Virus-like particles as a vaccine delivery system: Myths and facts

Advances in Experimental Medicine and Biology

Volumn 655, Issue , 2009, Pages 145-158

  Roy, Polly ^a   Noad, Rob ^b  

^a LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; LIPID; VIRUS LIKE PARTICLE VACCINE; WART VIRUS VACCINE; ANTIGEN; VACCINE; VIRUS VACCINE;

ARTICLE; BACULOVIRUS EXPRESSION SYSTEM; BLUETONGUE; DOSE RESPONSE; DRUG SAFETY; HEPATITIS E; HUMAN; IMMUNOSTIMULATION; INSECT CELL; MINK VIRAL ENTERITIS; NONHUMAN; PARVOVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; SINGLE DRUG DOSE; UNSPECIFIED SIDE EFFECT; UTERINE CERVIX CANCER; VACCINE PRODUCTION; VACCINIA; VIRUS CAPSID; VIRUS ENVELOPE; VIRUS LIKE AGENT; ANIMAL; CHEMISTRY; DRUG DELIVERY SYSTEM; GENE TRANSFER; GENETICS; IMMUNE SYSTEM; IMMUNOLOGY; INSECT; REVIEW; VIRION; VIRUS; VIRUS INFECTION;

PAPILLOMAVIRIDAE;

ANIMALS; ANTIGENS; DRUG DELIVERY SYSTEMS; GENE TRANSFER TECHNIQUES; HUMANS; IMMUNE SYSTEM; INSECTS; LIPIDS; VACCINES; VIRAL VACCINES; VIRION; VIRUS DISEASES; VIRUSES;

EID: 77955255595     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4419-1132-2_11     Document Type: Article

References (100)

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. (Pubitemid 16062513)
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. (Pubitemid 19273350)
3. Gheysen D, Jacobs E, de Foresta F et al. Assembly and release of HIV-l precursor Pr55gag virus-like particles from recombinant baculovirus-infecred insect cells. Cell 1989; 59(1):103-12. (Pubitemid 19248562)
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.
5. Schirmbeck R, Bohm W; Reimann J. Virus-like particles induce MHC class l-resrricted T-cell responses. Lessons learned from the hepatitis B small surface antigen . Intervirology 1996; 39(1-2) :111-9.
6. Paliard X, Liu Y, Wagner R, et al. Priming of strong, broad and long-lived HIV type 1 p55gag-specific CD8+ cytotoxic T-cdls after administration of a virus-like particle vaccine in rhesus macaques. AIDS Res Hum Retroviruses 2000 ; 16(3) :273-82. (Pubitemid 30111963)
7. Murata K, Lechrnann 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. (Pubitemid 36666652)
8. Noad R, Roy P. Virus-like particles as immunogens . Trends Microbiol 2003 ; 11(9):438-44. (Pubitemid 37101484)
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. (Pubitemid 34809674)
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.
11. Kirnbauer R, Booy F. Cheng N et al. Papillomavirus L1 major capsid protein self-assemblesinto virus-like particles that are highly immunogenic. Proc Natl Acad Sci USA 1992; 89(24) :12180-4 . (Pubitemid 23004809)
12. Sasagawa T, Pushko P, Steers G et al. Synthesis and assembly ofvirus-like particles of human papillomaviruses type 6 and type 16 in fission yeast Schizosaccharomyces pornbe. Virology 1995; 206(1) :126-35.
13. Dupuy C, Buzoni-Garel 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 Tlymphocytes in vaginal draining lymph nodes. J Virol 1999; 73 (11):9063-7 1. (Pubitemid 29487059)
14. Zhang LF. Zhou J, Chen S et al. HPV6b virus like particles are potent immunogens without adjuvantin man. Vaccine 2000; 18(11-12) :1051-8.
15. Koutsky LA, Ault KA, Wheder CM et al. A controlled trial of a human papillomavirus type 16 vaccine. N Engl J Med 2002 ; 347(21):1645-51. (Pubitemid 35340782)
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. (Pubitemid 32417699)
17. Harro CD, Pang IT, 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. (Pubitemid 32219815)
18. Franco EL, Harper DM. Vaccination against human papillomavirus infection: a new paradigm in cervical cancer control. Vaccine 2005; 23(17 -18):2388-94. (Pubitemid 40341489)
19. Harper DM, Franco EL, Wheder C et al. Efficacyof a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randornised controlled trial. Lancet 2004; 364(9447):1757-65. (Pubitemid 39488060)
20. Harper DM, Franco EL, Wheder CM et al. Sustained efficacyup 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.
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.
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 .
23. Antonis AF. Bruschke CJ, Rueda P et al. A novd recombinant virus-like particle vaccine for prevention of porcine parvovirus-induced reproductive failure. Vaccine 2006; 24(26) :5481-90. (Pubitemid 43831379)
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. (Pubitemid 28116920)
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. (Pubitemid 32900106)
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. (Pubitemid 29297618)
27. Tacker CO, Sztein MB, Losonsky GA et al. Humoral, mucosal and cdlular immune responses to oral Norwalk virus-like particles in volunteers. Clin Immunol 2003 ; 108(3) :241-7. (Pubitemid 37117370)
28. Li TC, Yarnakawa Y,Suzuki K et al. Expression and self-assembly of empty virus-likeparticles of hepatitis E virus. J Virol 1997: 71(10):7207-13. (Pubitemid 27391654)
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. (Pubitemid 32710299)
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. (Pubitemid 37510267)
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. (Pubitemid 29189897)
32. Caparros-Wanderley W,Clark B, Griffin BE. Effect of dose and long-term storage on the immunogenicity of murine polyomavirus VPl virus-like particles. Vaccine 2004: 22(3-4):352-61.
33. Brautigam S, Snezhkov E, Bishop DH. Formation of poliovirus-like particles by recombinant baculoviruses expressing the individual VPO,VP3 and VP1 proteins by comparison to particles derived from the expressed poliovirus polyprotein. Virology 1993: 192(2):512-24.
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. (Pubitemid 129646917)
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. (Pubitemid 20104888)
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.
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. (Pubitemid 23155619)
38. Roy P. Orbiviruses. In: Knipe DM, Howley PM, eds, Fields' Virology, Fourth Edition. Philadelphia: Lippincott Williams and Wilkins, 2001:1835-1869 .
39. Roy P, French T, Erasmus BJ. Protective efficacyof virus-like particles for bluetongue disease. Vaccine 1992: 10(1):28-32.
40. Roy P, Bishop DH, LeBlois H et al, Long-lasting protection of sheep against bluetongue challenge afier vaccination with virus-like particles: evidence for homologou s and partial heterologous protection. Vaccine 1994: 12(9):805-11. (Pubitemid 24190561)
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. (Pubitemid 20148441)
42. Sabara M, Parker M, Aha P et al. Assembly of double-shelled rotavirusllke particles by simultaneous expression of recombinant VP6 and VP7 proteins . J Virol 1991: 65(12) :6994-7.
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. (Pubitemid 29074757)
44. Madore HP, Estes MK, Zarley CD et al. Biochemical and immunologic comparison ofvirus-like particles for a rotavirus subunit vaccine. Vaccine 1999; 17(19):2461-71. (Pubitemid 29268370)
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. (Pubitemid 34135963)
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. (Pubitemid 43290412)
47. Bertolotri-Ciarlct A, Ciarler M, Crawford SE et al. Immunogenicity and protective efficacyof rotavirus 2/6-virus-likeparticles produced by a dual baculovirusexpressionvector and administered intramuscularly, intranasally, or orally to mice. Vaccine 2003; 21(25-26):3885-900. (Pubitemid 37338216)
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. (Pubitemid 43228716)
49. Agnello D, Herve CA, Lavaux A ee al. Inrrarectal immunization with rotavirus 2/6 virus-like particles indu ces an anti-roravirus immune response localized in the intestinal mucosa and protects against rotavirus infection in mice. J Virol 2006: 80(8):3823-32.
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.
51. Baumert TF, Ito S, Wong DT et al. Hepat itis C virus structural proteins assemble into viruslike particles in insect cells. J Virol 1998; 72(5) :3827-36. (Pubitemid 28188682)
52. Latham T, Galarza JM. Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. J Virol 2001: 75(13) :6154-65. (Pubitemid 32553146)
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. (Pubitemid 38781538)
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. (Pubitemid 39330479)
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. (Pubitemid 38625848)
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. (Pubitemid 30111959)
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. (Pubitemid 26390700)
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 . (Pubitemid 34615593)
59. Lechmann M. Murata K. Satoi J et al. Hepatitis C virus-like particles induce virus-specifichumoral and cellular immune responses in mice. Hepatology 2001; 34(2) :417-23.
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. (Pubitemid 40586463)
61. Pushko P, Tumpey TM. Bu F et al. Influenza virus-like particles comprised of the HA. NA and Ml proteins of H9N2 influenza virus induce protective immune responses in BALBlc mice. Vaccine 2005; 23(50) :5751-9. (Pubitemid 41668881)
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. (Pubitemid 39551003)
63. Beyer T. Herrmann M. ReiserC et al. Bacterial carriers and virus-like-particlesas antigen deliverydevices: role of dendritic cells in antigen presentation. Curr Drug Targets Infect Disord 2001; 1(3):287-302.
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. (Pubitemid 36793024)
65. Sedlik C, Saron M, SarrasecaJ et al. Recombinant parvovirus-like particles as an antigen carrier: a novel nonreplicative exogenous antigen to elicit protective antiviral cytotoxic Tvcells, Proc Natl Acad Sci USA 1997; 94(14) :7503-8. (Pubitemid 27345345)
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. (Pubitemid 40215707)
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.
68. Charpllienne A, Nejmeddine M BM. Parez N, Neumann E. Hewar E, Trugnan G, Cohen J. Individual rotavirus-like particles containing 120 molecules of fluorescent protein are visible in living cells. J Biol Chern 2001; 276(31) :29361-29367.
69. Ghosh MK. Deriaud E. Saron MF et al. Induction of protective anti-viral cyto toxic Tvcells by a tubular structure capable of carrying large foreign sequences. Vaccine 2002; 20(9 -10):1369-77 . (Pubitemid 34131678)
70. Ghosh MK, Borca MY, 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. (Pubitemid 35373866)
71. Larke N. Murphy A. Wirblich C et al. Induction of human immunodeficiency virus type l -specific Tvcells by a bluetongue virus tubule-vectored vaccine prime-recombinant modified virus Ankara boost regimen. J Virol 2005; 79(23) :14822-33.
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-l disease progression . Vaccine 2002; 20(17-18) :2343-7. (Pubitemid 34497045)
73. Kirnbauer R. Taub J. Greenstone H et al. Efficient self-assembly of human papillomavirus type 16 Ll and Ll -L2 into virus-like particles. J Virol 1993; 67(12 ):6929-36. (Pubitemid 23343814)
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.
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. (Pubitemid 24294936)
76. Pletneva MA. Sosnovtsev SV.Sosnovcseva SA et al. Characterization of a recombinant human calicivirus capsid protein expressed in mammalian cells. Virus Res 1998; 55(2) :129-41. (Pubitemid 28345168)
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. (Pubitemid 29035656)
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. (Pubitemid 33117112)
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.
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. (Pubitemid 24033991)
81. Hoque M. Shimizu N. Ishizu K et al. Chimeric virus-like panicle formation of adeno-associared virus. Biochem Biophys Res Commun 1999: 266(2):371-6. (Pubitemid 30028675)
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.
83. Noreborn MH. Verschueren CA. Koch G et al. Simultaneous expression of recombinant baculovirusencoded chicken anaemia virus (CAV) proteins VPl and VP2 is required for formation of the CAV-specific neutralizing epitope . J Gen Virol 1998; 79(Pt 12) 3073-7. (Pubitemid 29002345)
84. Albina E. Truong C. Huret E et al An experimental model for post-weaning multisystemic wasting syndrome (PMWS) in growing piglets. J Comp Pathol 2001; 125(4):292-303. (Pubitemid 34023742)
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.
86. Kosukegawa A. Arisaka F,Takayama M et al. Purification and characterization ofvirus-like particles and pentamers produced by the expression of SV40 capsid proteins in insect cells. Biochim Biophys Acta 1996: 1290( 1):37-45. (Pubitemid 26173323)
87. Chang D. Fung CY. Ou WC et al. Self-assembly of the JC virus major capsid protein . VPl. expressed in insect cells. J Gen Virol 1997; 78(Pt 6):1435-9. (Pubitemid 27281346)
88. Brautigam S. Snezhkov E. Bishop DH. Formation of poliovirus-like particles by recombinant baculoviruses expressing the individual VPO. VP3 and VP1 proteins by comparison to panicles derived from the expressed poliovirus polyprocein. Virology 1993; 192(2):512-24.
89. Crawford SE. Labbe M. Cohen J et al, Characterization of virus-like panicles produced by the expression of rotavirus capsid proteins in insect cells. J Virol 1994: 68(9):5945-22.
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. (Pubitemid 19133969)
91. Rasmussen L. Battles JK. Ennis WH et al. Characterization ofvirus-like panicles produced by a recombinant baculovirus containing the gag gene of the bovine immunodeficiency-like virus. Virology 1990; 178(2) :435-51. (Pubitemid 20349881)
92. Morikawa S. Booth TF. Bishop DH. Analysesof the requirements for the synthesis ofvirus-like particles by feline immunodeficiency virus gag using baculovirus vectors. Virology 1991; 183(1):288-97.
93. Thomsen DR. Meyet 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.
94. Rafuar 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. (Pubitemid 28127848)
95. Kakker N. Mikhailov M. Nermut MV et al. Bovine leukemia virus Gag panicle assembly in insect cells: Formation of chimeric particles by domain-switched leukemia/lentitivirus Gag polyprotein. Virology 1999: 2(265) :303-318.
96. Johnson MC. Scobie HM. Vogr VM. PR domain of rous sarcoma virus Gag causes an assembly/budding defect in insect cells. J Virol 2001; 75(9):4407-12. (Pubitemid 32410154)
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.
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 Hanraan virus. Virus Res 1995; 38(2-3) :111-24.
99. Fernandez-Arias A. Risco C. Martinez S et al, Expression of ORF Al of infectious bursal disease virus results in the formation of virus-like particles. J Gen Virol 1998; 79(Pt 5):1047-54. (Pubitemid 28203845)
100. Martinez-Torrecuadrada JL. Saubi N. Pages-Marne A et al. Structuredcpendent efficacy of infectious bursal disease virus (IBDV) recombinant vaccines. Vaccine 2003; 21(23) :3342-50. (Pubitemid 36700433)