Preparation of recombinant vaccines

Biotechnology Annual Review

Volumn 13, Issue , 2007, Pages 65-94

  Soler, Eric ^a   Houdebine, Louis Marie ^b  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b INRA Institut National de la Recherche Agronomique   (France)

Author keywords

adjuvants; epitope carrier; recombinant proteins; transgenic animals.; vaccine; VLP

Indexed keywords

ALUMINUM POTASSIUM SULFATE; ANTHRAX VACCINE; ANTITHROMBIN III; CHOLERA TOXIN; CPG OLIGODEOXYNUCLEOTIDE; ESCHERICHIA COLI ENTEROTOXIN; HEPATITIS A VACCINE; HEPATITIS B VACCINE; HEPATITIS C VACCINE; HERPES VACCINE; INFLUENZA VACCINE; INSULIN; ISCOM; LIPOSOME; MICROSPHERE; PHOSPHORYL LIPID A; PLANT EXTRACT; POLYGLACTIN; POLYLACTIDE; POLYMER; POTATO EXTRACT; PROTEIN VP2; PROTEIN VP6; RECOMBINANT HEPATITIS B VACCINE; RECOMBINANT VACCINE; ROTAVIRUS VACCINE; SEVERE ACUTE RESPIRATORY SYNDROME VACCINE; TOBACCO EXTRACT; TOMATO EXTRACT; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANTHRAX; COST; DIARRHEA; DRUG EFFICACY; DRUG FORMULATION; DRUG POTENCY; DRUG SAFETY; DRUG SYNTHESIS; GENE EXPRESSION; HEPATITIS B; HEPATITIS C; HOST PATHOGEN INTERACTION; HUMAN; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOGENICITY; INFLUENZA; INJECTION SITE REACTION; INNATE IMMUNITY; MYALGIA; NONHUMAN; PEPTIDE SYNTHESIS; POTATO; REVIEW; SEVERE ACUTE RESPIRATORY SYNDROME; TOBACCO; TOMATO; TRANSGENE; TRANSGENIC ANIMAL; TRANSGENIC PLANT; VACCINATION; VACCINE PRODUCTION; VIRUS IMMUNITY; VIRUS INFECTION; VIRUS LIKE AGENT;

BIOTECHNOLOGY; PROTEIN ENGINEERING; RECOMBINANT PROTEINS; VACCINES, SYNTHETIC;

ANIMALIA;

EID: 34548648296     PISSN: 13872656     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S1387-2656(07)13004-0     Document Type: Review

References (119)

1. Wood D. WHO informal consultation on quality, safety and efficacy specifications for live attenuated rotavirus vaccines Mexico City, Mexico, 8-9 February 2005. Vaccine 23 (2005) 5478-5487
2. Roberts L. Vaccines: rotavirus vaccines' second chance. Science 305 (2004) 1890-1893
3. Glass R.I. New hope for defeating rotavirus. Sci Am 294 (2006) 46-51 54-55
4. Noad R., and Roy P. Virus-like particles as immunogens. Trends Microbiol 11 (2003) 438-444
5. Rodriguez-Ortega M.J., Norais N., Bensi G., Liberatori S., Capo S., Mora M., Scarselli M., Doro F., Ferrari G., Garaguso I., Maggi T., Neumann A., Covre A., Telford J.L., and Grandi G. Characterization and identification of vaccine candidate proteins through analysis of the group A Streptococcus surface proteome. Nat Biotechnol 24 (2006) 191-197
6. Musser J.M. The next chapter in reverse vaccinology. Nat Biotechnol 24 (2006) 157-158
7. Choi A.H., Basu M., McNeal M.M., Flint J., VanCott J.L., Clements J.D., and Ward R.L. Functional mapping of protective domains and epitopes in the rotavirus VP6 protein. J Virol 74 (2000) 11574-11580
8. Choi A.H., McNeal M.M., Basu M., Bean J.A., VanCott J.L., Clements J.D., and Ward R.L. Functional mapping of protective epitopes within the rotavirus VP6 protein in mice belonging to different haplotypes. Vaccine 21 (2003) 761-767
9. Baneyx F., and Mujacic M. Recombinant protein folding and misfolding in E. coli. Nat Biotechnol 22 (2004) 1399-1408
10. Choi A.H., McNeal M.M., Basu M., Flint J.A., Stone S.C., Clements J.D., Bean J.A., Poe S.A., VanCott J.L., and Ward R.L. Intranasal or oral immunization of inbred and outbred mice with murine or human rotavirus VP6 proteins protects against viral shedding after challenge with murine rotaviruses. Vaccine 20 (2002) 3310-3321
11. Choi A.H., McNeal M.M., Flint J.A., Basu M., Lycke N.Y., Clements J.D., Bean J.A., Davis H.L., McCluskie M.J., VanCott J.L., and Ward R.L. The level of protection against rotavirus shedding in mice following immunization with a chimeric VP6 protein is dependent on the route and the coadministered adjuvant. Vaccine 20 (2002) 1733-1740
12. Hamilton S.R., Bobrowicz P., Bobrowicz B., Davidson R.C., Li H., Mitchell T., Nett J.H., Rausch S., Stadheim T.A., Wischnewski H., Wildt S., and Gerngross T.U. Production of complex human glycoproteins in yeast. Science 301 (2003) 1244-1246
13. Fries S., Glazomitsky K., Woods A., Forrest G., Hsu A., Olewinski R., Robinson D., and Chartrain M. Evaluation of disposable bioreactors. Bio Process Int 3 Suppl. 6 (2005) 36-44
14. Umana P., Jean-Mairet J., Moudry R., Amstutz H., and Bailey J.E. Engineered glycoforms of an antineuroblastoma IgG1 with optimized antibody-dependent cellular cytotoxic activity. Nat Biotechnol 17 (1999) 176-180
15. Weikert S., Papac D., Briggs J., Cowfer D., Tom S., Gawlitzek M., Lofgren J., Mehta S., Chisholm V., Modi N., Eppler S., Carroll K., Chamow S., Peers D., Berman P., and Krummen L. Engineering Chinese hamster ovary cells to maximize sialic acid content of recombinant glycoproteins. Nat Biotechnol 17 (1999) 1116-1121
16. Raju T.S., Briggs J.B., Borge S.M., and Jones A.J. Species-specific variation in glycosylation of IgG: evidence for the species-specific sialylation and branch-specific galactosylation and importance for engineering recombinant glycoprotein therapeutics. Glycobiology 10 (2000) 477-486
17. Koles K., van Berkel P.H., Pieper F.R., Nuijens J.H., Mannesse M.L., Vliegenthart J.F., and Kamerling J.P. N- and O-glycans of recombinant human C1 inhibitor expressed in the milk of transgenic rabbits. Glycobiology 14 (2004) 51-64
18. Edmunds T., Van Patten S.M., Pollock J., Hanson E., Bernasconi R., Higgins E., Manavalan P., Ziomek C., Meade H., McPherson J.M., and Cole E.S. Transgenically produced human antithrombin: structural and functional comparison to human plasma-derived antithrombin. Blood 91 (1998) 4561-4571
19. Stowers A.W., Chen Lh L.H., Zhang Y., Kennedy M.C., Zou L., Lambert L., Rice T.J., Kaslow D.C., Saul A., Long C.A., Meade H., and Miller L.H. A recombinant vaccine expressed in the milk of transgenic mice protects Aotus monkeys from a lethal challenge with Plasmodium falciparum. Proc Natl Acad Sci USA 99 (2002) 339-344
20. Ma J.K., Chikwamba R., Sparrow P., Fischer R., Mahoney R., and Twyman R.M. Plant-derived pharmaceuticals-the road forward. Trends Plant Sci 10 (2005) 580-585
21. Gomord V., Chamberlain P., Jefferis R., and Faye L. Biopharmaceutical production in plants: problems, solutions and opportunities. Trends Biotechnol 23 (2005) 559-565
22. Kirk D.D., McIntosh K., Walmsley A.M., and Peterson R.K. Risk analysis for plant-made vaccines. Transgenic Res 14 (2005) 449-462
23. Abranches R., Marcel S., Arcalis E., Altmann F., Fevereiro P., and Stoger E. Plants as bioreactors: a comparative study suggests that Medicago truncatula is a promising production system. J Biotechnol 120 (2005) 121-134
24. Leon-Banares R., Gonzalez-Ballester D., Galvan A., and Fernandez E. Transgenic microalgae as green cell-factories. Trends Biotechnol 22 (2004) 45-52
25. Hellwig S., Drossard J., Twyman R.M., and Fischer R. Plant cell cultures for the production of recombinant proteins. Nat Biotechnol 22 (2004) 1415-1422
26. Matsumura T., Itchoda N., and Tsunemitsu H. Production of immunogenic VP6 protein of bovine group A rotavirus in transgenic potato plants. Arch Virol 147 (2002) 1263-1270
27. Yu J., and Langridge W. Expression of rotavirus capsid protein VP6 in transgenic potato and its oral immunogenicity in mice. Transgenic Res 12 (2003) 163-169
28. Pogrebnyak N., Golovkin M., Andrianov V., Spitsin S., Smirnov Y., Egolf R., and Koprowski H. Severe acute respiratory syndrome (SARS) S protein production in plants: development of recombinant vaccine. Proc Natl Acad Sci USA 102 (2005) 9062-9067
29. Ashraf S., Singh P.K., Yadav D.K., Shahnawaz M., Mishra S., Sawant S.V., and Tuli R. High level expression of surface glycoprotein of rabies virus in tobacco leaves and its immunoprotective activity in mice. J Biotechnol 119 (2005) 1-14
30. Richter L.J., Thanavala Y., Arntzen C.J., and Mason H.S. Production of hepatitis B surface antigen in transgenic plants for oral immunization. Nat Biotechnol 18 (2000) 1167-1171
31. Kong Q., Richter L., Yang Y.F., Arntzen C.J., Mason H.S., and Thanavala Y. Oral immunization with hepatitis B surface antigen expressed in transgenic plants. Proc Natl Acad Sci USA 98 (2001) 11539-11544
32. Ma S., and Jevnikar A.M. Transgenic rice for allergy immunotherapy. Proc Natl Acad Sci USA 102 (2005) 17255-17256
33. Takagi H., Hiroi T., Yang L., Tada Y., Yuki Y., Takamura K., Ishimitsu R., Kawauchi H., Kiyono H., and Takaiwa F. A rice-based edible vaccine expressing multiple T cell epitopes induces oral tolerance for inhibition of Th2-mediated IgE responses. Proc Natl Acad Sci USA 102 (2005) 17525-17530
34. Giritch A., Marillonnet S., Engler C., van Eldik G., Botterman J., Klimyuk V., and Gleba Y. Rapid high-yield expression of full-size IgG antibodies in plants coinfected with noncompeting viral vectors. Proc Natl Acad Sci USA 103 (2006) 14701-14706
35. Houdebine L.M. Use of transgenic animals to improve human health and animal production. Reprod Domest Anim 40 (2005) 269-281
36. Houdebine LM. Transgenic Animal Models and Target Validation, Totowa, Humana Press Inc., 2006.
37. Soler E., Thepot D., Rival-Gervier S., Jolivet G., and Houdebine L. Preparation of recombinant proteins in milk to improve human and animal health. Reprod Nutr Dev 1-10 (2006)
38. Houdebine L.M. Antibody manufacture in transgenic animals and comparisons with other systems. Curr Opin Biotechnol 13 (2002) 625-629
39. Zhu L., van de Lavoir M.C., Albanese J., Beenhouwer D.O., Cardarelli P.M., Cuison S., Deng D.F., Deshpande S., Diamond J.H., Green L., Halk E.L., Heyer B.S., Kay R.M., Kerchner A., Leighton P.A., Mather C.M., Morrison S.L., Nikolov Z.L., Passmore D.B., Pradas-Monne A., Preston B.T., Rangan V.S., Shi M., Srinivasan M., White S.G., Winters-Digiacinto P., Wong S., Zhou W., and Etches R.J. Production of human monoclonal antibody in eggs of chimeric chickens. Nat Biotechnol 23 (2005) 1159-1169
40. van de Lavoir M.C., Diamond J.H., Leighton P.A., Mather-Love C., Heyer B.S., Bradshaw R., Kerchner A., Hooi L.T., Gessaro T.M., Swanberg S.E., Delany M.E., and Etches R.J. Germline transmission of genetically modified primordial germ cells. Nature 441 (2006) 766-769
41. Dyck M.K., Lacroix D., Pothier F., and Sirard M.A. Making recombinant proteins in animals- - different systems, different applications. Trends Biotechnol 21 (2003) 394-399
42. Royer C., Jalabert A., Da Rocha M., Grenier A.M., Mauchamp B., Couble P., and Chavancy G. Biosynthesis and cocoon-export of a recombinant globular protein in transgenic silkworms. Transgenic Res 14 (2005) 463-472
43. Markaki M., Drabek D., Livadaras I., and Craig R.K. Stable expression of human Growth Hormone over 50 generations in transgenic insect larvae. Transgenic Res 16 (2007) 99-107
44. Houdebine L.M. The methods to generate transgenic animals and to control transgene expression. J Biotechnol 98 (2002) 145-160
45. Rival-Gervier S., Viglietta C., Maeder C., Attal J., and Houdebine L.M. Position-independent and tissue-specific expression of porcine whey acidic protein gene from a bacterial artificial chromosome in transgenic mice. Mol Reprod Dev 63 (2002) 161-167
46. Giersing B and Dubovsky F. Malaria Vaccine Initiative, Bioforum Europe, 2006, p. 34.
47. Soler E., Le Saux A., Guinut F., Passet B., Cohen R., Merle C., Charpilienne A., Fourgeux C., Sorel V., Piriou A., Schwartz-Cornil I., Cohen J., and Houdebine L.M. Production of two vaccinating recombinant rotavirus proteins in the milk of transgenic rabbits. Transgenic Res 14 (2005) 833-844
48. Lubon H. Transgenic animal bioreactors in biotechnology and production of blood proteins. Biotechnol Annu Rev 4 (1998) 1-54
49. Gupta R.K. Aluminum compounds as vaccine adjuvants. Adv Drug Deliver Rev 32 (1998) 155-172
50. Corthesy B., Benureau Y., Perrier C., Fourgeux C., Parez N., Greenberg H., and Schwartz-Cornil I. Rotavirus anti-VP6 secretory IgA contributes to protection via intracellular neutralization but not via immune exclusion. J Virol 80 (2006) 10692-10699
51. Audibert F.M., and Lise L.D. Adjuvants: current status, clinical perspectives and future prospects. Immunol Today 14 (1993) 281-284
52. Goto N., Kato H., Maeyama J., Eto K., and Yoshihara S. Studies on the toxicities of aluminium hydroxide and calcium phosphate as immunological adjuvants for vaccines. Vaccine 11 (1993) 914-918
53. Petrovsky N. Novel human polysaccharide adjuvants with dual Th1 and Th2 potentiating activity. Vaccine 24 Suppl 2 (2006) S2-26-9
54. Morein B., Sundquist B., Hoglund S., Dalsgaard K., and Osterhaus A. Iscom, a novel structure for antigenic presentation of membrane proteins from enveloped viruses. Nature 308 (1984) 457-460
55. Sanders M.T., Brown L.E., Deliyannis G., and Pearse M.J. ISCOM-based vaccines: the second decade. Immunol Cell Biol 83 (2005) 119-128
56. Polakos N.K., Drane D., Cox J., Ng P., Selby M.J., Chien D., O'Hagan D.T., Houghton M., and Paliard X. Characterization of hepatitis C virus core-specific immune responses primed in rhesus macaques by a nonclassical ISCOM vaccine. J Immunol 166 (2001) 3589-3598
57. Smith R.E., Donachie A.M., Grdic D., Lycke N., and Mowat A.M. Immune-stimulating complexes induce an IL-12-dependent cascade of innate immune responses. J Immunol 162 (1999) 5536-5546
58. Rimmelzwaan G.F., Nieuwkoop N., Brandenburg A., Sutter G., Beyer W.E., Maher D., Bates J., and Osterhaus A.D. A randomized, double blind study in young healthy adults comparing cell mediated and humoral immune responses induced by influenza ISCOM vaccines and conventional vaccines. Vaccine 19 (2000) 1180-1187
59. Zakhartchouk A.N., Sharon C., Satkunarajah M., Auperin T., Viswanathan S., Mutwiri M. Petric G., See R.H., Brunham R.C., Finlay B.B., Cameron C., Kelvin D.J., Cochrane A., Rini J.M., and Babiuk L.A. Immunogenicity of a receptor-binding domain of SARS coronavirus spike protein in mice: implications for a subunit vaccine. Vaccine 25 (2007) 136-143
60. Brazolot Millan C.L., Weeratna R., Krieg A.M., Siegrist C.A., and Davis H.L. CpG DNA can induce strong Th1 humoral and cell-mediated immune responses against hepatitis B surface antigen in young mice. Proc Natl Acad Sci USA 95 (1998) 15553-15558
61. Davis H.L., Weeratna R., Waldschmidt T.J., Tygrett L., Schorr J., and Krieg A.M. CpG DNA is a potent enhancer of specific immunity in mice immunized with recombinant hepatitis B surface antigen. J Immunol 160 (1998) 870-876
62. Moldoveanu Z., Love-Homan L., Huang W.Q., and Krieg A.M. CpG DNA, a novel immune enhancer for systemic and mucosal immunization with influenza virus. Vaccine 16 (1998) 1216-1224
63. Mitchell L.A., Joseph A., Kedar E., Barenholz Y., and Galun E. Mucosal immunization against hepatitis A: antibody responses are enhanced by co-administration of synthetic oligodeoxynucleotides and a novel cationic lipid. Vaccine 24 (2006) 5300-5310
64. Tengvall S., Lundqvist A., Eisenberg R.J., Cohen G.H., and Harandi A.M. Mucosal administration of CpG oligodeoxynucleotide elicits strong CC and CXC chemokine responses in the vagina and serves as a potent Th1-tilting adjuvant for recombinant gD2 protein vaccination against genital herpes. J Virol 80 (2006) 5283-5291
65. Agnello D., Herve C.A., Lavaux A., Darniot M., Guillon P., Charpilienne A., and Pothier P. 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 (2006) 3823-3832
66. Klinman D.M. Adjuvant activity of CpG oligodeoxynucleotides. Int Rev Immunol 25 (2006) 135-154
67. Halperin S.A., Van Nest G., Smith B., Abtahi S., Whiley H., and Eiden J.J. A phase I study of the safety and immunogenicity of recombinant hepatitis B surface antigen co-administered with an immunostimulatory phosphorothioate oligonucleotide adjuvant. Vaccine 21 (2003) 2461-2467
68. Cooper C.L., Davis H.L., Morris M.L., Efler S.M., Adhami M.A., Krieg A.M., Cameron D.W., and Heathcote J. CPG 7909, an immunostimulatory TLR9 agonist oligodeoxynucleotide, as adjuvant to Engerix-B HBV vaccine in healthy adults: a double-blind phase I/II study. J Clin Immunol 24 (2004) 693-701
69. Siegrist C.A., Pihlgren M., Tougne C., Efler S.M., Morris M.L., AlAdhami M.J., Cameron D.W., Cooper C.L., Heathcote J., Davis H.L., and Lambert P.H. Co-administration of CpG oligonucleotides enhances the late affinity maturation process of human anti-hepatitis B vaccine response. Vaccine 23 (2004) 615-622
70. Klinman D.M. CpG oligonucleotides accelerate and boost the immune response elicited by AVA, the licensed anthrax vaccine. Expert Rev Vaccines 5 (2006) 365-369
71. Krieg A.M. Therapeutic potential of Toll-like receptor 9 activation. Nat Rev Drug Discov 5 (2006) 471-484
72. Foss D.L., and Murtaugh M.P. Mechanisms of vaccine adjuvanticity at mucosal surfaces. Anim Health Res Rev 1 (2000) 3-24
73. Eriksson K., and Holmgren J. Recent advances in mucosal vaccines and adjuvants. Curr Opin Immunol 14 (2002) 666-672
74. Bertolotti-Ciarlet A., Ciarlet M., Crawford S.E., Conner M.E., and Estes M.K. Immunogenicity and protective efficacy of rotavirus 2/6-virus-like particles produced by a dual baculovirus expression vector and administered intramuscularly, intranasally, or orally to mice. Vaccine 21 (2003) 3885-3900
75. Parez N., Fourgeux C., Mohamed A., Dubuquoy C., Pillot M., Dehee A., Charpilienne A., Poncet D., Schwartz-Cornil I., and Garbarg-Chenon A. Rectal immunization with rotavirus like particles induces systemic and mucosal humoral immune responses and protects mice against rotavirus infection. J Virol 80 (2006) 1752-1761
76. Dickinson B.L., and Clements J.D. Dissociation of E. coli heat-labile enterotoxin adjuvanticity from ADP-ribosyltransferase activity. Infect Immun 63 (1995) 1617-1623
77. Yuan L., Geyer A., Hodgins D.C., Fan Z., Qian Y., Chang K.O., Crawford S.E., Parreno V., Ward L.A., Estes M.K., Conner M.E., and Saif L.J. Intranasal administration of 2/6-rotavirus-like particles with mutant E. coli heat-labile toxin (LT-R192G) induces antibody-secreting cell responses but not protective immunity in gnotobiotic pigs. J Virol 74 (2000) 8843-8853
78. O'Neal C.M., Clements J.D., Estes M.K., and Conner M.E. Rotavirus 2/6 viruslike particles administered intranasally with cholera toxin, E. coli heat-labile toxin (LT), and LT-R192G induce protection from rotavirus challenge. J Virol 72 (1998) 3390-3393
79. Eriksson A.M., Schon K.M., and Lycke N.Y. The cholera toxin-derived CTA1-DD vaccine adjuvant administered intranasally does not cause inflammation or accumulate in the nervous tissues. J Immunol 173 (2004) 3310-3319
80. Lycke N. From toxin to adjuvant: the rational design of a vaccine adjuvant vector, CTA1-DD/ISCOM. Cell Microbiol 6 (2004) 23-32
81. De Filette M., Ramne A., Birkett A., Lycke N., Lowenadler B., Min Jou W., Saelens X., and Fiers W. The universal influenza vaccine M2e-HBc administered intranasally in combination with the adjuvant CTA1-DD provides complete protection. Vaccine 24 (2006) 544-551
82. Haan L., Verweij W.R., Holtrop M., Brands R., van Scharrenburg G.J., Palache A.M., Agsteribbe E., and Wilschut J. Nasal or intramuscular immunization of mice with influenza subunit antigen and the B subunit of E. coli heat-labile toxin induces IgA- or IgG-mediated protective mucosal immunity. Vaccine 19 (2001) 2898-2907
83. Adamsson J., Lindblad M., Lundqvist A., Kelly D., Holmgren J., and Harandi A.M. Novel immunostimulatory agent based on CpG oligodeoxynucleotide linked to the nontoxic B subunit of cholera toxin. J Immunol 176 (2006) 4902-4913
84. De Magistris M.T. Zonula occludens toxin as a new promising adjuvant for mucosal vaccines. Vaccine 24 Suppl 2 (2006) S2-60-1
85. De Magistris M.T. Mucosal delivery of vaccine antigens and its advantages in pediatrics. Adv Drug Deliv Rev 58 (2006) 52-67
86. Villa P., and Ghezzi P. Animal models of endotoxic shock. Methods Mol Med 98 (2004) 199-206
87. Gustafson G.L., and Rhodes M.J. Bacterial cell wall products as adjuvants: early interferon gamma as a marker for adjuvants that enhance protective immunity. Res Immunol 143 (1992) 483-488 discussion 573-574
88. Okemoto K., Kawasaki K., Hanada K., Miura M., and Nishijima M. A potent adjuvant monophosphoryl lipid A triggers various immune responses, but not secretion of IL-1beta or activation of caspase-1. J Immunol 176 (2006) 1203-1208
89. Li P., Allen H., Banerjee S., Franklin S., Herzog L., Johnston C., McDowell J., Paskind M., Rodman L., Salfeld J., et al. Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80 (1995) 401-411
90. Durrant L.G., and Spendlove I. Cancer vaccines entering Phase III clinical trials. Expert Opin Emerg Drugs 8 (2003) 489-500
91. Harper D.M., Franco E.L., Wheeler C., Ferris D.G., Jenkins D., Schuind A., Zahaf T., Innis B., Naud P., De Carvalho N.S., Roteli-Martins C.M., Teixeira J., Blatter M.M., Korn A.P., Quint W., and Dubin G. Efficacy 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 (2004) 1757-1765
92. Giannini S.L., Hanon E., Moris P., Van Mechelen M., Morel S., Dessy F., Fourneau M.A., Colau B., Suzich J., Losonksy G., Martin M.T., Dubin G., and Wettendorff M.A. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine 24 (2006) 5937-5949
93. Harper D.M., Franco E.L., Wheeler C.M., Moscicki A.B., Romanowski B., Roteli-Martins C.M., Jenkins D., Schuind A., Costa Clemens S.A., and Dubin G. Sustained efficacy up to 4.5 years of a bivalent L1 virus-like particle vaccine against human papillomavirus types 16 and 18: follow-up from a randomised control trial. Lancet 367 (2006) 1247-1255
94. Bernstein D. Glycoprotein D adjuvant herpes simplex virus vaccine. Expert Rev Vaccines 4 (2005) 615-627
95. Dupont J., Altclas J., Lepetic A., Lombardo M., Vazquez V., Salgueira C., Seigelchifer M., Arndtz N., Antunez E., von Eschen K., and Janowicz Z. A controlled clinical trial comparing the safety and immunogenicity of a new adjuvanted hepatitis B vaccine with a standard hepatitis B vaccine. Vaccine 24 (2006) 7167-7174
96. Wheeler A.W., Marshall J.S., and Ulrich J.T. A Th1-inducing adjuvant, MPL, enhances antibody profiles in experimental animals suggesting it has the potential to improve the efficacy of allergy vaccines. Int Arch Allergy Immunol 126 (2001) 135-139
97. Brandtzaeg P., Farstad I.N., and Haraldsen G. Regional specialization in the mucosal immune system: primed cells do not always home along the same track. Immunol Today 20 (1999) 267-277
98. Dell K., Koesters R., Linnebacher M., Klein C., and Gissmann L. Intranasal immunization with human papillomavirus type 16 capsomeres in the presence of non-toxic cholera toxin-based adjuvants elicits increased vaginal immunoglobulin levels. Vaccine 24 (2006) 2238-2247
99. van Ginkel F.W., Jackson R.J., Yuki Y., and McGhee J.R. Cutting edge: the mucosal adjuvant cholera toxin redirects vaccine proteins into olfactory tissues. J Immunol 165 (2000) 4778-4782
100. Fujihashi K., Koga T., van Ginkel F.W., Hagiwara Y., and McGhee J.R. A dilemma for mucosal vaccination: efficacy versus toxicity using enterotoxin-based adjuvants. Vaccine 20 (2002) 2431-2438
101. Belyakov I.M., Hammond S.A., Ahlers J.D., Glenn G.M., and Berzofsky J.A. Transcutaneous immunization induces mucosal CTLs and protective immunity by migration of primed skin dendritic cells. J Clin Invest 113 (2004) 998-1007
102. Glenn G.M., and Kenney R.T. Mass vaccination: solutions in the skin. Curr Top Microbiol Immunol 304 (2006) 247-268
103. Bachmann M.F., Rohrer U.H., Kundig T.M., Burki K., Hengartner H., and Zinkernagel R.M. The influence of antigen organization on B cell responsiveness. Science 262 (1993) 1448-1451
104. Chackerian B., Lowy D.R., and Schiller J.T. Induction of autoantibodies to mouse CCR5 with recombinant papillomavirus particles. Proc Natl Acad Sci USA 96 (1999) 2373-2378
105. Chackerian B., Lenz P., Lowy D.R., and Schiller J.T. Determinants of autoantibody induction by conjugated papillomavirus virus-like particles. J Immunol 169 (2002) 6120-6126
106. Jondal M., Schirmbeck R., and Reimann J. MHC class I-restricted CTL responses to exogenous antigens. Immunity 5 (1996) 295-302
107. Sedlik C., Dridi A., Deriaud E., Saron M.F., Rueda P., Sarraseca J., Casal J.I., and Leclerc C. Intranasal delivery of recombinant parvovirus-like particles elicits cytotoxic T-cell and neutralizing antibody responses. J Virol 73 (1999) 2739-2744
108. Storni T., Lechner F., Erdmann I., Bachi T., Jegerlehner A., Dumrese T., Kundig T.M., Ruedl C., and Bachmann M.F. Critical role for activation of antigen-presenting cells in priming of cytotoxic T cell responses after vaccination with virus-like particles. J Immunol 168 (2002) 2880-2886
109. Ohlschlager P., Osen W., Dell K., Faath S., Garcea R.L., Jochmus I., Muller M., Pawlita M., Schafer K., Sehr P., Staib C., Sutter G., and Gissmann L. Human papillomavirus type 16 L1 capsomeres induce L1-specific cytotoxic T lymphocytes and tumor regression in C57BL/6 mice. J Virol 77 (2003) 4635-4645
110. Kratz P.A., Bottcher B., and Nassal M. Native display of complete foreign protein domains on the surface of hepatitis B virus capsids. Proc Natl Acad Sci USA 96 (1999) 1915-1920
111. Nassal M., Skamel C., Kratz P.A., Wallich R., Stehle T., and Simon M.M. A fusion product of the complete Borrelia burgdorferi outer surface protein A (OspA) and the hepatitis B virus capsid protein is highly immunogenic and induces protective immunity similar to that seen with an effective lipidated OspA vaccine formula. Eur J Immunol 35 (2005) 655-665
112. Ruedl C., Schwarz K., Jegerlehner A., Storni T., Manolova V., and Bachmann M.F. Virus-like particles as carriers for T-cell epitopes: limited inhibition of T-cell priming by carrier-specific antibodies. J Virol 79 (2005) 717-724
113. Niikura M., Takamura S., Kim G., Kawai S., Saijo M., Morikawa S., Kurane I., Li T.C., Takeda N., and Yasutomi Y. Chimeric recombinant hepatitis E virus-like particles as an oral vaccine vehicle presenting foreign epitopes. Virology 293 (2002) 273-280
114. Charpilienne A., Nejmeddine M., Berois M., Parez N., Neumann E., Hewat E., Trugnan G., and Cohen J. Individual rotavirus-like particles containing 120 molecules of fluorescent protein are visible in living cells. J Biol Chem 276 (2001) 29361-29367
115. Rueda P., Moron G., Sarraseca J., Leclerc C., and Casal J.I. Influence of flanking sequences on presentation efficiency of a CD8+ cytotoxic T-cell epitope delivered by parvovirus-like particles. J Gen Virol 85 (2004) 563-572
116. Mihailova M., Boos M., Petrovskis I., Ose V., Skrastina D., Fiedler M., Sominskaya I., Ross S., Pumpens P., Roggendorf M., and Viazov S. Recombinant virus-like particles as a carrier of B- and T-cell epitopes of hepatitis C virus (HCV). Vaccine 24 (2006) 4369-4377
117. Sedlik C., Saron M., Sarraseca J., Casal I., and Leclerc C. Recombinant parvovirus-like particles as an antigen carrier: a novel nonreplicative exogenous antigen to elicit protective antiviral cytotoxic T cells. Proc Natl Acad Sci USA 94 (1997) 7503-7508
118. Walsh G. Biopharmaceutical benchmarks 2006. Nat Biotechnol 24 (2006) 769-776
119. Soler E, Parez N, Passet B, Dubuquoy C, Riffault S, Pillot M, Houdebine LM, Schwartz-Cornil I, Recombinant rotavirus inner core proteins produced in the milk of transgenic rabbits confer a high level of protection after intrarectal delivery. Vaccine (in preparation); manuscript number JVAC-D-07-00356R1.