昆虫杆状病毒表达载体系统在疫苗研究中的应用进展
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摘要
昆虫杆状病毒表达载体系统(Baculovirus expression vector system,BEVS)已成功应用于多种蛋白的表达,并为疫苗开发提供了充足的原材料。相比其他表达系统,BEVS具有许多优势:杆状病毒专一寄生于无脊椎动物,安全性高;重组蛋白表达水平高;可对重组蛋白进行正确折叠和翻译后修饰,获得具有生物活性的蛋白;适应于多基因表达如病毒样颗粒(Virus-like particle)的复杂设计;适用于大规模无血清培养等。为了更好地理解BEVS在疫苗研究中的应用前景,文中将从BEVS的发展及其在疫苗研究中的应用等方面进行综述。
Baculovirus expression vector system(BEVS) has been successfully applied to the over-expression of various proteins, thus providing sufficient materials for vaccine research. Compared to other systems, BEVS has many advantages:baculovirus solely being parasitic in invertebrates, the resultant products conferring high safety to mammalian, high expression level of recombinant proteins, preferable folding for eukaryotic protein, proper post-translational modification required for biological function, suitable for multiple genes co-expression and large-scale production with serum-free culture media. To better understand the advantages and prospective of BEVS for the vaccine research, this article will review the development of BEVS and its application on vaccine research.
Baculovirus expression vector system(BEVS) has been successfully applied to the over-expression of various proteins, thus providing sufficient materials for vaccine research. Compared to other systems, BEVS has many advantages:baculovirus solely being parasitic in invertebrates, the resultant products conferring high safety to mammalian, high expression level of recombinant proteins, preferable folding for eukaryotic protein, proper post-translational modification required for biological function, suitable for multiple genes co-expression and large-scale production with serum-free culture media. To better understand the advantages and prospective of BEVS for the vaccine research, this article will review the development of BEVS and its application on vaccine research.
引文
[1]Kong M,Zuo H,Zhu FF,et al.The interaction between baculoviruses and their insect hosts.Dev Comp Immunol,2018,83:114-123.
[2]Liu YP,Wang FH,Sun ZJ,et al.Progress of studies and application on baculovirus expression vector system.Chin Bull Entomol,2006,43(1):1-5(in Chinese).刘永平,王方海,苏志坚,等.昆虫杆状病毒表达载体系统的研究及应用.昆虫知识,2006,43(1):1-5.
[3]King AMQ,Adams MJ,Carstens EB,et al.Ninth Report of the International Committee on Taxonomy of Viruses.London:Elsevier,2012.
[4]Blissard GW,Rohrmann GF.Baculovirus diversity and molecular biology.Annu Rev Entomol,1990,35:127-155.
[5]Smith GE,Summers MD,Fraser MJ.Production of human beta interferon in insect cells infected with a baculovirus expression vector.Mol Cell Biol,1983,3(12):2156-2165.
[6]Sokolenko S,George S,Wagner A,et al.Co-expression vs.co-infection using baculovirus expression vectors in insect cell culture:benefits and drawbacks.Biotechnol Adv,2012,30(3):766-781.
[7]Feng M,Wu XF.Research progresses in the interaction between baculovirus envelope protein gp64and host cell surface factors.Sci Seric,2014,40(5):911-916(in Chinese).冯敏,吴小峰.昆虫杆状病毒囊膜蛋白GP64与宿主细胞表面因子互作的研究综述.蚕业科学,2014,40(5):911-916.
[8]Hu YC,Yao K,Wu TY.Baculovirus as an expression and/or delivery vehicle for vaccine antigens.Expert Rev Vaccines,2008,7(3):363-371.
[9]Lee GJ,Lee SH,Lee YJ,et al.Nanostructural characterization of Sf9 cells during virus-like particles generation.Scanning,2016,38(6):735-742.
[10]Krammer F,Schinko T,Palmberger D,et al.Trichoplusia ni cells(High FiveTM)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,2010,45(3):226-234.
[11]Baxter R,Patriarca PA,Ensor K,et al.Evaluation of the safety,reactogenicity and immunogenicity of FluBlok?trivalent recombinant baculovirusexpressed hemagglutinin influenza vaccine administered intramuscularly to healthy adults 50-64years of age.Vaccine,2011,29(12):2272-2278.
[12]Legardinier S,Klett D,Poirier JC,et al.Mammalian-like nonsialyl complex-type N-glycosylation of equine gonadotropins in MimicTMinsect cells.Glycobiology,2005,15(8):776-790.
[13]Steele KH,Stone BJ,Franklin KM,et al.Improving the baculovirus expression vector system with vankyrin-enhanced technology.Biotechnol Prog,2017,33(6):1496-1507.
[14]Hashimoto Y,Zhang S,Zhang SY,et al.Erratum to:BTI-Tnao38,a new cell line derived from Trichoplusia ni,is permissive for AcMNPV infection and produces high levels of recombinant proteins BMC Biotechnol,2012,12:12.
[15]Kitts PA,Possee RD.A method for producing recombinant baculovirus expression vectors at high frequency.Biotechniques,1993,14(5):810-817.
[16]Hitchman RB,Possee RD,King LA.Baculovirus expression systems for recombinant protein production in insect cells.Recent Pat Biotechnol2009,3(1):46-54.
[17]Luckow VA,Lee SC,Barry GF,et al.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,1993,67(8):4566-4579.
[18]Patel G,Nasmyth K,Jones N.A new method for the isolation of recombinant baculovirus.Nucleic Acids Res,1992,20(1):97-104.
[19]Kaba SA,Salcedo AM,Wafula PO,et al.Development of a chitinase and v-cathepsin negative bacmid for improved integrity of secreted recombinant proteins.J Virol Methods,2004,122(1):113-118.
[20]Ishimwe E,Hodgson JJ,Passarelli AL.Expression of the Cydia pomonella granulovirus matrix metalloprotease enhances Autographa californica multiple nucleopolyhedrovirus virulence and can partially substitute for viral cathepsin.Virology2015,481:166-178.
[21]Bieniossek C,Imasaki T,Takagi Y,et al.MultiBac:expanding the research toolbox for multiprotein complexes.Trends Biochem Sci,2012,37(2):49-57.
[22]Weissmann F,Petzold G,VanderLinden R,et al.biGBac enables rapid gene assembly for the expression of large multisubunit protein complexes.Proc Natl Acad Sci USA,2016,113(19):E2564-E2569.
[23]Zhang ZG,Yang J,Barford D.Recombinant expression and reconstitution of multiprotein complexes by the USER cloning method in the insect cell-baculovirus expression system.Methods,2016,95:13-25.
[24]Martínez-Solís M,Gómez-Sebastián S,Escribano JM,et al.A novel baculovirus-derived promoter with high activity in the baculovirus expression system.PeerJ,2016,4(11):e2183.
[25]Bleckmann M,Schürig M,Chen FF,et al.Identification of essential genetic baculoviral elements for recombinant protein expression by transactivation in Sf21 insect cells.PLoS ONE,2016,11(3):e0149424.
[26]Zhang XY,Xu KY,Ou YM,et al.Development of a baculovirus vector carrying a small hairpin RNA for suppression of sf-caspase-1 expression and improvement of recombinant protein production BMC Biotechnol,2018,18:24.
[27]Liu Q,Ding C.Advances in research of partial functional genes of baculovirus.Chin J Virol,2001,17(2):183-187(in Chinese).刘强,丁翠.杆状病毒部分功能基因的研究进展.病毒学报,2001,17(2):183-187.
[28]Berger I,Fitzgerald DJ,Richmond TJ.Baculovirus expression system for heterologous multiprotein complexes.Nat Biotechnol,2004,22(12):1583-1587.
[29]Hitchman RB,Possee RD,Crombie AT,et al.Genetic modification of a baculovirus vector for increased expression in insect cells.Cell Biol Toxicol,2010,26(1):57-68.
[30]Keil GM,Pollin R,Müller C,et al.BacMam platform for vaccine antigen delivery//Brun A,Ed.Vaccine Technologies for Veterinary Viral Diseases.New York:Humana Press,2016:105-119.
[31]Drugmand JC,Schneider YJ,Agathos SN.Insect cells as factories for biomanufacturing.Biotechnol Adv,2012,30(5):1140-1157.
[32]Vicente T,Rold?o A,Peixoto C,et al.Large-scale production and purification of VLP-based vaccines.JInvertebr Pathol,2011,107(S1):S42-S48.
[33]Mena JA,Kamen AA.Insect cell technology is a versatile and robust vaccine manufacturing platform.Expert Rev Vaccines,2011,10(7):1063-1081.
[34]Cutts FT,Franceschi S,Goldie S,et al.Human papillomavirus and HPV vaccines:a review.Bull World Health Organ,2007,85(9):719-726.
[35]Cox MMJ,Patriarca PA,Treanor J.FluBlok,a recombinant hemagglutinin influenza vaccine.Influenza Other Respi Viruses,2008,2(6):211-219.
[36]Harper DM,Franco EL,Wheeler C,et al.Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and18 in young women:a randomised controlled trial.Lancet,2004,364(9447):1757-1765.
[37]Harper DM,Franco EL,Wheeler CM,et al.Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types16 and 18:follow-up from a randomised control trial.Lancet,2006,367(9518):1247-1255.
[38]Paavonen J,Jenkins D,Bosch FX,et al.Efficacy of a prophylactic adjuvanted bivalent L1 virus-likeparticle vaccine against infection with human papillomavirus types 16 and 18 in young women:an interim analysis of a phase III double-blind,randomised controlled trial.Lancet,2007,369(9580):2161-2170.
[39]Paavonen J,Naud P,Salmerón J,et al.Efficacy of human papillomavirus(HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types(PATRICIA):final analysis of a double-blind,randomised study in young women.Lancet,2009,374(9686):301-314.
[40]Schwarz TF.Clinical update of the AS04-Adjuvanted human Papillomavirus-16/18 cervical cancer vaccine,cervarix?.Adv Ther,2009,26(11):983-998.
[41]Cox MMJ,Izikson R,Post P,et al.Safety,efficacy,and immunogenicity of Flublok in the prevention of seasonal influenza in adults.Ther Adv Vaccines,2015,3(4):97-108.
[42]Karch CP,Burkhard P.Vaccine technologies:from whole organisms to rationally designed protein assemblies.Biochem Pharmacol,2016,120:1-14.
[43]Keitel WA,Treanor JJ,El Sahly HM,et al.Comparative immunogenicity of recombinant influenza hemagglutinin(rHA)and trivalent inactivated vaccine(TIV)among persons≥65 years old.Vaccine,2009,28(2):379-385.
[44]Treanor JJ,El Sahly H,King J,et al.Protective efficacy of a trivalent recombinant hemagglutinin protein vaccine(FluBlok?)against influenza in healthy adults:a randomized,placebo-controlled trial.Vaccine,2011,29(44):7733-7739.
[45]Uttenthal?,Le Potier MF,Romero L,et al.Classical swine fever(CSF)marker vaccine:trial I.Challenge studies in weaner pigs.Vet Microbiol,2001,83(2):85-106.
[46]Depner KR,Bouma A,Koenen F,et al.Classical swine fever(CSF)marker vaccine:trial II.Challenge study in pregnant sows.Vet Microbiol,2001,83(2):107-120.
[47]van Oirschot JT.Vaccinology of classical swine fever:from lab to field.Vet Microbiol,2003,96(4):367-384.
[48]Moormann RJM,Bouma A,Kramps JA,et al.Development of a classical swine fever subunit marker vaccine and companion diagnostic test.Vet Microbiol,2000,73(2/3):209-219.
[49]Fachinger V,Bischoff R,Jedidia SB,et al.The effect of vaccination against porcine circovirus type 2 in pigs suffering from porcine respiratory disease complex.Vaccine,2008,26(11):1488-1499.
[50]Segalés J.Best practice and future challenges for vaccination against porcine circovirus type 2.Expert Rev Vaccines,2015,14(3):473-487.
[51]Blanchard P,MahéD,Cariolet R,et al.Protection of swine against post-weaning multisystemic wasting syndrome(PMWS)by porcine circovirus type 2(PCV2)proteins.Vaccine,2003,21(31):4565-4575.
[52]Beam CA,MacCallum C,Herold KC,et al.GADvaccine reduces insulin loss in recently diagnosed type 1 diabetes:findings from a Bayesian meta-analysis.Diabetologia,2017,60(1):43-49.
[53]Agardh CD,Lynch KF,Palmér M,et al.GAD65vaccination:5 years of follow-up in a randomised dose-escalating study in adult-onset autoimmune diabetes.Diabetologia,2009,52(7):1363-1368.
[54]El-Kamary SS,Pasetti MF,Mendelman PM,et al.Adjuvanted intranasal norwalk virus-like particle vaccine elicits antibodies and antibody-secreting cells that express homing receptors for mucosal and peripheral lymphoid tissues.J Infect Dis,2010,202(11):1649-1658.
[55]Atmar RL,Bernstein DI,Harro CD,et al.Norovirus vaccine against experimental human norwalk virus illness.New Engl J Med,2011,365(23):2178-2187.
[56]Smith G,Raghunandan R,Wu YY,et al.Respiratory syncytial virus fusion glycoprotein expressed in insect cells form protein nanoparticles that induce protective immunity in cotton rats.PLoS ONE,2012,7(11):e50852.
[57]Fries L,Shinde V,Stoddard JJ,et al.Immunogenicity and safety of a respiratory syncytial virus fusion protein(RSV F)nanoparticle vaccine in older adults.Immun Ageing,2017,14:8.
[58]Smith G,Liu Y,Flyer D,et al.Novel hemagglutinin nanoparticle influenza vaccine with Matrix-MTMadjuvant induces hemagglutination inhibition,neutralizing,and protective responses in ferrets against homologous and drifted A(H3N2)subtypes.Vaccine,2017,35(40):5366-5372.
[59]López-Macías C,Ferat-Osorio E,Tenorio-Calvo Aet al.Safety and immunogenicity of a virus-like particle pandemic influenza A(H1N1)2009 vaccine in a blinded,randomized,placebo-controlled trial of adults in Mexico.Vaccine,2011,29(44):7826-7834.
[60]Bernstein DI,El Sahly HM,Keitel WA,et al.Safety and immunogenicity of a candidate parvovirus B19vaccine.Vaccine,2011,29(43):7357-7363.
[61]Raghunandan R,Lu HX,Zhou B,et al.An insect cell derived respiratory syncytial virus(RSV)Fnanoparticle vaccine induces antigenic site IIantibodies and protects against RSV challenge in cotton rats by active and passive immunization.Vaccine,2014,32(48):6485-6492.
[62]Hsieh MS,He JL,Wu TY,et al.A secretary bi-cistronic baculovirus expression system with improved production of the HA1 protein of H6influenza virus in insect cells and Spodoptera litura larvae.J Immunol Methods,2018,459:81-89.
[63]Dennehy PH.Rotavirus vaccines:an overview.Clin Microbiol Rev,2008,21(1):198-208.
[64]Renukaradhya GJ,Meng XJ,Calvert JG,et al Inactivated and subunit vaccines against porcine reproductive and respiratory syndrome:current status and future direction.Vaccine,2015,33(27):3065-3072.
[65]Crawford SE,LabbéM,Cohen J,et al.Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells.J Virol,1994,68(9):5945-5952.
[66]Driggers RW,Ho CY,Korhonen EM,et al.Zika virus infection with prolonged maternal viremia and fetal brain abnormalities.New Engl J Med,2016,374(22):2142-2151.
[67]Adams Waldorf KM,Stencel-Baerenwald JE,Kapur RP,et al.Fetal brain lesions after subcutaneous inoculation of Zika virus in a pregnant nonhuman primate.Nat Med,2016,22(11):1256-1259.
[68]Dai SY,Zhang T,Zhang YF,et al.Zika virus baculovirus-expressed virus-like particles induce neutralizing antibodies in mice.Virol Sin,2018,33(3):213-226.
[69]Zhang W,Dai WL,Zhang C,et al.A virus-like particle-based tetravalent vaccine for hand,foot,and mouth disease elicits broad and balanced protective immunity.Emerg Microbes Infect,2018,7:94.
[70]Yoshida S,Kondoh D,Arai E,et al.Baculovirus virions displaying Plasmodium berghei circumsporozoite protein protect mice against malaria sporozoite infection.Virology,2003,316(1):161-170.
[71]Prabakaran M,Velumani S,He F,et al.Protective immunity against influenza H5N1 virus challenge in mice by intranasal co-administration of baculovirus surface-displayed HA and recombinant CTB as an adjuvant.Virology,2008,380(2):412-420.
[72]Deng L,Mohan T,Chang TZ,et al.Double-layered protein nanoparticles induce broad protection against divergent influenza A viruses.Nat Commun,2018,9:359.
[73]Syed Musthaq S,Madhan S,Sahul Hameed AS,et al.Localization of VP28 on the baculovirus envelope and its immunogenicity against white spot syndrome virus in Penaeus monodon.Virology,2009,391(2):315-324.
[74]Lee JY,Chang J.Recombinant baculovirus-based vaccine expressing M2 protein induces protective CD8+T-cell immunity against respiratory syncytial virus infection.J Microbiol,2017,55(11):900-908.
[75]Sim SH,Kim JY,Seong BL,et al.Baculovirus displaying hemagglutinin elicits broad cross-protection against influenza in mice.PLoSONE,2016,11(3):e0152485.
[2]Liu YP,Wang FH,Sun ZJ,et al.Progress of studies and application on baculovirus expression vector system.Chin Bull Entomol,2006,43(1):1-5(in Chinese).刘永平,王方海,苏志坚,等.昆虫杆状病毒表达载体系统的研究及应用.昆虫知识,2006,43(1):1-5.
[3]King AMQ,Adams MJ,Carstens EB,et al.Ninth Report of the International Committee on Taxonomy of Viruses.London:Elsevier,2012.
[4]Blissard GW,Rohrmann GF.Baculovirus diversity and molecular biology.Annu Rev Entomol,1990,35:127-155.
[5]Smith GE,Summers MD,Fraser MJ.Production of human beta interferon in insect cells infected with a baculovirus expression vector.Mol Cell Biol,1983,3(12):2156-2165.
[6]Sokolenko S,George S,Wagner A,et al.Co-expression vs.co-infection using baculovirus expression vectors in insect cell culture:benefits and drawbacks.Biotechnol Adv,2012,30(3):766-781.
[7]Feng M,Wu XF.Research progresses in the interaction between baculovirus envelope protein gp64and host cell surface factors.Sci Seric,2014,40(5):911-916(in Chinese).冯敏,吴小峰.昆虫杆状病毒囊膜蛋白GP64与宿主细胞表面因子互作的研究综述.蚕业科学,2014,40(5):911-916.
[8]Hu YC,Yao K,Wu TY.Baculovirus as an expression and/or delivery vehicle for vaccine antigens.Expert Rev Vaccines,2008,7(3):363-371.
[9]Lee GJ,Lee SH,Lee YJ,et al.Nanostructural characterization of Sf9 cells during virus-like particles generation.Scanning,2016,38(6):735-742.
[10]Krammer F,Schinko T,Palmberger D,et al.Trichoplusia ni cells(High FiveTM)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,2010,45(3):226-234.
[11]Baxter R,Patriarca PA,Ensor K,et al.Evaluation of the safety,reactogenicity and immunogenicity of FluBlok?trivalent recombinant baculovirusexpressed hemagglutinin influenza vaccine administered intramuscularly to healthy adults 50-64years of age.Vaccine,2011,29(12):2272-2278.
[12]Legardinier S,Klett D,Poirier JC,et al.Mammalian-like nonsialyl complex-type N-glycosylation of equine gonadotropins in MimicTMinsect cells.Glycobiology,2005,15(8):776-790.
[13]Steele KH,Stone BJ,Franklin KM,et al.Improving the baculovirus expression vector system with vankyrin-enhanced technology.Biotechnol Prog,2017,33(6):1496-1507.
[14]Hashimoto Y,Zhang S,Zhang SY,et al.Erratum to:BTI-Tnao38,a new cell line derived from Trichoplusia ni,is permissive for AcMNPV infection and produces high levels of recombinant proteins BMC Biotechnol,2012,12:12.
[15]Kitts PA,Possee RD.A method for producing recombinant baculovirus expression vectors at high frequency.Biotechniques,1993,14(5):810-817.
[16]Hitchman RB,Possee RD,King LA.Baculovirus expression systems for recombinant protein production in insect cells.Recent Pat Biotechnol2009,3(1):46-54.
[17]Luckow VA,Lee SC,Barry GF,et al.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,1993,67(8):4566-4579.
[18]Patel G,Nasmyth K,Jones N.A new method for the isolation of recombinant baculovirus.Nucleic Acids Res,1992,20(1):97-104.
[19]Kaba SA,Salcedo AM,Wafula PO,et al.Development of a chitinase and v-cathepsin negative bacmid for improved integrity of secreted recombinant proteins.J Virol Methods,2004,122(1):113-118.
[20]Ishimwe E,Hodgson JJ,Passarelli AL.Expression of the Cydia pomonella granulovirus matrix metalloprotease enhances Autographa californica multiple nucleopolyhedrovirus virulence and can partially substitute for viral cathepsin.Virology2015,481:166-178.
[21]Bieniossek C,Imasaki T,Takagi Y,et al.MultiBac:expanding the research toolbox for multiprotein complexes.Trends Biochem Sci,2012,37(2):49-57.
[22]Weissmann F,Petzold G,VanderLinden R,et al.biGBac enables rapid gene assembly for the expression of large multisubunit protein complexes.Proc Natl Acad Sci USA,2016,113(19):E2564-E2569.
[23]Zhang ZG,Yang J,Barford D.Recombinant expression and reconstitution of multiprotein complexes by the USER cloning method in the insect cell-baculovirus expression system.Methods,2016,95:13-25.
[24]Martínez-Solís M,Gómez-Sebastián S,Escribano JM,et al.A novel baculovirus-derived promoter with high activity in the baculovirus expression system.PeerJ,2016,4(11):e2183.
[25]Bleckmann M,Schürig M,Chen FF,et al.Identification of essential genetic baculoviral elements for recombinant protein expression by transactivation in Sf21 insect cells.PLoS ONE,2016,11(3):e0149424.
[26]Zhang XY,Xu KY,Ou YM,et al.Development of a baculovirus vector carrying a small hairpin RNA for suppression of sf-caspase-1 expression and improvement of recombinant protein production BMC Biotechnol,2018,18:24.
[27]Liu Q,Ding C.Advances in research of partial functional genes of baculovirus.Chin J Virol,2001,17(2):183-187(in Chinese).刘强,丁翠.杆状病毒部分功能基因的研究进展.病毒学报,2001,17(2):183-187.
[28]Berger I,Fitzgerald DJ,Richmond TJ.Baculovirus expression system for heterologous multiprotein complexes.Nat Biotechnol,2004,22(12):1583-1587.
[29]Hitchman RB,Possee RD,Crombie AT,et al.Genetic modification of a baculovirus vector for increased expression in insect cells.Cell Biol Toxicol,2010,26(1):57-68.
[30]Keil GM,Pollin R,Müller C,et al.BacMam platform for vaccine antigen delivery//Brun A,Ed.Vaccine Technologies for Veterinary Viral Diseases.New York:Humana Press,2016:105-119.
[31]Drugmand JC,Schneider YJ,Agathos SN.Insect cells as factories for biomanufacturing.Biotechnol Adv,2012,30(5):1140-1157.
[32]Vicente T,Rold?o A,Peixoto C,et al.Large-scale production and purification of VLP-based vaccines.JInvertebr Pathol,2011,107(S1):S42-S48.
[33]Mena JA,Kamen AA.Insect cell technology is a versatile and robust vaccine manufacturing platform.Expert Rev Vaccines,2011,10(7):1063-1081.
[34]Cutts FT,Franceschi S,Goldie S,et al.Human papillomavirus and HPV vaccines:a review.Bull World Health Organ,2007,85(9):719-726.
[35]Cox MMJ,Patriarca PA,Treanor J.FluBlok,a recombinant hemagglutinin influenza vaccine.Influenza Other Respi Viruses,2008,2(6):211-219.
[36]Harper DM,Franco EL,Wheeler C,et al.Efficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and18 in young women:a randomised controlled trial.Lancet,2004,364(9447):1757-1765.
[37]Harper DM,Franco EL,Wheeler CM,et al.Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types16 and 18:follow-up from a randomised control trial.Lancet,2006,367(9518):1247-1255.
[38]Paavonen J,Jenkins D,Bosch FX,et al.Efficacy of a prophylactic adjuvanted bivalent L1 virus-likeparticle vaccine against infection with human papillomavirus types 16 and 18 in young women:an interim analysis of a phase III double-blind,randomised controlled trial.Lancet,2007,369(9580):2161-2170.
[39]Paavonen J,Naud P,Salmerón J,et al.Efficacy of human papillomavirus(HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types(PATRICIA):final analysis of a double-blind,randomised study in young women.Lancet,2009,374(9686):301-314.
[40]Schwarz TF.Clinical update of the AS04-Adjuvanted human Papillomavirus-16/18 cervical cancer vaccine,cervarix?.Adv Ther,2009,26(11):983-998.
[41]Cox MMJ,Izikson R,Post P,et al.Safety,efficacy,and immunogenicity of Flublok in the prevention of seasonal influenza in adults.Ther Adv Vaccines,2015,3(4):97-108.
[42]Karch CP,Burkhard P.Vaccine technologies:from whole organisms to rationally designed protein assemblies.Biochem Pharmacol,2016,120:1-14.
[43]Keitel WA,Treanor JJ,El Sahly HM,et al.Comparative immunogenicity of recombinant influenza hemagglutinin(rHA)and trivalent inactivated vaccine(TIV)among persons≥65 years old.Vaccine,2009,28(2):379-385.
[44]Treanor JJ,El Sahly H,King J,et al.Protective efficacy of a trivalent recombinant hemagglutinin protein vaccine(FluBlok?)against influenza in healthy adults:a randomized,placebo-controlled trial.Vaccine,2011,29(44):7733-7739.
[45]Uttenthal?,Le Potier MF,Romero L,et al.Classical swine fever(CSF)marker vaccine:trial I.Challenge studies in weaner pigs.Vet Microbiol,2001,83(2):85-106.
[46]Depner KR,Bouma A,Koenen F,et al.Classical swine fever(CSF)marker vaccine:trial II.Challenge study in pregnant sows.Vet Microbiol,2001,83(2):107-120.
[47]van Oirschot JT.Vaccinology of classical swine fever:from lab to field.Vet Microbiol,2003,96(4):367-384.
[48]Moormann RJM,Bouma A,Kramps JA,et al.Development of a classical swine fever subunit marker vaccine and companion diagnostic test.Vet Microbiol,2000,73(2/3):209-219.
[49]Fachinger V,Bischoff R,Jedidia SB,et al.The effect of vaccination against porcine circovirus type 2 in pigs suffering from porcine respiratory disease complex.Vaccine,2008,26(11):1488-1499.
[50]Segalés J.Best practice and future challenges for vaccination against porcine circovirus type 2.Expert Rev Vaccines,2015,14(3):473-487.
[51]Blanchard P,MahéD,Cariolet R,et al.Protection of swine against post-weaning multisystemic wasting syndrome(PMWS)by porcine circovirus type 2(PCV2)proteins.Vaccine,2003,21(31):4565-4575.
[52]Beam CA,MacCallum C,Herold KC,et al.GADvaccine reduces insulin loss in recently diagnosed type 1 diabetes:findings from a Bayesian meta-analysis.Diabetologia,2017,60(1):43-49.
[53]Agardh CD,Lynch KF,Palmér M,et al.GAD65vaccination:5 years of follow-up in a randomised dose-escalating study in adult-onset autoimmune diabetes.Diabetologia,2009,52(7):1363-1368.
[54]El-Kamary SS,Pasetti MF,Mendelman PM,et al.Adjuvanted intranasal norwalk virus-like particle vaccine elicits antibodies and antibody-secreting cells that express homing receptors for mucosal and peripheral lymphoid tissues.J Infect Dis,2010,202(11):1649-1658.
[55]Atmar RL,Bernstein DI,Harro CD,et al.Norovirus vaccine against experimental human norwalk virus illness.New Engl J Med,2011,365(23):2178-2187.
[56]Smith G,Raghunandan R,Wu YY,et al.Respiratory syncytial virus fusion glycoprotein expressed in insect cells form protein nanoparticles that induce protective immunity in cotton rats.PLoS ONE,2012,7(11):e50852.
[57]Fries L,Shinde V,Stoddard JJ,et al.Immunogenicity and safety of a respiratory syncytial virus fusion protein(RSV F)nanoparticle vaccine in older adults.Immun Ageing,2017,14:8.
[58]Smith G,Liu Y,Flyer D,et al.Novel hemagglutinin nanoparticle influenza vaccine with Matrix-MTMadjuvant induces hemagglutination inhibition,neutralizing,and protective responses in ferrets against homologous and drifted A(H3N2)subtypes.Vaccine,2017,35(40):5366-5372.
[59]López-Macías C,Ferat-Osorio E,Tenorio-Calvo Aet al.Safety and immunogenicity of a virus-like particle pandemic influenza A(H1N1)2009 vaccine in a blinded,randomized,placebo-controlled trial of adults in Mexico.Vaccine,2011,29(44):7826-7834.
[60]Bernstein DI,El Sahly HM,Keitel WA,et al.Safety and immunogenicity of a candidate parvovirus B19vaccine.Vaccine,2011,29(43):7357-7363.
[61]Raghunandan R,Lu HX,Zhou B,et al.An insect cell derived respiratory syncytial virus(RSV)Fnanoparticle vaccine induces antigenic site IIantibodies and protects against RSV challenge in cotton rats by active and passive immunization.Vaccine,2014,32(48):6485-6492.
[62]Hsieh MS,He JL,Wu TY,et al.A secretary bi-cistronic baculovirus expression system with improved production of the HA1 protein of H6influenza virus in insect cells and Spodoptera litura larvae.J Immunol Methods,2018,459:81-89.
[63]Dennehy PH.Rotavirus vaccines:an overview.Clin Microbiol Rev,2008,21(1):198-208.
[64]Renukaradhya GJ,Meng XJ,Calvert JG,et al Inactivated and subunit vaccines against porcine reproductive and respiratory syndrome:current status and future direction.Vaccine,2015,33(27):3065-3072.
[65]Crawford SE,LabbéM,Cohen J,et al.Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells.J Virol,1994,68(9):5945-5952.
[66]Driggers RW,Ho CY,Korhonen EM,et al.Zika virus infection with prolonged maternal viremia and fetal brain abnormalities.New Engl J Med,2016,374(22):2142-2151.
[67]Adams Waldorf KM,Stencel-Baerenwald JE,Kapur RP,et al.Fetal brain lesions after subcutaneous inoculation of Zika virus in a pregnant nonhuman primate.Nat Med,2016,22(11):1256-1259.
[68]Dai SY,Zhang T,Zhang YF,et al.Zika virus baculovirus-expressed virus-like particles induce neutralizing antibodies in mice.Virol Sin,2018,33(3):213-226.
[69]Zhang W,Dai WL,Zhang C,et al.A virus-like particle-based tetravalent vaccine for hand,foot,and mouth disease elicits broad and balanced protective immunity.Emerg Microbes Infect,2018,7:94.
[70]Yoshida S,Kondoh D,Arai E,et al.Baculovirus virions displaying Plasmodium berghei circumsporozoite protein protect mice against malaria sporozoite infection.Virology,2003,316(1):161-170.
[71]Prabakaran M,Velumani S,He F,et al.Protective immunity against influenza H5N1 virus challenge in mice by intranasal co-administration of baculovirus surface-displayed HA and recombinant CTB as an adjuvant.Virology,2008,380(2):412-420.
[72]Deng L,Mohan T,Chang TZ,et al.Double-layered protein nanoparticles induce broad protection against divergent influenza A viruses.Nat Commun,2018,9:359.
[73]Syed Musthaq S,Madhan S,Sahul Hameed AS,et al.Localization of VP28 on the baculovirus envelope and its immunogenicity against white spot syndrome virus in Penaeus monodon.Virology,2009,391(2):315-324.
[74]Lee JY,Chang J.Recombinant baculovirus-based vaccine expressing M2 protein induces protective CD8+T-cell immunity against respiratory syncytial virus infection.J Microbiol,2017,55(11):900-908.
[75]Sim SH,Kim JY,Seong BL,et al.Baculovirus displaying hemagglutinin elicits broad cross-protection against influenza in mice.PLoSONE,2016,11(3):e0152485.