Use of baculovirus expression system for generation of virus-like particles: Successes and challenges

Protein Expression and Purification

Volumn 90, Issue 2, 2013, Pages 104-116

  Liu, Fuxiao ^a,b   Wu, Xiaodong ^a   Li, Lin ^a   Liu, Zengshan ^b   Wang, Zhiliang ^a  

^a OIE Reference Laboratory for Peste des Petits Ruminants National Research Center for Exotic Animal Diseases China Animal Health and Epidemiology Center   (China)

^b JILIN UNIVERSITY   (China)

Author keywords

Baculovirus; Baculovirus expression system; Bioprocess; Insect cells; Post translational modification; Virus like particle

Indexed keywords

HEXAPODA;

RECOMBINANT PROTEIN; VIRUS LIKE PARTICLE VACCINE;

ANIMAL; BACULOVIRUS; BACULOVIRUS EXPRESSION SYSTEM; BIOPROCESS; GENE VECTOR; GENETICS; HUMAN; INSECT CELLS; METABOLISM; POST-TRANSLATIONAL MODIFICATION; PROTEIN PROCESSING; REVIEW; VIRION; VIRUS-LIKE PARTICLE;

BACULOVIRUS; BACULOVIRUS EXPRESSION SYSTEM; BIOPROCESS; INSECT CELLS; POST-TRANSLATIONAL MODIFICATION; VIRUS-LIKE PARTICLE;

ANIMALS; BACULOVIRIDAE; GENETIC VECTORS; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECOMBINANT PROTEINS; VACCINES, VIRUS-LIKE PARTICLE; VIRION;

EID: 84879283150     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2013.05.009     Document Type: Review

References (168)

1. G.E. Smith, M.D. Summers, and M.J. Fraser Production of human beta interferon in insect cells infected with a baculovirus expression vector Mol. Cell. Biol. 3 1983 2156 2165
2. S.A. Miele, M.J. Garavaglia, M.N. Belaich, and P.D. Ghiringhelli Baculovirus: molecular insights on their diversity and conservation Int. J. Evol. Biol. 2011 2011 379424
3. T. Latham, and J.M. Galarza Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins J. Virol. 75 2001 6154 6165
4. L. Croizier, F.X. Jousset, J.C. Veyrunes, M. Lopez-Ferber, M. Bergoin, and G. Croizier Protein requirements for assembly of virus-like particles of Junonia coenia densovirus in insect cells J. Gen. Virol. 81 2000 1605 1613
5. T.J. Kemp, M. Safaeian, A. Hildesheim, Y. Pan, K.J. Penrose, C. Porras, J.T. Schiller, D.R. Lowy, R. Herrero, and L.A. Pinto Kinetic and HPV infection effects on cross-type neutralizing antibody and avidity responses induced by Cervarix((R)) Vaccine 31 2012 165 170
6. J.W. Wang, and R.B. Roden Virus-like particles for the prevention of human papillomavirus-associated malignancies Expert Rev. Vaccines 12 2013 129 141
7. L. Buonaguro, M. Tagliamonte, M.L. Tornesello, and F.M. Buonaguro Developments in virus-like particle-based vaccines for infectious diseases and cancer Expert Rev. Vaccines 10 2011 1569 1583
8. N. Tomiya, M.J. Betenbaugh, and Y.C. Lee Humanization of lepidopteran insect-cell-produced glycoproteins Acc. Chem. Res. 36 2003 613 620
9. J.J. Aumiller, H. Mabashi-Asazuma, A. Hillar, X. Shi, and D.L. Jarvis A new glycoengineered insect cell line with an inducibly mammalianized protein N-glycosylation pathway Glycobiology 22 2012 417 428
10. R.D. Possee, R.B. Hitchman, K.S. Richards, S.G. Mann, E. Siaterli, C.P. Nixon, H. Irving, R. Assenberg, D. Alderton, R.J. Owens, and L.A. King Generation of baculovirus vectors for the high-throughput production of proteins in insect cells Biotechnol. Bioeng. 101 2008 1115 1122
11. V.A. Luckow, S.C. Lee, G.F. Barry, and P.O. Olins Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli J. Virol. 67 1993 4566 4579
12. M. Boudjelal, S.J. Mason, R.M. Katso, J.M. Fleming, J.H. Parham, J.P. Condreay, R.V. Merrihew, and W.J. Cairns The application of BacMam technology in nuclear receptor drug discovery Biotechnol. Annu. Rev. 11 2005 101 125
13. J.A. Fornwald, Q. Lu, D. Wang, and R.S. Ames Gene expression in mammalian cells using BacMam, a modified baculovirus system Methods Mol. Biol. 388 2007 95 114
14. W.S. Chen, O.B. Villaflores, T.R. Jinn, M.T. Chan, Y.C. Chang, and T.Y. Wu Expression of recombinant human interferon-gamma with antiviral activity in the bi-cistronic baculovirus-insect/larval system Biosci. Biotechnol. Biochem. 75 2011 1342 1348
15. A. Yousefi, F. Fotouhi, S. Hosseinzadeh, M.T. Kheiri, B. Farahmand, S. Montazeri, and F. Mousavi Expression of antigenic determinants of the haemagglutinin large subunit of novel influenza virus in insect cells Folia Biol. (Praha) 58 2012 151 156
16. U. Ahrens, V. Kaden, C. Drexler, and N. Visser Efficacy of the classical swine fever (CSF) marker vaccine Porcilis Pesti in pregnant sows Vet. Microbiol. 77 2000 83 97
17. M.G. Aucoin, J.A. Mena, and A.A. Kamen Bioprocessing of baculovirus vectors: a review Curr. Gene Ther. 10 2010 174 186
18. J.J. Treanor, H. El Sahly, J. King, I. Graham, R. Izikson, R. Kohberger, P. Patriarca, and M. Cox Protective efficacy of a trivalent recombinant hemagglutinin protein vaccine (FluBlok(R)) against influenza in healthy adults: a randomized, placebo-controlled trial Vaccine 29 2011 7733 7739
19. R. Baxter, P.A. Patriarca, K. Ensor, R. Izikson, K.L. Goldenthal, and M.M. Cox Evaluation of the safety, reactogenicity and immunogenicity of FluBlok(R) trivalent recombinant baculovirus-expressed hemagglutinin influenza vaccine administered intramuscularly to healthy adults 50-64 years of age Vaccine 29 2011 2272 2278
20. D.R. Thomsen, A.L. Meyer, and L.E. Post Expression of feline leukaemia virus gp85 and gag proteins and assembly into virus-like particles using the baculovirus expression vector system J. Gen. Virol. 73 Pt 7 1992 1819 1824
21. X. Jiang, M. Wang, D.Y. Graham, and M.K. Estes Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein J. Virol. 66 1992 6527 6532
22. C. Martinez, K. Dalsgaard, J.A. Lopez de Turiso, E. Cortes, C. Vela, and J.I. Casal Production of porcine parvovirus empty capsids with high immunogenic activity Vaccine 10 1992 684 690
23. A.S. Belyaev, and P. Roy Development of baculovirus triple and quadruple expression vectors: co-expression of three or four bluetongue virus proteins and the synthesis of bluetongue virus-like particles in insect cells Nucleic Acids Res. 21 1993 1219 1223
24. S. Brautigam, E. Snezhkov, and D.H. Bishop 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 192 1993 512 524
25. R. Kirnbauer, J. Taub, H. Greenstone, R. Roden, M. Durst, L. Gissmann, D.R. Lowy, and J.T. Schiller Efficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles J. Virol. 67 1993 6929 6936
26. J.D. Tatman, V.G. Preston, P. Nicholson, R.M. Elliott, and F.J. Rixon Assembly of herpes simplex virus type 1 capsids using a panel of recombinant baculoviruses J. Gen. Virol. 75 Pt 5 1994 1101 1113
27. S.E. Crawford, M. Labbe, J. Cohen, M.H. Burroughs, Y.J. Zhou, and M.K. Estes Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells J. Virol. 68 1994 5945 5952
28. C. Sedlik, M. Saron, J. Sarraseca, I. Casal, and C. Leclerc Recombinant parvovirus-like particles as an antigen carrier: a novel nonreplicative exogenous antigen to elicit protective antiviral cytotoxic T cells Proc. Natl. Acad. Sci. U.S.A. 94 1997 7503 7508
29. S. Maree, S. Durbach, and H. Huismans Intracellular production of African horsesickness virus core-like particles by expression of the two major core proteins, VP3 and VP7, in insect cells J. Gen. Virol. 79 1998 333 337
30. L. Buonaguro, F.M. Buonaguro, M.L. Tornesello, D. Mantas, E. Beth-Giraldo, R. Wagner, S. Michelson, M.C. Prevost, H. Wolf, and G. Giraldo High efficient production of Pr55(gag) virus-like particles expressing multiple HIV-1 epitopes, including a gp120 protein derived from an Ugandan HIV-1 isolate of subtype A Antiviral Res. 49 2001 35 47
31. Y. Ho, P.H. Lin, C.Y. Liu, S.P. Lee, and Y.C. Chao Assembly of human severe acute respiratory syndrome coronavirus-like particles Biochem. Biophys. Res. Commun. 318 2004 833 838
32. S. Caballero, S. Guix, E. Ribes, A. Bosch, and R.M. Pinto Structural requirements of astrovirus virus-like particles assembled in insect cells J. Virol. 78 2004 13285 13292
33. Y.C. Chung, J.H. Huang, C.W. Lai, H.C. Sheng, S.R. Shih, M.S. Ho, and Y.C. Hu Expression, purification and characterization of enterovirus-71 virus-like particles World J. Gastroenterol. 12 2006 921 927
34. B. Di Martino, F. Marsilio, and P. Roy Assembly of feline calicivirus-like particle and its immunogenicity Vet. Microbiol. 120 2007 173 178
35. A. Kosukegawa, F. Arisaka, M. Takayama, H. Yajima, A. Kaidow, and H. Handa Purification and characterization of virus-like particles and pentamers produced by the expression of SV40 capsid proteins in insect cells Biochim. Biophys. Acta 1290 1996 37 45
36. L. Liu, C.C. Celma, and P. Roy Rift Valley fever virus structural proteins: expression, characterization and assembly of recombinant proteins Virol. J. 5 2008 82
37. L.J. Liu, T. Suzuki, H. Tsunemitsu, M. Kataoka, N. Ngata, N. Takeda, T. Wakita, T. Miyamura, and T.C. Li Efficient production of type 2 porcine circovirus-like particles by a recombinant baculovirus Arch. Virol. 153 2008 2291 2295
38. P. Tao, M. Luo, D. Zhu, S. Qu, Z. Yang, M. Gao, D. Guo, and Z. Pan Virus-like particle vaccine comprised of the HA, NA, and M1 proteins of an avian isolated H5N1 influenza virus induces protective immunity against homologous and heterologous strains in mice Viral Immunol. 22 2009 273 281
39. Y. Sun, R. Carrion Jr., L. Ye, Z. Wen, Y.T. Ro, K. Brasky, A.E. Ticer, E.E. Schwegler, J.L. Patterson, R.W. Compans, and C. Yang Protection against lethal challenge by Ebola virus-like particles produced in insect cells Virology 383 2009 12 21
40. H.Y. Jeoung, W.H. Lee, W. Jeong, B.H. Shin, H.W. Choi, H.S. Lee, and D.J. An Immunogenicity and safety of the virus-like particle of the porcine encephalomyocarditis virus in pig Virol. J. 8 2011 170
41. V.K. Deo, Y. Tsuji, T. Yasuda, T. Kato, N. Sakamoto, H. Suzuki, and E.Y. Park Expression of an RSV-gag virus-like particle in insect cell lines and silkworm larvae J. Virol. Methods 177 2011 147 152
42. H. Yamaji, M. Nakamura, M. Kuwahara, Y. Takahashi, T. Katsuda, and E. Konishi Efficient production of Japanese encephalitis virus-like particles by recombinant lepidopteran insect cells Appl Microbiol Biotechnol 97 2013 1071 1079
43. Q. Liu, K. Yan, Y. Feng, X. Huang, Z. Ku, Y. Cai, F. Liu, J. Shi, and Z. Huang A virus-like particle vaccine for coxsackievirus A16 potently elicits neutralizing antibodies that protect mice against lethal challenge Vaccine 30 2012 6642 6648
44. B. Mohana Subramanian, M. Madhanmohan, R. Sriraman, R.V. Chandrasekhar Reddy, S. Yuvaraj, K. Manikumar, S. Rajalakshmi, S.B. Nagendrakumar, S.K. Rana, and V.A. Srinivasan Development of foot-and-mouth disease virus (FMDV) serotype O virus-like-particles (VLPs) vaccine and evaluation of its potency Antivir Res 96 2012 288 295
45. S.W. Metz, J. Gardner, C. Geertsema, T.T. Le, L. Goh, J.M. Vlak, A. Suhrbier, and G.P. Pijlman Effective chikungunya virus-like particle vaccine produced in insect cells PLoS Negl. Trop. Dis. 7 2013 e2124
46. S. Pillay, A. Meyers, A.L. Williamson, and E.P. Rybicki Optimization of chimeric HIV-1 virus-like particle production in a baculovirus-insect cell expression system Biotechnol. Prog. 25 2009 1153 1160
47. A. Bertolotti-Ciarlet, L.J. White, R. Chen, B.V. Prasad, and M.K. Estes Structural requirements for the assembly of Norwalk virus-like particles J. Virol. 76 2002 4044 4055
48. H. Tsukamoto, M.A. Kawano, T. Inoue, T. Enomoto, R.U. Takahashi, N. Yokoyama, N. Yamamoto, T. Imai, K. Kataoka, Y. Yamaguchi, and H. Handa Evidence that SV40 VP1-DNA interactions contribute to the assembly of 40-nm spherical viral particles Genes Cells 12 2007 1267 1279
49. E.A. Hewat, T.F. Booth, and P. Roy Structure of correctly self-assembled bluetongue virus-like particles J. Struct. Biol. 112 1994 183 191
50. T.J. French, J.J. Marshall, and P. Roy Assembly of double-shelled, viruslike particles of bluetongue virus by the simultaneous expression of four structural proteins J. Virol. 64 1990 5695 5700
51. T.J. French, and P. Roy Synthesis of bluetongue virus (BTV) corelike particles by a recombinant baculovirus expressing the two major structural core proteins of BTV J. Virol. 64 1990 1530 1536
52. L.A. Palomares, J.A. Mena, and O.T. Ramirez Simultaneous expression of recombinant proteins in the insect cell-baculovirus system: production of virus-like particles Methods 56 2012 389 395
53. M.J. Adang, and L.K. Miller Molecular cloning of DNA complementary to mRNA of the baculovirus Autographa californica nuclear polyhedrosis virus: location and gene products of RNA transcripts found late in infection J. Virol. 44 1982 782 793
54. G.E. Smith, M.J. Fraser, and M.D. Summers Molecular engineering of the Autographa californica nuclear polyhedrosis virus genome: deletion mutations within the polyhedrin gene J. Virol. 46 1983 584 593
55. J.M. Vlak, F.A. Klinkenberg, K.J. Zaal, M. Usmany, E.C. Klinge-Roode, J.B. Geervliet, J. Roosien, and J.W. van Lent Functional studies on the p10 gene of Autographa californica nuclear polyhedrosis virus using a recombinant expressing a p10-beta-galactosidase fusion gene J. Gen. Virol. 69 Pt 4 1988 765 776
56. T.J. Wickham, T. Davis, R.R. Granados, M.L. Shuler, and H.A. Wood Screening of insect cell lines for the production of recombinant proteins and infectious virus in the baculovirus expression system Biotechnol. Prog. 8 1992 391 396
57. P.W. Roelvink, M.M. van Meer, C.A. de Kort, R.D. Possee, B.D. Hammock, and J.M. Vlak Dissimilar expression of Autographa californica multiple nucleocapsid nuclear polyhedrosis virus polyhedrin and p10 genes J. Gen. Virol. 73 Pt 6 1992 1481 1489
58. B.C. Bonning, P.W. Roelvink, J.M. Vlak, R.D. Possee, and B.D. Hammock Superior expression of juvenile hormone esterase and beta-galactosidase from the basic protein promoter of Autographa californica nuclear polyhedrosis virus compared to the p10 protein and polyhedrin promoters J. Gen. Virol. 75 Pt 7 1994 1551 1556
59. M.R. DiFalco, E. Bakopanos, M. Patricelli, G. Chan, and L.F. Congote The influence of various insect cell lines, p10 and polyhedrin promoters in the production of secreted insulin-like growth factor-interleukin-3 chimeras in the baculovirus expression system J. Biotechnol. 56 1997 49 56
60. E. Pajot-Augy, V. Bozon, J.J. Remy, L. Couture, and R. Salesse Critical relationship between glycosylation of recombinant lutropin receptor ectodomain and its secretion from baculovirus-infected insect cells Eur. J. Biochem. 260 1999 635 648
61. R.E. Hawtin, T. Zarkowska, K. Arnold, C.J. Thomas, G.W. Gooday, L.A. King, J.A. Kuzio, and R.D. Possee Liquefaction of Autographa californica nucleopolyhedrovirus-infected insects is dependent on the integrity of virus-encoded chitinase and cathepsin genes Virology 238 1997 243 253
62. J.M. Slack, J. Kuzio, and P. Faulkner Characterization of v-cath, a cathepsin L-like proteinase expressed by the baculovirus Autographa californica multiple nuclear polyhedrosis virus J. Gen. Virol. 76 Pt 5 1995 1091 1098
63. S. Sokolenko, S. George, A. Wagner, A. Tuladhar, J.M. Andrich, and M.G. Aucoin Co-expression vs. co-infection using baculovirus expression vectors in insect cell culture: benefits and drawbacks Biotechnol. Adv. 30 2012 766 781
64. H. Chaabihi, M.H. Ogliastro, M. Martin, C. Giraud, G. Devauchelle, and M. Cerutti Competition between baculovirus polyhedrin and p10 gene expression during infection of insect cells J. Virol. 67 1993 2664 2671
65. S. Trowitzsch, C. Bieniossek, Y. Nie, F. Garzoni, and I. Berger New baculovirus expression tools for recombinant protein complex production J. Struct. Biol. 172 2010 45 54
66. S. Trowitzsch, D. Palmberger, D. Fitzgerald, Y. Takagi, and I. Berger MultiBac complexomics Expert Rev. Proteomics 9 2012 363 373
67. C. Bieniossek, T. Imasaki, Y. Takagi, and I. Berger MultiBac: expanding the research toolbox for multiprotein complexes Trends Biochem. Sci. 37 2012 49 57
68. D.J. Fitzgerald, P. Berger, C. Schaffitzel, K. Yamada, T.J. Richmond, and I. Berger Protein complex expression by using multigene baculoviral vectors Nat. Meth. 3 2006 1021 1032
69. I. Berger, D.J. Fitzgerald, and T.J. Richmond Baculovirus expression system for heterologous multiprotein complexes Nat. Biotechnol. 22 2004 1583 1587
70. T. Ohkawa, K. Majima, and S. Maeda A cysteine protease encoded by the baculovirus Bombyx mori nuclear polyhedrosis virus J. Virol. 68 1994 6619 6625
71. R.B. Hitchman, R.D. Possee, E. Siaterli, K.S. Richards, A.J. Clayton, L.E. Bird, R.J. Owens, D.C. Carpentier, F.L. King, J.O. Danquah, K.G. Spink, and L.A. King Improved expression of secreted and membrane-targeted proteins in insect cells Biotechnol. Appl. Biochem. 56 2010 85 93
72. R.B. Hitchman, R.D. Possee, A.T. Crombie, A. Chambers, K. Ho, E. Siaterli, O. Lissina, H. Sternard, R. Novy, K. Loomis, L.E. Bird, R.J. Owens, and L.A. King Genetic modification of a baculovirus vector for increased expression in insect cells Cell Biol. Toxicol. 26 2010 57 68
73. K.S. Lee, Y.H. Je, S.D. Woo, H.D. Sohn, and B.R. Jin Production of a cellulase in silkworm larvae using a recombinant Bombyx mori nucleopolyhedrovirus lacking the virus-encoded chitinase and cathepsin genes Biotechnol. Lett. 28 2006 645 650
74. T. Suzuki, T. Kanaya, H. Okazaki, K. Ogawa, A. Usami, H. Watanabe, K. Kadono-Okuda, M. Yamakawa, H. Sato, H. Mori, S. Takahashi, and K. Oda Efficient protein production using a Bombyx mori nuclear polyhedrosis virus lacking the cysteine proteinase gene J. Gen. Virol. 78 Pt 12 1997 3073 3080
75. E. van Anken, and I. Braakman Versatility of the endoplasmic reticulum protein folding factory Crit. Rev. Biochem. Mol. Biol. 40 2005 191 228
76. E. Ailor, and M.J. Betenbaugh Modifying secretion and post-translational processing in insect cells Curr. Opin. Biotechnol. 10 1999 142 145
77. T. Lenhard, and H. Reilander Engineering the folding pathway of insect cells: generation of a stably transformed insect cell line showing improved folding of a recombinant membrane protein Biochem. Biophys. Res. Commun. 238 1997 823 830
78. M. Nakajima, T. Kato, S. Kanamasa, and E.Y. Park Molecular chaperone-assisted production of human alpha-1,4-N-acetylglucosaminyltransferase in silkworm larvae using recombinant BmNPV bacmids Mol. Biotechnol. 43 2009 67 75
79. L. Zhang, G. Wu, C.G. Tate, A. Lookene, and G. Olivecrona Calreticulin promotes folding/dimerization of human lipoprotein lipase expressed in insect cells (sf21) J. Biol. Chem. 278 2003 29344 29351
80. T. Kato, T. Murata, T. Usui, and E.Y. Park Improvement of the production of GFPuv-beta1,3-N-acetylglucosaminyltransferase 2 fusion protein using a molecular chaperone-assisted insect-cell-based expression system Biotechnol. Bioeng. 89 2005 424 433
81. C.G. Tate, E. Whiteley, and M.J. Betenbaugh Molecular chaperones stimulate the functional expression of the cocaine-sensitive serotonin transporter J. Biol. Chem. 274 1999 17551 17558
82. N. Yokoyama, M. Hirata, K. Ohtsuka, Y. Nishiyama, K. Fujii, M. Fujita, K. Kuzushima, T. Kiyono, and T. Tsurumi Co-expression of human chaperone Hsp70 and Hsdj or Hsp40 co-factor increases solubility of overexpressed target proteins in insect cells Biochim. Biophys. Acta 1493 2000 119 124
83. M.J. Betenbaugh, E. Ailor, E. Whiteley, P. Hinderliter, and T.A. Hsu Chaperone and foldase coexpression in the baculovirus-insect cell expression system Cytotechnology 20 1996 149 159
84. N.J. Colley, E.K. Baker, M.A. Stamnes, and C.S. Zuker The cyclophilin homolog ninaA is required in the secretory pathway Cell 67 1991 255 263
85. N. Tomiya, E. Ailor, S.M. Lawrence, M.J. Betenbaugh, and Y.C. Lee Determination of nucleotides and sugar nucleotides involved in protein glycosylation by high-performance anion-exchange chromatography: sugar nucleotide contents in cultured insect cells and mammalian cells Anal. Biochem. 293 2001 129 137
86. A.M. Toth, C. Geisler, J.J. Aumiller, and D.L. Jarvis Factors affecting recombinant Western equine encephalitis virus glycoprotein production in the baculovirus system Protein Expr. Purif. 80 2011 274 282
87. A.A. El-Kholy, E.R. Abdou, D.I. Rady, and M.M. Elseafy Baculovirus expression and diagnostic utility of the glycoprotein E of bovine herpesvirus-1.1 Egyptian strain "Abu-Hammad" J. Virol. Methods 191 2013 33 40
88. M. Rouhbakhsh, R. Halabian, N. Masroori, M. Mohammadi Pour, P. Bahmani, A. Mohammadi Roush, A. Jahanian-Najafabadi, and M. Habibi Roudkenar Isolation, Cloning and High- Level Expression of Neutrophil Gelatinase-Associated Lipocalin Lipocalin2 by Baculovirus Expression System through Gateway Technology Iran J. Basic Med. Sci. 15 2012 845 852
89. D.L. Jarvis Developing baculovirus-insect cell expression systems for humanized recombinant glycoprotein production Virology 310 2003 1 7
90. F. Altmann, E. Staudacher, I.B. Wilson, and L. Marz Insect cells as hosts for the expression of recombinant glycoproteins Glycoconj. J. 16 1999 109 123
91. S. Watanabe, T. Kokuho, H. Takahashi, M. Takahashi, T. Kubota, and S. Inumaru Sialylation of N-glycans on the recombinant proteins expressed by a baculovirus-insect cell system under beta-N-acetylglucosaminidase inhibition J. Biol. Chem. 277 2002 5090 5093
92. N. Tomiya, S. Narang, Y.C. Lee, and M.J. Betenbaugh Comparing N-glycan processing in mammalian cell lines to native and engineered lepidopteran insect cell lines Glycoconj J 21 2004 343 360
93. X. Cheng, R.N. Cole, J. Zaia, and G.W. Hart Alternative O-glycosylation/O-phosphorylation of the murine estrogen receptor beta Biochemistry (Mosc) 39 2000 11609 11620
94. X. Cheng, and G.W. Hart Alternative O-glycosylation/O-phosphorylation of serine-16 in murine estrogen receptor beta: post-translational regulation of turnover and transactivation activity J. Biol. Chem. 276 2001 10570 10575
95. K. Sugyiama, H. Ahorn, I. Maurer-Fogy, and T. Voss Expression of human interferon-alpha 2 in Sf9 cells. Characterization of O-linked glycosylation and protein heterogeneities Eur. J. Biochem. 217 1993 921 927
96. M. Lopez, D. Tetaert, S. Juliant, M. Gazon, M. Cerutti, A. Verbert, and P. Delannoy O-glycosylation potential of lepidopteran insect cell lines Biochim. Biophys. Acta 1427 1999 49 61
97. T. Okada, H. Ihara, R. Ito, M. Nakano, K. Matsumoto, Y. Yamaguchi, N. Taniguchi, and Y. Ikeda N-Glycosylation engineering of lepidopteran insect cells by the introduction of the beta1,4-N-acetylglucosaminyltransferase III gene Glycobiology 20 2010 1147 1159
98. D. Palmberger, I.B. Wilson, I. Berger, R. Grabherr, and D. Rendic SweetBac: a new approach for the production of mammalianised glycoproteins in insect cells PLoS One 7 2012 e34226
99. E.Y. Yun, T.W. Goo, S.W. Kim, K.H. Choi, J.S. Hwang, S.W. Kang, and O.Y. Kwon Galatosylation and sialylation of mammalian glycoproteins produced by baculovirus-madiated gene expression in insect cells Biotechnol. Lett. 27 2005 1035 1039
100. K.H. Chang, J.M. Yang, H.O. Chun, and I.S. Chung Enhanced activity of recombinant beta-secretase from Drosophila melanogaster S2 cells transformed with cDNAs encoding human beta1,4-galactosyltransferase and Galbeta1,4-GlcNAc alpha2,6-sialyltransferase J. Biotechnol. 116 2005 359 367
101. H. Mabashi-Asazuma, X. Shi, C. Geisler, C.W. Kuo, K.H. Khoo, and D.L. Jarvis Impact of a human CMP-sialic acid transporter on recombinant glycoprotein sialylation in glycoengineered insect cells Glycobiology 23 2013 199 210
102. S.A. Chen, T.Y. Lee, and Y.Y. Ou Incorporating significant amino acid pairs to identify O-linked glycosylation sites on transmembrane proteins and non-transmembrane proteins BMC Bioinformatics 11 2010 536
103. W. Dowling, E. Thompson, C. Badger, J.L. Mellquist, A.R. Garrison, J.M. Smith, J. Paragas, R.J. Hogan, and C. Schmaljohn Influences of glycosylation on antigenicity, immunogenicity, and protective efficacy of ebola virus GP DNA vaccines J. Virol. 81 2007 1821 1837
104. C.C. Wang, J.R. Chen, Y.C. Tseng, C.H. Hsu, Y.F. Hung, S.W. Chen, C.M. Chen, K.H. Khoo, T.J. Cheng, Y.S. Cheng, J.T. Jan, C.Y. Wu, C. Ma, and C.H. Wong Glycans on influenza hemagglutinin affect receptor binding and immune response Proc. Natl. Acad. Sci. U.S.A. 106 2009 18137 18142
105. B.K. Gavrilov, K. Rogers, I.J. Fernandez-Sainz, L.G. Holinka, M.V. Borca, and G.R. Risatti Effects of glycosylation on antigenicity and immunogenicity of classical swine fever virus envelope proteins Virology 420 2011 135 145
106. A. Fournillier, C. Wychowski, D. Boucreux, T.F. Baumert, J.C. Meunier, D. Jacobs, S. Muguet, E. Depla, and G. Inchauspe Induction of hepatitis C virus E1 envelope protein-specific immune response can be enhanced by mutation of N-glycosylation sites J. Virol. 75 2001 12088 12097
107. F. Helle, G. Vieyres, L. Elkrief, C.I. Popescu, C. Wychowski, V. Descamps, S. Castelain, P. Roingeard, G. Duverlie, and J. Dubuisson Role of N-linked glycans in the functions of hepatitis C virus envelope proteins incorporated into infectious virions J. Virol. 84 2010 11905 11915
108. Y.S. Pan, H.J. Wei, C.C. Chang, C.H. Lin, T.S. Wei, S.C. Wu, and D.K. Chang Construction and characterization of insect cell-derived influenza VLP: cell binding, fusion, and EGFP incorporation J. Biomed. Biotechnol. 2010 2010 506363
109. J.G. Choi, M.C. Kim, H.M. Kang, K.I. Kim, K.J. Lee, C.K. Park, J.H. Kwon, J.H. Kim, and Y.J. Lee Protective efficacy of baculovirus-derived influenza virus-like particles bearing H5 HA alone or in combination with M1 in chickens Vet. Microbiol. 162 2013 623 630
110. F.S. Quan, C. Huang, R.W. Compans, and S.M. Kang Virus-like particle vaccine induces protective immunity against homologous and heterologous strains of influenza virus J. Virol. 81 2007 3514 3524
111. A. Roldao, M.C. Mellado, L.R. Castilho, M.J. Carrondo, and P.M. Alves Virus-like particles in vaccine development Expert Rev. Vaccines 9 2010 1149 1176
112. F. Krammer, S. Nakowitsch, P. Messner, D. Palmberger, B. Ferko, and R. Grabherr Swine-origin pandemic H1N1 influenza virus-like particles produced in insect cells induce hemagglutination inhibiting antibodies in BALB/c mice Biotechnol. J. 5 2010 17 23
113. Z. Wen, L. Ye, Y. Gao, L. Pan, K. Dong, Z. Bu, R.W. Compans, and C. Yang Immunization by influenza virus-like particles protects aged mice against lethal influenza virus challenge Antiviral Res. 84 2009 215 224
114. X. Gao, W. Wang, Y. Li, S. Zhang, Y. Duan, L. Xing, Z. Zhao, P. Zhang, Z. Li, R. Li, X. Wang, and P. Yang Enhanced Influenza VLP vaccines comprising matrix-2 ectodomain and nucleoprotein epitopes protects mice from lethal challenge Antiviral Res. 98 2013 4 11
115. C.Y. Wu, Y.C. Yeh, J.T. Chan, Y.C. Yang, J.R. Yang, M.T. Liu, H.S. Wu, and P.W. Hsiao A VLP vaccine induces broad-spectrum cross-protective antibody immunity against H5N1 and H1N1 subtypes of influenza A virus PLoS One 7 2012 e42363
116. A.C. Steven, J.F. Conway, N. Cheng, N.R. Watts, D.M. Belnap, A. Harris, S.J. Stahl, and P.T. Wingfield Structure, assembly, and antigenicity of hepatitis B virus capsid proteins Adv. Virus Res. 64 2005 125 164
117. J. Dubuisson, and C.M. Rice Hepatitis C virus glycoprotein folding: disulfide bond formation and association with calnexin J. Virol. 70 1996 778 786
118. M. Sapp, C. Fligge, I. Petzak, J.R. Harris, and R.E. Streeck Papillomavirus assembly requires trimerization of the major capsid protein by disulfides between two highly conserved cysteines J. Virol. 72 1998 6186 6189
119. B.C. Bundy, and J.R. Swartz Efficient disulfide bond formation in virus-like particles J. Biotechnol. 154 2011 230 239
120. S. Laurent, J.F. Vautherot, M.F. Madelaine, G. Le Gall, and D. Rasschaert Recombinant rabbit hemorrhagic disease virus capsid protein expressed in baculovirus self-assembles into viruslike particles and induces protection J. Virol. 68 1994 6794 6798
121. M. Sapp, C. Volpers, M. Muller, and R.E. Streeck Organization of the major and minor capsid proteins in human papillomavirus type 33 virus-like particles J. Gen. Virol. 76 Pt 9 1995 2407 2412
122. K.I. Ishizu, H. Watanabe, S.I. Han, S.N. Kanesashi, M. Hoque, H. Yajima, K. Kataoka, and H. Handa Roles of disulfide linkage and calcium ion-mediated interactions in assembly and disassembly of virus-like particles composed of simian virus 40 VP1 capsid protein J. Virol. 75 2001 61 72
123. Y. Kushima, T. Wakita, and M. Hijikata A disulfide-bonded dimer of the core protein of hepatitis C virus is important for virus-like particle production J. Virol. 84 2010 9118 9127
124. S.H. Choi, S.Y. Kim, K.J. Park, Y.J. Kim, and S.B. Hwang Hepatitis C virus core protein is efficiently released into the culture medium in insect cells J. Biochem. Mol. Biol. 37 2004 735 740
125. Y. Tsuchiya, K. Morioka, J. Shirai, and K. Yoshida Structural requirements of signal peptide in insect cell Nucleic Acids Symp. Ser. (Oxf) 2004 181 182
126. M. Olczak, and T. Olczak Comparison of different signal peptides for protein secretion in nonlytic insect cell system Anal. Biochem. 359 2006 45 53
127. D.R. O'Reilly, L.K. Miller, and V.A. Luckow Baculovirus Expression Vectors: A Laboratory Manual 1994 Oxford University Press New York
128. D.C. Tessier, D.Y. Thomas, H.E. Khouri, F. Laliberte, and T. Vernet Enhanced secretion from insect cells of a foreign protein fused to the honeybee melittin signal peptide Gene 98 1991 177 183
129. D.L. Jarvis, M.D. Summers, A. Garcia Jr., and D.A. Bohlmeyer Influence of different signal peptides and prosequences on expression and secretion of human tissue plasminogen activator in the baculovirus system J. Biol. Chem. 268 1993 16754 16762
130. J.A. Veenstra Mono- and dibasic proteolytic cleavage sites in insect neuroendocrine peptide precursors Arch. Insect Biochem. Physiol. 43 2000 49 63
131. P.E. Cruz, P.C. Martins, P.M. Alves, C.C. Peixoto, H. Santos, J.L. Moreira, and M.J. Carrondo Proteolytic activity in infected and noninfected insect cells: degradation of HIV-1 Pr55gag particles Biotechnol. Bioeng. 65 1999 133 143
132. K. Kuroda, M. Veit, and H.D. Klenk Retarded processing of influenza virus hemagglutinin in insect cells Virology 180 1991 159 165
133. L.F. Cassidy, D.S. Lyles, and J.S. Abramson Depression of polymorphonuclear leukocyte functions by purified influenza virus hemagglutinin and sialic acid-binding lectins J. Immunol. 142 1989 4401 4406
134. F.M. Pringle, J. Kalmakoff, and V.K. Ward Analysis of the capsid processing strategy of Thosea asigna virus using baculovirus expression of virus-like particles J. Gen. Virol. 82 2001 259 266
135. A. Schneemann, R. Dasgupta, J.E. Johnson, and R.R. Rueckert Use of recombinant baculoviruses in synthesis of morphologically distinct viruslike particles of flock house virus, a nodavirus J. Virol. 67 1993 2756 2763
136. A. Palucha, A. Loniewska, S. Satheshkumar, A.M. Boguszewska-Chachulska, M. Umashankar, M. Milner, A.L. Haenni, and H.S. Savithri Virus-like particles: models for assembly studies and foreign epitope carriers Prog. Nucleic Acid Res. Mol. Biol. 80 2005 135 168
137. R.A. Bright, D.M. Carter, S. Daniluk, F.R. Toapanta, A. Ahmad, V. Gavrilov, M. Massare, P. Pushko, N. Mytle, T. Rowe, G. Smith, and T.M. Ross Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin Vaccine 25 2007 3871 3878
138. K. Mahmood, R.A. Bright, N. Mytle, D.M. Carter, C.J. Crevar, J.E. Achenbach, P.M. Heaton, T.M. Tumpey, and T.M. Ross H5N1 VLP vaccine induced protection in ferrets against lethal challenge with highly pathogenic H5N1 influenza viruses Vaccine 26 2008 5393 5399
139. P. Pushko, T.M. Tumpey, F. Bu, J. Knell, R. Robinson, and G. Smith 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 23 2005 5751 5759
140. F. Krammer, T. Schinko, D. Palmberger, C. Tauer, P. Messner, and R. Grabherr 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 2010 226 234
141. J.T. Schiller, X. Castellsague, L.L. Villa, and A. Hildesheim An update of prophylactic human papillomavirus L1 virus-like particle vaccine clinical trial results Vaccine 26 Suppl. 10 2008 K53 K61
142. A. Usami, S. Ishiyama, C. Enomoto, H. Okazaki, K. Higuchi, M. Ikeda, T. Yamamoto, M. Sugai, Y. Ishikawa, Y. Hosaka, T. Koyama, Y. Tobita, S. Ebihara, T. Mochizuki, Y. Asano, and H. Nagaya Comparison of recombinant protein expression in a baculovirus system in insect cells (Sf9) and silkworm J. Biochem. 149 2011 219 227
143. Y. Jiang, F. Deng, H. Wang, and Z. Hu An extensive analysis on the global codon usage pattern of baculoviruses Arch. Virol. 153 2008 2273 2282
144. D.B. Levin, and B. Whittome Codon usage in nucleopolyhedroviruses J. Gen. Virol. 81 2000 2313 2325
145. L.A. Palomares, and O.T. Ramírez Challenges for the production of virus-like particles in insect cells: the case of rotavirus-like particles Biochem. Eng. J. 45 2009 158 167
146. H.L. Vieira, C. Estevao, A. Roldao, C.C. Peixoto, M.F. Sousa, P.E. Cruz, M.J. Carrondo, and P.M. Alves Triple layered rotavirus VLP production: kinetics of vector replication, mRNA stability and recombinant protein production J. Biotechnol. 120 2005 72 82
147. A. Roldão, H.L.A. Vieira, P.M. Alves, R. Oliveira, and M.J.T. Carrondo Intracellular dynamics in rotavirus-like particles production: evaluation of multigene and monocistronic infection strategies Process Biochem. 41 2006 2188 2199
148. F. Krammer, T. Schinko, P. Messner, D. Palmberger, B. Ferko, and R. Grabherr Influenza virus-like particles as an antigen-carrier platform for the ESAT-6 epitope of Mycobacterium tuberculosis J. Virol. Methods 167 2010 17 22
149. P. Licari, and J.E. Bailey Modeling the population dynamics of baculovirus-infected insect cells: optimizing infection strategies for enhanced recombinant protein yields Biotechnol. Bioeng. 39 1992 432 441
150. J.A. Mena, O.T. Ramirez, and L.A. Palomares Population kinetics during simultaneous infection of insect cells with two different recombinant baculoviruses for the production of rotavirus-like particles BMC Biotechnol. 7 2007 39
151. Y.C. Hu, and W.E. Bentley Effect of MOI ratio on the composition and yield of chimeric infectious bursal disease virus-like particles by baculovirus co-infection: deterministic predictions and experimental results Biotechnol. Bioeng. 75 2001 104 119
152. Y.C. Hu, and W.E. Bentley A kinetic and statistical-thermodynamic model for baculovirus infection and virus-like particle assembly in suspended insect cells Chem. Eng. Sci. 55 2000 3991 4008
153. W.E. Bentley, B. Kebede, T. Franey, and M.-Y. Wang Segregated characterization of recombinant epoxide hydrolase synthesis via the baculovirus/insect cell expression system Chem. Eng. Sci. 49 1994 4133 4141
154. C.D. De Gooijer, R.H. Koken, F.L. Van Lier, M. Kool, J.M. Vlak, and J. Tramper A structured dynamic model for the baculovirus infection process in insect-cell reactor configurations Biotechnol. Bioeng. 40 1992 537 548
155. J.F. Power, S. Reid, K.M. Radford, P.F. Greenfield, and L.K. Nielsen Modeling and optimization of the baculovirus expression vector system in batch suspension culture Biotechnol. Bioeng. 44 1994 710 719
156. E.I. Tsao, M.R. Mason, M.A. Cacciuttolo, S.H. Bowen, and G. Folena-Wasserman Production of parvovirus B19 vaccine in insect cells co-infected with double baculoviruses Biotechnol. Bioeng. 49 1996 130 138
157. T. Vicente, A. Roldao, C. Peixoto, M.J. Carrondo, and P.M. Alves Large-scale production and purification of VLP-based vaccines J. Invertebr. Pathol. 107 Suppl. 2011 S42 S48
158. J.A. Mena, and A.A. Kamen Insect cell technology is a versatile and robust vaccine manufacturing platform Expert Rev. Vaccines 10 2011 1063 1081
159. A. Prel, G. Le Gall-Recule, and V. Jestin 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 2008 513 520
160. Z.R. Zhou, M.L. Wang, F. Deng, T.X. Li, Z.H. Hu, and H.L. Wang Production of CCHF virus-like particle by a baculovirus-insect cell expression system Virol. Sin. 26 2011 338 346
161. A.P. Schmitt, G.P. Leser, D.L. Waning, and R.A. Lamb Requirements for budding of paramyxovirus simian virus 5 virus-like particles J. Virol. 76 2002 3952 3964
162. R. Morenweiser Downstream processing of viral vectors and vaccines Gene Ther. 12 Suppl. 1 2005 S103 S110
163. L. Huhti, V. Blazevic, K. Nurminen, T. Koho, V.P. Hytonen, and T. Vesikari A comparison of methods for purification and concentration of norovirus GII-4 capsid virus-like particles Arch. Virol. 155 2010 1855 1858
164. L. Maranga, P. Rueda, A.F. Antonis, C. Vela, J.P. Langeveld, J.I. Casal, and M.J. Carrondo Large scale production and downstream processing of a recombinant porcine parvovirus vaccine Appl. Microbiol. Biotechnol. 59 2002 45 50
165. C. Peixoto, M.F. Sousa, A.C. Silva, M.J. Carrondo, and P.M. Alves Downstream processing of triple layered rotavirus like particles J. Biotechnol. 127 2007 452 461
166. T. Koho, T. Mantyla, P. Laurinmaki, L. Huhti, S.J. Butcher, T. Vesikari, M.S. Kulomaa, and V.P. Hytonen Purification of norovirus-like particles (VLPs) by ion exchange chromatography J. Virol. Methods 181 2012 6 11
167. M. Marek, M.M. van Oers, F.F. Devaraj, J.M. Vlak, and O.W. Merten Engineering of baculovirus vectors for the manufacture of virion-free biopharmaceuticals Biotechnol. Bioeng. 108 2011 1056 1067
168. F. Fernandes, A.P. Teixeira, N. Carinhas, M.J. Carrondo, and P.M. Alves Insect cells as a production platform of complex virus-like particles Expert Rev. Vaccines 12 2013 225 236 Interest