The application of virus-like particles as vaccines and biological vehicles

Applied Microbiology and Biotechnology

Volumn 99, Issue 24, 2015, Pages 10415-10432

  Yan, Dan ^a   Wei, Yan Quan ^a   Guo, Hui Chen ^a   Sun, Shi Qi ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Diagnostic technology; Drug delivery; Vaccine; Virus like particles; VLPs

Indexed keywords

AMINO ACIDS; BIOCOMPATIBILITY; DIAGNOSIS; DISEASE CONTROL; DRUG DELIVERY; EPITOPES; VACCINES;

CONTROL AND PREVENTION; DIAGNOSTIC TECHNOLOGIES; GLUTAMIC ACID RESIDUES; LARGE SURFACE AREA; STRUCTURAL PROTEINS; THERAPEUTIC VACCINES; VIRUS-LIKE PARTICLES; VLPS;

VIRUSES;

DRUG CARRIER; DRUG VEHICLE; EPITOPE; INACTIVATED VACCINE; LIVE VACCINE; NANOMATERIAL; VIRUS LIKE PARTICLE VACCINE; VIRUS PROTEIN; VIROSOME;

AMINO ACID; ANTIGEN; CHEMICAL METHOD; DISEASE CONTROL; DRUG; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC ENGINEERING; PROTEIN; VACCINE; VIRUS PARTICLE;

AMINO ACID SEQUENCE; BIOCOMPATIBILITY; CELL TRANSPORT; CHRONIC DISEASE; CONJUGATION; DISEASE CONTROL; DRUG DELIVERY SYSTEM; EPIDEMIC; HEPATITIS A; HUMAN; HUMORAL IMMUNITY; IMMUNOLOGICAL TOLERANCE; INFLUENZA; INNATE IMMUNITY; MEASLES; MUMPS; NONHUMAN; POLIOMYELITIS VIRUS; PROPHYLAXIS; RECOMBINANT DNA TECHNOLOGY; REVIEW; RUBELLA; SOLUBILITY; SURFACE AREA; TUMOR GROWTH; VACCINATION; VIRUS CAPSID; VIRUS LIKE AGENT; VIRUS MORPHOLOGY; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM;

MIRIDAE;

DRUG CARRIERS; DRUG DELIVERY SYSTEMS; VACCINES, VIRUS-LIKE PARTICLE; VIROSOMES;

EID: 84948380716     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-015-7000-8     Document Type: Review

References (217)

1. Acuna R, Cifuentes-Munoz N, Marquez C, Bulling M, Klingstrom J, Mancini R, Lozach PY, Tischler ND (2013) Hantavirus Gn and Gc glycoproteins self-assemble into virus-like particles. J Virol. doi:10.1128/JVI.03118-13
2. Agnello D, Herve CA, Lavaux A, Darniot M, Guillon P, Charpilienne A, Pothier P (2006) Intrarectal immunization with rotavirus 2/6 virus-like particles induces an antirotavirus immune response localized in the intestinal mucosa and protects against rotavirus infection in mice. J Virol 80(8):3823–3832. doi:10.1128/JVI.80.8.3823-3832.2006
3. Al-Barwani F, Donaldson B, Pelham SJ, Young SL, Ward VK (2014) Antigen delivery by virus-like particles for immunotherapeutic vaccination. Ther Deliv 5(11):1223–1240. doi:10.4155/tde.14.74
4. Amanna IJ, Slifka MK (2009) Wanted, dead or alive: new viral vaccines. Antiviral Res 84(2):119–130. doi:10.1016/j.antiviral.2009.08.008
5. Andrade S, Pinho F, Ribeiro AM, Carreira M, Casanueva FF, Roy P, Monteiro MP (2013) Immunization against active ghrelin using virus-like particles for obesity treatment. Curr Pharm Des 19(36):6551–6558
6. Arcangeli C, Circelli P, Donini M, Aljabali AA, Benvenuto E, Lomonossoff GP, Marusic C (2014) Structure-based design and experimental engineering of a plant virus nanoparticle for the presentation of immunogenic epitopes and as a drug carrier. J Biomol Struct Dyn 32(4):630–647. doi:10.1080/07391102.2013.785920
7. Arora U, Tyagi P, Swaminathan S, Khanna N (2012) Chimeric hepatitis B core antigen virus-like particles displaying the envelope domain III of dengue virus type 2. J Nanobiotechnol 10:30. doi:10.1186/1477-3155-10-30
8. Azizgolshani O, Garmann RF, Cadena-Nava R, Knobler CM, Gelbart WM (2013) Reconstituted plant viral capsids can release genes to mammalian cells. Virology 441(1):12–17. doi:10.1016/j.virol.2013.03.001
9. Bayer ME, Blumberg BS, Werner B (1968) Particles associated with Australia antigen in the sera of patients with leukaemia, Down’s syndrome and hepatitis. Nature 218(5146):1057–1059
10. Bazan SB, de Alencar Muniz Chaves A, Aires KA, Cianciarullo AM, Garcea RL, Ho PL (2009) Expression and characterization of HPV-16 L1 capsid protein in Pichia pastoris. Arch Virol 154(10):1609–1617. doi:10.1007/s00705-009-0484-8
11. Bellier B, Klatzmann D (2013) Virus-like particle-based vaccines against hepatitis C virus infection. Expert Rev Vaccines 12(2):143–154. doi:10.1586/erv.13.10
12. Blumberg BS, Alter HJ, Visnich S (1965) A “new” antigen in leukemia sera. JAMA 191:541–546
13. Boisgérault F, Morón G, Leclerc C (2002) Virus-like particles: a new family of delivery systems. Expert Rev Vaccines 1(1):101–109. doi:10.1586/14760584.1.1.101
14. Brady JN, Consigli RA (1978) Chromatographic separation of the polyoma virus proteins and renaturation of the isolated VP1 major capsid protein. J Virol 27(2):436–442
15. Brandenburg B, Stockl L, Gutzeit C, Roos M, Lupberger J, Schwartlander R, Gelderblom H, Sauer IM, Hofschneider PH, Hildt E (2005) A novel system for efficient gene transfer into primary human hepatocytes via cell-permeable hepatitis B virus-like particle. Hepatology 42(6):1300–1309. doi:10.1002/hep.20950
16. Bright RA, Carter DM, Daniluk S, Toapanta FR, Ahmad A, Gavrilov V, Massare M, Pushko P, Mytle N, Rowe T, Smith G, Ross TM (2007) Influenza virus-like particles elicit broader immune responses than whole virion inactivated influenza virus or recombinant hemagglutinin. Vaccine 25(19):3871–3878. doi:10.1016/j.vaccine.2007.01.106
17. Bright RA, Carter DM, Crevar CJ, Toapanta FR, Steckbeck JD, Cole KS, Kumar NM, Pushko P, Smith G, Tumpey TM, Ross TM (2008) Cross-clade protective immune responses to influenza viruses with H5N1 HA and NA elicited by an influenza virus-like particle. PLoS One 3(1):e1501. doi:10.1371/journal.pone.0001501
18. Brown SD, Fiedler JD, Finn MG (2009) Assembly of hybrid bacteriophage Qbeta virus-like particles. Biochemistry 48(47):11155–11157. doi:10.1021/bi901306p
19. Bucarey SA, Noriega J, Reyes P, Tapia C, Saenz L, Zuniga A, Tobar JA (2009) The optimized capsid gene of porcine circovirus type 2 expressed in yeast forms virus-like particles and elicits antibody responses in mice fed with recombinant yeast extracts. Vaccine 27(42):5781–5790. doi:10.1016/j.vaccine.2009.07.061
20. Buonaguro L, Tagliamonte M, Visciano ML (2013) Chemokine receptor interactions with virus-like particles. Methods Mol Biol 1013:57–66. doi:10.1007/978-1-62703-426-5_5
21. Burns CC, Diop OM, Sutter RW, Kew OM (2014) Vaccine-derived polioviruses. J Infect Dis 210(Suppl 1):S283–S293. doi:10.1093/infdis/jiu295
22. Chackerian B (2007) Virus-like particles: flexible platforms for vaccine development. Expert Rev Vaccines 6(3):381–390. doi:10.1586/14760584.6.3.381
23. Chackerian B, Lowy DR, Schiller JT (1999) Induction of autoantibodies to mouse CCR5 with recombinant papillomavirus particles. Proc Natl Acad Sci U S A 96(5):2373–2378
24. Chackerian B, Rangel M, Hunter Z, Peabody DS (2006) Virus and virus-like particle-based immunogens for Alzheimer’s disease induce antibody responses against amyloid-beta without concomitant T cell responses. Vaccine 24(37–39):6321–6331. doi:10.1016/j.vaccine.2006.05.059
25. Chandramouli S, Medina-Selby A, Coit D, Schaefer M, Spencer T, Brito LA, Zhang P, Otten G, Mandl CW, Mason PW, Dormitzer PR, Settembre EC (2013) Generation of a parvovirus B19 vaccine candidate. Vaccine 31(37):3872–3878. doi:10.1016/j.vaccine.2013.06.062
26. Charpilienne A, Nejmeddine M, Berois M, Parez N, Neumann E, Hewat E, Trugnan G, Cohen J (2001) Individual rotavirus-like particles containing 120 molecules of fluorescent protein are visible in living cells. J Biol Chem 276(31):29361–29367. doi:10.1074/jbc.M101935200
27. Chen LS, Wang M, Ou WC, Fung CY, Chen PL, Chang CF, Huang WS, Wang JY, Lin PY, Chang D (2010) Efficient gene transfer using the human JC virus-like particle that inhibits human colon adenocarcinoma growth in a nude mouse model. Gene Ther 17(8):1033–1041. doi:10.1038/gt.2010.50
28. Chen Y, Guo W, Xu Z, Yan Q, Luo Y, Shi Q, Chen D, Zhu L, Wang X (2011) A novel recombinant pseudorabies virus expressing parvovirus VP2 gene: immunogenicity and protective efficacy in swine. Virol J 8:307. doi:10.1186/1743-422X-8-307
29. Chen Z, Li C, Zhu Y, Wang B, Meng C, Liu G (2012) Immunogenicity of virus-like particles containing modified goose parvovirus VP2 protein. Virus Res 169(1):306–309. doi:10.1016/j.virusres.2012.08.009
30. Cheong WS, Reiseger J, Turner SJ, Boyd R, Netter HJ (2009) Chimeric virus-like particles for the delivery of an inserted conserved influenza A-specific CTL epitope. Antiviral Res 81(2):113–122. doi:10.1016/j.antiviral.2008.10.003
31. Chi JN, Wu CY, Chien MS, Wu PC, Wu CM, Huang C (2014) The preparation of porcine circovirus type 2 (PCV2) virus-like particles using a recombinant pseudorabies virus and its application to vaccine development. J Biotechnol 181:12–19. doi:10.1016/j.jbiotec.2014.04.006
32. Chiou SS, Crill WD, Chen LK, Chang GJ (2008) Enzyme-linked immunosorbent assays using novel Japanese encephalitis virus antigen improve the accuracy of clinical diagnosis of flavivirus infections. Clin Vaccine Immunol 15(5):825–835. doi:10.1128/CVI.00004-08
33. Chou MI, Hsieh YF, Wang M, Chang JT, Chang D, Zouali M, Tsay GJ (2010) In vitro and in vivo targeted delivery of IL-10 interfering RNA by JC virus-like particles. J Biomed Sci 17:51. doi:10.1186/1423-0127-17-51
34. Chroboczek J, Szurgot I, Szolajska E (2014) Virus-like particles as vaccine. Acta Biochim Pol 61(3):531–539
35. Chung YC, Huang JH, Lai CW, Sheng HC, Shih SR, Ho MS, Hu YC (2006) Expression, purification and characterization of enterovirus-71 virus-like particles. World J Gastroenterol 12(6):921–927
36. Chung YC, Ho MS, Wu JC, Chen WJ, Huang JH, Chou ST, Hu YC (2008) Immunization with virus-like particles of enterovirus 71 elicits potent immune responses and protects mice against lethal challenge. Vaccine 26(15):1855–1862. doi:10.1016/j.vaccine.2008.01.058
37. Clark KB, Lin SC, Humphrey C, Foytich K, Esona M, Wang Y, Liu M, Jiang B (2009) Expression and characterization of human group C rotavirus virus-like particles in insect cells. Virology 387(2):267–272. doi:10.1016/j.virol.2009.02.023
38. Cornuz J, Zwahlen S, Jungi WF, Osterwalder J, Klingler K, van Melle G, Bangala Y, Guessous I, Muller P, Willers J, Maurer P, Bachmann MF, Cerny T (2008) A vaccine against nicotine for smoking cessation: a randomized controlled trial. PLoS One 3(6):e2547. doi:10.1371/journal.pone.0002547
39. Cortes-Perez NG, Sapin C, Jaffrelo L, Daou S, Grill JP, Langella P, Seksik P, Beaugerie L, Chwetzoff S, Trugnan G (2010) Rotavirus-like particles: a novel nanocarrier for the gut. J Biomed Biotechnol 2010:317545. doi:10.1155/2010/317545
40. Cox MM (2005) Cell-based protein vaccines for influenza. Curr Opin Mol Ther 7(1):24–29
41. Cubas R, Zhang S, Li M, Chen C, Yao Q (2011) Chimeric Trop2 virus-like particles: a potential immunotherapeutic approach against pancreatic cancer. J Immunother 34(3):251–263. doi:10.1097/CJI.0b013e318209ee72
42. Deo VK, Yoshimatsu K, Otsuki T, Dong J, Kato T, Park EY (2013) Display of Neospora caninum surface protein related sequence 2 on Rous sarcoma virus-derived gag protein virus-like particles. J Biotechnol 165(1):69–75. doi:10.1016/j.jbiotec.2013.02.013
43. Di Martino B, Marsilio F, Roy P (2007) Assembly of feline calicivirus-like particle and its immunogenicity. Vet Microbiol 120(1–2):173–178. doi:10.1016/j.vetmic.2006.10.021
44. Ding FX, Wang F, Lu YM, Li K, Wang KH, He XW, Sun SH (2009) Multiepitope peptide-loaded virus-like particles as a vaccine against hepatitis B virus-related hepatocellular carcinoma. Hepatology 49(5):1492–1502. doi:10.1002/hep.22816
45. Easterbrook JD, Schwartzman LM, Gao J, Kash JC, Morens DM, Couzens L, Wan H, Eichelberger MC, Taubenberger JK (2012) Protection against a lethal H5N1 influenza challenge by intranasal immunization with virus-like particles containing 2009 pandemic H1N1 neuraminidase in mice. Virology 432(1):39–44. doi:10.1016/j.virol.2012.06.003
46. Edman JC, Hallewell RA, Valenzuela P, Goodman HM, Rutter WJ (1981) Synthesis of hepatitis B surface and core antigens in E. coli. Nature 291(5815):503–506
47. Esteves K (1988) Safety of oral poliomyelitis vaccine: results of a WHO enquiry. Bull World Health Organ 66(6):739–746
48. Fachinger V, Bischoff R, Jedidia SB, Saalmuller A, Elbers K (2008) The effect of vaccination against porcine circovirus type 2 in pigs suffering from porcine respiratory disease complex. Vaccine 26(11):1488–1499. doi:10.1016/j.vaccine.2007.11.053
49. Fakruddin JM, Lempicki RA, Gorelick RJ, Yang J, Adelsberger JW, Garcia-Pineres AJ, Pinto LA, Lane HC, Imamichi T (2007) Noninfectious papilloma virus-like particles inhibit HIV-1 replication: implications for immune control of HIV-1 infection by IL-27. Blood 109(5):1841–1849. doi:10.1182/blood-2006-02-001578
50. Fort M, Sibila M, Allepuz A, Mateu E, Roerink F, Segales J (2008) Porcine circovirus type 2 (PCV2) vaccination of conventional pigs prevents viremia against PCV2 isolates of different genotypes and geographic origins. Vaccine 26:1063–1071. doi:10.1016/j.vaccine.2007.12.019
51. Freivalds J, Kotelovica S, Voronkova T, Ose V, Tars K, Kazaks A (2013) Yeast-expressed bacteriophage-like particles for the packaging of nanomaterials. Mol Biotechnol. doi:10.1007/s12033-013-9686-0
52. Fulurija A, Lutz TA, Sladko K, Osto M, Wielinga PY, Bachmann MF, Saudan P (2008) Vaccination against GIP for the treatment of obesity. PLoS One 3:e3163. doi:10.1371/journal.pone.0003163
53. Garrone P, Fluckiger AC, Mangeot PE, Gauthier E, Dupeyrot-Lacas P, Mancip J, Cangialosi A, Du Chene I, LeGrand R, Mangeot I, Lavillette D, Bellier B, Cosset FL, Tangy F, Klatzmann D, Dalba C (2011) A prime-boost strategy using virus-like particles pseudotyped for HCV proteins triggers broadly neutralizing antibodies in macaques. Sci Transl Med 3(94):94ra71. doi:10.1126/scitranslmed.3002330
54. Gilbert L, Toivola J, Lehtomaki E, Donaldson L, Kapyla P, Vuento M, Oker-Blom C (2004) Assembly of fluorescent chimeric virus-like particles of canine parvovirus in insect cells. Biochem Biophys Res Commun 313(4):878–887
55. Goldmann C, Petry H, Frye S, Ast O, Ebitsch S, Jentsch KD, Kaup FJ, Weber F, Trebst C, Nisslein T, Hunsmann G, Weber T, Luke W (1999) 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
56. Gorelik J, Shevchuk A, Ramalho M, Elliott M, Lei C, Higgins CF, Lab MJ, Klenerman D, Krauzewicz N, Korchev Y (2002) Scanning surface confocal microscopy for simultaneous topographical and fluorescence imaging: application to single virus-like particle entry into a cell. Proc Natl Acad Sci U S A 99(25):16018–16023. doi:10.1073/pnas.252458399
57. Grgacic EV, Anderson DA (2006) Virus-like particles: passport to immune recognition. Methods 40(1):60–65. doi:10.1016/j.ymeth.2006.07.018
58. Gromadzka B, Szewczyk B, Konopa G, Fitzner A, Kesy A (2006) Recombinant VP60 in the form of virion-like particles as a potential vaccine against rabbit hemorrhagic disease virus. Acta Biochim Pol 53(2):371–376
59. Guillen G, Aguilar JC, Dueñas S, Hermida L, Iglesias E, Penton E, Lobaina Y, Lopez M, Mussachio A, Falcon V, Alvarez L, Martinez G, Gil L, Valdes I, Izquierdo A, Lazo L, Marcos E, Guzman G, Muzio V, Herrera L (2013) Virus-like particles as nanovaccine candidates. Adv Nat Sci: Nanosci Nanotechnol 4(1):015005. doi:10.1088/2043-6262/4/1/015005
60. Guo HC, Sun SQ, Jin Y, Yang SL, Wei YQ, Sun DH, Yin SH, Ma JW, Liu ZX, Guo JH, Luo JX, Yin H, Liu XT, Liu DX (2013) Foot-and-mouth disease virus-like particles produced by a SUMO fusion protein system in Escherichia coli induce potent protective immune responses in guinea pigs, swine and cattle. Vet Res 44:48. doi:10.1186/1297-9716-44-48
61. Habjan M, Penski N, Wagner V, Spiegel M, Overby AK, Kochs G, Huiskonen JT, Weber F (2009) Efficient production of Rift Valley fever virus-like particles: the antiviral protein MxA can inhibit primary transcription of bunyaviruses. Virology 385(2):400–408. doi:10.1016/j.virol.2008.12.011
62. Hagensee ME, Yaegashi N, Galloway DA (1993) 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
63. Harrington PR, Yount B, Johnston RE, Davis N, Moe C, Baric RS (2002) Systemic, mucosal, and heterotypic immune induction in mice inoculated with Venezuelan equine encephalitis replicons expressing Norwalk virus-like particles. J Virol 76(2):730–742
64. Haynes JR, Dokken L, Wiley JA, Cawthon AG, Bigger J, Harmsen AG, Richardson C (2009) Influenza-pseudotyped Gag virus-like particle vaccines provide broad protection against highly pathogenic avian influenza challenge. Vaccine 27(4):530–541. doi:10.1016/j.vaccine.2008.11.011
65. Ho Y, Lin PH, Liu CY, Lee SP, Chao YC (2004) Assembly of human severe acute respiratory syndrome coronavirus-like particles. Biochem Biophys Res Commun 318(4):833–838. doi:10.1016/j.bbrc.2004.04.111
66. Horaud F (1993) Ethical and safety considerations for the use in clinical trials of new attenuated poliovirus strains. Dev Biol Stand 78:149–154, discussion 154-5
67. Huhti L, Tamminen K, Vesikari T, Blazevic V (2013) Characterization and immunogenicity of norovirus capsid-derived virus-like particles purified by anion exchange chromatography. Arch Virol 158(5):933–942. doi:10.1007/s00705-012-1565-7
68. Hunter Z, Smyth HD, Durfee P, Chackerian B (2009) Induction of mucosal and systemic antibody responses against the HIV coreceptor CCR5 upon intramuscular immunization and aerosol delivery of a virus-like particle based vaccine. Vaccine 28(2):403–414. doi:10.1016/j.vaccine.2009.10.035
69. Huret C, Desjardins D, Miyalou M, Levacher B, Amadoudji Zin M, Bonduelle O, Combadiere B, Dalba C, Klatzmann D, Bellier B (2013) Recombinant retrovirus-derived virus-like particle-based vaccines induce hepatitis C virus-specific cellular and neutralizing immune responses in mice. Vaccine 31(11):1540–1547. doi:10.1016/j.vaccine.2012.05.025
70. Ionescu RM, Przysiecki CT, Liang X, Garsky VM, Fan J, Wang B, Troutman R, Rippeon Y, Flanagan E, Shiver J, Shi L (2006) Pharmaceutical and immunological evaluation of human papillomavirus viruslike particle as an antigen carrier. J Pharm Sci 95(1):70–79. doi:10.1002/jps.20493
71. Jariyapong P, Chotwiwatthanakun C, Somrit M, Jitrapakdee S, Xing L, Cheng HR, Weerachatyanukul W (2013a) Encapsulation and delivery of plasmid DNA by virus-like nanoparticles engineered from Macrobrachium rosenbergii nodavirus. Virus Res. doi:10.1016/j.virusres.2013.10.021
72. Jariyapong P, Xing L, van Houten NE, Li TC, Weerachatyanukul W, Hsieh B, Moscoso CG, Chen CC, Niikura M, Cheng RH (2013b) Chimeric hepatitis E virus-like particle as a carrier for oral-delivery. Vaccine 31(2):417–424. doi:10.1016/j.vaccine.2012.10.073
73. Jegerlehner A, Tissot A, Lechner F, Sebbel P, Erdmann I, Kundig T, Bachi T, Storni T, Jennings G, Pumpens P, Renner WA, Bachmann MF (2002) A molecular assembly system that renders antigens of choice highly repetitive for induction of protective B cell responses. Vaccine 20(25–26):3104–3112
74. Jennings GT, Bachmann MF (2008) The coming of age of virus-like particle vaccines. Biol Chem 389(5):521–536
75. Jennings GT, Bachmann MF (2009) Immunodrugs: therapeutic VLP-based vaccines for chronic diseases. Annu Rev Pharmacol Toxicol 49:303–326. doi:10.1146/annurev-pharmtox-061008-103129
76. Jeoung HY, Lee WH, Jeong W, Ko YJ, Choi CU, An DJ (2010) Immune responses and expression of the virus-like particle antigen of the porcine encephalomyocarditis virus. Res Vet Sci 89(2):295–300. doi:10.1016/j.rvsc.2010.03.012
77. Jeoung HY, Lee WH, Jeong W, Shin BH, Choi HW, Lee HS, An DJ (2011) Immunogenicity and safety of virus-like particle of the porcine encephalomyocarditis virus in pig. Virol J 8:170. doi:10.1186/1743-422X-8-170
78. Jouvenet N, Bieniasz PD, Simon SM (2008) Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454(7201):236–240. doi:10.1038/nature06998
79. Ju H, Wei N, Wang Q, Wang C, Jing Z, Guo L, Liu D, Gao M, Ma B, Wang J (2011) Goose parvovirus structural proteins expressed by recombinant baculoviruses self-assemble into virus-like particles with strong immunogenicity in goose. Biochem Biophys Res Commun 409(1):131–136. doi:10.1016/j.bbrc.2011.04.129
80. Kalia M, Chandra V, Rahman SA, Sehgal D, Jameel S (2009) Heparan sulfate proteoglycans are required for cellular binding of the hepatitis E virus ORF2 capsid protein and for viral infection. J Virol 83(24):12714–12724. doi:10.1128/jvi.00717-09
81. Kang SM, Yoo DG, Lipatov AS, Song JM, Davis CT, Quan FS, Chen LM, Donis RO, Compans RW (2009) Induction of long-term protective immune responses by influenza H5N1 virus-like particles. PLoS One 4(3):e4667. doi:10.1371/journal.pone.0004667
82. Kawano M, Matsui M, Handa H (2013) SV40 virus-like particles as an effective delivery system and its application to a vaccine carrier. Expert Rev Vaccines 12(2):199–210. doi:10.1586/erv.12.149
83. Kawano M, Morikawa K, Suda T, Ohno N, Matsushita S, Akatsuka T, Handa H, Matsui M (2014) Chimeric SV40 virus-like particles induce specific cytotoxicity and protective immunity against influenza A virus without the need of adjuvants. Virology 448:159–167. doi:10.1016/j.virol.2013.10.010
84. Kazaks A, Balmaks R, Voronkova T, Ose V, Pumpens P (2008) Melanoma vaccine candidates from chimeric hepatitis B core virus-like particles carrying a tumor-associated MAGE-3 epitope. Biotechnol J 3(11):1429–1436. doi:10.1002/biot.200800160
85. Keller SA, Bauer M, Manolova V, Muntwiler S, Saudan P, Bachmann MF (2010) Cutting edge: limited specialization of dendritic cell subsets for MHC class II-associated presentation of viral particles. J Immunol 184:26–29. doi:10.4049/jimmunol.0901540
86. Kim Y, Chang KO, Kim WY, Saif LJ (2002) Production of hybrid double- or triple-layered virus-like particles of group A and C rotaviruses using a baculovirus expression system. Virology 302(1):1–8. doi:10.1006/viro.2002.1610
87. Kirnbauer R, Booy F, Cheng N, Lowy DR, Schiller JT (1992) Papillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic. Proc Natl Acad Sci U S A 89(24):12180–12184
88. Konduru K, Bradfute SB, Jacques J, Manangeeswaran M, Nakamura S, Morshed S, Wood SC, Bavari S, Kaplan GG (2011) Ebola virus glycoprotein Fc fusion protein confers protection against lethal challenge in vaccinated mice. Vaccine 29(16):2968–2977. doi:10.1016/j.vaccine.2011.01.113
89. Krammer F, Schinko T, Messner P, Palmberger D, Ferko B, Grabherr R (2010) Influenza virus-like particles as an antigen-carrier platform for the ESAT-6 epitope of Mycobacterium tuberculosis. J Virol Methods 167(1):17–22. doi:10.1016/j.jviromet.2010.03.003
90. Kushnir N, Streatfield SJ, Yusibov V (2012) Virus-like particles as a highly efficient vaccine platform: diversity of targets and production systems and advances in clinical development. Vaccine 31(1):58–83. doi:10.1016/j.vaccine.2012.10.083
91. Lai H, Chen Q (2012) Bioprocessing of plant-derived virus-like particles of Norwalk virus capsid protein under current Good Manufacture Practice regulations. Plant Cell Rep 31(3):573–584. doi:10.1007/s00299-011-1196-6
92. Lee DH, Park JK, Lee YN, Song JM, Kang SM, Lee JB, Park SY, Choi IS, Song CS (2011) H9N2 avian influenza virus-like particle vaccine provides protective immunity and a strategy for the differentiation of infected from vaccinated animals. Vaccine 29(23):4003–4007. doi:10.1016/j.vaccine.2011.03.067
93. Lee KW, Tey BT, Ho KL, Tan WS (2012) Delivery of chimeric hepatitis B core particles into liver cells. J Appl Microbiol 112(1):119–131. doi:10.1111/j.1365-2672.2011.05176.x
94. Lee DH, Bae SW, Park JK, Kwon JH, Yuk SS, Song JM, Kang SM, Kwon YK, Kim HY, Song CS (2013) Virus-like particle vaccine protects against H3N2 canine influenza virus in dog. Vaccine 31(32):3268–3273. doi:10.1016/j.vaccine.2013.05.023
95. Lee YN, Kim MC, Lee YT, Hwang HS, Cho MK, Lee JS, Ko EJ, Kwon YM, Kang SM (2014) AS04-adjuvanted virus-like particles containing multiple M2 extracellular domains of influenza virus confer improved protection. Vaccine 32(35):4578–4585. doi:10.1016/j.vaccine.2014.06.040
96. Li ML, Cripe TP, Estes PA, Lyon MK, Rose RC, Garcea RL (1997) Expression of the human papillomavirus type 11 L1 capsid protein in Escherichia coli: characterization of protein domains involved in DNA binding and capsid assembly. J Virol 71(4):2988–2995
97. Li F, Zhang ZP, Peng JC, Cui ZQ, Pang DW, Li K, Wei HP, Zhou YF, Wen JK, Zhang XE (2009) Imaging viral behavior in mammalian cells with self-assembled capsid-quantum-dot hybrid particles. Small 5(6):718–726. doi:10.1002/smll.200801303
98. Li HY, Han JF, Qin CF, Chen R (2013a) Virus-like particles for enterovirus 71 produced from Saccharomyces cerevisiae potently elicits protective immune responses in mice. Vaccine 31(32):3281–3287. doi:10.1016/j.vaccine.2013.05.019
99. Li X, Xu X, Jin A, Jia Q, Zhou H, Kang S, Lou Y, Gao J, Lu J (2013b) Self-assembled HCV core virus-like particles targeted and inhibited tumor cell migration and invasion. Nanoscale Res Lett 8(1):401. doi:10.1186/1556-276X-8-401
100. Li J, Sun Y, Jia T, Zhang R, Zhang K, Wang L (2014) Messenger RNA vaccine based on recombinant MS2 virus-like particles against prostate cancer. Int J Cancer 134(7):1683–1694. doi:10.1002/ijc.28482
101. Lin MC, Wang M, Fang CY, Chen PL, Shen CH, Chang D (2014) Inhibition of BK virus replication in human kidney cells by BK virus large tumor antigen-specific shRNA delivered by JC virus-like particles. Antiviral Res 103:25–31. doi:10.1016/j.antiviral.2013.12.013
102. Liu WJ, Liu XS, Zhao KN, Leggatt GR, Frazer IH (2000) Papillomavirus virus-like particles for the delivery of multiple cytotoxic T cell epitopes. Virology 273(2):374–382. doi:10.1006/viro.2000.0435
103. Liu L, Celma CC, Roy P (2008) Rift Valley fever virus structural proteins: expression, characterization and assembly of recombinant proteins. Virol J 5:82. doi:10.1186/1743-422X-5-82
104. Liu W, Jiang H, Zhou J, Yang X, Tang Y, Fang D, Jiang L (2010) Recombinant dengue virus-like particles from Pichia pastoris: efficient production and immunological properties. Virus Genes 40(1):53–59. doi:10.1007/s11262-009-0418-2
105. Lorenzo LJ, Duenas-Carrera S, Falcon V, Acosta-Rivero N, Gonzalez E, de la Rosa MC, Menendez I, Morales J (2001) Assembly of truncated HCV core antigen into virus-like particles in Escherichia coli. Biochem Biophys Res Commun 281(4):962–965. doi:10.1006/bbrc.2001.4449
106. Lua LH, Connors NK, Sainsbury F, Chuan YP, Wibowo N, Middelberg AP (2014) Bioengineering virus-like particles as vaccines. Biotechnol Bioeng 111(3):425–440. doi:10.1002/bit.25159
107. Malboeuf CM, Simon DA, Lee YE, Lankes HA, Dewhurst S, Frelinger JG, Rose RC (2007) Human papillomavirus-like particles mediate functional delivery of plasmid DNA to antigen presenting cells in vivo. Vaccine 25(17):3270–3276. doi:10.1016/j.vaccine.2007.01.067
108. Manayani DJ, Thomas D, Dryden KA, Reddy V, Siladi ME, Marlett JM, Rainey GJ, Pique ME, Scobie HM, Yeager M, Young JA, Manchester M, Schneemann A (2007) A viral nanoparticle with dual function as an anthrax antitoxin and vaccine. PLoS Pathog 3(10):1422–1431. doi:10.1371/journal.ppat.0030142
109. Marelli UK, Rechenmacher F, Sobahi TR, Mas-Moruno C, Kessler H (2013) Tumor targeting via integrin ligands. Front Oncol 3:222. doi:10.3389/fonc.2013.00222
110. Martelli P, Ferrari L, Morganti M, De Angelis E, Bonilauri P, Guazzetti S, Caleffi A, Borghetti P (2011) One dose of a porcine circovirus 2 subunit vaccine induces humoral and cell-mediated immunity and protects against porcine circovirus-associated disease under field conditions. Vet Microbiol 149(3–4):339–351. doi:10.1016/j.vetmic.2010.12.008
111. Martin Caballero J, Garzon A, Gonzalez-Cintado L, Kowalczyk W, Jimenez Torres I, Calderita G, Rodriguez M, Gondar V, Bernal JJ, Ardavin C, Andreu D, Zurcher T, von Kobbe C (2012) Chimeric infectious bursal disease virus-like particles as potent vaccines for eradication of established HPV-16 E7-dependent tumors. PLoS One 7(12):e52976. doi:10.1371/journal.pone.0052976
112. Matic S, Rinaldi R, Masenga V, Noris E (2011) Efficient production of chimeric human papillomavirus 16 L1 protein bearing the M2e influenza epitope in Nicotiana benthamiana plants. BMC Biotechnol 11:106. doi:10.1186/1472-6750-11-106
113. Mazeike E, Gedvilaite A, Blohm U (2012) Induction of insert-specific immune response in mice by hamster polyomavirus VP1 derived virus-like particles carrying LCMV GP33 CTL epitope. Virus Res 163(1):2–10. doi:10.1016/j.virusres.2011.08.003
114. McAleer WJ, Buynak EB, Maigetter RZ, Wampler DE, Miller WJ, Hilleman MR (1984) Human hepatitis B vaccine from recombinant yeast. Nature 307(5947):178–180
115. McGinnes LW, Pantua H, Laliberte JP, Gravel KA, Jain S, Morrison TG (2010) Assembly and biological and immunological properties of Newcastle disease virus-like particles. J Virol 84(9):4513–4523. doi:10.1128/jvi.01931-09
116. McKee SJ, Bergot AS, Leggatt GR (2015) Recent progress in vaccination against human papillomavirus-mediated cervical cancer. Rev Med Virol 25(Suppl 1):54–71. doi:10.1002/rmv.1824
117. Mena JA, Ramirez OT, Palomares LA (2005) Quantification of rotavirus-like particles by gel permeation chromatography. J Chromatogr B Analyt Technol Biomed Life Sci 824(1–2):267–276. doi:10.1016/j.jchromb.2005.07.034
118. Mihailova M, Boos M, Petrovskis I, Ose V, Skrastina D, Fiedler M, Sominskaya I, Ross S, Pumpens P, Roggendorf M, Viazov S (2006) Recombinant virus-like particles as a carrier of B- and T-cell epitopes of hepatitis C virus (HCV). Vaccine 24(20):4369–4377. doi:10.1016/j.vaccine.2006.02.051
119. Mohana Subramanian B, Madhanmohan M, Sriraman R, Chandrasekhar Reddy RV, Yuvaraj S, Manikumar K, Rajalakshmi S, Nagendrakumar SB, Rana SK, Srinivasan VA (2012) Development of foot-and-mouth disease virus (FMDV) serotype O virus-like-particles (VLPs) vaccine and evaluation of its potency. Antiviral Res 96(3):288–295. doi:10.1016/j.antiviral.2012.09.019
120. Moon KB, Lee J, Kang S, Kim M, Mason HS, Jeon JH, Kim HS (2014) Overexpression and self-assembly of virus-like particles in Nicotiana benthamiana by a single-vector DNA replicon system. Appl Microbiol Biotechnol 98(19):8281–8290. doi:10.1007/s00253-014-5901-6
121. Mortola E, Roy P (2004) Efficient assembly and release of SARS coronavirus-like particles by a heterologous expression system. FEBS Lett 576(1–2):174–178. doi:10.1016/j.febslet.2004.09.009
122. Murata K, Lechmann M, Qiao M, Gunji T, Alter HJ, Liang TJ (2003) Immunization with hepatitis C virus-like particles protects mice from recombinant hepatitis C virus-vaccinia infection. Proc Natl Acad Sci U S A 100:6753–6758. doi:10.1073/pnas.1131929100
123. Nagesha HS, Wang LF, Hyatt AD, Morrissy CJ, Lenghaus C, Westbury HA (1995) Self-assembly, antigenicity, and immunogenicity of the rabbit haemorrhagic disease virus (Czechoslovakian strain V-351) capsid protein expressed in baculovirus. Arch Virol 140(6):1095–1108
124. Naslund J, Lagerqvist N, Habjan M, Lundkvist A, Evander M, Ahlm C, Weber F, Bucht G (2009) Vaccination with virus-like particles protects mice from lethal infection of Rift Valley fever virus. Virology 385(2):409–415. doi:10.1016/j.virol.2008.12.012
125. Niikura M, Takamura S, Kim G, Kawai S, Saijo M, Morikawa S, Kurane I, Li TC, Takeda N, Yasutomi Y (2002) Chimeric recombinant hepatitis E virus-like particles as an oral vaccine vehicle presenting foreign epitopes. Virology 293(2):273–280. doi:10.1006/viro.2001.1240
126. Ogasawara Y, Amexis G, Yamaguchi H, Kajigaya S, Leppla SH, Young NS (2006) Recombinant viral-like particles of parvovirus B19 as antigen carriers of anthrax protective antigen. In Vivo 20(3):319–324
127. Ohtaki N, Takahashi H, Kaneko K, Gomi Y, Ishikawa T, Higashi Y, Kurata T, Sata T, Kojima A (2010) Immunogenicity and efficacy of two types of West Nile virus-like particles different in size and maturation as a second-generation vaccine candidate. Vaccine 28(40):6588–6596. doi:10.1016/j.vaccine.2010.07.055
128. Overby AK, Popov V, Neve EP, Pettersson RF (2006) Generation and analysis of infectious virus-like particles of uukuniemi virus (bunyaviridae): a useful system for studying bunyaviral packaging and budding. J Virol 80(21):10428–10435. doi:10.1128/jvi.01362-06
129. Pan Q, He K, Huang K (2008) Development of recombinant porcine parvovirus-like particles as an antigen carrier formed by the hybrid VP2 protein carrying immunoreactive epitope of porcine circovirus type 2. Vaccine 26(17):2119–2126. doi:10.1016/j.vaccine.2008.02.037
130. Parez N, Fourgeux C, Mohamed A, Dubuquoy C, Pillot M, Dehee A, Charpilienne A, Poncet D, Schwartz-Cornil I, Garbarg-Chenon A (2006) Rectal immunization with rotavirus virus-like particles induces systemic and mucosal humoral immune responses and protects mice against rotavirus infection. J Virol 80(4):1752–1761. doi:10.1128/JVI.80.4.1752-1761.2006
131. Park JK, Lee DH, Yuk SS, To EO, Kwon JH, Noh JY, Kim BY, Choi SW, Kang SM, Lee JB, Park SY, Choi IS, Song CS (2014) Virus-like particle vaccine confers protection against a lethal NDV challenge in chickens and allows DIVA strategy. Clin Vaccine Immunol. doi:10.1128/CVI.00636-13
132. Pastori C, Tudor D, Diomede L, Drillet AS, Jegerlehner A, Rohn TA, Bomsel M, Lopalco L (2012) Virus like particle based strategy to elicit HIV-protective antibodies to the alpha-helic regions of gp41. Virology 431(1–2):1–11. doi:10.1016/j.virol.2012.05.005
133. Pastrana DV, Vass WC, Lowy DR, Schiller JT (2001) NHPV16 VLP vaccine induces human antibodies that neutralize divergent variants of HPV16. Virology 279(1):361–369. doi:10.1006/viro.2000.0702
134. Patel KG, Swartz JR (2011) Surface functionalization of virus-like particles by direct conjugation using azide-alkyne click chemistry. Bioconjug Chem 22(3):376–387. doi:10.1021/bc100367u
135. Patterson DP, Schwarz B, El-Boubbou K, van der Oost J, Prevelige PE, Douglas T (2012) Virus-like particle nanoreactors: programmed encapsulation of the thermostable CelB glycosidase inside the P22 capsid. Soft Matter 8(39):10158. doi:10.1039/c2sm26485d
136. Patterson DP, Rynda-Apple A, Harmsen AL, Harmsen AG, Douglas T (2013) Biomimetic antigenic nanoparticles elicit controlled protective immune response to influenza. ACS Nano 7(4):3036–3044. doi:10.1021/nn4006544
137. Peabody DS, Manifold-Wheeler B, Medford A, Jordan SK, do Carmo Caldeira J, Chackerian B (2008) Immunogenic display of diverse peptides on virus-like particles of RNA phage MS2. J Mol Biol 380(1):252–263. doi:10.1016/j.jmb.2008.04.049
138. Peralta A, Molinari P, Taboga O (2009) Chimeric recombinant rotavirus-like particles as a vehicle for the display of heterologous epitopes. Virol J 6:192. doi:10.1186/1743-422x-6-192
139. Peretti S, Schiavoni I, Pugliese K, Federico M (2005) Cell death induced by the herpes simplex virus-1 thymidine kinase delivered by human immunodeficiency virus-1-based virus-like particles. Mol Ther 12(6):1185–1196. doi:10.1016/j.ymthe.2005.06.474
140. Pineo CB, Hitzeroth II, Rybicki EP (2013) Immunogenic assessment of plant-produced human papillomavirus type 16 L1/L2 chimaeras. Plant Biotechnol J 11(8):964–975. doi:10.1111/pbi.12089
141. Plotkin SA (2005) Vaccines: past, present and future. Nat Med 11(4 Suppl):S5–S11. doi:10.1038/nm1209
142. Pokorski JK, Hovlid ML, Finn MG (2011) Cell targeting with hybrid Qβ virus-like particles displaying epidermal growth factor. Chembiochem: Eur J Chem Biol 12(16):2441–2447
143. Ponterio E, Petrizzo A, Di Bartolo I, Buonaguro FM, Buonaguro L, Ruggeri FM (2013) Pattern of activation of human antigen presenting cells by genotype GII.4 norovirus virus-like particles. J Transl Med 11:127. doi:10.1186/1479-5876-11-127
144. Pumpens P, Grens E (2001) HBV core particles as a carrier for B cell/T cell epitopes. Intervirology 44(2–3):98–114. doi:10.1159/000050037
145. Pyo HM, Masic A, Woldeab N, Embury-Hyatt C, Lin L, Shin YK, Song JY, Babiuk S, Zhou Y (2012) Pandemic H1N1 influenza virus-like particles are immunogenic and provide protective immunity to pigs. Vaccine 30(7):1297–1304. doi:10.1016/j.vaccine.2011.12.083
146. Quan FS, Vunnava A, Compans RW, Kang SM (2010) Virus-like particle vaccine protects against 2009 H1N1 pandemic influenza virus in mice. PLoS One 5(2):e9161. doi:10.1371/journal.pone.0009161
147. Raghunandan R (2011) Virus-like particles: innate immune stimulators. Expert Rev Vaccines 10(4):409–411. doi:10.1586/erv.11.37
148. Ramqvist T, Andreasson K, Dalianis T (2007) Vaccination, immune and gene therapy based on virus-like particles against viral infections and cancer. Expert Opin Biol Ther 7(7):997–1007. doi:10.1517/14712598.7.7.997
149. Rohn TA, Jennings GT, Hernandez M, Grest P, Beck M, Zou Y, Kopf M, Bachmann MF (2006) Vaccination against IL-17 suppresses autoimmune arthritis and encephalomyelitis. Eur J Immunol 36:2857–2867. doi:10.1002/eji.200636658
150. Rohn TA, Ralvenius WT, Paul J, Borter P, Hernandez M, Witschi R, Grest P, Zeilhofer HU, Bachmann MF, Jennings GT (2011) A virus-like particle-based anti-nerve growth factor vaccine reduces inflammatory hyperalgesia: potential long-term therapy for chronic pain. J Immunol 186(3):1769–1780. doi:10.4049/jimmunol.1000030
151. Roldao A, Mellado MC, Castilho LR, Carrondo MJ, Alves PM (2010) Virus-like particles in vaccine development. Expert Rev Vaccines 9(10):1149–1176. doi:10.1586/erv.10.115
152. Roose K, Baets SD, Schepens B, Saelens X (2013) Hepatitis B core-based virus-like particles to present heterologous epitopes. Expert Rev Vaccines 12(2):183–198. doi:10.1586/erv.12.150
153. Sanchez-Rodriguez SP, Munch-Anguiano L, Echeverria O, Vazquez-Nin G, Mora-Pale M, Dordick JS, Bustos-Jaimes I (2012) Human parvovirus B19 virus-like particles: in vitro assembly and stability. Biochimie 94(3):870–878. doi:10.1016/j.biochi.2011.12.006
154. Sanders BP, Liu Y, Brandjes A, van Hoek V, de Los Rios Oakes I, Lewis J, Wimmer E, Custers JH, Schuitemaker H, Cello J, Edo-Matas D (2015) Brunenders: a partially attenuated historic poliovirus type I vaccine strain. J Gen Virol. doi:10.1099/vir.0.000197
155. Santi L, Batchelor L, Huang Z, Hjelm B, Kilbourne J, Arntzen CJ, Chen Q, Mason HS (2008) An efficient plant viral expression system generating orally immunogenic Norwalk virus-like particles. Vaccine 26(15):1846–1854. doi:10.1016/j.vaccine.2008.01.053
156. Sasnauskas K, Bulavaite A, Hale A, Jin L, Knowles WA, Gedvilaite A, Dargeviciute A, Bartkeviciute D, Zvirbliene A, Staniulis J, Brown DW, Ulrich R (2002) Generation of recombinant virus-like particles of human and non-human polyomaviruses in yeast Saccharomyces cerevisiae. Intervirology 45(4–6):308–317
157. Schott JW, Galla M, Godinho T, Baum C, Schambach A (2011) Viral and non-viral approaches for transient delivery of mRNA and proteins. Curr Gene Ther 11(5):382–398
158. Shin YC, Folk WR (2003) Formation of polyomavirus-like particles with different VP1 molecules that bind the urokinase plasminogen activator receptor. J Virol 77(21):11491–11498
159. Singh P, Destito G, Schneemann A, Manchester M (2006) Canine parvovirus-like particles, a novel nanomaterial for tumor targeting. J Nanobiotechnol 4:2. doi:10.1186/1477-3155-4-2
160. Skrastina D, Petrovskis I, Petraityte R, Sominskaya I, Ose V, Lieknina I, Bogans J, Sasnauskas K, Pumpens P (2013) Chimeric derivatives of hepatitis B virus core particles carrying major epitopes of the rubella virus E1 glycoprotein. Clin Vaccine Immunol 20(11):1719–1728. doi:10.1128/CVI.00533-13
161. Smith GE, Flyer DC, Raghunandan R, Liu Y, Wei Z, Wu Y, Kpamegan E, Courbron D, Fries LF 3rd, Glenn GM (2013) Development of influenza H7N9 virus like particle (VLP) vaccine: homologous A/Anhui/1/2013 (H7N9) protection and heterologous A/chicken/Jalisco/CPA1/2012 (H7N3) cross-protection in vaccinated mice challenged with H7N9 virus. Vaccine 31(40):4305–4313. doi:10.1016/j.vaccine.2013.07.043
162. Sominskaya I, Skrastina D, Dislers A, Vasiljev D, Mihailova M, Ose V, Dreilina D, Pumpens P (2010) Construction and immunological evaluation of multivalent hepatitis B virus (HBV) core virus-like particles carrying HBV and HCV epitopes. Clin Vaccine Immunol 17(6):1027–1033. doi:10.1128/CVI.00468-09
163. Sonderegger I, Rohn TA, Kurrer MO, Iezzi G, Zou Y, Kastelein RA, Bachmann MF, Kopf M (2006) Neutralization of IL-17 by active vaccination inhibits IL-23-dependent autoimmune myocarditis. Eur J Immunol 36:2849–2856. doi:10.1002/eji.200636484
164. Souza AC, Vasques RM, Inoue-Nagata AK, Lacorte C, Maldaner FR, Noronha EF, Nagata T (2013) Expression and assembly of Norwalk virus-like particles in plants using a viral RNA silencing suppressor gene. Appl Microbiol Biotechnol 97(20):9021–9027. doi:10.1007/s00253-013-5077-5
165. Speiser DE, Schwarz K, Baumgaertner P, Manolova V, Devevre E, Sterry W, Walden P, Zippelius A, Conzett KB, Senti G, Voelter V, Cerottini JP, Guggisberg D, Willers J, Geldhof C, Romero P, Kundig T, Knuth A, Dummer R, Trefzer U, Bachmann MF (2010) Memory and effector CD8 T-cell responses after nanoparticle vaccination of melanoma patients. J Immunother 33(8):848–858. doi:10.1097/CJI.0b013e3181f1d614
166. Spohn G, Schwarz K, Maurer P, Illges H, Rajasekaran N, Choi Y, Jennings GT, Bachmann MF (2005) Protection against osteoporosis by active immunization with TRANCE/RANKL displayed on virus-like particles. J Immunol 175(9):6211–6218
167. Spohn G, Guler R, Johansen P, Keller I, Jacobs M, Beck M, Rohner F, Bauer M, Dietmeier K, Kundig TM, Jennings GT, Brombacher F, Bachmann MF (2007) A virus-like particle-based vaccine selectively targeting soluble TNF-alpha protects from arthritis without inducing reactivation of latent tuberculosis. J Immunol 178(11):7450–7457
168. Spohn G, Keller I, Beck M, Grest P, Jennings GT, Bachmann MF (2008) Active immunization with IL-1 displayed on virus-like particles protects from autoimmune arthritis. Eur J Immunol 38(3):877–887. doi:10.1002/eji.200737989
169. Spohn G, Jennings GT, Martina BE, Keller I, Beck M, Pumpens P, Osterhaus AD, Bachmann MF (2010) A VLP-based vaccine targeting domain III of the West Nile virus E protein protects from lethal infection in mice. Virol J 7:146. doi:10.1186/1743-422X-7-146
170. Stewart M, Dubois E, Sailleau C, Breard E, Viarouge C, Desprat A, Thiery R, Zientara S, Roy P (2013) Bluetongue virus serotype 8 virus-like particles protect sheep against virulent virus infection as a single or multi-serotype cocktail immunogen. Vaccine 31(3):553–558. doi:10.1016/j.vaccine.2012.11.016
171. Storni T, Ruedl C, Schwarz K, Schwendener RA, Renner WA, Bachmann MF (2004) 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
172. Sun S, Li W, Sun Y, Pan Y, Li J (2011) A new RNA vaccine platform based on MS2 virus-like particles produced in Saccharomyces cerevisiae. Biochem Biophys Res Commun 407(1):124–128. doi:10.1016/j.bbrc.2011.02.122
173. Swenson DL, Warfield KL, Kuehl K, Larsen T, Hevey MC, Schmaljohn A, Bavari S, Aman MJ (2004) Generation of Marburg virus-like particles by co-expression of glycoprotein and matrix protein. FEMS Immunol Med Microbiol 40(1):27–31
174. Swenson DL, Warfield KL, Negley DL, Schmaljohn A, Aman MJ, Bavari S (2005) Virus-like particles exhibit potential as a pan-filovirus vaccine for both Ebola and Marburg viral infections. Vaccine 23(23):3033–3042. doi:10.1016/j.vaccine.2004.11.070
175. Takeda S, Shiosaki K, Kaneda Y, Nakasatomi T, Yoshizaki H, Someya K, Konno Y, Eda Y, Kino Y, Yamamoto N, Honda M (2004) Hemagglutinating virus of Japan protein is efficient for induction of CD4+ T-cell response by a hepatitis B core particle-based HIV vaccine. Clin Immunol 112(1):92–105. doi:10.1016/j.clim.2004.04.001
176. Tan M, Jiang X (2005) Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol 13(6):285–293. doi:10.1016/j.tim.2005.04.004
177. Tan M, Huang P, Meller J, Zhong W, Farkas T, Jiang X (2003) Mutations within the P2 domain of norovirus capsid affect binding to human histo-blood group antigens: evidence for a binding pocket. J Virol 77(23):12562–12571
178. Tan M, Fang P, Chachiyo T, Xia M, Huang P, Fang Z, Jiang W, Jiang X (2008) Noroviral P particle: structure, function and applications in virus-host interaction. Virology 382(1):115–123. doi:10.1016/j.virol.2008.08.047
179. Tartour E, Benchetrit F, Haicheur N, Adotevi O, Fridman WH (2002) Synthetic and natural non-live vectors: rationale for their clinical development in cancer vaccine protocols. Vaccine 20(Suppl 4):A32–A39
180. Teunissen EA, de Raad M, Mastrobattista E (2013) Production and biomedical applications of virus-like particles derived from polyomaviruses. J Control Release 172(1):305–321. doi:10.1016/j.jconrel.2013.08.026
181. Tissot AC, Maurer P, Nussberger J, Sabat R, Pfister T, Ignatenko S, Volk HD, Stocker H, Muller P, Jennings GT, Wagner F, Bachmann MF (2008) Effect of immunisation against angiotensin II with CYT006-AngQb on ambulatory blood pressure: a double-blind, randomised, placebo-controlled phase IIa study. Lancet 371(9615):821–827. doi:10.1016/S0140-6736(08)60381-5
182. Tissot AC, Renhofa R, Schmitz N, Cielens I, Meijerink E, Ose V, Jennings GT, Saudan P, Pumpens P, Bachmann MF (2010) Versatile virus-like particle carrier for epitope based vaccines. PLoS One 5(3):e9809. doi:10.1371/journal.pone.0009809
183. Touze A, Gaitan J, Arnold F, Cazal R, Fleury MJ, Combelas N, Sizaret PY, Guyetant S, Maruani A, Baay M, Tognon M, Coursaget P (2010) Generation of Merkel cell polyomavirus (MCV)-like particles and their application to detection of MCV antibodies. J Clin Microbiol 48(5):1767–1770. doi:10.1128/JCM.01691-09
184. Tscherne DM, Manicassamy B, Garcia-Sastre A (2010) An enzymatic virus-like particle assay for sensitive detection of virus entry. J Virol Methods 163(2):336–343. doi:10.1016/j.jviromet.2009.10.020
185. Tyler M, Tumban E, Peabody DS, Chackerian B (2014) The use of hybrid virus-like particles to enhance the immunogenicity of a broadly protective HPV vaccine. Biotechnol Bioeng 111(12):2398–2406. doi:10.1002/bit.25311
186. Ungaro F, Conte C, Quaglia F, Tornesello ML, Buonaguro FM, Buonaguro L (2013) VLPs and particle strategies for cancer vaccines. Expert Rev Vaccines 12(10):1173–1193. doi:10.1586/14760584.2013.836909
187. Vacher G, Kaeser MD, Moser C, Gurny R, Borchard G (2013) Recent advances in mucosal immunization using virus-like particles. Mol Pharm 10(5):1596–1609. doi:10.1021/mp300597g
188. Valenzuela P, Medina A, Rutter WJ, Ammerer G, Hall BD (1982) Synthesis and assembly of hepatitis B virus surface antigen particles in yeast. Nature 298(5872):347–350
189. Vidyasagar P, Sridevi VN, Rajan S, Praveen A, Srikanth A, Abhinay G, Siva Kumar V, Verma RR, Rajendra L (2014) Generation and characterization of neutralizing monoclonal antibodies against baculo-expressed HPV 16 VLPs. Eur J Microbiol Immunol (Bp) 4(1):56–64. doi:10.1556/EuJMI.4.2014.1.5
190. Vieira HL, Estevao C, Roldao A, Peixoto CC, Sousa MF, Cruz PE, Carrondo MJ, Alves PM (2005) Triple layered rotavirus VLP production: kinetics of vector replication, mRNA stability and recombinant protein production. J Biotechnol 120(1):72–82. doi:10.1016/j.jbiotec.2005.03.026
191. Voronkova T, Kazaks A, Ose V, Ozel M, Scherneck S, Pumpens P, Ulrich R (2007) Hamster polyomavirus-derived virus-like particles are able to transfer in vitro encapsidated plasmid DNA to mammalian cells. Virus Genes 34(3):303–314. doi:10.1007/s11262-006-0028-1
192. Wang T, Zhang Z, Gao D, Li F, Wei H, Liang X, Cui Z, Zhang XE (2011) Encapsulation of gold nanoparticles by simian virus 40 capsids. Nanoscale 3(10):4275–4282. doi:10.1039/c1nr10568j
193. Wang HB, Fang G, Yu WZ, Du F, Fan CX, Liu QL, Hao LX, Liu Y, Zheng JS, Qin ZY, Xia W, Zhang SY, Yin ZD, Jing Q, Zhang YX, Huang RN, Yang RP, Tong WB, Qi Q, Guan XJ, Jing YL, Ma QL, Wang J, Ma XZ, Chen N, Zheng HR, Li YQ, Ma C, Su QR, Reilly KH, Luo HM, Wu XP, Wen N, Yang WZ (2014) An outbreak of type Pi vaccine-derived poliovirus in Sichuan Province, China: emergence and circulation in an under-immunized population. PLoS One 9(12):e113880. doi:10.1371/journal.pone.0113880
194. Warfield KL, Bosio CM, Welcher BC, Deal EM, Mohamadzadeh M, Schmaljohn A, Aman MJ, Bavari S (2003) Ebola virus-like particles protect from lethal Ebola virus infection. Proc Natl Acad Sci U S A 100(26):15889–15894. doi:10.1073/pnas.2237038100
195. Warfield KL, Swenson DL, Demmin G, Bavari S (2005) Filovirus-like particles as vaccines and discovery tools. Expert Rev Vaccines 4(3):429–440. doi:10.1586/14760584.4.3.429
196. Warfield KL, Posten NA, Swenson DL, Olinger GG, Esposito D, Gillette WK, Hopkins RF, Costantino J, Panchal RG, Hartley JL, Aman MJ, Bavari S (2007a) Filovirus-like particles produced in insect cells: immunogenicity and protection in rodents. J Infect Dis 196(Suppl 2):S421–S429. doi:10.1086/520612
197. Warfield KL, Swenson DL, Olinger GG, Kalina WV, Aman MJ, Bavari S (2007b) Ebola virus-like particle-based vaccine protects nonhuman primates against lethal Ebola virus challenge. J Infect Dis 196(Suppl 2):S430–S437. doi:10.1086/520583
198. Wei B, Wei Y, Zhang K, Wang J, Xu R, Zhan S, Lin G, Wang W, Liu M, Wang L, Zhang R, Li J (2009) Development of an antisense RNA delivery system using conjugates of the MS2 bacteriophage capsids and HIV-1 TAT cell-penetrating peptide. Biomed Pharmacother 63(4):313–318. doi:10.1016/j.biopha.2008.07.086
199. Wei HJ, Chang W, Lin SC, Liu WC, Chang DK, Chong P, Wu SC (2011) Fabrication of influenza virus-like particles using M2 fusion proteins for imaging single viruses and designing vaccines. Vaccine 29(41):7163–7172. doi:10.1016/j.vaccine.2011.05.077
200. Wiessner C, Wiederhold KH, Tissot AC, Frey P, Danner S, Jacobson LH, Jennings GT, Luond R, Ortmann R, Reichwald J, Zurini M, Mir A, Bachmann MF, Staufenbiel M (2011) The second-generation active Abeta immunotherapy CAD106 reduces amyloid accumulation in APP transgenic mice while minimizing potential side effects. J Neurosci 31(25):9323–9331. doi:10.1523/jneurosci.0293-11.2011
201. Wu M, Sherwin T, Brown WL, Stockley PG (2005) Delivery of antisense oligonucleotides to leukemia cells by RNA bacteriophage capsids. Nanomedicine 1(1):67–76. doi:10.1016/j.nano.2004.11.011
202. Wu CY, Yeh YC, Yang YC, Chou C, Liu MT, Wu HS, Chan JT, Hsiao PW (2010) Mammalian expression of virus-like particles for advanced mimicry of authentic influenza virus. PLoS One 5(3):e9784. doi:10.1371/journal.pone.0009784
203. Wu PC, Lin WL, Wu CM, Chi JN, Chien MS, Huang C (2012) Characterization of porcine circovirus type 2 capsid particle assembly and its application to virus-like particle vaccine development. Appl Microbiol Biotechnol 95(6):1501–1507. doi:10.1007/s00253-012-4015-2
204. Xu J, Guo HC, Wei YQ, Dong H, Han SC, Ao D, Sun DH, Wang HM, Cao SZ, Sun SQ (2014) Self-assembly of virus-like particles of canine parvovirus capsid protein expressed from Escherichia coli and application as virus-like particle vaccine. Appl Microbiol Biotechnol. doi:10.1007/s00253-013-5485-6
205. Yamaji H, Konishi E (2013) Production of Japanese encephalitis virus-like particles in insect cells. Bioengineered 4(6):438–442. doi:10.4161/bioe.24514
206. Yang YK, Burkhard P (2012) Encapsulation of gold nanoparticles into self-assembling protein nanoparticles. J Nanobiotechnol 10:42. doi:10.1186/1477-3155-10-42
207. Yao Q, Zhang R, Guo L, Li M, Chen C (2004) Th cell-independent immune responses to chimeric hemagglutinin/simian human immunodeficiency virus-like particles vaccine. J Immunol 173(3):1951–1958
208. Ye X, Ku Z, Liu Q, Wang X, Shi J, Zhang Y, Kong L, Cong Y, Huang Z (2014) Chimeric virus-like particle vaccines displaying conserved enterovirus 71 epitopes elicit protective neutralizing antibodies in mice through divergent mechanisms. J Virol 88(1):72–81. doi:10.1128/JVI.01848-13
209. Yin S, Sun S, Yang S, Shang Y, Cai X, Liu X (2010) Self-assembly of virus-like particles of porcine circovirus type 2 capsid protein expressed from Escherichia coli. Virol J 7:166. doi:10.1186/1743-422X-7-166
210. Young SL, Wilson M, Wilson S, Beagley KW, Ward V, Baird MA (2006) Transcutaneous vaccination with virus-like particles. Vaccine 24(26):5406–5412. doi:10.1016/j.vaccine.2006.03.052
211. Zamarin D, Postow MA (2015) Immune checkpoint modulation: rational design of combination strategies. Pharmacol Ther 150:23–32. doi:10.1016/j.pharmthera.2015.01.003
212. Zamora E, Handisurya A, Shafti-Keramat S, Borchelt D, Rudow G, Conant K, Cox C, Troncoso JC, Kirnbauer R (2006) Papillomavirus-like particles are an effective platform for amyloid-beta immunization in rabbits and transgenic mice. J Immunol 177(4):2662–2670
213. Zhang R, Zhang S, Li M, Chen C, Yao Q (2010) Incorporation of CD40 ligand into SHIV virus-like particles (VLP) enhances SHIV-VLP-induced dendritic cell activation and boosts immune responses against HIV. Vaccine 28(31):5114–5127. doi:10.1016/j.vaccine.2010.03.079
214. Zhang S, Liang M, Gu W, Li C, Miao F, Wang X, Jin C, Zhang L, Zhang F, Zhang Q, Jiang L, Li M, Li D (2011) Vaccination with dengue virus-like particles induces humoral and cellular immune responses in mice. Virol J 8:333. doi:10.1186/1743-422X-8-333
215. Zhao Q, Chen W, Chen Y, Zhang L, Zhang J, Zhang Z (2011) Self-assembled virus-like particles from rotavirus structural protein VP6 for targeted drug delivery. Bioconjug Chem 22(3):346–352. doi:10.1021/bc1002532
216. Zielonka A, Gedvilaite A, Ulrich R, Luschow D, Sasnauskas K, Muller H, Johne R (2006) 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. doi:10.1016/j.virusres.2006.02.010
217. Zochowska M, Paca A, Schoehn G, Andrieu JP, Chroboczek J, Dublet B, Szolajska E (2009) Adenovirus dodecahedron, as a drug delivery vector. PLoS One 4(5):e5569. doi:10.1371/journal.pone.0005569