Fusion of the mycobacterium tuberculosis antigen 85A to an oligomerization domain enhances its immunogenicity in both mice and non-human primates

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Spencer, Alexandra J ^a   Hill, Fergal ^b   Honeycutt, Jared D ^a   Cottingham, Matthew G ^a   Bregu, Migena ^a   Rollier, Christine S ^a,c   Furze, Julie ^a   Draper, Simon J ^a   Søgaard, Karen C ^a,d   Gilbert, Sarah C ^a   Wyllie, David H ^a   Hill, Adrian V S ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Imaxio SA   (France)

^c CHURCHILL HOSPITAL   (United Kingdom)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA VACCINE; GAMMA INTERFERON; IMMUNOLOGICAL ADJUVANT; IMX 313; INTERLEUKIN 2; INTERLEUKIN 7 RECEPTOR; L SELECTIN; MYCOBACTERIUM ANTIGEN; MYCOBACTERIUM TUBERCULOSIS ANTIGEN 85A; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ACYLTRANSFERASE; ANTIGEN 85A, MYCOBACTERIUM TUBERCULOSIS; BACTERIAL ANTIGEN; BCG VACCINE; COMPLEMENT COMPONENT C4B BINDING PROTEIN; HYBRID PROTEIN; MVA VACCINE; TISSUE PLASMINOGEN ACTIVATOR; VIRUS VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; DRUG FORMULATION; EFFECTOR CELL; ENZYME LINKED IMMUNOSPOT ASSAY; FEMALE; FLOW CYTOMETRY; IMMUNOGENICITY; IN VIVO STUDY; MACACA MULATTA; MALE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; OLIGOMERIZATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; GENETICS; HUMAN; IMMUNOLOGY; METABOLISM; MYCOBACTERIUM TUBERCULOSIS; VACCINATION;

ANIMALIA; AVES; MACACA MULATTA; MUS; MYCOBACTERIUM TUBERCULOSIS; PRIMATES;

ACYLTRANSFERASES; ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIGENS, BACTERIAL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; COMPLEMENT C4B-BINDING PROTEIN; FEMALE; HUMANS; INTERFERON-GAMMA; MACACA MULATTA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; RECOMBINANT FUSION PROTEINS; TISSUE PLASMINOGEN ACTIVATOR; TUBERCULOSIS VACCINES; VACCINATION; VACCINES, DNA; VIRAL VACCINES;

EID: 84859040307     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033555     Document Type: Article

References (41)

1. Draper SJ, Heeney JL, (2010) Viruses as vaccine vectors for infectious diseases and cancer. Nat Rev Microbiol 8: 62-73.
2. Hill AV, (2006) Pre-erythrocytic malaria vaccines: towards greater efficacy. Nat Rev Immunol 6: 21-32.
3. Engel J, Kammerer RA, (2000) What are oligomerization domains good for? Matrix Biol 19: 283-288.
4. Chambers RS, Johnston SA, (2003) High-level generation of polyclonal antibodies by genetic immunization. Nat Biotechnol 21: 1088-1092.
5. Draper SJ, Moore AC, Goodman AL, Long CA, Holder AA, et al. (2008) Effective induction of high-titer antibodies by viral vector vaccines. Nat Med 14: 819-821.
6. Ogun SA, Dumon-Seignovert L, Marchand JB, Holder AA, Hill F, (2008) The oligomerization domain of C4-binding protein (C4bp) acts as an adjuvant, and the fusion protein comprised of the 19-kilodalton merozoite surface protein 1 fused with the murine C4bp domain protects mice against malaria. Infect Immun 76: 3817-3823.
7. Kask L, Hillarp A, Ramesh B, Dahlback B, Blom AM, (2002) Structural requirements for the intracellular subunit polymerization of the complement inhibitor C4b-binding protein. Biochemistry 41: 9349-9357.
8. Christiansen D, Devaux P, Reveil B, Evlashev A, Horvat B, et al. (2000) Octamerization enables soluble CD46 receptor to neutralize measles virus in vitro and in vivo. J Virol 74: 4672-4678.
9. Shinya E, Dervillez X, Edwards-Levy F, Duret V, Brisson E, et al. (1999) In-vivo delivery of therapeutic proteins by genetically-modified cells: comparison of organoids and human serum albumin alginate-coated beads. Biomed Pharmacother 53: 471-483.
10. Oudin S, Libyh MT, Goossens D, Dervillez X, Philbert F, et al. (2000) A soluble recombinant multimeric anti-Rh(D) single-chain Fv/CR1 molecule restores the immune complex binding ability of CR1-deficient erythrocytes. J Immunol 164: 1505-1513.
11. Libyh MT, Goossens D, Oudin S, Gupta N, Dervillez X, et al. (1997) A recombinant human scFv anti-Rh(D) antibody with multiple valences using a C-terminal fragment of C4-binding protein. Blood 90: 3978-3983.
12. Dervillez X, Huther A, Schuhmacher J, Griesinger C, Cohen JH, et al. (2006) Stable expression of soluble therapeutic peptides in eukaryotic cells by multimerisation: application to the HIV-1 fusion inhibitory peptide C46. ChemMedChem 1: 330-339.
13. Ibanga HB, Brookes RH, Hill PC, Owiafe PK, Fletcher HA, et al. (2006) Early clinical trials with a new tuberculosis vaccine, MVA85A, in tuberculosis-endemic countries: issues in study design. Lancet Infect Dis 6: 522-528.
14. McShane H, Pathan AA, Sander CR, Keating SM, Gilbert SC, et al. (2004) Recombinant modified vaccinia virus Ankara expressing antigen 85A boosts BCG-primed and naturally acquired antimycobacterial immunity in humans. Nat Med 10: 1240-1244.
15. Hawkridge T, Scriba TJ, Gelderbloem S, Smit E, Tameris M, et al. (2008) Safety and immunogenicity of a new tuberculosis vaccine, MVA85A, in healthy adults in South Africa. J Infect Dis 198: 544-552.
16. Brookes RH, Pathan AA, McShane H, Hensmann M, Price DA, et al. (2003) CD8+ T cell-mediated suppression of intracellular Mycobacterium tuberculosis growth in activated human macrophages. Eur J Immunol 33: 3293-3302.
17. Caruso AM, Serbina N, Klein E, Triebold K, Bloom BR, et al. (1999) Mice deficient in CD4 T cells have only transiently diminished levels of IFN-gamma, yet succumb to tuberculosis. J Immunol 162: 5407-5416.
18. van Pinxteren LA, Cassidy JP, Smedegaard BH, Agger EM, Andersen P, (2000) Control of latent Mycobacterium tuberculosis infection is dependent on CD8 T cells. Eur J Immunol 30: 3689-3698.
19. Williams A, Hall Y, Orme IM, (2009) Evaluation of new vaccines for tuberculosis in the guinea pig model. Tuberculosis (Edinb) 89: 389-397.
20. McShane H, Pathan AA, Sander CR, Goonetilleke NP, Fletcher HA, et al. (2005) Boosting BCG with MVA85A: the first candidate subunit vaccine for tuberculosis in clinical trials. Tuberculosis (Edinb) 85: 47-52.
21. Darrah PA, Patel DT, De Luca PM, Lindsay RW, Davey DF, et al. (2007) Multifunctional TH1 cells define a correlate of vaccine-mediated protection against Leishmania major. Nat Med 13: 843-850.
22. Seder RA, Darrah PA, Roederer M, (2008) T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 8: 247-258.
23. Huster KM, Koffler M, Stemberger C, Schiemann M, Wagner H, et al. (2006) Unidirectional development of CD8+ central memory T cells into protective Listeria-specific effector memory T cells. Eur J Immunol 36: 1453-1464.
24. Bachmann MF, Wolint P, Schwarz K, Jager P, Oxenius A, (2005) Functional properties and lineage relationship of CD8+ T cell subsets identified by expression of IL-7 receptor alpha and CD62L. J Immunol 175: 4686-4696.
25. Betts MR, Brenchley JM, Price DA, De Rosa SC, Douek DC, et al. (2003) Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J Immunol Methods 281: 65-78.
26. Liu J, Ewald BA, Lynch DM, Denholtz M, Abbink P, et al. (2008) Magnitude and phenotype of cellular immune responses elicited by recombinant adenovirus vectors and heterologous prime-boost regimens in rhesus monkeys. J Virol 82: 4844-4852.
27. Pitcher CJ, Hagen SI, Walker JM, Lum R, Mitchell BL, et al. (2002) Development and homeostasis of T cell memory in rhesus macaque. J Immunol 168: 29-43.
28. Liu J, O'Brien KL, Lynch DM, Simmons NL, La Porte A, et al. (2009) Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature 457: 87-91.
29. Fazekas de St Groth B, Smith AL, Higgins CA, (2004) T cell activation: in vivo veritas. Immunol Cell Biol 82: 260-268.
30. Smith AL, Wikstrom ME, Fazekas de St Groth B, (2000) Visualizing T cell competition for peptide/MHC complexes: a specific mechanism to minimize the effect of precursor frequency. Immunity 13: 783-794.
31. Grun JL, Maurer PH, (1989) Different T helper cell subsets elicited in mice utilizing two different adjuvant vehicles: the role of endogenous interleukin 1 in proliferative responses. Cell Immunol 121: 134-145.
32. Ulanova M, Tarkowski A, Hahn-Zoric M, Hanson LA, (2001) The Common vaccine adjuvant aluminum hydroxide up-regulates accessory properties of human monocytes via an interleukin-4-dependent mechanism. Infect Immun 69: 1151-1159.
33. Delamarre L, Couture R, Mellman I, Trombetta ES, (2006) Enhancing immunogenicity by limiting susceptibility to lysosomal proteolysis. J Exp Med 203: 2049-2055.
34. Bins AD, Wolkers MC, van den Boom MD, Haanen JB, Schumacher TN, (2007) In vivo antigen stability affects DNA vaccine immunogenicity. J Immunol 179: 2126-2133.
35. Taracha EL, Bishop R, Musoke AJ, Hill AV, Gilbert SC, (2003) Heterologous priming-boosting immunization of cattle with Mycobacterium tuberculosis 85A induces antigen-specific T-cell responses. Infect Immun 71: 6906-6914.
36. Geiser M, Cebe R, Drewello D, Schmitz R, (2001) Integration of PCR fragments at any specific site within cloning vectors without the use of restriction enzymes and DNA ligase. Biotechniques 31: 88-90 92.
37. Denis O, Tanghe A, Palfliet K, Jurion F, van den Berg TP, et al. (1998) Vaccination with plasmid DNA encoding mycobacterial antigen 85A stimulates a CD4+ and CD8+ T-cell epitopic repertoire broader than that stimulated by Mycobacterium tuberculosis H37Rv infection. Infect Immun 66: 1527-1533.
38. McShane H, Behboudi S, Goonetilleke N, Brookes R, Hill AV, (2002) Protective immunity against Mycobacterium tuberculosis induced by dendritic cells pulsed with both CD8(+)- and CD4(+)-T-cell epitopes from antigen 85A. Infect Immun 70: 1623-1626.
39. D'Souza S, Rosseels V, Romano M, Tanghe A, Denis O, et al. (2003) Mapping of murine Th1 helper T-Cell epitopes of mycolyl transferases Ag85A, Ag85B, and Ag85C from Mycobacterium tuberculosis. Infect Immun 71: 483-493.
40. Goonetilleke NP, McShane H, Hannan CM, Anderson RJ, Brookes RH, et al. (2003) Enhanced immunogenicity and protective efficacy against Mycobacterium tuberculosis of bacille Calmette-Guerin vaccine using mucosal administration and boosting with a recombinant modified vaccinia virus Ankara. J Immunol 171: 1602-1609.
41. Roederer M, Nozzi JL, Nason MC, (2011) SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79: 167-174.