Summary.
Papillomaviruses (PVs) are simple double-strand DNA viruses whose virion shells are T = 7 icosahedrons and composed of major capsid protein L1 and minor capsid protein L2.L1 alone or together with L2 can self-assemble into virus-like particles (VLPs) when expressed in eukaryotic or prokaryotic expression systems. Although the VLPs lack the virus genome DNA, their morphological and immunological characteristics are very similar to those of nature papillomaviruses. PV VLP vaccination can induce high titers of neutralizing antibodies and can effectively protect animals or humans from PV infection. Moreover, PV VLPs have been good candidates for vehicles to deliver epitopes or genes to target cells. They are widely used in the fields of vaccine development, neutralizing antibody detection, basic virologic research on papillomaviruses, and human papillomavirus (HPV) screening. Besides the structural biology and immunological basis for PV VLPs used as vehicles to deliver epitopes or genes, this review details the latest findings on chimeric papillomavirus VLPs and papillomavirus pseudoviruses, which are two important forms of PV VLPs used to transfer epitopes or genes.
Article PDF
Similar content being viewed by others
Abbreviations
- PV:
-
Papillomavirus
- VLPs:
-
virus-like particles
- cVLPs:
-
chimeric virus-like particles
- HPV:
-
human papillomavirus
- DCs:
-
dendritic cells
- LCs:
-
Langerhans cells
- IL:
-
interleukin
- TNF:
-
tumor necrosis factor
- INF:
-
interferon
- CTLs:
-
cytotoxic T lymphocytes
References
KA Ault AR Giuliano RP Edwards G Tamms LL Kim JF Smith KU Jansen M Allende FJ Taddeo D Skulsky E Barr (2004) ArticleTitleA phase I study to evaluate a human papillomavirus (HPV) type 18 L1 VLP vaccine Vaccine 22 3004–3007 Occurrence Handle15297048 Occurrence Handle1:CAS:528:DC%2BD2cXmsVCqtr4%3D
JG Baseman LA Koutsky (2005) ArticleTitleThe epidemiology of human papillomavirus infections J Clin Virol 32 IssueID[Suppl 1] S16–S24 Occurrence Handle15753008
HJ Bontkes JJ Ruizendaal D Kramer CJ Meijer E Hooijberg (2005) ArticleTitlePlasmacytoid dendritic cells are present in cervical carcinoma and become activated by human papillomavirus type 16 virus-like particles Gynecol Oncol 96 897–901 Occurrence Handle15721448
L Bousarghin AL Combita-Rojas A Touze S El Mehdaoui PY Sizaret MM Bravo P Coursaget (2002) ArticleTitleDetection of neutralizing antibodies against human papillomaviruses (HPV) by inhibition of gene transfer mediated by HPV pseudovirions J Clin Microbiol 40 926–932 Occurrence Handle11880418 Occurrence Handle1:CAS:528:DC%2BD38XisVKrs7Y%3D
F Breitburd R Kirnbauer NL Hubbert B Nonnenmacher C Trin-Dinh-Desmarquet G Orth JT Schiller DR Lowy (1995) ArticleTitleImmunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection J Virol 69 3959–3963 Occurrence Handle7745754 Occurrence Handle1:CAS:528:DyaK2MXls1yhsL8%3D
DR Brown JT Bryan JM Schroeder TS Robinson KH Fife CM Wheeler E Barr PR Smith L Chiacchierini A DiCello KU Jansen (2001) ArticleTitleNeutralization of human papillomavirus type 11 (HPV-11) by serum from women vaccinated with yeast-derived HPV-11 L1 virus-like particles: correlation with competitive radioimmunoassay titer J Infect Dis 184 1183–1186 Occurrence Handle11598842 Occurrence Handle1:CAS:528:DC%2BD3MXotlKitbk%3D
DR Brown KH Fife CM Wheeler LA Koutsky LM Lupinacci R Railkar G Suhr E Barr A Dicello W Li JF Smith A Tadesse KU Jansen (2004) ArticleTitleEarly assessment of the efficacy of a human papillomavirus type 16 L1 virus-like particle vaccine Vaccine 22 2936–2942 Occurrence Handle15246630 Occurrence Handle1:CAS:528:DC%2BD2cXls1WktLY%3D
CB Buck DV Pastrana DR Lowy JT Schiller (2004) ArticleTitleEfficient intracellular assembly of papillomaviral vectors J Virol 78 751–757 Occurrence Handle14694107 Occurrence Handle1:CAS:528:DC%2BD2cXjvFejsA%3D%3D
CB Buck CD Thompson YY Pang DR Lowy JT Schiller (2005) ArticleTitleMaturation of papillomavirus capsids J Virol 79 2839–2846 Occurrence Handle15709003 Occurrence Handle1:CAS:528:DC%2BD2MXitlaqurY%3D
B Chackerian DR Lowy JT Schiller (1999) ArticleTitleInduction of autoantibodies to mouse CCR5 with recombinant papillomavirus particles Proc Natl Acad Sci USA 96 2373–2378 Occurrence Handle10051649 Occurrence Handle1:CAS:528:DyaK1MXhvVSqtLY%3D
B Chackerian DR Lowy JT Schiller (2001) ArticleTitleConjugation of a self-antigen to papillomavirus-like particles allows for efficient induction of protective autoantibodies J Clin Invest 108 415–423 Occurrence Handle11489935 Occurrence Handle1:CAS:528:DC%2BD3MXlvVGltLs%3D
B Chackerian P Lenz DR Lowy JT Schiller (2002) ArticleTitleDeterminants of autoantibody induction by conjugated papillomavirus virus-like particles J Immunol 169 6120–6126 Occurrence Handle12444114 Occurrence Handle1:CAS:528:DC%2BD38Xpt1Kmtbk%3D
XS Chen RL Garcea I Goldberg G Casini SC Harrison (2000) ArticleTitleStructure of small virus-like particles assembled from the L1 protein of human papillomavirus 16 Mol Cell 5 557–567 Occurrence Handle10882140 Occurrence Handle1:CAS:528:DC%2BD3cXisVWrs7g%3D
AL Combita A Touze L Bousarghin PY Sizaret N Munoz P Coursaget (2001) ArticleTitleGene transfer using human papillomavirus pseudovirions varies according to virus genotype and requires cell surface heparan sulfate FEMS Microbiol Lett 204 183–188 Occurrence Handle11682199 Occurrence Handle1:CAS:528:DC%2BD3MXnslCitLk%3D
EM de Villiers C Fauquet TR Broker HU Bernard H zur Hausen (2004) ArticleTitleClassification of papillomaviruses Virology 324 17–27 Occurrence Handle15183049 Occurrence Handle1:CAS:528:DC%2BD2cXks1ersL0%3D
DM Da Silva JT Schiller WM Kast (2003) ArticleTitleHeterologous boosting increases immunogenicity of chimeric papillomavirus virus-like particle vaccines Vaccine 21 3219–3227 Occurrence Handle12804851 Occurrence Handle1:CAS:528:DC%2BD3sXksVyqsbc%3D
J Doorbar (2005) ArticleTitleThe papillomavirus life cycle J Clin Virol 32 IssueID[Suppl 1] S7–S15 Occurrence Handle15753007 Occurrence Handle1:CAS:528:DC%2BD2MXhvF2rtLc%3D
P Drobni N Mistry N McMillan M Evander (2003) ArticleTitleCarboxy-fluorescein diacetate, succinimidyl ester labeled papillomavirus virus-like particles fluoresce after internalization and interact with heparan sulfate for binding and entry Virology 310 163–172 Occurrence Handle12788640 Occurrence Handle1:CAS:528:DC%2BD3sXkt1yjtL0%3D
RT Emeny CM Wheeler KU Jansen WC Hunt TM Fu JF Smith S MacMullen MT Esser X Paliard (2002) ArticleTitlePriming of human papillomavirus type 11-specific humoral and cellular immune responses in college-aged women with a virus-like particle vaccine J Virol 76 7832–7842 Occurrence Handle12097595 Occurrence Handle1:CAS:528:DC%2BD38XltlKqsbw%3D
M Evander IH Frazer E Payne YM Qi K Hengst NA McMillan (1997) ArticleTitleIdentification of the alpha6 integrin as a candidate receptor for papillomaviruses J Virol 71 2449–2456 Occurrence Handle9032382 Occurrence Handle1:CAS:528:DyaK2sXht1WqsrY%3D
TG Evans W Bonnez RC Rose S Koenig L Demeter JA Suzich D O’Brien M Campbell WI White J Balsley RC Reichman (2001) ArticleTitleA Phase 1 study of a recombinant viruslike particle vaccine against human papillomavirus type 11 in healthy adult volunteers J Infect Dis 183 1485–1493 Occurrence Handle11319684 Occurrence Handle1:CAS:528:DC%2BD3MXjvFygsb8%3D
SC Fausch DM Da Silva MP Rudolf WM Kast (2002) ArticleTitleHuman papillomavirus virus-like particles do not activate Langerhans cells: a possible immune escape mechanism used by human papillomaviruses J Immunol 169 3242–3249 Occurrence Handle12218143 Occurrence Handle1:CAS:528:DC%2BD38XntFahu7c%3D
SC Fausch DM Da Silva WM Kast (2003) ArticleTitleDifferential uptake and cross-presentation of human papillomavirus virus-like particles by dendritic cells and Langerhans cells Cancer Res 63 3478–3482 Occurrence Handle12839929 Occurrence Handle1:CAS:528:DC%2BD3sXltVGrtLs%3D
SC Fausch LM Fahey DM Da Silva WM Kast (2005) ArticleTitleHuman papillomavirus can escape immune recognition through Langerhans cell phosphoinositide 3-kinase activation J Immunol 174 7172–7178 Occurrence Handle15905561 Occurrence Handle1:CAS:528:DC%2BD2MXkt1Omurc%3D
SC Fausch DM Da Silva WM Kast (2005) ArticleTitleHeterologous papillomavirus virus-like particles and human papillomavirus virus-like particle immune complexes activate human Langerhans cells Vaccine 23 1720–1729 Occurrence Handle15705478 Occurrence Handle1:CAS:528:DC%2BD2MXhtlajsLk%3D
R Fayad H Zhang D Quinn Y Huang L Qiao (2004) ArticleTitleOral administration with papillomavirus pseudovirus encoding IL-2 fully restores mucosal and systemic immune responses to vaccinations in aged mice J Immunol 173 2692–2698 Occurrence Handle15294987 Occurrence Handle1:CAS:528:DC%2BD2cXmt1Oks74%3D
KH Fife CM Wheeler LA Koutsky E Barr DR Brown MA Schiff NB Kiviat KU Jansen H Barber JF Smith A Tadesse K Giacoletti PR Smith G Suhr DA Johnson (2004) ArticleTitleDose-ranging studies of the safety and immunogenicity of human papillomavirus Type 11 and Type 16 virus-like particle candidate vaccines in young healthy women Vaccine 22 2943–2952 Occurrence Handle15246631 Occurrence Handle1:CAS:528:DC%2BD2cXls1Wktb4%3D
IH Frazer (2004) ArticleTitlePrevention of cervical cancer through papillomavirus vaccination Nat Rev Immunol 4 46–54 Occurrence Handle14704767 Occurrence Handle1:CAS:528:DC%2BD2cXkvVCiug%3D%3D
EJ Freyschmidt A Alonso G Hartmann L Gissmann (2004) ArticleTitleActivation of dendritic cells and induction of T cell responses by HPV 16 L1/E7 chimeric virus-like particles are enhanced by CpG ODN or sorbitol Antivir Ther 9 479–489 Occurrence Handle15456078 Occurrence Handle1:CAS:528:DC%2BD2cXovVWrtrY%3D
T Giroglou L Florin F Schafer RE Streeck M Sapp (2001) ArticleTitleHuman papillomavirus infection requires cell surface heparan sulfate J Virol 75 1565–1570 Occurrence Handle11152531 Occurrence Handle1:CAS:528:DC%2BD3MXkvVGisw%3D%3D
HL Greenstone JD Nieland KE de Visser ML De Bruijn R Kirnbauer RB Roden DR Lowy WM Kast JT Schiller (1998) ArticleTitleChimeric papillomavirus virus-like particles elicit antitumor immunity against the E7 oncoprotein in an HPV16 tumor model Proc Natl Acad Sci USA 95 1800–1805 Occurrence Handle9465097 Occurrence Handle1:CAS:528:DyaK1cXht1Wqu7c%3D
DM Harper EL Franco C Wheeler DG Ferris D Jenkins A Schuind T Zahaf B Innis P Naud NS De Carvalho CM Roteli-Martins J Teixeira MM Blatter AP Korn W Quint G Dubin (2004) ArticleTitleEfficacy of a bivalent L1 virus-like particle vaccine in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial Lancet 364 1757–1765 Occurrence Handle15541448 Occurrence Handle1:CAS:528:DC%2BD2cXpslGju78%3D
RM Ionescu CT Przysiecki X Liang VM Garsky J Fan B Wang R Troutman Y Rippeon E Flanagan J Shiver L Shi (2006) ArticleTitlePharmaceutical and immunological evaluation of human papillomavirus virus like particle as an antigen carrier J Pharm Sci 95 70–79 Occurrence Handle16315228 Occurrence Handle1:CAS:528:DC%2BD28XlvVShsQ%3D%3D
JG Joyce JS Tung CT Przysiecki JC Cook ED Lehman JA Sands KU Jansen PM Keller (1999) ArticleTitleThe L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes J Biol Chem 274 5810–5822 Occurrence Handle10026203 Occurrence Handle1:STN:280:DyaK1M7ltVeksw%3D%3D
SM Kang Q Yao L Guo RW Compans (2003) ArticleTitleMucosal immunization with virus-like particles of simian immunodeficiency virus conjugated with cholera toxin subunit B J Virol 77 9823–9830 Occurrence Handle12941891 Occurrence Handle1:CAS:528:DC%2BD3sXntFShsLg%3D
K Kawana H Yoshikawa Y Taketani K Yoshiike T Kanda (1998) ArticleTitleIn vitro construction of pseudovirions of human papillomavirus type 16: incorporation of plasmid DNA into reassembled L1/L2 capsids J Virol 72 10298–10300 Occurrence Handle9811779 Occurrence Handle1:CAS:528:DyaK1cXns1Sns7w%3D
R Kirnbauer F Booy N Cheng DR Lowy JT Schiller (1992) ArticleTitlePapillomavirus L1 major capsid protein self-assembles into virus-like particles that are highly immunogenic Proc Natl Acad Sci USA 89 12180–12184 Occurrence Handle1334560 Occurrence Handle1:CAS:528:DyaK3sXnvV2itA%3D%3D
R Kirnbauer J Taub H Greenstone R Roden M Durst L Gissmann DR Lowy JT Schiller (1993) ArticleTitleEfficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles J Virol 67 6929–6936 Occurrence Handle8230414 Occurrence Handle1:CAS:528:DyaK2cXislamsQ%3D%3D
IM Klagge S Schneider-Schaulies (1999) ArticleTitleVirus interactions with dendritic cells J Gen Virol 80 IssueIDPt 4 823–833 Occurrence Handle10211949 Occurrence Handle1:CAS:528:DyaK1MXitlGnsbg%3D
LA Koutsky KA Ault CM Wheeler DR Brown E Barr FB Alvarez LM Chiacchierini KU Jansen (2002) ArticleTitleA controlled trial of a human papillomavirus type 16 vaccine N Engl J Med 347 1645–1651 Occurrence Handle12444178 Occurrence Handle1:CAS:528:DC%2BD38XovFSjurs%3D
DW Kowalczyk AP Wlazlo S Shane HC Ertl (2001) ArticleTitleVaccine regimen for prevention of sexually transmitted infections with human papillomavirus type 16 Vaccine 19 3583–3590 Occurrence Handle11348726 Occurrence Handle1:CAS:528:DC%2BD3MXjtlCjsLg%3D
P Lenz PM Day YY Pang SA Frye PN Jensen DR Lowy JT Schiller (2001) ArticleTitlePapillomavirus-like particles induce acute activation of dendritic cells J Immunol 166 5346–5355 Occurrence Handle11313370 Occurrence Handle1:CAS:528:DC%2BD3MXjtFyrt7k%3D
P Lenz DR Lowy JT Schiller (2005) ArticleTitlePapillomavirus virus-like particles induce cytokines characteristic of innate immune responses in plasmacytoid dendritic cells Eur J Immunol 35 1548–1556 Occurrence Handle15832296 Occurrence Handle1:CAS:528:DC%2BD2MXksVKnt7Y%3D
WJ Liu L Gissmann XY Sun A Kanjanahaluethai M Muller J Doorbar J Zhou (1997) ArticleTitleSequence close to the N-terminus of L2 protein is displayed on the surface of bovine papillomavirus type 1 virions Virology 227 474–483 Occurrence Handle9018146 Occurrence Handle1:CAS:528:DyaK2sXpt1SksA%3D%3D
WJ Liu XS Liu KN Zhao GR Leggatt IH Frazer (2000) ArticleTitlePapillomavirus virus-like particles for the delivery of multiple cytotoxic T cell epitopes Virology 273 374–382 Occurrence Handle10915608 Occurrence Handle1:CAS:528:DC%2BD3cXltFelsrY%3D
Y Liu IH Frazer WJ Liu XS Liu N McMillan KN Zhao (2001) ArticleTitleEfficiency of delivery of DNA to cells by bovine papillomavirus type-1 L1/L2 pseudovirions Appl Microbiol Biotechnol 56 150–156 Occurrence Handle11499923 Occurrence Handle1:CAS:528:DC%2BD3MXls1ShtL4%3D
SW Ludmerer D Benincasa GE Mark SuffixIII (1996) ArticleTitleTwo amino acid residues confer type specificity to a neutralizing, conformationally dependent epitope on human papillomavirus type 11 J Virol 70 4791–4794 Occurrence Handle8676509 Occurrence Handle1:CAS:528:DyaK28XjsFygt78%3D
SW Ludmerer D Benincasa GE Mark SuffixIII ND Christensen (1997) ArticleTitleA neutralizing epitope of human papillomavirus type 11 is principally described by a continuous set of residues which overlap a distinct linear, surface-exposed epitope J Virol 71 3834–3839 Occurrence Handle9094659 Occurrence Handle1:CAS:528:DyaK2sXisFWiu70%3D
SW Ludmerer WL McClements XM Wang JC Ling KU Jansen ND Christensen (2000) ArticleTitleHPV11 mutant virus-like particles elicit immune responses that neutralize virus and delineate a novel neutralizing domain Virology 266 237–245 Occurrence Handle10639310 Occurrence Handle1:CAS:528:DC%2BD3cXks1ertg%3D%3D
WL McClements XM Wang JC Ling DM Skulsky ND Christensen KU Jansen SW Ludmerer (2001) ArticleTitleA novel human papillomavirus type 6 neutralizing domain comprising two discrete regions of the major capsid protein L1 Virology 289 262–268 Occurrence Handle11689049 Occurrence Handle1:CAS:528:DC%2BD3MXnvFGhs7g%3D
M Muller L Gissmann RJ Cristiano XY Sun IH Frazer AB Jenson A Alonso H Zentgraf J Zhou (1995) ArticleTitlePapillomavirus capsid binding and uptake by cells from different tissues and species J Virol 69 948–954 Occurrence Handle7815562 Occurrence Handle1:CAS:528:DyaK2MXjtlGqsbY%3D
M Muller J Zhou TD Reed C Rittmuller A Burger J Gabelsberger J Braspenning L Gissmann (1997) ArticleTitleChimeric papillomavirus-like particles Virology 234 93–111 Occurrence Handle9234950 Occurrence Handle1:CAS:528:DyaK2sXkvFCktL8%3D
N Munoz FX Bosch S de Sanjose R Herrero X Castellsague KV Shah PJ Snijders CJ Meijer (2003) ArticleTitleEpidemiologic classification of human papillomavirus types associated with cervical cancer N Engl J Med 348 518–527 Occurrence Handle12571259
D Nardelli-Haefliger F Lurati D Wirthner F Spertini JT Schiller DR Lowy F Ponci P De Grandi (2005) ArticleTitleImmune responses induced by lower airway mucosal immunisation with a human papillomavirus type 16 virus-like particle vaccine Vaccine 23 3634–3641 Occurrence Handle15882523 Occurrence Handle1:CAS:528:DC%2BD2MXjvFeltbw%3D
JD Nieland DM Da Silva MP Velders KE de Visser JT Schiller M Muller WM Kast (1999) ArticleTitleChimeric papillomavirus virus-like particles induce a murine self-antigen-specific protective and therapeutic antitumor immune response J Cell Biochem 73 145–152 Occurrence Handle10227378 Occurrence Handle1:CAS:528:DyaK1MXitlent7Y%3D
YK Oh T Sohn JS Park MJ Kang HG Choi JA Kim WK Kim JJ Ko CK Kim (2004) ArticleTitleEnhanced mucosal and systemic immunogenicity of human papillomavirus-like particles encapsidating interleukin-2 gene adjuvant Virology 328 266–273 Occurrence Handle15464846 Occurrence Handle1:CAS:528:DC%2BD2cXotF2nu70%3D
JJ Orozco JJ Carter LA Koutsky DA Galloway (2005) ArticleTitleHumoral immune response recognizes a complex set of epitopes on human papillomavirus type 6 l1 capsomers J Virol 79 9503–9514 Occurrence Handle16014913 Occurrence Handle1:CAS:528:DC%2BD2MXmvVemu70%3D
SR Pagliusi AM Teresa (2004) ArticleTitleEfficacy and other milestones for human papillomavirus vaccine introduction Vaccine 23 569–578 Occurrence Handle15630792
J Paintsil M Muller M Picken L Gissmann J Zhou (1996) ArticleTitleCarboxyl terminus of bovine papillomavirus type-1 L1 protein is not required for capsid formation Virology 223 238–244 Occurrence Handle8806558 Occurrence Handle1:CAS:528:DyaK28XlsVemt7Y%3D
DV Pastrana WC Vass DR Lowy JT Schiller (2001) ArticleTitleNHPV16 VLP vaccine induces human antibodies that neutralize divergent variants of HPV16 Virology 279 361–369 Occurrence Handle11145917 Occurrence Handle1:CAS:528:DC%2BD3MXhs1ehsg%3D%3D
DV Pastrana CB Buck YY Pang CD Thompson PE Castle PC FitzGerald KS Kruger DR Lowy JT Schiller (2004) ArticleTitleReactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18 Virology 321 205–216 Occurrence Handle15051381 Occurrence Handle1:CAS:528:DC%2BD2cXis1Wgur0%3D
S Peng IH Frazer GJ Fernando J Zhou (1998) ArticleTitlePapillomavirus virus-like particles can deliver defined CTL epitopes to the MHC class I pathway Virology 240 147–157 Occurrence Handle9448699 Occurrence Handle1:CAS:528:DyaK1cXlsVyhtw%3D%3D
AP Pinto HC Baggio GB Guedes (2005) ArticleTitleSexually-transmitted viral diseases in women: clinical and epidemiological aspects and advances in laboratory diagnosis Braz J Infect Dis 9 241–250 Occurrence Handle16224631
LA Pinto J Edwards PE Castle CD Harro DR Lowy JT Schiller D Wallace W Kopp JW Adelsberger MW Baseler JA Berzofsky A Hildesheim (2003) ArticleTitleCellular immune responses to human papillomavirus (HPV)-16 L1 in healthy volunteers immunized with recombinant HPV-16 L1 virus-like particles J Infect Dis 188 327–338 Occurrence Handle12854090 Occurrence Handle1:CAS:528:DC%2BD3sXmslShur4%3D
LA Pinto PE Castle RB Roden CD Harro DR Lowy JT Schiller D Wallace M Williams W Kopp IH Frazer JA Berzofsky A Hildesheim (2005) ArticleTitleHPV-16 L1 VLP vaccine elicits a broad-spectrum of cytokine responses in whole blood Vaccine 23 3555–3564 Occurrence Handle15855014 Occurrence Handle1:CAS:528:DC%2BD2MXjsFGqtbo%3D
Reis e Sousa A Sher P Kaye (1999) ArticleTitleThe role of dendritic cells in the induction and regulation of immunity to microbial infection Curr Opin Immunol 11 392–399 Occurrence Handle10448137 Occurrence Handle1:CAS:528:DyaK1MXlt1CksrY%3D
RB Roden HL Greenstone R Kirnbauer FP Booy J Jessie DR Lowy JT Schiller (1996) ArticleTitleIn vitro generation and type-specific neutralization of a human papillomavirus type 16 virion pseudotype J Virol 70 5875–5883 Occurrence Handle8709207 Occurrence Handle1:CAS:528:DyaK28XkvFGhsLw%3D
O Rommel J Dillner C Fligge C Bergsdorf X Wang HC Selinka M Sapp (2005) ArticleTitleHeparan sulfate proteoglycans interact exclusively with conformationally intact HPV L1 assemblies: basis for a virus-like particle ELISA J Med Virol 75 114–121 Occurrence Handle15543569 Occurrence Handle1:CAS:528:DC%2BD2MXhs1Ghtg%3D%3D
JL Rossi L Gissmann K Jansen M Muller (2000) ArticleTitleAssembly of human papillomavirus type 16 pseudovirions in Saccharomyces cerevisiae Hum Gene Ther 11 1165–1176 Occurrence Handle10834618 Occurrence Handle1:CAS:528:DC%2BD3cXjsF2gsL8%3D
MP Rudolf SC Fausch DM Da Silva WM Kast (2001) ArticleTitleHuman dendritic cells are activated by chimeric human papillomavirus type-16 virus-like particles and induce epitope-specific human T cell responses in vitro J Immunol 166 5917–5924 Occurrence Handle11342606 Occurrence Handle1:CAS:528:DC%2BD3MXjsFCqsrc%3D
W Ruiz WL McClements KU Jansen MT Esser (2005) ArticleTitleKinetics and isotype profile of antibody responses in rhesus macaques induced following vaccination with HPV 6, 11, 16 and 18 L1-virus-like particles formulated with or without Merck aluminum adjuvant J Immune Based Ther Vaccines 3 2 Occurrence Handle15842730
JR Sadeyen S Tourne M Shkreli PY Sizaret P Coursaget (2003) ArticleTitleInsertion 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 Virology 309 32–40 Occurrence Handle12726724 Occurrence Handle1:CAS:528:DC%2BD3sXjtlWltr4%3D
M Sapp HC Selinka (2005) ArticleTitlePseudovirions as specific tools for investigation of virus interactions with cells Methods Mol Biol 292 197–212 Occurrence Handle15507710 Occurrence Handle1:CAS:528:DC%2BD2MXjt1antw%3D%3D
K Schafer M Muller S Faath A Henn W Osen H Zentgraf A Benner L Gissmann I Jochmus (1999) ArticleTitleImmune response to human papillomavirus 16 L1E7 chimeric virus-like particles: induction of cytotoxic T cells and specific tumor protection Int J Cancer 81 881–888 Occurrence Handle10362134 Occurrence Handle1:STN:280:DyaK1M3ovV2rsg%3D%3D
W Shi J Liu Y Huang L Qiao (2001) ArticleTitlePapillomavirus pseudovirus: a novel vaccine to induce mucosal and systemic cytotoxic T-lymphocyte responses J Virol 75 10139–10148 Occurrence Handle11581382 Occurrence Handle1:CAS:528:DC%2BD3MXns1Whtrw%3D
K Slupetzky S Shafti-Keramat P Lenz S Brandt A Grassauer M Sara R Kirnbauer (2001) ArticleTitleChimeric papillomavirus-like particles expressing a foreign epitope on capsid surface loops J Gen Virol 82 2799–2804 Occurrence Handle11602792 Occurrence Handle1:CAS:528:DC%2BD3MXotlKmu70%3D
Y Stauffer K Raj K Masternak P Beard (1998) ArticleTitleInfectious human papillomavirus type 18 pseudovirions J Mol Biol 283 529–536 Occurrence Handle9784363 Occurrence Handle1:CAS:528:DyaK1cXntlalsLw%3D
T Storni C Ruedl K Schwarz RA Schwendener WA Renner MF Bachmann (2004) ArticleTitleNonmethylated CG motifs packaged into virus-like particles induce protective cytotoxic T cell responses in the absence of systemic side effects J Immunol 172 1777–1785 Occurrence Handle14734761 Occurrence Handle1:CAS:528:DC%2BD2cXptl2hsg%3D%3D
JA Suzich SJ Ghim FJ Palmer-Hill WI White JK Tamura JA Bell JA Newsome AB Jenson R Schlegel (1995) ArticleTitleSystemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas Proc Natl Acad Sci USA 92 11553–11557 Occurrence Handle8524802 Occurrence Handle1:CAS:528:DyaK2MXpvVOnsr8%3D
TM Tan RC Ting (1995) ArticleTitleIn vitro and in vivo inhibition of human papillomavirus type 16 E6 and E7 genes Cancer Res 55 4599–4605 Occurrence Handle7553636 Occurrence Handle1:CAS:528:DyaK2MXoslWmsLw%3D
TW Tobery JF Smith N Kuklin D Skulsky C Ackerson L Huang L Chen JC Cook WL McClements KU Jansen (2003) ArticleTitleEffect of vaccine delivery system on the induction of HPV16L1-specific humoral and cell-mediated immune responses in immunized rhesus macaques Vaccine 21 1539–1547 Occurrence Handle12615451 Occurrence Handle1:CAS:528:DC%2BD3sXhs1Knurw%3D
A Touze P Coursaget (1998) ArticleTitleIn vitro gene transfer using human papillomavirus-like particles Nucleic Acids Res 26 1317–1323 Occurrence Handle9469843 Occurrence Handle1:CAS:528:DyaK1cXhvFejs7k%3D
BL Trus RB Roden HL Greenstone M Vrhel JT Schiller FP Booy (1997) ArticleTitleNovel structural features of bovine papillomavirus capsid revealed by a three-dimensional reconstruction to 9 A resolution Nat Struct Biol 4 413–420 Occurrence Handle9145113 Occurrence Handle1:CAS:528:DyaK2sXivFWqsrc%3D
F Unckell RE Streeck M Sapp (1997) ArticleTitleGeneration and neutralization of pseudovirions of human papillomavirus type 33 J Virol 71 2934–2939 Occurrence Handle9060652 Occurrence Handle1:CAS:528:DyaK2sXhvVGnurk%3D
DM von Knebel C Rittmuller H zur Hausen M Durst (1992) ArticleTitleInhibition of tumorigenicity of cervical cancer cells in nude mice by HPV E6–E7 anti-sense RNA Int J Cancer 51 831–834
A Varsani AL Williamson D de Villiers I Becker ND Christensen EP Rybicki (2003) ArticleTitleChimeric human papillomavirus type 16 (HPV-16) L1 particles presenting the common neutralizing epitope for the L2 minor capsid protein of HPV-6 and HPV-16 J Virol 77 8386–8393 Occurrence Handle12857908 Occurrence Handle1:CAS:528:DC%2BD3sXlslWrur8%3D
LL Villa RL Costa CA Petta RP Andrade KA Ault AR Giuliano CM Wheeler LA Koutsky C Malm M Lehtinen FE Skjeldestad SE Olsson M Steinwall DR Brown RJ Kurman BM Ronnett MH Stoler A Ferenczy DM Harper GM Tamms J Yu L Lupinacci R Railkar FJ Taddeo KU Jansen MT Esser HL Sings AJ Saah E Barr (2005) ArticleTitleProphylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial Lancet Oncol 6 271–278 Occurrence Handle15863374
C Volpers F Unckell P Schirmacher RE Streeck M Sapp (1995) ArticleTitleBinding and internalization of human papillomavirus type 33 virus-like particles by eukaryotic cells J Virol 69 3258–3264 Occurrence Handle7745672 Occurrence Handle1:CAS:528:DyaK2MXls1yisb8%3D
MT Wakabayashi DM Da Silva RK Potkul WM Kast (2002) ArticleTitleComparison of human papillomavirus type 16 L1 chimeric virus-like particles versus L1/L2 chimeric virus-like particles in tumor prevention Intervirology 45 300–307 Occurrence Handle12566713 Occurrence Handle1:CAS:528:DC%2BD3sXosVOltg%3D%3D
M Yan J Peng IA Jabbar X Liu L Filgueira IH Frazer R Thomas (2004) ArticleTitleDespite differences between dendritic cells and Langerhans cells in the mechanism of papillomavirus-like particle antigen uptake, both cells cross-prime T cells Virology 324 297–310 Occurrence Handle15207617 Occurrence Handle1:CAS:528:DC%2BD2cXltVOiurY%3D
M Yan J Peng IA Jabbar X Liu L Filgueira IH Frazer R Thomas (2005) ArticleTitleActivation of dendritic cells by human papillomavirus-like particles through TLR4 and NF-kappaB-mediated signalling, moderated by TGF-beta Immunol Cell Biol 83 83–91 Occurrence Handle15661045 Occurrence Handle1:CAS:528:DC%2BD2MXhvFGns74%3D
R Yang FM Murillo H Cui R Blosser S Uematsu K Takeda S Akira RP Viscidi RB Roden (2004) ArticleTitlePapillomavirus-like particles stimulate murine bone marrow-derived dendritic cells to produce alpha interferon and Th1 immune responses via MyD88 J Virol 78 11152–11160 Occurrence Handle15452235 Occurrence Handle1:CAS:528:DC%2BD2cXotlKisrk%3D
R Yang FM Murillo KY Lin WH Yutzy S Uematsu K Takeda S Akira RP Viscidi RB Roden (2004) ArticleTitleHuman papillomavirus type-16 virus-like particles activate complementary defense responses in key dendritic cell subpopulations J Immunol 173 2624–2631 Occurrence Handle15294979 Occurrence Handle1:CAS:528:DC%2BD2cXmt1Olu74%3D
CS Yoon KD Kim SN Park SW Cheong (2001) ArticleTitlealpha(6) Integrin is the main receptor of human papillomavirus type 16 VLP Biochem Biophys Res Commun 283 668–673 Occurrence Handle11341777 Occurrence Handle1:CAS:528:DC%2BD3MXjt1Gnt7s%3D
H zur Hausen EM de Villiers L Gissmann (1981) ArticleTitlePapillomavirus infections and human genital cancer Gynecol Oncol 12 S124–S128 Occurrence Handle6273261 Occurrence Handle1:STN:280:Bi2D2szps1U%3D
H zur Hausen (2002) ArticleTitlePapillomaviruses and cancer: from basic studies to clinical application Nat Rev Cancer 2 342–350 Occurrence Handle12044010 Occurrence Handle1:CAS:528:DC%2BD38Xkt1eltbw%3D
H Zhang R Fayad X Wang D Quinn L Qiao (2004) ArticleTitleHuman immunodeficiency virus type 1 gag-specific mucosal immunity after oral immunization with papillomavirus pseudoviruses encoding gag J Virol 78 10249–10257 Occurrence Handle15367590 Occurrence Handle1:CAS:528:DC%2BD2cXotVemsrc%3D
H Zhang Y Huang R Fayad GT Spear L Qiao (2004) ArticleTitleInduction of mucosal and systemic neutralizing antibodies against human immunodeficiency virus type 1 (HIV-1) by oral immunization with bovine Papillomavirus-HIV-1 gp41 chimeric virus-like particles J Virol 78 8342–8348 Occurrence Handle15254206 Occurrence Handle1:CAS:528:DC%2BD2cXmtFCjsbk%3D
LF Zhang J Zhou S Chen LL Cai QY Bao FY Zheng JQ Lu J Padmanabha K Hengst K Malcolm IH Frazer (2000) ArticleTitleHPV6b virus like particles are potent immunogens without adjuvant in man Vaccine 18 1051–1058 Occurrence Handle10590325 Occurrence Handle1:STN:280:DC%2BD3c%2FlvF2rtw%3D%3D
KN Zhao XY Sun IH Frazer J Zhou (1998) ArticleTitleDNA packaging by L1 and L2 capsid proteins of bovine papillomavirus type 1 Virology 243 482–491 Occurrence Handle9568045 Occurrence Handle1:CAS:528:DyaK1cXisFynu7s%3D
KN Zhao K Hengst WJ Liu YH Liu XS Liu NA McMillan IH Frazer (2000) ArticleTitleBPV1 E2 protein enhances packaging of full-length plasmid DNA in BPV1 pseudovirions Virology 272 382–393 Occurrence Handle10873782 Occurrence Handle1:CAS:528:DC%2BD3cXktlSnurc%3D
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Xu, YF., Zhang, YQ., Xu, XM. et al. Papillomavirus virus-like particles as vehicles for the delivery of epitopes or genes. Arch Virol 151, 2133–2148 (2006). https://doi.org/10.1007/s00705-006-0798-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-006-0798-8