Recombinant vaccine displaying the loop-neutralizing determinant from protective antigen completely protects rabbits from experimental inhalation anthrax

Clinical and Vaccine Immunology

Volumn 20, Issue 3, 2013, Pages 341-349

  Oscherwitz, Jon ^a,b   Yu, Fen ^a   Jacobs, Jana L ^a   Ceasea, Kemp B ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b VA ANN ARBOR HEALTHCARE SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRAX VACCINE; BACTERIAL ANTIGEN; EPITOPE; HYBRID PROTEIN; MALTOSE BINDING PROTEIN; NEUTRALIZING ANTIBODY; P4 PEPTIDE; PEPTIDE; RECOMBINANT LOOP NEUTRALIZING DETERMINANT; RECOMBINANT VACCINE; UNCLASSIFIED DRUG;

AMES TEST; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTHRAX; ANTIBODY TITER; ANTIGEN SPECIFICITY; ARTICLE; BACILLUS ANTHRACIS; CONTROLLED STUDY; FEMALE; HELPER CELL; IMMUNIZATION; IMMUNOGENICITY; LETHAL DOSE; LETHAL GENE; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RABBIT; SCHISTOSOMA MANSONI; SURVIVOR; TANDEM REPEAT;

ANIMALS; ANTHRAX; ANTHRAX VACCINES; ANTIBODIES, BACTERIAL; ANTIBODIES, NEUTRALIZING; ANTIGENS, BACTERIAL; BACTERIAL TOXINS; DISEASE MODELS, ANIMAL; EPITOPES; FEMALE; HUMANS; MICE; RABBITS; RECOMBINANT FUSION PROTEINS; RESPIRATORY TRACT INFECTIONS; SURVIVAL ANALYSIS; VACCINES, SYNTHETIC;

EID: 84875049323     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00612-12     Document Type: Article

References (53)

1. Cote CK, Kaatz L, Reinhardt J, Bozue J, Tobery SA, Bassett AD, Sanz P, Darnell SC, Alem F, O'Brien AD, Welkos SL. 2012. Characterization of a multi-component anthrax vaccine designed to target the initial stages of infection as well as toxaemia. J. Med. Microbiol. 61:1380-1392.
2. Hermanson G, Whitlow V, Parker S, Tonsky K, Rusalov D, Ferrari M, Lalor P, Komai M, Mere R, Bell M, Brenneman K, Mateczun A, Evans T, Kaslow D, Galloway D, Hobart P. 2004. A cationic lipid-formulated plasmid DNA vaccine confers sustained antibody-mediated protection against aerosolized anthrax spores. Proc. Natl. Acad. Sci. U. S. A. 101: 13601-13606.
3. Chabot DJ, Scorpio A, Tobery SA, Little SF, Norris SL, Friedlander AM. 2004. Anthrax capsule vaccine protects against experimental infection. Vaccine 23:43-47.
4. Rhie GE, Roehrl MH, Mourez M, Collier RJ, Mekalanos JJ, Wang JY. 2003. A dually active anthrax vaccine that confers protection against both bacilli and toxins. Proc. Natl. Acad. Sci. U. S. A. 100:10925-10930.
5. Liu TH, Oscherwitz J, Schnepp B, Jacobs J, Yu F, Cease KB, Johnson PR. 2009. Genetic vaccines for anthrax based on recombinant adenoassociated virus vectors. Mol. Ther. 17:373-379.
6. Galloway D, Liner A, Legutki J, Mateczun A, Barnewall R, Estep J. 2004. Genetic immunization against anthrax. Vaccine 22:1604-1608.
7. Oscherwitz J, Yu F, Cease KB. 2009. A heterologous helper T-cell epitope enhances the immunogenicity of a multiple-antigenic-peptide vaccine targeting the cryptic loop-neutralizing determinant of Bacillus anthracis protective antigen. Infect. Immun. 77:5509-5518.
8. Oscherwitz J, Yu F, Jacobs JL, Liu TH, Johnson PR, Cease KB. 2009. Synthetic peptide vaccine targeting a cryptic neutralizing epitope in domain 2 of Bacillus anthracis protective antigen. Infect. Immun. 77:3380-3388.
9. Oscherwitz J, Yu F, Cease KB. 2010. A synthetic peptide vaccine directed against the 2-2-2-3 loop of domain 2 of protective antigen protects rabbits from inhalation anthrax. J. Immunol. 185:3661-3668.
10. Collier RJ, Young JA. 2003. Anthrax toxin. Annu. Rev. Cell. Dev. Biol. 19:45-70.
11. Duesbery NS, Webb CP, Leppla SH, Gordon VM, Klimpel KR, Copeland TD, Ahn NG, Oskarsson MK, Fukasawa K, Paull KD, Vande Woude GF. 1998. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science 280:734-737.
12. Leppla SH. 1982. Anthrax toxin edema factor: a bacterial adenylate cyclase that increases cyclic AMP concentrations of eukaryotic cells. Proc. Natl. Acad. Sci. U. S. A. 79:3162-3166.
13. Miller CJ, Elliott JL, Collier RJ. 1999. Anthrax protective antigen: prepore-to-pore conversion. Biochemistry 38:10432-10441.
14. Novak JM, Stein MP, Little SF, Leppla SH, Friedlander AM. 1992. Functional characterization of protease-treated Bacillus anthracis protective antigen. J. Biol. Chem. 267:17186-17193.
15. Singh Y, Khanna H, Chopra AP, Mehra V. 2001. A dominant negative mutant of Bacillus anthracis protective antigen inhibits anthrax toxin action in vivo. J. Biol. Chem. 276:22090-22094.
16. Singh Y, Klimpel KR, Arora N, Sharma M, Leppla SH. 1994. The chymotrypsin-sensitive site, FFD315, in anthrax toxin protective antigen is required for translocation of lethal factor. J. Biol. Chem. 269:29039-29046.
17. Gubbins MJ, Schmidt L, Tsang RS, Berry JD, Kabani A, Stewart DI. 2007. Development of a competitive enzyme linked immunosorbent assay to identify epitope specific antibodies in recipients of the U.S. licensed anthrax vaccine. J. Immunoassay Immunochem. 28:213-225.
18. Leader B, Baca QJ, Golan DE. 2008. Protein therapeutics: a summary and pharmacological classification. Nat. Rev. Drug Discov. 7:21-39.
19. Oscherwitz J, Zeigler ME, Gribbin TE, Cease KB. 1999. A V3 loop haptenic peptide sequence, when tandemly repeated, enhances immunogenicity by facilitating helper T-cell responses to a covalently linked carrier protein. Vaccine 17:2392-2399.
20. Godson GN, Ellis J, Svec P, Schlesinger DH, Nussenzweig V. 1983. Identification and chemical synthesis of a tandemly repeated immunogenic region of Plasmodium knowlesi circumsporozoite protein. Nature 305:29-33.
21. Enea VE, Arnot D, Schmidt EC, Cochrane A, Gwadz R, Nussenzweig RS. 1984. Circumsporozoite gene of Plasmodium cynomolgi (Gombak): cDNA cloning and expression of the repetitive circumsporozoite epitope. Proc. Natl. Acad. Sci. U. S. A. 81:7520-7524.
22. Burns JM, Jr., Shreffler WG, Rosman DE, Sleath PR, March CJ, Reed SG. 1992. Identification and synthesis of a major conserved antigenic epitope of Trypanosoma cruzi. Proc. Natl. Acad. Sci. U. S. A. 89:1239-1243.
23. Klein BS, Hogan LH, Jones JM. 1993. Immunological recognition of a 25-amino acid repeat arrayed in tandem on a major antigen of Blastomyces dermatitidis. J. Clin. Invest. 92:330-337.
24. Lowenadler B, Svennerholm A-M, Gidlund M, Holmgren E, Krook K, Svanholm C, Ulff S, Josephson S. 1990. Enhanced immunogenicity of recombinant peptide fusions containing multiple copies of a heterologous T helper epitope. Eur. J. Immunol. 20:1541-1545.
25. Lowenadler B, Lycke N, Svanholm C, Svennerholm A-M, Krook K, Gidlund M. 1992. T and B cell responses to chimeric proteins containing heterologous T helper epitopes inserted at different positions. Mol. Immunol. 29:1185-1190.
26. Lo-Man R, Martineau P, Hofnung M, Leclerc C. 1993. Induction of T cell responses by chimeric bacterial proteins expressing several copies of a viral T cell epitope. Eur. J. Immunol. 23:2998-3002.
27. Oscherwitz J, Hankenson FC, Yu F, Cease KB. 2006. Low-dose intraperitoneal Freund's adjuvant: toxicity and immunogenicity in mice using an immunogen targeting amyloid-beta peptide. Vaccine 24:3018-3025.
28. Oscherwitz J, Gribbin TE, Cease KB. 2010. A CD20 tandem-epitope immunogen elicits antibody in mice that binds murine cell surface CD20 and depletes splenic B cells in vivo. Mol. Immunol. 47:1484-1491. 29. Chen Y, Boros DL. 1998. Identification of the immunodominant T cell epitope of p38, a major egg antigen, and characterization of the epitopespecific Th responsiveness during murine schistosomiasis mansoni. J. Immunol. 160:5420-5427.
29. Sanger F, Nicklen S, Coulson AR. 1977. DNA sequencing with chainterminating inhibitors. Proc. Natl. Acad. Sci. U. S. A. 74:5463-5467.
30. Hering D, Thompson W, Hewetson J, Little S, Norris S, Pace-Templeton J. 2004. Validation of the anthrax lethal toxin neutralization assay. Biologicals 32:17-27.
31. Friguet B, Chaffotte AF, Djavadi-Ohaniance L, Goldberg ME. 1985. Measurements of the true affinity constant in solution of antigenantibody complexes by enzyme-linked immunosorbent assay. J. Immunol. Methods 77:305-319.
32. Zaucha GM, Pitt LM, Estep J, Ivins BE, Friedlander AM. 1998. The pathology of experimental anthrax in rabbits exposed by inhalation and subcutaneous inoculation. Arch. Pathol. Lab. Med. 122:982-992.
33. Rath S, Stanley CM, Steward MW. 1988. An inhibition enzyme immunoassay for estimating relative antibody affinity and affinity heterogeneity. J. Immunol. Methods 106:245-249.
34. Cote CK, Rossi CA, Kang AS, Morrow PR, Lee JS, Welkos SL. 2005. The detection of protective antigen (PA) associated with spores of Bacillus anthracis and the effects of anti-PA antibodies on spore germination and macrophage interactions. Microb. Pathog. 38:209-225.
35. Gershon RK, Paul WE. 1971. Effect of thymus-derived lymphocytes on amount and affinity of anti-hapten antibody. J. Immunol. 106:872-874.
36. Ingram RJ, Chu KK, Metan G, Maillere B, Doganay M, Ozkul Y, Dyson H, Williamson ED, Baillie L, Kim LU, Ascough S, Sriskandan S, Altmann DM, Oscherwitz J, Cease K. 2010. An epitope of Bacillus anthracis protective antigen that is cryptic in rabbits may be immunodominant in humans. Infect. Immun. 78:2353-2354.
37. Pitt ML, Little SF, Ivins BE, Fellows P, Barth J, Hewetson J, Gibbs P, Dertzbaugh M, Friedlander AM. 2001. In vitro correlate of immunity in a rabbit model of inhalational anthrax. Vaccine 19:4768-4773.
38. Ivins BE, Pitt ML, Fellows PF, Farchaus JW, Benner GE, Waag DM, Little SF, Anderson GW, Jr., Gibbs PH, Friedlander AM. 1998. Comparative efficacy of experimental anthrax vaccine candidates against inhalation anthrax in rhesus macaques. Vaccine 16:1141-1148.
39. Little SF, Ivins BE, Fellows PF, Pitt ML, Norris SL, Andrews GP. 2004. Defining a serological correlate of protection in rabbits for a recombinant anthrax vaccine. Vaccine 22:422-430
40. Reuveny S, White MD, Adar YY, Kafri Y, Altboum Z, Gozes Y, Kobiler D, Shafferman A, Velan B. 2001. Search for correlates of protective immunity conferred by anthrax vaccine. Infect. Immun. 69:2888-2893.
41. Schumacher WC, Storozuk CA, Dutta PK, Phipps AJ. 2008. Identification and characterization of Bacillus anthracis spores by multiparameter flow cytometry. Appl. Environ. Microbiol. 74:5220-5223.
42. Welkos S, Friedlander A, Weeks S, Little S, Mendelson I. 2002. In-vitro characterisation of the phagocytosis and fate of anthrax spores in macrophages and the effects of anti-PA antibody. J. Med. Microbiol. 51:821-831. 44. Welkos S, Little S, Friedlander A, Fritz D, Fellows P. 2001. The role of antibodies to Bacillus anthracis and anthrax toxin components in inhibiting the early stages of infection by anthrax spores. Microbiology 147: 1677-1685.
43. Fellows PF, Linscott MK, Ivins BE, Pitt ML, Rossi CA, Gibbs PH, Friedlander AM. 2001. Efficacy of a human anthrax vaccine in guinea pigs, rabbits, and rhesus macaques against challenge by Bacillus anthracis isolates of diverse geographical origin. Vaccine 19:3241-3247.
44. Chabot DJ, Joyce J, Caulfield M, Cook J, Hepler R, Wang S, Vietri NJ, Ruthel G, Shoop W, Pitt L, Leffel E, Ribot W, Friedlander AM. Efficacy of a capsule conjugate vaccine against inhalational anthrax in rabbits and monkeys. Vaccine 30:846-852.
45. Keitel WA, Treanor JJ, El Sahly HM, Evans TG, Kopper S, Whitlow V, Selinsky C, Kaslow DC, Rolland A, Smith LR, Lalor PA. 2009. Evaluation of a plasmid DNA-based anthrax vaccine in rabbits, nonhuman primates and healthy adults. Hum. Vaccin. 5:536-544.
46. Joellenbeck JM, Zwanziger LL, Durch JS, and BLStrom (ed). 2002. The anthrax vaccine: is it safe? Does it work? National Academies Press, Washington, DC.
47. Sever JL, Brenner AI, Gale AD, Lyle JM, Moulton LH, West DJ. 2002. Safety of anthrax vaccine: a review by the Anthrax Vaccine Expert Committee (AVEC) of adverse events reported to the Vaccine Adverse Event Reporting System (VAERS). Pharmacoepidemiol. Drug Saf. 11: 189-202.
48. Crowe SR, Ash LL, Engler RJ, Ballard JD, Harley JB, Farris AD, James JA. 2010. Select human anthrax protective antigen epitope-specific antibodies provide protection from lethal toxin challenge. J. Infect. Dis. 202: 251-260.
49. Reason D, Liberato J, Sun J, Keitel W, Zhou J. 2009. Frequency and domain specificity of toxin-neutralizing paratopes in the human antibody response to anthrax vaccine adsorbed. Infect. Immun. 77:2030-2035.
50. Reason DC, Ullal A, Liberato J, Sun J, Keitel W, Zhou J. 2008. Domain specificity of the human antibody response to Bacillus anthracis protective antigen. Vaccine 26:4041-4047.
51. Abboud N, Casadevall A. 2008. The immunogenicity of Bacillus anthracis protective antigen domains and the efficacy of elicited antibody responses depend on host genetic background. Clin. Vaccine Immunol. 15: 1115-1123.
52. Brossier F, Levy M, Landier A, Lafaye P, Mock M. 2004. Functional analysis of Bacillus anthracis protective antigen by using neutralizing monoclonal antibodies. Infect. Immun. 72:6313-6317.
53. Little SF, Leppla SH, Cora E. 1988. Production and characterization of monoclonal antibodies to the protective antigen component of Bacillus anthracis toxin. Infect. Immun. 56:1807-1813.