Induction of ebolavirus cross-species immunity using retrovirus-like particles bearing the Ebola virus glycoprotein lacking the mucin-like domain

Virology Journal

Volumn 9, Issue , 2012, Pages

  Ou, Wu ^a   Delisle, Josie ^a   Jacques, Jerome ^a   Shih, Joanna ^b   Price, Graeme ^a   Kuhn, Jens H ^c   Wang, Vivian ^d   Verthelyi, Daniela ^d   Kaplan, Gerardo ^a   Wilson, Carolyn A ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^d Center for Drug Evaluation and Review   (United States)

Author keywords

DNA vaccine; Ebola; Ebolavirus; Envelope glycoprotein; Filovirus; Mucin like domain; Retrovirus; Virus like particles

Indexed keywords

DNA; DNA VACCINE; MUCIN; NEUTRALIZING ANTIBODY; VIRUS GLYCOPROTEIN; EBOLA VACCINE; GLYCOPROTEIN; RECOMBINANT VACCINE; VIROSOME; VIROSOME VACCINE; VIRUS ANTIBODY; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CELL STRAIN HEK293; CONTROLLED STUDY; CROSS REACTION; EBOLA HEMORRHAGIC FEVER; EBOLA VIRUS; ENZYME LINKED IMMUNOSORBENT ASSAY; FILOVIRUS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOGENICITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARTICLE SIZE; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; RETROVIRUS; VIRUS LIKE AGENT; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CELLULAR IMMUNITY; FEMALE; GENETICS; IMMUNOLOGY; PROTEIN TERTIARY STRUCTURE;

EBOLA VIRUS; MARBURGVIRUS; MUS;

ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; CROSS REACTIONS; EBOLA VACCINES; EBOLAVIRUS; FEMALE; GLYCOPROTEINS; IMMUNITY, CELLULAR; MICE; MICE, INBRED BALB C; PROTEIN STRUCTURE, TERTIARY; RETROVIRIDAE; VACCINES, SYNTHETIC; VACCINES, VIROSOME; VIRAL PROTEINS; VIROSOMES;

EID: 84856078790     PISSN: None     EISSN: 1743422X     Source Type: Journal    
DOI: 10.1186/1743-422X-9-32     Document Type: Article

References (55)

1. Proposal for a revised taxonomy of the family Filoviridae: classification, names of taxa and viruses, and virus abbreviations. Kuhn JH, Becker S, Ebihara H, Geisbert TW, Johnson KM, Kawaoka Y, Lipkin WI, Negredo AI, Netesov SV, Nichol ST, et al. Arch Virol 2010 155 2083 2103 10.1007/s00705-010- 0814-x 21046175
2. Ebolavirus and Marburgvirus: insight the Filoviridae family. Ascenzi P, Bocedi A, Heptonstall J, Capobianchi MR, Di Caro A, Mastrangelo E, Bolognesi M, Ippolito G, Mol Aspects Med 2008 29 151 185 10.1016/j.mam.2007.09.005 18063023
3. Ebola virus: from discovery to vaccine. Feldmann H, Jones S, Klenk HD, Schnittler HJ, Nat Rev Immunol 2003 3 677 685 10.1038/nri1154 12974482 (Pubitemid 37328670)
4. Prospects for immunisation against Marburg and Ebola viruses. Geisbert TW, Bausch DG, Feldmann H, Rev Med Virol 2010 20 344 357 10.1002/rmv.661 20658513
5. Recent advances in Ebolavirus vaccine development. Richardson JS, Dekker JD, Croyle MA, Kobinger GP, Hum Vaccin 2010 6 439 449 10.4161/hv.6.6.11097 20671437
6. Progress in filovirus vaccine development: evaluating the potential for clinical use. Falzarano D, Geisbert TW, Feldmann H, Expert Rev Vaccines 2011 10 63 77 10.1586/erv.10.152 21162622
7. Covalent modifications of the ebola virus glycoprotein. Jeffers SA, Sanders DA, Sanchez A, J Virol 2002 76 12463 12472 10.1128/JVI.76.24.12463- 12472.2002 12438572 (Pubitemid 35386932)
8. Structure of the Ebola virus glycoprotein bound to an antibody from a human survivor. Lee JE, Fusco ML, Hessell AJ, Oswald WB, Burton DR, Saphire EO, Nat 2008 454 177 182 10.1038/nature07082 (Pubitemid 351969896)
9. Steric shielding of surface epitopes and impaired immune recognition induced by the ebola virus glycoprotein. Francica JR, Varela-Rohena A, Medvec A, Plesa G, Riley JL, Bates P, PLoS Pathog 2010 6 1001098 10.1371/journal.ppat. 1001098 20844579
10. Ebolavirus glycoprotein GP masks both its own epitopes and the presence of cellular surface proteins. Reynard O, Borowiak M, Volchkova VA, Delpeut S, Mateo M, Volchkov VE, J Virol 2009 83 9596 9601 10.1128/JVI.00784-09 19587051
11. Influences of glycosylation on antigenicity, immunogenicity, and protective efficacy of ebola virus GP DNA vaccines. Dowling W, Thompson E, Badger C, Mellquist JL, Garrison AR, Smith JM, Paragas J, Hogan RJ, Schmaljohn C, J Virol 2007 81 1821 1837 10.1128/JVI.02098-06 17151111 (Pubitemid 46214455)
12. Production and characterization of monoclonal antibodies against different epitopes of Ebola virus antigens. Shahhosseini S, Das D, Qiu X, Feldmann H, Jones SM, Suresh MR, J Virol Methods 2007 143 29 37 10.1016/j.jviromet.2007.02.004 17368819 (Pubitemid 46802822)
13. Epitopes required for antibody-dependent enhancement of Ebola virus infection. Takada A, Ebihara H, Feldmann H, Geisbert TW, Kawaoka Y, J Infect Dis 2007 196 Suppl 2 347 356 17940970
14. Epitopes involved in antibody-mediated protection from Ebola virus. Wilson JA, Hevey M, Bakken R, Guest S, Bray M, Schmaljohn AL, Hart MK, Sci 2000 287 1664 1666 10.1126/science.287.5458.1664 (Pubitemid 30127770)
15. Comprehensive analysis of ebola virus GP1 in viral entry. Manicassamy B, Wang J, Jiang H, Rong L, J Virol 2005 79 4793 4805 10.1128/JVI.79.8.4793-4805. 2005 15795265 (Pubitemid 40464230)
16. Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence. Simmons G, Wool-Lewis RJ, Baribaud F, Netter RC, Bates P, J Virol 2002 76 2518 2528 10.1128/jvi.76.5.2518-2528.2002 11836430 (Pubitemid 34150720)
17. Distinct cellular interactions of secreted and transmembrane Ebola virus glycoproteins. Yang Z, Delgado R, Xu L, Todd RF, Nabel EG, Sanchez A, Nabel GJ, Sci 1998 279 1034 1037 10.1126/science.279.5353.1034 (Pubitemid 28113305)
18. The primed ebolavirus glycoprotein (19-kilodalton GP1,2): sequence and residues critical for host cell binding. Dube D, Brecher MB, Delos SE, Rose SC, Park EW, Schornberg KL, Kuhn JH, White JM, J Virol 2009 83 2883 2891 10.1128/JVI.01956-08 19144707
19. Conserved receptor-binding domains of Lake Victoria marburgvirus and Zaire ebolavirus bind a common receptor. Kuhn JH, Radoshitzky SR, Guth AC, Warfield KL, Li W, Vincent MJ, Towner JS, Nichol ST, Bavari S, Choe H, et al. J Biol Chem 2006 281 15951 15958 10.1074/jbc.M601796200 16595665 (Pubitemid 43848488)
20. Virus-like particles as particulate vaccines. Buonaguro L, Tornesello ML, Buonaguro FM, Curr HIV Res 2010 8 299 309 10.2174/157016210791208659 20353398
21. Virus-like particles: flexible platforms for vaccine development. Chackerian B, Expert Rev Vaccines 2007 6 381 390 10.1586/14760584.6.3.381 17542753 (Pubitemid 46911601)
22. The coming of age of virus-like particle vaccines. Jennings GT, Bachmann MF, Biol Chem 2008 389 521 536 10.1515/BC.2008.064 18953718 (Pubitemid 351874198)
23. Development of more efficient and effective DNA vaccines. Apostolopoulos V, Weiner DB, Expert Rev Vaccines 2009 8 1133 1134 10.1586/erv.09.94 19722884
24. DNA vaccines for biodefense. Dupuy LC, Schmaljohn CS, Expert Rev Vaccines 2009 8 1739 1754 10.1586/erv.09.132 19943766
25. DNA vaccines: an historical perspective and view to the future. Liu MA, Immunol Rev 2011 239 62 84 10.1111/j.1600-065X.2010.00980.x 21198665
26. DNA vaccines encoding retrovirus-based virus-like particles induce efficient immune responses without adjuvant. Bellier B, Dalba C, Clerc B, Desjardins D, Drury R, Cosset FL, Collins M, Klatzmann D, Vaccine 2006 24 2643 2655 10.1016/j.vaccine.2005.11.034 16481074 (Pubitemid 43290396)
27. DNA vaccines expressing retrovirus-like particles are efficient immunogens to induce neutralizing antibodies. Bellier B, Huret C, Miyalou M, Desjardins D, Frenkiel MP, Despres P, Tangy F, Dalba C, Klatzmann D, Vaccine 2009 27 5772 5780 10.1016/j.vaccine.2009.07.059 19656495
28. Recombinant retrovirus-like particle forming DNA vaccines in prime-boost immunization and their use for hepatitis C virus vaccine development. Desjardins D, Huret C, Dalba C, Kreppel F, Kochanek S, Cosset FL, Tangy F, Klatzmann D, Bellier B, J Gene Med 2009 11 313 325 10.1002/jgm.1307 19248137
29. Single-round infectious particles enhance immunogenicity of a DNA vaccine against West Nile virus. Chang DC, Liu WJ, Anraku I, Clark DC, Pollitt CC, Suhrbier A, Hall RA, Khromykh AA, Nat Biotechnol 2008 26 571 577 10.1038/nbt1400 18425125 (Pubitemid 351668041)
30. HIV-1 subtype C Pr55gag virus-like particle vaccine efficiently boosts baboons primed with a matched DNA vaccine. Chege GK, Shephard EG, Meyers A, van Harmelen J, Williamson C, Lynch A, Gray CM, Rybicki EP, Williamson AL, J Gen Virol 2008 89 2214 2227 10.1099/vir.0.83501-0 18753231
31. Replication-competent vectors and empty virus-like particles: new retroviral vector designs for cancer gene therapy or vaccines. Dalba C, Bellier B, Kasahara N, Klatzmann D, Mol Ther 2007 15 457 466 10.1038/sj.mt.6300054 17245356
32. A DNA vaccine for Ebola virus is safe and immunogenic in a phase I clinical trial. Martin JE, Sullivan NJ, Enama ME, Gordon IJ, Roederer M, Koup RA, Bailer RT, Chakrabarti BK, Bailey MA, Gomez PL, et al. Clin Vaccine Immunol 2006 13 1267 1277 10.1128/CVI.00162-06 16988008 (Pubitemid 46768881)
33. Comparison of the protective efficacy of DNA and baculovirus-derived protein vaccines for EBOLA virus in guinea pigs. Mellquist-Riemenschneider JL, Garrison AR, Geisbert JB, Saikh KU, Heidebrink KD, Jahrling PB, Ulrich RG, Schmaljohn CS, Virus Res 2003 92 187 193 10.1016/S0168-1702(02)00338-6 12686428 (Pubitemid 36398464)
34. Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates. Sullivan NJ, Geisbert TW, Geisbert JB, Xu L, Yang ZY, Roederer M, Koup RA, Jahrling PB, Nabel GJ, Nat 2003 424 681 684 10.1038/nature01876 (Pubitemid 36987993)
35. Development of a preventive vaccine for Ebola virus infection in primates. Sullivan NJ, Sanchez A, Rollin PE, Yang ZY, Nabel GJ, Nat 2000 408 605 609 10.1038/35046108
36. Protection against lethal challenge by Ebola virus-like particles produced in insect cells. Sun Y, Carrion R Jr, Ye L, Wen Z, Ro YT, Brasky K, Ticer AE, Schwegler EE, Patterson JL, Compans RW, Yang C, Virol 2009 383 12 21 10.1016/j.virol.2008.09.020
37. Ebola virus-like particles protect from lethal Ebola virus infection. Warfield KL, Bosio CM, Welcher BC, Deal EM, Mohamadzadeh M, Schmaljohn A, Aman MJ, Bavari S, Proc Natl Acad Sci USA 2003 100 15889 15894 10.1073/pnas. 2237038100 14673108 (Pubitemid 38021085)
38. Filovirus-like particles produced in insect cells: immunogenicity and protection in rodents. Warfield KL, Posten NA, Swenson DL, Olinger GG, Esposito D, Gillette WK, Hopkins RF, Costantino J, Panchal RG, Hartley JL, et al. J Infect Dis 2007 196 Suppl 2 421 429 17940979
39. Proteolysis of the Ebola virus glycoproteins enhances virus binding and infectivity. Kaletsky RL, Simmons G, Bates P, J Virol 2007 81 13378 13384 10.1128/JVI.01170-07 17928356 (Pubitemid 350247834)
40. Identification of two amino acid residues on Ebola virus glycoprotein 1 critical for cell entry. Mpanju OM, Towner JS, Dover JE, Nichol ST, Wilson CA, Virus Res 2006 121 205 214 10.1016/j.virusres.2006.06.002 16839637 (Pubitemid 44467987)
41. Characterization of Ebola virus entry by using pseudotyped viruses: identification of receptor-deficient cell lines. Wool-Lewis RJ, Bates P, J Virol 1998 72 3155 3160 9525641 (Pubitemid 28175558)
42. Development and characterization of rabbit and mouse antibodies against ebolavirus envelope glycoproteins. Ou W, Delisle J, Konduru K, Bradfute S, Radoshitzky SR, Retterer C, Kota K, Bavari S, Kuhn JH, Jahrling PB, et al. J Virol Methods 2011 174 99 109 10.1016/j.jviromet.2011.04.003 21513741
43. Ebola virus glycoprotein Fc fusion protein confers protection against lethal challenge in vaccinated mice. Konduru K, Bradfute SB, Jacques J, Manangeeswaran M, Nakamura S, Morshed S, Wood SC, Bavari S, Kaplan GG, Vaccine 2011 29 2968 2977 10.1016/j.vaccine.2011.01.113 21329775
44. Immune protection of nonhuman primates against Ebola virus with single low-dose adenovirus vectors encoding modified GPs. Sullivan NJ, Geisbert TW, Geisbert JB, Shedlock DJ, Xu L, Lamoreaux L, Custers JH, Popernack PM, Yang ZY, Pau MG, et al. PLoS Med 2006 3 177 10.1371/journal.pmed.0030177 16683867 (Pubitemid 43987829)
45. Ebola virus-like particle-induced activation of NF-kappaB and Erk signaling in human dendritic cells requires the glycoprotein mucin domain. Martinez O, Valmas C, Basler CF, Virol 2007 364 342 354 10.1016/j.virol.2007.03. 020 (Pubitemid 46873712)
46. Human immunodeficiency virus type 1 incorporates both glycosyl phosphatidylinositol-anchored CD55 and CD59 and integral membrane CD46 at levels that protect from complement-mediated destruction. Saifuddin M, Hedayati T, Atkinson JP, Holguin MH, Parker CJ, Spear GT, J Gen Virol 1997 78 Pt 8 1907 1911 9266986 (Pubitemid 27367673)
47. Role of virion-associated glycosylphosphatidylinositol-linked proteins CD55 and CD59 in complement resistance of cell line-derived and primary isolates of HIV-1. Saifuddin M, Parker CJ, Peeples ME, Gorny MK, Zolla-Pazner S, Ghassemi M, Rooney IA, Atkinson JP, Spear GT, J Exp Med 1995 182 501 509 10.1084/jem.182.2.501 7543140
48. Host cell-derived complement control proteins CD55 and CD59 are incorporated into the virions of two unrelated enveloped viruses. Human T cell leukemia/lymphoma virus type I (HTLV-I) and human cytomegalovirus (HCMV). Spear GT, Lurain NS, Parker CJ, Ghassemi M, Payne GH, Saifuddin M, J Immunol 1995 155 4376 4381 7594597
49. Human CD59 incorporation into porcine endogenous retrovirus particles: implications for the use of transgenic pigs for xenotransplantation. Takefman DM, Spear GT, Saifuddin M, Wilson CA, J Virol 2002 76 1999 2002 10.1128/JVI.76.4.1999-2002.2002 11799196 (Pubitemid 34094648)
50. kat: a high-efficiency retroviral transduction system for primary human T lymphocytes. Finer MH, Dull TJ, Qin L, Farson D, Roberts MR, Blood 1994 83 43 50 8274751 (Pubitemid 24016514)
51. Protective cytotoxic T-cell responses induced by venezuelan equine encephalitis virus replicons expressing Ebola virus proteins. Olinger GG, Bailey MA, Dye JM, Bakken R, Kuehne A, Kondig J, Wilson J, Hogan RJ, Hart MK, J Virol 2005 79 14189 14196 10.1128/JVI.79.22.14189-14196.2005 16254354 (Pubitemid 41552717)
52. Induction of immune responses in mice and monkeys to Ebola virus after immunization with liposome-encapsulated irradiated Ebola virus: protection in mice requires CD4(+) T cells. Rao M, Bray M, Alving CR, Jahrling P, Matyas GR, J Virol 2002 76 9176 9185 10.1128/JVI.76.18.9176-9185.2002 12186901 (Pubitemid 34919876)
53. Phenylalanines at positions 88 and 159 of Ebolavirus envelope glycoprotein differentially impact envelope function. Ou W, King H, Delisle J, Shi D, Wilson CA, Virol 2010 396 135 142 10.1016/j.virol.2009.10.028
54. Viral and cellular factors governing hamster cell infection by murine and gibbon ape leukemia viruses. Wilson CA, Eiden MV, J Virol 1991 65 5975 5982 1717711
55. Matrix protein 2 vaccination and protection against influenza viruses, including subtype H5N1. Tompkins SM, Zhao ZS, Lo CY, Misplon JA, Liu T, Ye Z, Hogan RJ, Wu Z, Benton KA, Tumpey TM, Epstein SL, Emerg Infect Dis 2007 13 426 435 10.3201/eid1303.061125 17552096 (Pubitemid 46348126)