Virus-like particles in vaccine development

References

• Kleid DG, Yansura D, Small B et al. Cloned viral protein vaccine for foot-and-mouth disease: responses in cattle and swine. Science214(4525), 1125–1129 (1981).
   PubMed Web of Science ®Google Scholar
• Michel ML, Tiollais P. Hepatitis B vaccines: protective efficacy and therapeutic potential. Pathol. Biol. (Paris)58(4), 288–295 (2010).
   PubMed Web of Science ®Google Scholar
• Noad R, Roy P. Virus-like particles as immunogens. Trends Microbiol.11(9), 438–444 (2003).
   PubMed Web of Science ®Google Scholar
• Jegerlehner A, Storni T, Lipowsky G et al. Regulation of IgG antibody responses by epitope density and CD21-mediated costimulation. Eur. J. Immunol.32(11), 3305–3314 (2002).
   PubMed Web of Science ®Google Scholar
• Chackerian B, Lenz P, Lowy DR, Schiller JT. Determinants of autoantibody induction by conjugated papillomavirus virus-like particles. J. Immunol.169(11), 6120–6126 (2002).
   PubMed Web of Science ®Google Scholar
• Ludwig C, Wagner R. Virus-like particles-universal molecular toolboxes. Curr. Opin. Biotechnol.18(6), 537–545 (2007).
   PubMed Web of Science ®Google Scholar
• Kao JH, Chen DS. Global control of hepatitis B virus infection. Lancet Infect. Dis.2(7), 395–403 (2002).
   PubMed Web of Science ®Google Scholar
• Kane MA, Brooks A. New immunization initiatives and progress toward the global control of hepatitis B. Curr. Opin. Infect. Dis.15(5), 465–469 (2002).
   PubMed Web of Science ®Google Scholar
• Kane MA, Sherris J, Coursaget P, Aguado T, Cutts F. Chapter 15: HPV vaccine use in the developing world. Vaccine24(Suppl. 3), 132–139 (2006).
   Web of Science ®Google Scholar
• Valenzuela P, Gray P, Quiroga M et al. Nucleotide sequence of the gene coding for the major protein of hepatitis B virus surface antigen. Nature280(5725), 815–819 (1979).
   PubMed Web of Science ®Google Scholar
• Sninsky JJ, Siddiqui A, Robinson WS, Cohen SN. Cloning and endonuclease mapping of the hepatitis B viral genome. Nature279(5711), 346–348 (1979).
   PubMedGoogle Scholar
• Burrell CJ, Mackay P, Greenaway PJ, Hofschneider PH, Murray K. Expression in Escherichia coli of hepatitis B virus DNA sequences cloned in plasmid pBR322. Nature279(5708), 43–47 (1979).
   PubMedGoogle Scholar
• Charnay P, Pourcel C, Louise A, Fritsch A, Tiollais P. Cloning in Escherichia coli and physical structure of hepatitis B virion DNA. Proc. Natl Acad. Sci. USA76(5), 2222–2226 (1979).
   PubMedGoogle Scholar
• Fritsch A, Pourcel C, Charnay P, Tiollais P. Cloning of the hepatitis B virus genome in Escherichia coli. CR Hebd. Seances Acad. Sci. Ser. D Sci. Nat.287(16), 1453–1456 (1978).
   Google Scholar
• Vassileva A, Chugh DA, Swaminathan S, Khanna N. Effect of copy number on the expression levels of hepatitis B surface antigen in the methylotrophic yeast Pichia pastoris. Protein Expr. Purif.21(1), 71–80 (2001).
   PubMed Web of Science ®Google Scholar
• Janowicz ZA, Melber K, Merckelbach A et al. Simultaneous expression of the S and L surface antigens of hepatitis B, and formation of mixed particles in the methylotrophic yeast, Hansenula polymorpha. Yeast7(5), 431–443 (1991).
   PubMedGoogle Scholar
• Michel ML, Pontisso P, Sobczak E et al. Synthesis in animal cells of hepatitis B surface antigen particles carrying a receptor for polymerized human serum albumin. Proc. Natl Acad. Sci. USA81(24), 7708–7712 (1984).
   PubMed Web of Science ®Google Scholar
• Miyanohara A, Toh-e A, Nozaki C et al. Expression of hepatitis B surface antigen gene in yeast. Proc. Natl Acad. Sci. USA80(1), 1–5 (1983).
   PubMed Web of Science ®Google Scholar
• Valenzuela P, Medina A, Rutter WJ, Ammerer G, Hall BD. Synthesis and assembly of hepatitis B virus surface antigen particles in yeast. Nature298(5872), 347–350 (1982).
   PubMed Web of Science ®Google Scholar
• Zhou W, Bi J, Janson J-C et al. Molecular characterization of recombinant hepatitis B surface antigen from Chinese hamster ovary and Hansenula polymorpha cells by high-performance size exclusion chromatography and multi-angle laser light scattering. J. Chromatogr. B838(2), 71–77 (2006).
   Google Scholar
• Hardy E, Martinez E, Diago D et al. Large-scale production of recombinant hepatitis B surface antigen from Pichia pastoris. J. Biotechnol.77(2–3), 157–167 (2000).
   PubMed Web of Science ®Google Scholar
• Shapira MY, Zeira E, Adler R, Shouval D. Rapid seroprotection against hepatitis B following the first dose of a Pre-S1/Pre-S2/S vaccine. J. Hepatol.34(1), 123–127 (2001).
   PubMed Web of Science ®Google Scholar
• Bucher B, Francioli P, Geudelin B et al. Immunogenicity of a recombinant Pre-S2-containing hepatitis B vaccine versus plasma-derived vaccine administered as a booster. Eur. J. Clin. Microbiol. Infect. Dis.13(3), 212–217 (1994).
   Google Scholar
• Villa LL. Prophylactic HPV vaccines: reducing the burden of HPV-related diseases. Vaccine24(Suppl. 1), S23–S28 (2006).
   Google Scholar
• Bouvard V, Baan R, Straif K et al. A review of human carcinogens – part B: biological agents. Lancet Oncol.10(4), 321–322 (2009).
   PubMed Web of Science ®Google Scholar
• D’Souza G, Kreimer AR, Viscidi R et al. Case–control study of human papillomavirus and oropharyngeal cancer. N. Engl. J. Med.356(19), 1944–1956 (2007).
   PubMed Web of Science ®Google Scholar
• Parkin DM, Bray F. Chapter 2: the burden of HPV-related cancers. Vaccine24(Suppl. 3), S3/11–25 (2006).
   Web of Science ®Google Scholar
• Baker TS, Newcomb WW, Olson NH et al. Structures of bovine and human papillomaviruses. Analysis by cryoelectron microscopy and three-dimensional image reconstruction. Biophys. J.60(6), 1445–1456 (1991).
   PubMed Web of Science ®Google Scholar
• Chen XS, Garcea RL, Goldberg I, Casini G, Harrison SC. Structure of small virus-like particles assembled from the L1 protein of human papillomavirus 16. Mol. Cell.5(3), 557–567 (2000).
   PubMed Web of Science ®Google Scholar
• Suzich JA, Ghim SJ, Palmer-Hill FJ et al. Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. Proc. Natl Acad. Sci. USA92(25), 11553–11557 (1995).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Hagensee ME, Yaegashi N, Galloway DA. Self-assembly of human papillomavirus type 1 capsids by expression of the L1 protein alone or by coexpression of the L1 and L2 capsid proteins. J. Virol.67(1), 315–322 (1993).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Buckland BC. The process development challenge for a new vaccine. Nat. Med.11(4 Suppl.), S16–S19 (2005).
   PubMedGoogle Scholar
• Schiller JT, Castellsague X, Villa LL, Hildesheim A. An update of prophylactic human papillomavirus L1 virus-like particle vaccine clinical trial results. Vaccine26(Suppl. 10), K53–K61 (2008).
   PubMed Web of Science ®Google Scholar
• Smith JF, Brownlow M, Brown M et al. Antibodies from women immunized with Gardasil cross-neutralize HPV 45 pseudovirions. Hum. Vaccin.3(4), 109–115 (2007).
   PubMed Web of Science ®Google Scholar
• Pinto LA, Edwards J, Castle PE et al. Cellular immune responses to human papillomavirus (HPV)-16 L1 in healthy volunteers immunized with recombinant HPV-16 L1 virus-like particles. J. Infect. Dis.188(2), 327–338 (2003).
   PubMed Web of Science ®Google Scholar
• Emeny RT, Wheeler CM, Jansen KU et al. Priming of human papillomavirus type 11-specific humoral and cellular immune responses in college-aged women with a virus-like particle vaccine. J. Virol.76(15), 7832–7842 (2002).
   PubMed Web of Science ®Google Scholar
• Latham T, Galarza JM. Formation of wild-type and chimeric influenza virus-like particles following simultaneous expression of only four structural proteins. J. Virol.75(13), 6154–6165 (2001).
   PubMed Web of Science ®Google Scholar
• 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. Vaccine23(50), 5751–5759 (2005).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Pushko P, Tumpey TM, Van Hoeven N et al. Evaluation of influenza virus-like particles and Novasome adjuvant as candidate vaccine for avian influenza. Vaccine25(21), 4283–4290 (2007).
   PubMed Web of Science ®Google Scholar
• Quan FS, Huang C, Compans RW, Kang SM. Virus-like particle vaccine induces protective immunity against homologous and heterologous strains of influenza virus. J. Virol.81(7), 3514–3524 (2007).
   PubMed Web of Science ®Google Scholar
• Galarza JM, Latham T, Cupo A. Virus-like particle (VLP) vaccine conferred complete protection against a lethal influenza virus challenge. Viral Immunol.18(1), 244–251 (2005).
   PubMed Web of Science ®Google Scholar
• Shelly D, Cleave VV. Parvovirus B19 VLP vaccine manufacturing. Genet. Eng. Biotechnol. News29(16), 1–4 (2009).
   Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Ramqvist T, Andreasson A, Dalianis T. Vaccination, immune and gene therapy based on virus-like particles against viral infections and cancer. Expert Opin. Biol. Ther.7(7), 997–1007 (2007).
   PubMed Web of Science ®Google Scholar
• Neirynck S, Deroo T, Saelens X et al. A universal influenza A vaccine based on the extracellular domain of the M2 protein. Nat. Med.5(10), 1157–1163 (1999).
   PubMed Web of Science ®Google Scholar
• Weber J, Cheinsong-Popov R, Callow D et al. Immunogenicity of the yeast recombinant p17/p24:Ty virus-like particles (p24-VLP) in healthy volunteers. Vaccine13(9), 831–834 (1995).
   PubMed Web of Science ®Google Scholar
• Schodel F, Wirtz R, Peterson D et al. Immunity to malaria elicited by hybrid hepatitis B virus core particles carrying circumsporozoite protein epitopes. J. Exp. Med.180(3), 1037–1046 (1994).
   PubMed Web of Science ®Google Scholar
• Rutgers T, Gordon D, Gathoye AM et al. Hepatitis B surface antigen as carrier matrix for the repetitive epitope of the circumsporozoite protein of Plasmodium falciparum. Nat. Biotechnol.6, 1065–1070 (1988).
   Google Scholar
• Maurer P, Jennings GT, Willers J et al. A therapeutic vaccine for nicotine dependence: preclinical efficacy, and Phase I safety and immunogenicity. Eur. J. Immunol.35(7), 2031–2040 (2005).
   PubMed Web of Science ®Google Scholar
• Ambuhl PM, Tissot AC, Fulurija A et al. A vaccine for hypertension based on virus-like particles: preclinical efficacy and Phase I safety and immunogenicity. J. Hypertens25(1), 63–72 (2007).
   PubMed Web of Science ®Google Scholar
• Fiers W, De Filette M, El Bakkouri K et al. M2e-based universal influenza A vaccine. Vaccine27(45), 6280–6283 (2009).
   PubMed Web of Science ®Google Scholar
• Adams SE, Dawson KM, Gull K, Kingsman SM, Kingsman AJ. The expression of hybrid HIV:Ty virus-like particles in yeast. Nature329(6134), 68–70 (1987).
   PubMed Web of Science ®Google Scholar
• Peters BS, Cheingsong-Popov R, Callow D et al. A pilot Phase II study of the safety and immunogenicity of HIV p17/p24:VLP (p24-VLP) in asymptomatic HIV seropositive subjects. J. Infect.35(3), 231–235 (1997).
   PubMed Web of Science ®Google Scholar
• Lisziewicz J, Bakare N, Lori F. Therapeutic vaccination for future management of HIV/AIDS. Vaccine21(7–8), 620–623 (2003).
   PubMed Web of Science ®Google Scholar
• Smith D, Gow I, Colebunders R et al. Therapeutic vaccination (p24-VLP) of patients with advanced HIV-1 infection in the pre-HAART era does not alter CD4 cell decline. HIV Med.2(4), 272–275 (2001).
   PubMedGoogle Scholar
• Nardin EH, Oliveira GA, Calvo-Calle JM et al. Phase I testing of a malaria vaccine composed of hepatitis B virus core particles expressing Plasmodium falciparum circumsporozoite epitopes. Infect. Immun.72(11), 6519–6527 (2004).
   PubMed Web of Science ®Google Scholar
• Oliveira GA, Wetzel K, Calvo-Calle JM et al. Safety and enhanced immunogenicity of a hepatitis B core particle Plasmodium falciparum malaria vaccine formulated in adjuvant Montanide ISA 720 in a Phase I trial. Infect. Immun.73(6), 3587–3597 (2005).
   PubMed Web of Science ®Google Scholar
• Moorthy V, Reed Z, Smith PG. Measurement of malaria vaccine efficacy in Phase III trials: report of a WHO consultation. Vaccine25(28), 5115–5123 (2007).
   PubMedGoogle Scholar
• Cornuz J, Zwahlen S, Jungi WF et al. A vaccine against nicotine for smoking cessation: a randomized controlled trial. PLoS One3(6), e2547 (2008).
   PubMed Web of Science ®Google Scholar
• Tissot AC, Maurer P, Nussberger J et al. Effect of immunisation against angiotensin II with CYT006-AngQβ on ambulatory blood pressure: a double-blind, randomised, placebo-controlled Phase IIa study. Lancet371(9615), 821–827 (2008).
   PubMed Web of Science ®Google Scholar
• Storni T, Ruedl C, Schwarz K et al. Nonmethylated CG motifs packaged into virus-like particles induce protective cytotoxic T cell responses in the absence of systemic side effects. J. Immunol.172(3), 1777–1785 (2004).
   PubMed Web of Science ®Google Scholar
• Matthias S, Karl-Heinz W, Alain CT et al. O1–06–01: Immunization with Aβ1–6 coupled to the virus-like particle Qβ (CAD106) efficiently removes β-amyloid without inducing Aβ-reactive T-cells. Alzheimers Dement.2(3), S20 (2006).
   Google Scholar
• Bengt W. S2–04–06: safety, tolerability and immunogenicity of the Ab immunotherapeutic vaccine CAD106 in a first-in-man study in Alzheimer patients. Alzheimers Dement.4(4), T128 (2008).
   Google Scholar
• Kallstrom G, Warfield KL, Swenson DL et al. Analysis of Ebola virus and VLP release using an immunocapture assay. J. Virol. Methods127(1), 1–9 (2005).
   PubMed Web of Science ®Google Scholar
• Fromentin R, Majeau N, Laliberté Gagné ME et al. A method for in vitro assembly of hepatitis C virus core protein and for screening of inhibitors. Anal. Biochem.366(1), 37–45 (2007).
   Google Scholar
• Hou L, Wu H, Xu L, Yang F. Expression and self-assembly of virus-like particles of infectious hypodermal and hematopoietic necrosis virus in Escherichia coli. Arch. Virol.154(4), 547–553 (2009).
   Google Scholar
• Yu F, Joshi SM, Ma YM et al. Characterization of Rous sarcoma virus Gag particles assembled in vitro. J. Virol.75(6), 2753–2764 (2001).
   Google Scholar
• Lai WB, Middelberg APJ. The production of human papillomavirus type 16 vaccine product from Escherichia coli inclusion bodies. Bioprocess. Biosyst. Eng.25, 121–128 (2002).
   PubMedGoogle Scholar
• Zhang W, Carmichael J, Ferguson J et al. Expression of human papillomavirus type 16 L1 protein in Escherichia coli: denaturation, renaturation, and self-assembly of virus-like particles in vitro. Virology243(2), 423–431 (1998).
   PubMedGoogle Scholar
• Chromy LR, Pipas JM, Garcea RL. Chaperone-mediated in vitro assembly of Polyomavirus capsids. Proc. Natl Acad. Sci. USA100(18), 10477–10482 (2003).
   PubMed Web of Science ®Google Scholar
• Davis TR, Wood HA. Intrinsic glycosylation potentials of insect cell cultures and insect larvae. In Vitro Cell Dev. Biol. Anim.31(9), 659–663 (1995).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• 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.38(2–3), 111–124 (1995).
   Google Scholar
• Lechmann M, Murata K, Satoi J et al. Hepatitis C virus-like particles induce virus-specific humoral and cellular immune responses in mice. Hepatology34(2), 417–423 (2001).
   PubMed Web of Science ®Google Scholar
• Tatman JD, Preston VG, Nicholson P, Elliott RM, Rixon FJ. Assembly of herpes simplex virus type 1 capsids using a panel of recombinant baculoviruses. J. Gen. Virol.75(Pt 5), 1101–1113 (1994).
   PubMedGoogle Scholar
• 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), 421–429 (2007).
   PubMed Web of Science ®Google Scholar
• Nagy E, Huber P, Krell PJ, Derbyshire JB. 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.72(Pt 3), 753–756 (1991).
   Web of Science ®Google Scholar
• Almanza H, Cubillos C, Angulo I et al. Self-assembly of the recombinant capsid protein of a swine norovirus into virus-like particles and evaluation of monoclonal antibodies cross-reactive with a human strain from genogroup II. J. Clin. Microbiol.46(12), 3971–3979 (2008).
   Google Scholar
• Agrawal DK, Johnson JE. Assembly of the T = 4 Nudaurelia capensis omega virus capsid protein, post-translational cleavage, and specific encapsidation of its mRNA in a baculovirus expression system. Virology207(1), 89–97 (1995).
   Google Scholar
• Canady MA, Tihova M, Hanzlik TN, Johnson JE, Yeager M. Large conformational changes in the maturation of a simple RNA virus, nudaurelia capensis omega virus (NomegaV). J. Mol. Biol.299(3), 573–584 (2000).
   PubMed Web of Science ®Google Scholar
• Liu L, Celma CC, Roy P. Rift Valley fever virus structural proteins: expression, characterization and assembly of recombinant proteins. Virol. J.5, 82 (2008).
   Google Scholar
• Hervas-Stubbs S, Rueda P, Lopez L, Leclerc C. Insect baculoviruses strongly potentiate adaptive immune responses by inducing type I IFN. J. Immunol.178(4), 2361–2369 (2007).
   PubMed Web of Science ®Google Scholar
• Rueda P, Fominaya J, Langeveld JP et al. Effect of different baculovirus inactivation procedures on the integrity and immunogenicity of porcine parvovirus-like particles. Vaccine19(7–8), 726–734 (2000).
   Google Scholar
• Shioda T, Shibuta H. Production of human immunodeficiency virus (HIV)-like particles from cells infected with recombinant vaccinia viruses carrying the gag gene of HIV. Virology175(1), 139–148 (1990).
   PubMed Web of Science ®Google Scholar
• Haglund K, Forman J, Krausslich HG, Rose JK. Expression of human immunodeficiency virus type 1 Gag protein precursor and envelope proteins from a vesicular stomatitis virus recombinant: high-level production of virus-like particles containing HIV envelope. Virology268(1), 112–121 (2000).
   PubMed Web of Science ®Google Scholar
• Fernandez-Arias A, Risco C, Martinez S, Albar JP, Rodriguez JF. Expression of ORF A1 of infectious bursal disease virus results in the formation of virus-like particles. J. Gen. Virol.79(Pt 5), 1047–1054 (1998).
   PubMed Web of Science ®Google Scholar
• Levy HC, Bowman VD, Govindasamy L et al. Heparin binding induces conformational changes in adeno-associated virus serotype 2. J. Struct. Biol.165(3), 146–156 (2009).
   PubMed Web of Science ®Google Scholar
• Hammonds J, Chen X, Zhang X, Lee F, Spearman P. Advances in methods for the production, purification and characterization of HIV-1 Gag-Env pseudovirion vaccines. Vaccine25, 8036–8048 (2007).
   PubMed Web of Science ®Google Scholar
• Swenson DL, Warfield KL, Negley DL et al. Virus-like particles exhibit potential as a pan-filovirus vaccine for both Ebola and Marburg viral infections. Vaccine23(23), 3033–3042 (2005).
   PubMed Web of Science ®Google Scholar
• Taube S, Kurth A, Schreier E. Generation of recombinant norovirus-like particles (VLP) in the human endothelial kidney cell line 293T. Arch. Virol.150(7), 1425–1431 (2005).
   PubMedGoogle Scholar
• Holzer GW, Mayrhofer J, Leitner J et al. Overexpression of hepatitis B virus surface antigens including the preS1 region in a serum-free Chinese hamster ovary cell line. Protein Expr. Purif.29(1), 58–69 (2003).
   PubMed Web of Science ®Google Scholar
• Lee T, Inokoshi J, Namiki M, Takeshima H, Omura S. Production of hepatitis B virus surface antigen containing pre-S1 and pre-S2 domains by Chinese hamster ovary cells. Arch. Virol.106(1–2), 151–158 (1989).
   Google Scholar
• Ma Z, Yi X, Zhang Y. Enhanced intracellular accumulation of recombinant HBsAg in CHO cells by dimethyl sulfoxide. Process Biochem.43, 690–695 (2008).
   Google Scholar
• Madalinski K, Sylvan SP, Hellstrom U et al. Antibody responses to preS components after immunization of children with low doses of BioHepB. Vaccine20(1–2), 92–97 (2001).
   Google Scholar
• Matsuo E, Tani H, Lim C et al. Characterization of HCV-like particles produced in a human hepatoma cell line by a recombinant baculovirus. Biochem. Biophys. Res. Commun.340(1), 200–208 (2006).
   PubMed Web of Science ®Google Scholar
• Wang KC, Wu JC, Chung YC et al. Baculovirus as a highly efficient gene delivery vector for the expression of hepatitis δ virus antigens in mammalian cells. Biotechnol. Bioeng.89(4), 464–473 (2005).
   PubMed Web of Science ®Google Scholar
• Chen YH, Wu JC, Wang KC et al. Baculovirus-mediated production of HDV-like particles in BHK cells using a novel oscillating bioreactor. J. Biotechnol.118(2), 135–147 (2005).
   PubMed Web of Science ®Google Scholar
• Ehsani P, Khabiri A, Domansky NN. Polypeptides of hepatitis B surface antigen produced in transgenic potato. Gene190(1), 107–111 (1997).
   PubMed Web of Science ®Google Scholar
• Maloney BJ, Takeda N, Suzaki Y et al. Challenges in creating a vaccine to prevent hepatitis E. Vaccine23(15), 1870–1874 (2005).
   PubMed Web of Science ®Google Scholar
• Warzecha H, Mason HS, Lane C et al. Oral immunogenicity of human papillomavirus-like particles expressed in potato. J. Virol.77(16), 8702–8711 (2003).
   PubMed Web of Science ®Google Scholar
• Mason HS, Ball JM, Shi JJ et al. Expression of Norwalk virus capsid protein in transgenic tobacco and potato and its oral immunogenicity in mice. Proc. Natl Acad. Sci. USA93(11), 5335–5340 (1996).
   PubMed Web of Science ®Google Scholar
• Huang Z, Elkin G, Maloney BJ et al. Virus-like particle expression and assembly in plants: hepatitis B and Norwalk viruses. Vaccine23(15), 1851–1858 (2005).
   PubMed Web of Science ®Google Scholar
• Smith ML, Mason HS, Shuler ML. Hepatitis B surface antigen (HBsAg) expression in plant cell culture: kinetics of antigen accumulation in batch culture and its intracellular form. Biotechnol. Bioeng.80(7), 812–822 (2002).
   PubMed Web of Science ®Google Scholar
• Kapusta J, Modelska A, Figlerowicz M et al. A plant-derived edible vaccine against hepatitis B virus. FASEB J.13(13), 1796–1799 (1999).
   PubMed Web of Science ®Google Scholar
• Bragard C, Duncan GH, Wesley SV, Naidu RA, Mayo MA. Virus-like particles assemble in plants and bacteria expressing the coat protein gene of Indian peanut clump virus. J. Gen. Virol.81(Pt 1), 267–272 (2000).
   PubMedGoogle Scholar
• Huang Z, Chen Q, Hjelm B, Arntzen C, Mason H. A DNA replicon system for rapid high-level production of virus-like particles in plants. Biotechnol. Bioeng.103(4), 706–714 (2009).
   PubMed Web of Science ®Google Scholar
• Huang Z, Mason HS. Conformational analysis of hepatitis B surface antigen fusions in an Agrobacterium-mediated transient expression system. Plant Biotechnol. J.2(3), 241–249 (2004).
   PubMed Web of Science ®Google Scholar
• Huang Z, Santi L, LePore K et al. Rapid, high-level production of hepatitis B core antigen in plant leaf and its immunogenicity in mice. Vaccine24(14), 2506–2513 (2006).
   PubMed Web of Science ®Google Scholar
• Sojikul P, Buehner N, Mason HS. A plant signal peptide-hepatitis B surface antigen fusion protein with enhanced stability and immunogenicity expressed in plant cells. Proc. Natl Acad. Sci. USA100(5), 2209–2214 (2003).
   PubMed Web of Science ®Google Scholar
• Lim GMA. Transgenic plants in therapeutically valuable protein production. Transgenic Plant J.1, 256–266 (2007).
   Google Scholar
• Boijoux O, Boutonnet C, Giamarchi C et al. Chemical-based translational induction of luciferase expression: an efficient tool for in vivo screening of protein farnesylation inhibitors. Mol. Pharmacol.67(6), 1829–1833 (2005).
   Google Scholar
• Roos AK, Eriksson F, Timmons JA et al. Skin electroporation: effects on transgene expression, DNA persistence and local tissue environment. PLoS One4(9), e7226 (2009).
   PubMed Web of Science ®Google Scholar
• Bertram J. MATra - Magnet assisted transfection: combining nanotechnology and magnetic forces to improve intracellular delivery of nucleic acids. Curr. Pharm. Biotechnol.7(4), 277–285 (2006).
   Google Scholar
• Coroadinha AS, Schucht R, Gama-Norton L et al. The use of recombinase mediated cassette exchange in retroviral vector producer cell lines: predictability and efficiency by transgene exchange. J. Biotechnol.124(2), 457–468 (2006).
   Google Scholar
• Zhao QQ, Chen JL, Lv TF et al. N/P ratio significantly influences the transfection efficiency and cytotoxicity of a polyethylenimine/chitosan/DNA complex. Biol. Pharm. Bull.32(4), 706–710 (2009).
   Google Scholar
• Zheng XZ, Li HL, Du LF, Wang HP, Gu Q. Comparative analysis of gene transfer to human and rat retinal pigment epithelium cell line by a combinatorial use of recombinant adeno- associated virus and ultrasound or/and microbubbles. Bosn J. Basic Med. Sci.9(3), 174–181 (2009).
   Google Scholar
• Molinas MMB, Beer C, Hesse F et al. Intracellular nucleotide pools for optimizing product-oriented transient transfection of HEK293 cells in suspension. In: 18th ESACT Meeting: Animal Cell Technology Meets Genomics. Gòdia FF M (Ed.). Springer, The Netherlands, 83–86 (2003).
   Google Scholar
• Liu C, Dalby B, Chen W, Kilzer JM, Chiou HC. Transient transfection factors for high-level recombinant protein production in suspension cultured mammalian cells. Mol. Biotechnol.39(2), 141–153 (2008).
   PubMed Web of Science ®Google Scholar
• Masotti A, Mossa G, Cametti C et al. Comparison of different commercially available cationic liposome-DNA lipoplexes: parameters influencing toxicity and transfection efficiency. Colloids Surf. B Biointerfaces68(2), 136–144 (2009).
   PubMed Web of Science ®Google Scholar
• Chong KW, Lee AY, Koay ES, Seet SJ, Cheung NS. pH dependent high transfection efficiency of mouse neuroblastomas using TransFectin. J. Neurosci. Methods158(1), 56–63 (2006).
   Google Scholar
• Jacobsen LB, Calvin SA, Colvin KE, Wright M. FuGENE 6 Transfection Reagent: the gentle power. Methods33(2), 104–112 (2004).
   Google Scholar
• Wu CY, Yeh YC, Yang YC et al. Mammalian expression of virus-like particles for advanced mimicry of authentic influenza virus. PLoS One5(3), e9784 (2010).
   PubMed Web of Science ®Google Scholar
• Harvey TJ, Liu WJ, Wang XJ et al. Tetracycline-inducible packaging cell line for production of flavivirus replicon particles. J. Virol.78(1), 531–538 (2004).
   PubMed Web of Science ®Google Scholar
• Hong S, Hwang D-Y, Yoon S et al. Functional analysis of various promoters in lentiviral vectors at different stages of in vitro differentiation of mouse embryonic stem cells. Mol. Ther.15(9), 1630–1639 (2007).
   PubMed Web of Science ®Google Scholar
• Morris TD, Miller LK. Promoter influence on baculovirus-mediated gene expression in permissive and nonpermissive insect cell lines. J. Virol.66(12), 7397–7405 (1992).
   PubMed Web of Science ®Google Scholar
• Pajot-Augy E, Bozon V, Remy JJ, Couture L, Salesse R. Critical relationship between glycosylation of recombinant lutropin receptor ectodomain and its secretion from baculovirus-infected insect cells. Eur. J. Biochem.260(3), 635–648 (1999).
   Google Scholar
• Roldão A, Carrondo MJT, Alves PM, Oliveira R. Stochastic simulation of protein expression in the baculovirus/insect cells system. Comput. Chem. Eng.32(1–2), 68–77 (2008).
   Web of Science ®Google Scholar
• Bernal V, Carinhas N, Yokomizo AY, Carrondo MJ, Alves PM. Cell density effect in the baculovirus-insect cells system: a quantitative analysis of energetic metabolism. Biotechnol. Bioeng.104(1), 162–180 (2009).
   PubMed Web of Science ®Google Scholar
• Cruz PE, Cunha A, Peixoto CC et al. Optimization of the production of virus-like particles in insect cells. Biotechnol. Bioeng.60(4), 408–418 (1998).
   Google Scholar
• Xi SZ, Banks LM. Baculovirus expression of the human papillomavirus type 16 capsid proteins: detection of L1-L2 protein complexes. J. Gen. Virol.72(Pt 12), 2981–2988 (1991).
   Google Scholar
• Cruz PE, Peixoto CC, Moreira JL, Carrondo MJT. Production and quality analysis of Pr55gag particles produced in baculovirus-infected insect cells. J. Chem. Technol. Biotechnol.72(2), 149–158 (1999).
   Google Scholar
• Ferreira TB, Ferreira AL, Carrondo MJ, Alves PM. Effect of re-feed strategies and non-ammoniagenic medium on adenovirus production at high cell densities. J. Biotechnol.119(3), 272–280 (2005).
   Google Scholar
• Power JF, Reid S, Radford KM, Greenfield PF, Nielsen LK. Modeling and optimization of the baculovirus expression vector system in batch suspension culture. Biotechnol. Bioeng.44(6), 710–719 (1994).
   Google Scholar
• Ferreira TB, Carrondo MJ, Alves PM. Effect of ammonia production on intracellular pH: Consequent effect on adenovirus vector production. J. Biotechnol.129(3), 433–438 (2007).
   Google Scholar
• Carinhas N, Bernal V, Monteiro F et al. Improving baculovirus production at high cell density through manipulation of energy metabolism. Metab. Eng.12(1), 39–52 (2009).
   Google Scholar
• Lee YY, Wong KT, Nissom PM, Wong DC, Yap MG. Transcriptional profiling of batch and fed-batch protein-free 293-HEK cultures. Metab. Eng.9(1), 52–67 (2007).
   Google Scholar
• Maranga L, Brazao TF, Carrondo MJ. Virus-like particle production at low multiplicities of infection with the baculovirus insect cell system. Biotechnol. Bioeng.84(2), 245–253 (2003).
   Google Scholar
• van Lier FL, van Duijnhoven GC, de Vaan MM, Vlak JM, Tramper J. Continuous β-galactosidase production in insect cells with a p10 gene based baculovirus vector in a two-stage bioreactor system. Biotechnol. Prog.10(1), 60–64 (1994).
   Google Scholar
• Kompier R, Tramper J, Vlak JM. A continuous process for the production of baculovirus using insect cell cultures. Biotechnol. Lett.10, 849–854 (1988).
   Google Scholar
• Caron AW, Tom RL, Kamen AA, Massie B. Baculovirus expression system scaleup by perfusion of high-density Sf-9 cell cultures. Biotechnol. Bioeng.43(9), 881–891 (1994).
   PubMed Web of Science ®Google Scholar
• Kumar N, Gammell P, Meleady P, Henry M, Clynes M. Differential protein expression following low temperature culture of suspension CHO-K1 cells. BMC Biotechnol.8, 42 (2008).
   PubMedGoogle Scholar
• Maranga L, Cunha A, Clemente J, Cruz P, Carrondo MJ. Scale-up of virus-like particles production: effects of sparging, agitation and bioreactor scale on cell growth, infection kinetics and productivity. J. Biotechnol.107(1), 55–64 (2004).
   PubMed Web of Science ®Google Scholar
• Murhammer D, Goochee C. Scale up of insect cell cultures: protective effects of Pluronic F-68. Biotechnol.6, 1411–1418 (1988).
   Google Scholar
• Xie L, Metallo C, Warren J et al. Large-scale propagation of a replication-defective adenovirus vector in stirred-tank bioreactor PER.C6 cell culture under sparging conditions. Biotechnol. Bioeng.83(1), 45–52 (2003).
   PubMed Web of Science ®Google Scholar
• Wang MY, Pulliam TR, Valle M, Vakharia VN, Bentley WE. Kinetic analysis of alkaline protease activity, recombinant protein production and metabolites for infected insect (Sf9) cells under different DO levels. J. Biotechnol.46, 243–245 (1996).
   Google Scholar
• Konz JO, King J, Cooney CL. Effects of oxygen on recombinant protein expression. Biotechnol. Prog.14(3), 393–409 (1998).
   Google Scholar
• Mellado MCM, Mena JA, Lopes A et al. Impact of physicochemical parameters on in vitro assembly and disassembly kinetics of recombinant triple-layered rotavirus-like particles. Biotech. Bioeng.104(4), 674–686 (2009).
   PubMed Web of Science ®Google Scholar
• Roldão A, Mellado MCM, Lima JC et al. A computational model for multilayered virus-like particles (VLP) assembly: the case of a rotavirus VLP. Biophys. J. (2010) (In Press).
   Google Scholar
• Rodrigues T, Carvalho A, Carmo M et al. Scaleable purification process for gene therapy retroviral vectors. J. Gene Med.9(4), 233–243 (2007).
   Google Scholar
• Tsuchida N, Bhaduri S, Raskas HJ, Green M. Partial purification of intracellular murine sarcoma-leukemia virus RNA species by membrane filtration. Intervirology1(1), 27–33 (1973).
   Google Scholar
• Aboud M, Wolfson M, Hassan Y, Huleihel M. Rapid purification of extracellular and intracellular Moloney murine leukemia virus. Arch. Virol.71(3), 185–195 (1982).
   Google Scholar
• Peixoto C, Sousa MF, Silva AC, Carrondo MJ, Alves PM. Downstream processing of triple layered rotavirus like particles. J. Biotechnol.127(3), 452–461 (2007).
   PubMed Web of Science ®Google Scholar
• Mellado MC, Peixoto C, Cruz PE, Carrondo MJ, Alves PM. Purification of recombinant rotavirus VP7 glycoprotein for the study of in vitro rotavirus-like particles assembly. J. Chromatogr. B874(1–2), 89–94 (2008).
   PubMed Web of Science ®Google Scholar
• Peixoto C, Ferreira TB, Sousa MF, Carrondo MJ, Alves PM. Towards purification of adenoviral vectors based on membrane technology. Biotechnol. Prog.24(6), 1290–1296 (2008).
   PubMedGoogle Scholar
• Vicente T, Peixoto C, Carrondo MJ, Alves PM. Purification of recombinant baculoviruses for gene therapy using membrane processes. Gene Ther.16(6), 766–775 (2009).
   PubMed Web of Science ®Google Scholar
• Negrete A, Ling TC, Lyddiatt A. Production of adenoviral vectors and its recovery. Process Biochem.42(7), 1107–1113 (2007).
   Google Scholar
• Moreira JL, Alves PM, Feliciano AS, Aunins JG, Carrondo MJT. Serum-free and serum-containing media for growth of suspended BHK aggregates in stirred vessels. Enzyme Microb. Technol.17(5), 437–444 (1995).
   Google Scholar
• Vicente T, Sousa MFQ, Peixoto C et al. Anion-exchange membrane chromatography for purification of rotavirus-like particles. J. Membr. Sci.311(1–2), 270–283 (2008).
   Web of Science ®Google Scholar
• Morenweiser R. Downstream processing of viral vectors and vaccines. Gene Ther.12(Suppl. 1), S103–S110 (2005).
   PubMed Web of Science ®Google Scholar
• Vieira H, Estêvão C, Roldão A et al. Triple layered rotavirus VLP assembly: kinetics of vector replication, mRNA stability and recombinant protein production. J. Biotechnol.120(1), 72–82 (2005).
   PubMed Web of Science ®Google Scholar
• Meghrous J, Aucoin MG, Jacob D et al. Production of recombinant adeno-associated viral vectors using a baculovirus/insect cell suspension culture system: from shake flasks to a 20-l bioreactor. Biotechnol. Prog.21(1), 154–160 (2005).
   Google Scholar
• Mena JA, Ramirez OT, Palomares LA. Quantification of rotavirus-like particles by gel permeation chromatography. J. Chromatogr. B824(1–2), 267–276 (2005).
   Google Scholar
• Mellado MC, Franco C, Coelho A, Alves PM, Simplicio AL. Sodium dodecyl sulfate-capillary gel electrophoresis analysis of rotavirus-like particles. J. Chromatogr. A1192(1), 166–172 (2008).
   PubMed Web of Science ®Google Scholar
• Franco CF, Mellado MCM, Alves PM, Coelho AV. Monitoring virus-like particle and viral protein production by intact cell MALDI-TOF mass spectrometry. Talanta80(4), 1561–1518 (2009).
   Google Scholar
• Teixeira AP, Portugal CA, Carinhas N et al.In situ 2D fluorometry and chemometric monitoring of mammalian cell cultures. Biotechnol. Bioeng.102(4), 1098–1106 (2009).
   Google Scholar
• Teixeira AP, Oliveira R, Alves PM, Carrondo MJ. Advances in on-line monitoring and control of mammalian cell cultures: supporting the PAT initiative. Biotechnol. Adv.27(6), 726–732 (2009).
   PubMed Web of Science ®Google Scholar
• Murawski MR, McGinnes LW, Finberg RW et al. Newcastle disease virus-like particles containing respiratory syncytial virus G protein induced protection in Balb/C mice, with no evidence of immunopathology. J. Virol.84(2), 1110–1123 (2009).
   Google Scholar
• Jegerlehner A, Tissot A, Lechner F et al. A molecular assembly system that renders antigens of choice highly repetitive for induction of protective B cell responses. Vaccine20(25–26), 3104–3112 (2002).
   PubMed Web of Science ®Google Scholar
• Jennings GT, Bachmann MF. The coming of age of virus-like particle vaccines. Biol. Chem.389(5), 521–536 (2008).
   PubMed Web of Science ®Google Scholar
• Chackerian B, Lowy DR, Schiller JT. Conjugation of a self-antigen to papillomavirus-like particles allows for efficient induction of protective autoantibodies. J. Clin. Invest.108(3), 415–423 (2001).
   PubMed Web of Science ®Google Scholar
• Gleiter S, Lilie H. Coupling of antibodies via protein Z on modified polyoma virus-like particles. Protein Sci.10(2), 434–444 (2001).
   PubMed Web of Science ®Google Scholar
• Lechner F, Jegerlehner A, Tissot AC et al. Virus-like particles as a modular system for novel vaccines. Intervirology45(4–6), 212–217 (2002).
   PubMed Web of Science ®Google Scholar
• Ionescu RM, Przysiecki CT, Liang X et al. Pharmaceutical and immunological evaluation of human papillomavirus viruslike particle as an antigen carrier. J. Pharm. Sci.95(1), 70–79 (2006).
   PubMed Web of Science ®Google Scholar
• Grgacic EV, Anderson DA. Virus-like particles: passport to immune recognition. Methods40(1), 60–65 (2006).
   PubMed Web of Science ®Google Scholar
• Lai CY, Hu HP, King CC, Wang WK. Incorporation of dengue virus replicon into virus-like particles by a cell line stably expressing precursor membrane and envelope proteins of dengue virus type 2. J. Biomed. Sci.15(1), 15–27 (2008).
   Google Scholar
• Slupetzky K, Gambhira R, Culp TD et al. A papillomavirus-like particle (VLP) vaccine displaying HPV16 L2 epitopes induces cross-neutralizing antibodies to HPV11. Vaccine25(11), 2001–2010 (2007).
   PubMed Web of Science ®Google Scholar
• Willis S, Davidoff C, Schilling J et al. Virus-like particles as quantitative probes of membrane protein interactions. Biochemistry47(27), 6988–6990 (2008).
   Google Scholar
• Jones JW, Greene TA, Grygon CA, Doranz BJ, Brown MP. Cell-free assay of G-protein-coupled receptors using fluorescence polarization. J. Biomol. Screen13(5), 424–429 (2008).
   PubMed Web of Science ®Google Scholar
• Ohtake N, Niikura K, Suzuki T et al. Low pH-triggered model drug molecule release from virus-like particles. Chembiochem.11(7), 959–962 (2010).
   PubMed Web of Science ®Google Scholar
• Aucoin MG, Jacob D, Chahal PS et al. Virus-like particle and viral vector production using the baculovirus expression vector system/insect cell system: adeno-associated virus-based products. Methods Mol. Biol.388, 281–296 (2007).
   Google Scholar
• Prel A, Le Gall-Recule 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).
   PubMed Web of Science ®Google Scholar
• Rodgers RE, Chang D, Cai X, Consigli RA. Purification of recombinant budgerigar fledgling disease virus VP1 capsid protein and its ability for in vitro capsid assembly. J. Virol.68(5), 3386–3390 (1994).
   PubMed Web of Science ®Google Scholar
• French TJ, Marshall JJ, Roy P. Assembly of double-shelled, viruslike particles of bluetongue virus by the simultaneous expression of four structural proteins. J. Virol.64(12), 5695–5700 (1990).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Zielonka A, Gedvilaite A, Ulrich R et al. Generation of virus-like particles consisting of the major capsid protein VP1 of goose hemorrhagic polyomavirus and their application in serological tests. Virus Res.120(1–2), 128–137 (2006).
   PubMed Web of Science ®Google Scholar
• Cregg JM, Tschopp JF, Stillamn C et al. High-level expression and efficient assembly of hepatitis B surface antigen in the methylotrophic yeast. Pichia pastoris. Biotechnology5, 479–485 (1987).
   Web of Science ®Google Scholar
• Gu MB, Park MH, Kim DI. Growth rate control in fed-batch cultures of recombinant Saccharomyces cerevisiae producing hepatitis B surface antigen (HBsAg). Appl. Microbiol. Biotechnol.35(1), 46–30 (1991).
   PubMedGoogle Scholar
• Kee GS, Jin J, Balasundaram B et al. Exploiting the intracellular compartmentalization characteristics of the S. cerevisiae host cell for enhancing primary purification of lipid-envelope virus-like particles. Biotechnol. Prog.26(1), 26–33 (2009).
   Google Scholar
• Takehara K, Ireland D, Bishop DH. Co-expression of the hepatitis B surface and core antigens using baculovirus multiple expression vectors. J. Gen. Virol.69(Pt 11), 2763–2777 (1988).
   PubMedGoogle Scholar
• Bundy BC, Franciszkowicz MJ, Swartz JR. Escherichia coli-based cell-free synthesis of virus-like particles. Biotechnol. Bioeng.100(1), 28–37 (2008).
   Google Scholar
• Zlotnick A, Cheng N, Conway JF et al. Dimorphism of hepatitis B virus capsids is strongly influenced by the C-terminus of the capsid protein. Biochemistry35(23), 7412–7421 (1996).
   PubMed Web of Science ®Google Scholar
• James ER, van Zyl WH, Gorgens JF. Increased hepatitis B surface antigen production by recombinant Aspergillus niger through the optimization of agitation and dissolved oxygen concentration. Appl. Microbiol. Biotechnol.75(2), 279–288 (2007).
   Google Scholar
• Sastri M, Kekuda R, Gopinath K et al. Assembly of physalis mottle virus capsid protein in Escherichia coli and the role of amino and carboxy termini in the formation of the icosahedral particles. J. Mol. Biol.272(4), 541–552 (1997).
   Google Scholar
• Wagner R, Deml L, Notka F et al. Safety and immunogenicity of recombinant human immunodeficiency virus-like particles in rodents and rhesus macaques. Intervirology39(1–2), 93–103 (1996).
   Google Scholar
• Sakuragi S, Goto T, Sano K, Morikawa Y. HIV type 1 Gag virus-like particle budding from spheroplasts of Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA99(12), 7956–7961 (2002).
   Google Scholar
• Pillay S, Meyers A, Williamson AL, Rybicki EP. Optimization of chimeric HIV-1 virus-like particle production in a baculovirus-insect cell expression system. Biotechnol. Prog.25(4), 1153–1160 (2009).
   PubMed Web of Science ®Google Scholar
• Park MA, Kim HJ, Kim HJ. Optimum conditions for production and purification of human papillomavirus type 16 L1 protein from Saccharomyces cerevisiae. Protein Expr. Purif.59(1), 175–181 (2008).
   Google Scholar
• Bazan SB, de Alencar Muniz Chaves A, Aires KA et al. Expression and characterization of HPV-16 L1 capsid protein in Pichia pastoris. Arch. Virol.154(10), 1609–1617 (2009).
   PubMed Web of Science ®Google Scholar
• Schadlich L, Senger T, Kirschning CJ, Muller M, Gissmann L. Refining HPV 16 L1 purification from E. coli: reducing endotoxin contaminations and their impact on immunogenicity. Vaccine27(10), 1511–1522 (2009).
   PubMed Web of Science ®Google Scholar
• Hu YC, Bentley WE. 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(1), 104–119 (2001).
   PubMed Web of Science ®Google Scholar
• Krammer F, Schinko T, Palmberger D et al. 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).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Sasnauskas K, Bulavaite A, Hale A et al. Generation of recombinant virus-like particles of human and non-human polyomaviruses in yeast Saccharomyces cerevisiae. Intervirology45(4–6), 308–317 (2002).
   PubMed Web of Science ®Google Scholar
• Hooker JM, Kovacs EW, Francis MB. Interior surface modification of bacteriophage MS2. J. Am. Chem. Soc.126(12), 3718–3719 (2004).
   PubMed Web of Science ®Google Scholar
• Legendre D, Fastrez J. Production in Saccharomyces cerevisiae of MS2 virus-like particles packaging functional heterologous mRNAs. J. Biotechnol.117(2), 183–194 (2005).
   Google Scholar
• McGinnes LW, Pantua H, Laliberte JP et al. Assembly and biological and immunological properties of Newcastle disease virus-like particles. J. Virol.84(9), 4513–4523 (2010).
   Google Scholar
• Xia M, Farkas T, Jiang X. Norovirus capsid protein expressed in yeast forms virus-like particles and stimulates systemic and mucosal immunity in mice following an oral administration of raw yeast extracts. J. Med. Virol.79(1), 74–83 (2007).
   PubMedGoogle Scholar
• Tan M, Zhong W, Song D, Thornton S, Jiang X. E. coli-expressed recombinant norovirus capsid proteins maintain authentic antigenicity and receptor binding capability. J. Med. Virol.74(4), 641–649 (2004).
   Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Chandran D, Shahana PV, Rani GS et al. Display of neutralizing epitopes of canine parvovirus and a T-cell epitope of the fusion protein of canine distemper virus on chimeric tymovirus-like particles and its use as a vaccine candidate both against canine parvo and canine distemper. Vaccine28(1), 132–139 (2009).
   Google Scholar
• Montross L, Watkins S, Moreland RB et al. Nuclear assembly of polyomavirus capsids in insect cells expressing the major capsid protein VP1. J. Virol.65(9), 4991–4998 (1991).
   PubMed Web of Science ®Google Scholar
• Leavitt AD, Roberts TM, Garcea RL. Polyoma virus major capsid protein, VP1. Purification after high level expression in Escherichia coli. J. Biol. Chem.260(23), 12803–12809 (1985).
   PubMed Web of Science ®Google Scholar
• Maranga L, Rueda P, Antonis AF et al. Large scale production and downstream processing of a recombinant porcine parvovirus vaccine. Appl. Microbiol. Biotechnol.59(1), 45–50 (2002).
   Google Scholar
• Laurent S, Vautherot JF, Madelaine MF, Le Gall G, Rasschaert D. Recombinant rabbit hemorrhagic disease virus capsid protein expressed in baculovirus self-assembles into viruslike particles and induces protection. J. Virol.68(10), 6794–6798 (1994).
   PubMed Web of Science ®Google Scholar
• Kim Y, Chang KO, Kim WY, Saif LJ. Production of hybrid double- or triple-layered virus-like particles of group A and C rotaviruses using a baculovirus expression system. Virology3021–8 (2002).
   Google Scholar
• Jiang B, Barniak V, Smith RP et al. Synthesis of rotavirus-like particles in insect cells: comparative and quantitative analysis. Biotechnol. Bioeng.60(3), 369–374 (1998).
   Google Scholar
• Molinari P, Peralta A, Taboga O. Production of rotavirus-like particles in Spodoptera frugiperda larvae. J. Virol. Methods147(2), 364–367 (2008).
   PubMed Web of Science ®Google Scholar
• Mortola E, Roy P. Efficient assembly and release of SARS coronavirus-like particles by a heterologous expression system. FEBS Lett.576(1–2), 174–178 (2004).
   PubMed Web of Science ®Google Scholar
• Yamshchikov GV, Ritter GD, Vey M, Compans RW. Assembly of SIV virus-like particles containing envelope proteins using a baculovirus expression system. Virology214(1), 50–58 (1995).
   PubMed Web of Science ®Google Scholar
• Kanesashi SN, Ishizu K, Kawano MA et al. Simian virus 40 VP1 capsid protein forms polymorphic assemblies in vitro. J. Gen. Virol.84(Pt 7), 1899–1905 (2003).
   PubMed Web of Science ®Google Scholar
• Ko YJ, Choi KS, Nah JJ et al. Noninfectious virus-like particle antigen for detection of swine vesicular disease virus antibodies in pigs by enzyme-linked immunosorbent assay. Clin. Diagn. Lab. Immunol.12(8), 922–929 (2005).
   PubMedGoogle Scholar
• Quan FS, Compans RW, Nguyen HH, Kang SM. Induction of heterosubtypic immunity to influenza virus by intranasal immunization. J. Virol.82(3), 1350–1359 (2008).
   PubMed Web of Science ®Google Scholar
• Wang BZ, Quan FS, Kang SM et al. Incorporation of membrane-anchored flagellin into influenza virus-like particles enhances the breadth of immune responses. J. Virol.82(23), 11813–11823 (2008).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Crevar CJ, Ross TM. Elicitation of protective immune responses using a bivalent H5N1 VLP vaccine. Virol. J.5, 131 (2008).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• D’Aoust MA, Lavoie PO, Couture MM et al. Influenza virus-like particles produced by transient expression in Nicotiana benthamiana induce a protective immune response against a lethal viral challenge in mice. Plant Biotechnol. J.6(9), 930–940 (2008).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Szecsi J, Boson B, Johnsson P et al. Induction of neutralising antibodies by virus-like particles harbouring surface proteins from highly pathogenic H5N1 and H7N1 influenza viruses. Virol. J.3, 70 (2006).
   PubMed Web of Science ®Google Scholar
• Krammer F, Nakowitsch S, Messner P et al. 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 (2009).
   Google Scholar
• Quan FS, Vunnava A, Compans RW, Kang SM. Virus-like particle vaccine protects against 2009 H1N1 pandemic influenza virus in mice. PLoS One5(2), e9161 (2010).
   PubMed Web of Science ®Google Scholar
• 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).
   PubMed Web of Science ®Google Scholar
• Kang SM, Song JM, Quan FS, Compans RW. Influenza vaccines based on virus-like particles. Virus Res.143(2), 140–146 (2009).
   PubMed Web of Science ®Google Scholar
• Liu WJ, Liu XS, Zhao KN, Leggatt GR, Frazer IH. Papillomavirus virus-like particles for the delivery of multiple cytotoxic T cell epitopes. Virology273(2), 374–382 (2000).
   PubMed Web of Science ®Google Scholar
• Zamora E, Handisurya A, Shafti-Keramat S et al. Papillomavirus-like particles are an effective platform for amyloid-β immunization in rabbits and transgenic mice. J. Immunol.177(4), 2662–2670 (2006).
   PubMed Web of Science ®Google Scholar
• Kratz PA, Bottcher B, Nassal M. Native display of complete foreign protein domains on the surface of hepatitis B virus capsids. Proc. Natl Acad. Sci. USA96(5), 1915–1920 (1999).
   PubMed Web of Science ®Google Scholar
• Lee KW, Tan WS. Recombinant hepatitis B virus core particles: association, dissociation and encapsidation of green fluorescent protein. J. Virol. Methods151, 172–180 (2008).
   PubMed Web of Science ®Google Scholar
• Mihailova M, Boos M, Petrovskis I et al. Recombinant virus-like particles as a carrier of B- and T-cell epitopes of hepatitis C virus (HCV). Vaccine24(20), 4369–4377 (2006).
   PubMed Web of Science ®Google Scholar
• Pumpens P, Grens E. HBV core particles as a carrier for B cell/T cell epitopes. Intervirology44(2–3), 98–114 (2001).
   PubMed Web of Science ®Google Scholar
• Pumpens P, Razanskas R, Pushko P et al. Evaluation of HBs, HBc, and frCP virus-like particles for expression of human papillomavirus 16 E7 oncoprotein epitopes. Intervirology45(1), 24–32 (2002).
   PubMed Web of Science ®Google Scholar
• De Filette M, Min Jou W, Birkett A et al. Universal influenza A vaccine: optimization of M2-based constructs. Virology337(1), 149–161 (2005).
   PubMed Web of Science ®Google Scholar
• Jin H, Xiao W, Xiao C et al. Protective immune responses against foot-and-mouth disease virus by vaccination with a DNA vaccine expressing virus-like particles. Viral Immunol.20(3), 429–440 (2007).
   Google Scholar
• Bisht H, Chugh DA, Raje M, Swaminathan SS, Khanna N. Recombinant dengue virus type 2 envelope/hepatitis B surface antigen hybrid protein expressed in Pichia pastoris can function as a bivalent immunogen. J. Biotechnol.99(2), 97–110 (2002).
   PubMedGoogle Scholar
• Eckhart L, Raffelsberger W, Ferko B et al. Immunogenic presentation of a conserved gp41 epitope of human immunodeficiency virus type 1 on recombinant surface antigen of hepatitis B virus. J. Gen. Virol.77(Pt 9), 2001–2008 (1996).
   PubMed Web of Science ®Google Scholar
• Netter HJ, Macnaughton TB, Woo WP, Tindle R, Gowans EJ. Antigenicity and immunogenicity of novel chimeric hepatitis B surface antigen particles with exposed hepatitis C virus epitopes. J. Virol.75(5), 2130–2141 (2001).
   PubMed Web of Science ®Google Scholar
• Schlienger K, Mancini M, Riviere Y et al. Human immunodeficiency virus type 1 major neutralizing determinant exposed on hepatitis B surface antigen particles is highly immunogenic in primates. J. Virol.66(4), 2570–2576 (1992).
   PubMedGoogle Scholar
• Niikura M, Takamura S, Kim G et al. Chimeric recombinant hepatitis E virus-like particles as an oral vaccine vehicle presenting foreign epitopes. Virology293(2), 273–280 (2002).
   PubMed Web of Science ®Google Scholar
• Deml L, Speth C, Dierich MP, Wolf H, Wagner R. Recombinant HIV-1 Pr55gag virus-like particles: potent stimulators of innate and acquired immune responses. Mol. Immunol.42(2), 259–277 (2005).
   PubMed Web of Science ®Google Scholar
• Doan LX, Li M, Chen C, Yao Q. Virus-like particles as HIV-1 vaccines. Rev. Med. Virol.15(2), 75–88 (2005).
   PubMed Web of Science ®Google Scholar
• Buonaguro L, Buonaguro FM, Tornesello ML et al. 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(1), 35–47 (2001).
   PubMed Web of Science ®Google Scholar
• Guo L, Lu X, Kang SM et al. Enhancement of mucosal immune responses by chimeric influenza HA/SHIV virus-like particles. Virology313(2), 502–513 (2003).
   PubMed Web of Science ®Google Scholar
• Dale CJ, Liu XS, De Rose R et al. Chimeric human papilloma virus-simian/human immunodeficiency virus virus-like-particle vaccines: immunogenicity and protective efficacy in macaques. Virology301(1), 176–187 (2002).
   PubMed Web of Science ®Google Scholar
• Frazer IH, Quinn M, Nicklin JL et al. Phase 1 study of HPV16-specific immunotherapy with E6E7 fusion protein and ISCOMATRIX adjuvant in women with cervical intraepithelial neoplasia. Vaccine23(2), 172–181 (2004).
   PubMed Web of Science ®Google Scholar
• Sadeyen JR, Tourne S, Shkreli M, Sizaret PY, Coursaget P. Insertion of a foreign sequence on capsid surface loops of human papillomavirus type 16 virus-like particles reduces their capacity to induce neutralizing antibodies and delineates a conformational neutralizing epitope. Virology309(1), 32–40 (2003).
   PubMed Web of Science ®Google Scholar
• Wakabayashi MT, Da Silva DM, Potkul RK, Kast WM. Comparison of human papillomavirus type 16 L1 chimeric virus-like particles versus L1/L2 chimeric virus-like particles in tumor prevention. Intervirology45(4–6), 300–307 (2002).
   PubMed Web of Science ®Google Scholar
• Paz De la Rosa G, Monroy-Garcia A, Mora-Garcia Mde L et al. An HPV 16 L1-based chimeric human papilloma virus-like particles containing a string of epitopes produced in plants is able to elicit humoral and cytotoxic T-cell activity in mice. Virol. J.6, 2 (2009).
   Google Scholar
• Oh YK, Sohn T, Park JS et al. Enhanced mucosal and systemic immunogenicity of human papillomavirus-like particles encapsidating interleukin-2 gene adjuvant. Virology328(2), 266–273 (2004).
   PubMedGoogle Scholar
• Chackerian B, Rangel M, Hunter Z, Peabody DS. Virus and virus-like particle-based immunogens for Alzheimer’s disease induce antibody responses against amyloid-β without concomitant T cell responses. Vaccine24(37–39), 6321–6331 (2006).
   PubMed Web of Science ®Google Scholar
• Krammer F, Schinko T, Messner P et al. Influenza virus-like particles as an antigen-carrier platform for the ESAT-6 epitope of Mycobacterium tuberculosis. J. Virol. Methods167(1), 17–22 (2010).
   PubMed Web of Science ®Google Scholar
• Citkowicz A, Petry H, Harkins RN et al. Characterization of virus-like particle assembly for DNA delivery using asymmetrical flow field-flow fractionation and light scattering. Anal. Biochem.376(2), 163–172 (2008).
   PubMed Web of Science ®Google Scholar
• Brinkman M, Walter J, Grein S et al. Beneficial therapeutic effects with different particulate structures of murine polyomavirus VP1-coat protein carrying self or non-self CD8 T cell epitopes against murine melanoma. Cancer Immunol. Immunother.54(6), 611–622 (2005).
   PubMed Web of Science ®Google Scholar
• Amexis G, Young NS. Parvovirus B19 empty capsids as antigen carriers for presentation of antigenic determinants of dengue 2 virus. J. Infect. Dis.194(6), 790–794 (2006).
   PubMed Web of Science ®Google Scholar
• Maurer P, Bachmann MF. Therapeutic vaccines for nicotine dependence. Curr. Opin. Mol. Ther.8(1), 11–16 (2006).
   PubMed Web of Science ®Google Scholar
• Spohn G, Keller I, Beck M et al. Active immunization with IL-1 displayed on virus-like particles protects from autoimmune arthritis. Eur. J. Immunol.38(3), 877–887 (2008).
   PubMed Web of Science ®Google Scholar
• Peacey M, Wilson S, Baird MA, Ward VK. Versatile RHDV virus-like particles: incorporation of antigens by genetic modification and chemical conjugation. Biotechnol. Bioeng.98(5), 968–977 (2007).
   PubMedGoogle Scholar
• Kimchi-Sarfaty C, Gottesman MM. SV40 pseudovirions as highly efficient vectors for gene transfer and their potential application in cancer therapy. Curr. Pharm. Biotechnol.5(5), 451–458 (2004).
   Google Scholar
• Takahashi RU, Kanesashi SN, Inoue T et al. Presentation of functional foreign peptides on the surface of SV40 virus-like particles. J. Biotechnol.135(4), 385–392 (2008).
   PubMed Web of Science ®Google Scholar