitis C virus-vaccinia infection. Proc Natl Acad Sci USA 2003; 100(11):6753–8.CrossRefPubMedGoogle Scholar
  8. 8.
    Noad R, Roy P. Virus-like particles as immunogens. Trends Microbiol 2003; 11(9):438–44.CrossRefPubMedGoogle Scholar
  9. 9.
    Maranga L, Rueda P, Antonis AF et al. Large scale production and downstream processing of a recombinant porcine parvovirus vaccine. Appl Microbiol Biotechnol 2002; 59(1):45–50.CrossRefPubMedGoogle Scholar
  10. 10.
    Zhou J, Sun XY, Stenzel DJ et al. Expression of vaccinia recombinant HPV 16 L1 and L2 ORF proteins in epithelial cells is sufficient for assembly of HPV virion-like particles. Virology 1991; 185(1):251–7.CrossRefPubMedGoogle Scholar
  11. 11.
    Kirnbauer R, Booy F, Cheng N et al. Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci USA 1992; 89(24):12180–4.CrossRefPubMedGoogle Scholar
  12. 12.
    Sasagawa T, Pushko P, Steers G et al. Synthesis and assembly of virus-like particles of human papillomaviruses type 6 and type 16 in fission yeast Schizosaccharomyces pombe. Virology 1995; 206(1):126–35.CrossRefPubMedGoogle Scholar
  13. 13.
    Dupuy C, Buzoni-Gatel D, Touze A et al. Nasal immunization of mice with human papillomavirus type 16 (HPV-16) virus-like particles or with the HPV-16 L1 gene elicits specific cytotoxic T lymphocytes in vaginal draining lymph nodes. J Virol 1999; 73 (11):9063–71.PubMedGoogle Scholar
  14. 14.
    Zhang LF, Zhou J, Chen S et al. HPV6b virus like particles are potent immunogens without adjuvant in man. Vaccine 2000; 18(11–12):1051–8.CrossRefPubMedGoogle Scholar
  15. 15.
    Koutsky LA, Ault KA, Wheeler CM et al. A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 2002; 347(21):1645–51.CrossRefPubMedGoogle Scholar
  16. 16.
    Evans TG, Bonnez W, Rose RC et al. A Phase 1 study of a recombinant viruslike particle vaccine against human papillomavirus type 11 in healthy adult volunteers. J Infect Dis 2001; 183(10):1485–93.CrossRefPubMedGoogle Scholar
  17. 17.
    Harro CD, Pang YY, Roden RB et al. Safety and immunogenicity trial in adult volunteers of a human papillomavirus 16 L1 virus-like particle vaccine. J Natl Cancer Inst 2001; 93(4):284–92.CrossRefPubMedGoogle Scholar
  18. 18.
    Franco EL, Harper DM. Vaccination against human papillomavirus infection: a new paradigm in cervical cancer control. Vaccine 2005; 23(17–18):2388–94.CrossRefPubMedGoogle Scholar
  19. 19.
    Harper DM, Franco EL, Wheeler C et al. Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet 2004; 364(9447):1757–65.CrossRefPubMedGoogle Scholar
  20. 20.
    Harper DM, Franco EL, Wheeler CM et al. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet 2006; 367(9518):1247–55.CrossRefPubMedGoogle Scholar
  21. 21.
    Lopez de Turiso JA, Cortes E, Martinez C et al. Recombinant vaccine for canine parvovirus in dogs. J Virol 1992; 66(5):2748–53.PubMedGoogle Scholar
  22. 22.
    Martinez C, Dalsgaard K, Lopez de Turiso JA et al. Production of porcine parvovirus empty capsids with high immunogenic activity. Vaccine 1992; 10(10):684–90.CrossRefPubMedGoogle Scholar
  23. 23.
    Antonis AF, Bruschke CJ, Rueda P et al. A novel recombinant virus-like particle vaccine for prevention of porcine parvovirus-induced reproductive failure. Vaccine 2006; 24(26):5481–90.CrossRefPubMedGoogle Scholar
  24. 24.
    Ball JM, Hardy ME, Atmar RL et al. Oral immunization with recombinant Norwalk virus-like particles induces a systemic and mucosal immune response in mice. J Virol 1998; 72(2):1345–53.PubMedGoogle Scholar
  25. 25.
    Guerrero RA, Ball JM, Krater SS et al. Recombinant Norwalk virus-like particles administered intranasally to mice induce systemic and mucosal (fecal and vaginal) immune responses. J Virol 2001; 75(20):9713–22.CrossRefPubMedGoogle Scholar
  26. 26.
    Ball JM, Graham DY, Opekun AR et al. Recombinant Norwalk virus-like particles given orally to volunteers: phase I study. Gastroenterology 1999; 117(1):40–8.CrossRefPubMedGoogle Scholar
  27. 27.
    Tacket CO, Sztein MB, Losonsky GA et al. Humoral, mucosal and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin Immunol 2003; 108(3):241–7.CrossRefPubMedGoogle Scholar
  28. 28.
    Li TC, Yamakawa Y, Suzuki K et al. Expression and self-assembly of empty virus-like particles of hepatitis E virus. J Virol 1997; 71(10):7207–13.PubMedGoogle Scholar
  29. 29.
    Li T, Takeda N, Miyamura T. Oral administration of hepatitis E virus-like particles induces a systemic and mucosal immune response in mice. Vaccine 2001; 19(25–26):3476–84.CrossRefPubMedGoogle Scholar
  30. 30.
    Li TC, Suzaki Y, Ami Y et al. Protection of cynomolgus monkeys against HEV infection by oral administration of recombinant hepatitis e virus-like particles. Vaccine 2004; 22(3–4):370–7.CrossRefPubMedGoogle Scholar
  31. 31.
    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 1999; 73(5):4465–9.PubMedGoogle Scholar
  32. 32.
    Caparros-Wanderley W, Clark B, Griffin BE. Effect of dose and long-term storage on the immunogenicity of murine polyomavirus VP1 virus-like particles. Vaccine 2004; 22(3–4):352–61.CrossRefPubMedGoogle Scholar
  33. 33.
    Brautigam S, Snezhkov E, Bishop DH. Formation of poliovirus-like particles by recombinant baculoviruses expressing the individual VP0, VP3 and VP1 proteins by comparison to particles derived from the expressed poliovirus polyprotein. Virology 1993; 192(2):512–24.CrossRefPubMedGoogle Scholar
  34. 34.
    Kibenge FS, Qian B, Nagy E et al. Formation of virus-like particles when the polyprotein gene (segment A) of infectious bursal disease virus is expressed in insect cells. Can J Vet Res 1999; 63(1):49–55.PubMedGoogle Scholar
  35. 35.
    French TJ, Roy P. Synthesis of bluetongue virus (BTV) corelike particles by a recombinant baculovirus expressing the two major structural core proteins of BTV. J Virol 1990; 64(4):1530–6.PubMedGoogle Scholar
  36. 36.
    Belyaev AS, Hails RS, Roy P. High-level expression of five foreign genes by a single recombinant baculovirus. Gene 1995; 156(2):229–33.CrossRefPubMedGoogle Scholar
  37. 37.
    Belyaev AS, Roy P. Development of baculovirus triple and quadruple expression vectors: coexpression of three or four bluetongue virus proteins and the synthesis of bluetongue virus-like particles in insect cells. Nucleic Acids Research 1993; 21(5):1219–23.CrossRefPubMedGoogle Scholar
  38. 38.
    Roy P. Orbiviruses. In: Knipe DM, Howley PM, eds. Fields’ Virology, Fourth Edition. Philadelphia: Lippincott Williams and Wilkins, 2001:1835–1869.Google Scholar
  39. 39.
    Roy P, French T, Erasmus BJ. Protective efficacy of virus-like particles for bluetongue disease. Vaccine 1992; 10(1):28–32.CrossRefPubMedGoogle Scholar
  40. 40.
    Roy P, Bishop DH, LeBlois H et al. Long-lasting protection of sheep against bluetongue challenge after vaccination with virus-like particles: evidence for homologous and partial heterologous protection. Vaccine 1994; 12(9):805–11.CrossRefPubMedGoogle Scholar
  41. 41.
    Roy P, Urakawa T, Van Dijk AA et al. Recombinant virus vaccine for bluetongue disease in sheep. J Virol 1990; 64(5):1998–2003.PubMedGoogle Scholar
  42. 42.
    Sabara M, Parker M, Aha P et al. Assembly of double-shelled rotaviruslike particles by simultaneous expression of recombinant VP6 and VP7 proteins. J Virol 1991; 65(12):6994–7.PubMedGoogle Scholar
  43. 43.
    Jiang B, Estes MK, Barone C et al. Heterotypic protection from rotavirus infection in mice vaccinated with virus-like particles. Vaccine 1999; 17(7–8):1005–13.CrossRefPubMedGoogle Scholar
  44. 44.
    Madore HP, Estes MK, Zarley CD et al. Biochemical and immunologic comparison of virus-like particles for a rotavirus subunit vaccine. Vaccine 1999; 17(19):2461–71.CrossRefPubMedGoogle Scholar
  45. 45.
    Kim Y, Nielsen PR, Hodgins D et al. Lactogenic antibody responses in cows vaccinated with recombinant bovine rotavirus-like particles (VLPs) of two serotypes or inactivated bovine rotavirus vaccines. Vaccine 2002; 20(7–8):1248–58.CrossRefPubMedGoogle Scholar
  46. 46.
    Nguyen TV, Yuan L, MS PA et al. Low titer maternal antibodies can both enhance and suppress B cell responses to a combined live attenuated human rotavirus and VLP-ISCOM vaccine. Vaccine 2006; 24(13):2302–16.CrossRefPubMedGoogle Scholar
  47. 47.
    Bertolotti-Ciarlet A, Ciarlet M, Crawford SE et al. 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. Vaccine 2003; 21(25–26):3885–900.CrossRefPubMedGoogle Scholar
  48. 48.
    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 2006; 80(4):1752–61.CrossRefPubMedGoogle Scholar
  49. 49.
    Agnello D, Herve CA, Lavaux A et al. Intrarectal immunization with rotavirus 2/6 virus-like particles induces an anti-rotavirus immune response localized in the intestinal mucosa and protects against rotavirus infection in mice. J Virol 2006; 80(8):3823–32.CrossRefPubMedGoogle Scholar
  50. 50.
    Yamshchikov GV, Ritter GD, Vey M et al. Assembly of SIV virus-like particles containing envelope proteins using a baculovirus expression system. Virology 1995; 214(1):50–8.CrossRefPubMedGoogle Scholar
  51. 51.
    Baumert TF, Ito S, Wong DT et al. Hepatitis C virus structural proteins assemble into viruslike particles in insect cells. J Virol 1998; 72(5):3827–36.PubMedGoogle Scholar
  52. 52.
    Latham T, Galarza JM. Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. Virol 2001; 75(13):6154–65.CrossRefGoogle Scholar
  53. 53.
    Jeong SH, Qiao M, Nascimbeni M et al. Immunization with hepatitis C virus-like particles induces humoral and cellular immune responses in nonhuman primates. J Virol 2004; 78(13):6995–7003.CrossRefPubMedGoogle Scholar
  54. 54.
    Mortola E, Roy P. Efficient assembly and release of SARS coronavirus-like particles by a heterologous expression system. FEBS Lett 2004; 576(1–2):174–8.CrossRefPubMedGoogle Scholar
  55. 55.
    Ho Y, Lin PH, Liu CY et al. Assembly of human severe acute respiratory syndrome coronavirus-like particles. Biochem Biophys Res Commun 2004; 318(4):833–8.CrossRefPubMedGoogle Scholar
  56. 56.
    Yao Q, Kuhlmann FM, Eller R et al. Production and characterization of simian—human immunodeficiency virus-like particles. AIDS Res Hum Retroviruses 2000; 16(3):227–36.CrossRefPubMedGoogle Scholar
  57. 57.
    Wagner R, Deml L, Notka F et al. Safety and immunogenicity of recombinant human immunodeficiency virus-like particles in rodents and rhesus macaques. Intervirology 1996; 39(1–2):93–103.PubMedGoogle Scholar
  58. 58.
    Yao Q, Vuong V, Li M et al. Intranasal immunization with SIV virus-like particles (VLPs) elicits systemic and mucosal immunity. Vaccine 2002; 20(19–20):2537–45.CrossRefPubMedGoogle Scholar
  59. 59.
    Lechmann M, Murata K, Satoi J et al. Hepatitis C virus-like particles induce virus-specific humoral and cellular immune responses in mice. Hepatology 2001; 34(2):417–23.CrossRefPubMedGoogle Scholar
  60. 60.
    Galarza JM, Latham T, Cupo A. Virus-like particle (VLP) vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol 2005; 18(1):244–51.CrossRefPubMedGoogle Scholar
  61. 61.
    Pushko P, Tumpey TM, Bu F et al. Influenza virus-like particles comprised of the HA, NA and M1 proteins of H9N2 influenza virus induce protective immune responses in BALB/c mice. Vaccine 2005; 23(50):5751–9.CrossRefPubMedGoogle Scholar
  62. 62.
    Garcea RL, Gissmann L. Virus-like particles as vaccines and vessels for the delivery of small molecules. Curr Opin Biotechnol 2004; 15(6):513–7.CrossRefPubMedGoogle Scholar
  63. 63.
    Beyer T, Herrmann M, Reiser C et al. Bacterial carriers and virus-like-particles as antigen delivery devices: role of dendritic cells in antigen presentation. Curr Drug Targets Infect Disord 2001; 1(3):287–302.CrossRefPubMedGoogle Scholar
  64. 64.
    Fausch SC, Da Silva DM, Kast WM. Differential uptake and cross-presentation of human papillomavirus virus-like particles by dendritic cells and Langerhans cells. Cancer Res 2003; 63(13):3478–82.PubMedGoogle Scholar
  65. 65.
    Sedlik C, Saron M, Sarraseca J et al. Recombinant parvovirus-like particles as an antigen carrier: a novel nonreplicative exogenous antigen to elicit protective antiviral cytotoxic T-cells. Proc Natl Acad Sci USA 1997; 94(14):7503–8.CrossRefPubMedGoogle Scholar
  66. 66.
    Fausch SC, Da Silva, DM, Kast WM. Heterologous papillomavirus virus-like particles and human papillomavirus virus-like particle immune complexes activate human Langerhans cells. Vaccine 2005; 23(14):1720–9.CrossRefPubMedGoogle Scholar
  67. 67.
    Lo-Man R, Rueda P, Sedlik C et al. A recombinant virus-like particle system derived from parvovirus as an efficient antigen carrier to elicit a polarized Th1 immune response without adjuvant. Eur J Immunol 1998; 28(4):1401–7.CrossRefPubMedGoogle Scholar
  68. 68.
    Charpilienne A, Nejmeddine M BM, Parez N, Neumann E, Hewat E, Trugnan G, Cohen J. Individual rotavirus-like particles containing 120 molecules of fluorescent protein are visible in living cells. J Biol Chem 2001; 276(31):29361–29367.CrossRefPubMedGoogle Scholar
  69. 69.
    Ghosh MK, Deriaud E, Saron MF et al. Induction of protective anti-viral cytotoxic T-cells by a tubular structure capable of carrying large foreign sequences. Vaccine 2002; 20(9–10):1369–77.CrossRefPubMedGoogle Scholar
  70. 70.
    Ghosh MK, Borca MV, Roy P. Virus-derived tubular structure displaying foreign sequences on the surface elicit CD4 + Th cell and protective humoral responses. Virology 2002; 302(2):383–92.CrossRefPubMedGoogle Scholar
  71. 71.
    Larke N, Murphy A, Wirblich C et al. Induction of human immunodeficiency virus type 1-specific T-cells by a bluetongue virus tubule-vectored vaccine prime-recombinant modified virus Ankara boost regimen. J Virol 2005; 79(23):14822–33.CrossRefPubMedGoogle Scholar
  72. 72.
    Lindenburg CE, Stolte I, Langendam MW et al. Long-term follow-up: no effect of therapeutic vaccination with HIV-1 p17/p24:Ty virus-like particles on HIV-1 disease progression. Vaccine 2002; 20(17–18):2343–7.CrossRefPubMedGoogle Scholar
  73. 73.
    Kirnbauer R, Taub J, Greenstone H et al. Efficient self-assembly of human papillomavirus type 16 L1 and L1–L2 into virus-like particles. J Virol 1993; 67(12):6929–36.PubMedGoogle Scholar
  74. 74.
    Jiang X, Wang M, Graham DY et al. Expression, self-assembly and anti-genicity of the Norwalk virus capsid protein. J Virol 1992; 66(11):6527–32.PubMedGoogle Scholar
  75. 75.
    Laurent S, Vautherot JF, Madelaine MF et al. Recombinant rabbit hemorrhagic disease virus capsid protein expressed in baculovirus self-assembles into viruslike particles and induces protection. J Virol 1994; 68(10):6794–8.PubMedGoogle Scholar
  76. 76.
    Pletneva MA, Sosnovtsev SV, Sosnovtseva SA et al. Characterization of a recombinant human calicivirus capsid protein expressed in mammalian cells. Virus Res 1998; 55(2):129–41.CrossRefPubMedGoogle Scholar
  77. 77.
    Hale AD, Crawford SE, Ciarlet M et al. Expression and self-assembly of Grimsby virus: anti-genic distinction from Norwalk and Mexico viruses. Clin Diagn Lab Immunol 1999; 6(1):142–5.PubMedGoogle Scholar
  78. 78.
    Belliot G, Noel JS, Li JF et al. Characterization of capsid genes, expressed in the baculovirus system, of three new genetically distinct strains of “Norwalk-like viruses”. J Clin Microbiol 2001; 39(12):4288–95.CrossRefPubMedGoogle Scholar
  79. 79.
    Brown CS, Van Lent JW, Vlak JM et al. Assembly of empty capsids by using baculovirus recombinants expressing human parvovirus B19 structural proteins. J Virol 1991; 65(5):2702–6.PubMedGoogle Scholar
  80. 80.
    Christensen J, Alexandersen S, Bloch B et al. Production of mink enteritis parvovirus empty capsids by expression in a baculovirus vector system: a recombinant vaccine for mink enteritis parvovirus in mink. J Gen Virol 1994; 75(Pt 1):149–55.CrossRefPubMedGoogle Scholar
  81. 81.
    Hoque M, Shimizu N, Ishizu K et al. Chimeric virus-like particle formation of adeno-associated virus. Biochem Biophys Res Commun 1999; 266(2):371–6.CrossRefPubMedGoogle Scholar
  82. 82.
    Koch G, van Roozelaar DJ, Verschueren CA et al. Immunogenic and protective properties of chicken anaemia virus proteins expressed by baculovirus. Vaccine 1995; 13(8):763–70.CrossRefPubMedGoogle Scholar
  83. 83.
    Noteborn MH, Verschueren CA, Koch G et al. Simultaneous expression of recombinant baculovirus-encoded chicken anaemia virus (CAV) proteins VP1 and VP2 is required for formation of the CAV-specific neutralizing epitope. J Gen Virol 1998; 79(Pt 12):3073–7.PubMedGoogle Scholar
  84. 84.
    Albina E, Truong C, Hutet E et al. An experimental model for post-weaning multisystemic wasting syndrome (PMWS) in growing piglets. J Comp Pathol 2001; 125(4):292–303.CrossRefPubMedGoogle Scholar
  85. 85.
    Kim Y, Kim J, Kang K et al. Characterization of the recombinant proteins of porcine circovirus type2 field isolate expressed in the baculovirus system. J Vet Sci 2002; 3(1):19–23.PubMedGoogle Scholar
  86. 86.
    Kosukegawa A, Arisaka F, Takayama M et al. Purification and characterization of virus-like particles and pentamers produced by the expression of SV40 capsid proteins in insect cells. Biochim Biophys Acta 1996; 1290(1):37–45.PubMedGoogle Scholar
  87. 87.
    Chang D, Fung CY, Ou WC et al. Self-assembly of the JC virus major capsid protein, VP1, expressed in insect cells. J Gen Virol 1997; 78(Pt 6):1435–9.PubMedGoogle Scholar
  88. 88.
    Brautigam S, Snezhkov E, Bishop DH. Formation of poliovirus-like particles by recombinant baculoviruses expressing the individual VP0, VP3 and VP1 proteins by comparison to particles derived from the expressed poliovirus polyprotein. Virology 1993; 192(2):512–24.CrossRefPubMedGoogle Scholar
  89. 89.
    Crawford SE, Labbe M, Cohen J et al. Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells. J Virol 1994; 68(9):5945–22.PubMedGoogle Scholar
  90. 90.
    Overton HA, Fujii Y, Price IR et al. The protease and gag gene products of the human immunodeficiency virus: authentic cleavage and post-translational modification in an insect cell expression system. Virology 1989; 170(1):107–116.CrossRefPubMedGoogle Scholar
  91. 91.
    Rasmussen L, Battles JK, Ennis WH et al. Characterization of virus-like particles produced by a recombinant baculovirus containing the gag gene of the bovine immunodeficiency-like virus. Virology 1990; 178(2):435–51.CrossRefPubMedGoogle Scholar
  92. 92.
    Morikawa S, Booth TF, Bishop DH. Analyses of the requirements for the synthesis of virus-like particles by feline immunodeficiency virus gag using baculovirus vectors. Virology 1991; 183(1):288–97.CrossRefPubMedGoogle Scholar
  93. 93.
    Thomsen DR, Meyer AL, Post LE. Expression of feline leukaemia virus gp85 and gag proteins and assembly into virus-like particles using the baculovirus expression vector system. J Gen Virol 1992; 73 (Pt 7):1819–24.CrossRefPubMedGoogle Scholar
  94. 94.
    Rafnar B, Tobin GJ, Nagashima K et al. Immune response to recombinant visna virus Gag and Env precursor proteins synthesized in insect cells. Virus Res 1998; 53(2):107–20.CrossRefPubMedGoogle Scholar
  95. 95.
    Kakker N, Mikhailov M, Nermut MV et al. Bovine leukemia virus Gag particle assembly in insect cells: Formation of chimeric particles by domain-switched leukemia/lentitivirus Gag polyprotein. Virology 1999; 2(265):303–318.Google Scholar
  96. 96.
    Johnson MC, Scobie HM, Vogt VM. PR domain of rous sarcoma virus Gag causes an assembly/budding defect in insect cells. J Virol 2001; 75(9):4407–12.CrossRefPubMedGoogle Scholar
  97. 97.
    Nagy E, Huber P, Krell PJ et al. Synthesis of Newcastle disease virus (NDV)-like envelopes in insect cells infected with a recombinant baculovirus expressing the haemagglutinin-neuraminidase of NDV. J Gen Virol 1991; 72(Pt 3):753–6.CrossRefPubMedGoogle Scholar
  98. 98.
    Betenbaugh M, Yu M, Kuehl K et al. Nucleocapsid-and virus-like particles assemble in cells infected with recombinant baculoviruses or vaccinia viruses expressing the M and the S segments of Hantaan virus. Virus Res 1995; 38(2–3):111–24.CrossRefPubMedGoogle Scholar
  99. 99.
    Fernandez-Arias A, Risco C, Martinez S et al. Expression of ORF A1 of infectious bursal disease virus results in the formation of virus-like particles. J Gen Virol 1998; 79(Pt 5):1047–54.PubMedGoogle Scholar
  100. 100.
    Martinez-Torrecuadrada JL, Saubi N, Pages-Mante A et al. Structure dependent efficacy of infectious bursal disease virus (IBDV) recombinant vaccines. Vaccine 2003; 21(23):3342–50.CrossRefPubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2009

Authors and Affiliations

  1. 1.Department of Infectious and Tropical DiseasesLondon School of Hygiene and Tropical MedicineLondonUK

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