Recombinant protective antigen 102 (rPA102): profile of a second-generation anthrax vaccine

References

• Brachman PS, Friedlander AM, Grabenstein JD. Anthrax vaccine. In: Vaccines (Fourth Edition).SA, Orenstein WA (Eds). Elsevier Inc., USA,887–903 (2004).
   Google Scholar
• Dixon TC, Meselson M, Guillemin J, Hanna PC. Anthrax. Medical progress.N. Engl. J. Med.341, 815–826 (1999).
   PubMed Web of Science ®Google Scholar
• Swartz MN. Recognition and management of anthrax – an update. N. Engl. J. Med.345(22), 1621–1626 (2001).
   PubMed Web of Science ®Google Scholar
• Holty J-EC, Bravata DM, Liu H et al. Systematic review: a century of inhalational anthrax cases from 1900 to 2005. Ann. Intern. Med.144(4), 270–280 (2006).
   PubMed Web of Science ®Google Scholar
• Inglesby TV, O’Toole T, Henderson DA et al. Anthrax as a biological weapon, 2002. Updated recommendations for management. JAMA287(17), 2236–2252 (2002).
   PubMed Web of Science ®Google Scholar
• Mikesell P, Ivins BE, Ristroph JD, Dreier TM. Evidence for plasmid-mediated toxin production in Bacillus anthracis. Infect. Immun.39, 371–376 (1983).
   PubMed Web of Science ®Google Scholar
• Barth H, Aktories K, Popoff MR, Stiles BG. Binary bacterial toxins: biochemistry, biology, and applications of common Clostridium and Bacillus proteins. Microbiol. Mol. Biol. Rev.68(3), 373–402 (2004).
   PubMed Web of Science ®Google Scholar
• Bradley KA, Mogridge J, Mourez M, Collier RJ, Young JAT. Identification of the cellular receptor for anthrax toxin. Nature414, 225–233 (2001).
   PubMed Web of Science ®Google Scholar
• Scobie H, Rainey J, Bradley K, Young J. Human capillary morphogenesisi protein 2 functions as an anthrax receptor. Proc. Natl Acad. Sci. USA100, 5170–5174 (2003).
   PubMed Web of Science ®Google Scholar
• Petosa C, Collier RJ, Klimpel KR, Leppla SH, Liddington RC. Crystal structure of the anthrax toxin protective antigen. Nature385, 833–838 (1997).
   PubMed Web of Science ®Google Scholar
• Krantz BA, Melnyk RA, Zhang S et al. A phenylalanine clamp catalyzes protein translocation through the anthrax toxin spore. Science309, 777–785 (2005).
   PubMed Web of Science ®Google Scholar
• Lacy DB, Lin HC, Melnyk RA et al. A model of anthrax toxin lethal factor bound to protective antigen. Proc. Natl Acad. Sci. USA102(45), 16409–16414 (2005).
   Google Scholar
• Duesbery NS, Webb CP, Leppla SH et al. Proteolytic inactivation of MAP-kinase-kinase by anthrax lethal factor. Science280, 734–737 (1998).
   PubMed Web of Science ®Google Scholar
• Park JM, Greten FR, Li Z-W, Karin M. Macrophage apoptosis by anthrax lethal factor through p38 MAP kinase inhibition. Science297, 2048–2051 (2002).
   PubMed Web of Science ®Google Scholar
• Agrawal A, Lingappa J, Leppla SH et al. Impairment of dendritic cells and adaptive immunity by anthrax lethal toxin. Nature424, 329–334 (2003).
   PubMed Web of Science ®Google Scholar
• Moayeri M, Haines D, Young HA, Leppla SH. Bacillus anthracis lethal toxin induces TNF-α-independent hypoxia-mediated toxicity in mice. J. Clin. Invest.112 (5), 670–682 (2003).
   PubMed Web of Science ®Google Scholar
• Kirby JE. Anthrax lethal toxin induces human endothelial cell apoptosis. Infect. Immun.72 (1), 430–439 (2004).
   PubMed Web of Science ®Google Scholar
• During R L, Li W, Hao B et al. Anthrax lethal toxin paralyzes neutrophil actin-based motility. J. Infect. Dis.192, 837–845 (2005).
   PubMed Web of Science ®Google Scholar
• Kau J-H, Sun D-S, Tsai W-J et al. Antiplatelet activities of anthrax lethal toxin are associated with suppressed p42/44 and p38 mitogen-activated protein kinase pathways in the platelets. J. Infect. Dis.192, 1465–1474 (2005).
   PubMed Web of Science ®Google Scholar
• Leppla S. Anthrax toxin edema factor: A bacterial adenylate cyclase that increases cyclic AMP concentrations in eukaryotic cells. Proc. Natl Acad. Sci. USA79, 3162–3166 (1982).
   PubMed Web of Science ®Google Scholar
• Voth D, Hamm E, Nguyen L et al. Bacillus anthracis oedema toxin as a cause of tissue necrosis and cell type-specific cytotoxicity. Cell Microbiol.7, 1139–1149 (2005).
   Google Scholar
• Makino S, Watarai M, Cheun H, Shirahata T, Uchida I. Effect of the lower molecular capsule released from the cell surface of Baccillus anthracis on the pathogenesis on anthrax. J. Infect. Dis.186, 227–233 (2002).
   PubMed Web of Science ®Google Scholar
• Kozel TR, Murphy WJ, Brandt S et al. mAbs to Bacillus anthracis capsular antigen for immunoprotection in anthrax and detection of antigenemia. Proc. Natl Acad. Sci. USA101(14), 5042–5047 (2004).
   PubMed Web of Science ®Google Scholar
• Harrison LH, Ezzell JW, Abshire TG, Kidd S, Kaufman AF. Evaluation of serological tests for diagnosis of anthrax after an outbreak of cutaneous anthrax in Paraguay. J. Infect. Dis.160(4), 706–710 (1989).
   PubMed Web of Science ®Google Scholar
• Quinn CP, Semenova VA, Elie CM et al. Specific, sensitive and quantitative enzyme-linked immunosorbent assay for human immunoglobulin G antibodies to anthrax toxin protective antigen. Emerg. Infect. Dis.8(10), 1103–1110 (2002).
   PubMed Web of Science ®Google Scholar
• Quinn CP, Dull PM, Semenova V et al. Immune responses to Bacillus anthracis protective antigen in patients with bioterrorism-related cutaneous or inhalation anthrax. J. Infect. Dis.190, 1228–1236 (2004).
   PubMed Web of Science ®Google Scholar
• Brachman PS, Gold H, Plotkin SA et al. Field evaluation of a human anthrax vaccine. Am. J. Public Health52(4), 632–645 (1962).
   PubMed Web of Science ®Google Scholar
• Welkos S, Little S, Friedlander A, Fritz D, Fellows P. The role of antibodies to Bacillus anthracis and anthrax toxin components in inhibiting the early stages of infection by anthrax spores. Microbiology147, 1677–1685 (2001).
   PubMedGoogle Scholar
• Welkos S, Friedlander A, Weeks S, Little S, Mendelson I. 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 (2002).
   PubMed Web of Science ®Google Scholar
• Brey RN. Molecular basis for improved anthrax vaccines. Adv. Drug Deliv. Rev57, 1266–1292 (2005).
   PubMed Web of Science ®Google Scholar
• Chen Z, Moayeri M, Zhou Y-H et al. Efficient neutralization of anthrax toxin by chimpanzee monoclonal antibodies against protective antigen. J. Infect. Dis.193, 625–633 (2006).
   PubMed Web of Science ®Google Scholar
• Little SF, Ivins BE, Fellows PF, Friedlander AM. Passive protection by polyclonal antibodies against Bacillus anthracis infection in guinea pigs. Infect. Immun.65, 5171–5175 (1997).
   PubMed Web of Science ®Google Scholar
• Mabry R, Rani M, Geiger R et al. Passive protection against anthrax by using a high-affinity antitoxin antibody fragment lacking in Fc region. Infect. Immun.73(12), 8362–8368 (2005).
   PubMed Web of Science ®Google Scholar
• Cui X, Li Y, Moayeri M et al. Late treatment with a protective antigen-directed monoclonal antibody improves hemodynamic function and survival in a lethal toxin-infused rat model of anthrax sepsis. J. Infect. Dis.191, 422–434 (2005).
   PubMed Web of Science ®Google Scholar
• Williamson ED, Hodgson I, Walker NJ et al. Immunogenicity of recombinant protective antigen and efficacy against aerosol challenge with anthrax. Infect. Immun.73(9), 5978–5987 (2005).
   PubMed Web of Science ®Google Scholar
• Peterson JW, Comer JE, Noffsinger DM et al. Human monoclonal anti-protective antigen antibody completely protects rabbits and is synergistic with ciprofloxacin in protecting mice and guinea pigs against inhalation anthrax. Infect. Immun.74(2), 1016–1024 (2006).
   PubMed Web of Science ®Google Scholar
• Little SF, Ivins BE, Webster WM et al. Duration of protection of rabbits after vaccination with Bacillus anthracis recombinant protective antigen vaccine. Vaccine24(14), 2530–2536 (2006).
   PubMed Web of Science ®Google Scholar
• Ivins B, Fellows P, Pitt L et al. Experimental anthrax vaccines: efficacy of adjuvants combined with protective antigen against an aerosol Bacillus anthracis spore challenge in guinea pigs. Vaccine13(18), 1779–1784 (1995).
   PubMed Web of Science ®Google Scholar
• McBride B, Mogg A, Telfer JL et al. Protective efficacy of a recombinant preotective antigen against Bacillus anthracis challenge and asessment of immunological markers. Vaccine16(8), 810–817 (1998).
   PubMed Web of Science ®Google Scholar
• Ivins BE, Pitt MLM, Fellows PF et al. Comparative efficacy of experimental anthrax vaccine candidates against inhalation anthrax in rhesus macaques. Vaccine16 (11/12), 1141–1148 (1998).
   PubMed Web of Science ®Google Scholar
• Hahn UK, Aichler M, Boehm R, Beyer W. Comparison of the immunological memory after DNA vaccination and protein vaccination against anthrax in sheep. Vaccine24(21), 4595–4597(2006).
   PubMed Web of Science ®Google Scholar
• Pitt MLM, Little SF, Ivins B et al. In vitro correlate of immunity in a rabbit model of inhalational anthrax. Vaccine19, 4768–4773 (2001).
   PubMed Web of Science ®Google Scholar
• Little SF, Ivins BE, Fellows PF et al. Defining a serological correlate of protection in rabbits for a recombinant anthrax vaccine. Vaccine22, 422–430 (2004).
   PubMed Web of Science ®Google Scholar
• Weiss S, Kobiler D, Levy H et al. Immunological correlates for protection against intranasal challenge of Bacillus anthracis spores conferred by a protective antigen-based vaccine in rabbits. Infect. Immun.74(1), 394–398 (2006).
   PubMed Web of Science ®Google Scholar
• Peachman KK, Rao M, Alving CR et al. Correlation between lethal toxin-neutralizing antibody titers and protection from intranasal challenge with Bacillus anthracis ames strain spores in mice after transcutaneous immunization with recombinant anthrax protective antigen. Infect. Immun.74(1), 794–797 (2006).
   PubMed Web of Science ®Google Scholar
• Kobiler D, Gozes Y, Rosenberg H et al. Efficiency of protection of guinea pigs against infection with Bacillus anthracis spores by passive immunization. Infect. Immun.70(2), 544–550 (2002).
   PubMed Web of Science ®Google Scholar
• Price BM, Liner AL, Park S et al. Protection against anthrax lethal toxin challenge by genetic immunization with a plasmid encoding the lethal factor protein. Infect. Immun.69 (7), 4509–4515 (2001).
   PubMed Web of Science ®Google Scholar
• Galloway D, Liner A, Legutki J et al. Genetic immunization against anthrax. Vaccine22, 1604–1608 (2004).
   PubMed Web of Science ®Google Scholar
• Hermanson G, Whitlow V, Parker S et al. A cationic lipid-formulated plasmid DNA vaccine confers sustained antibody-mediated protection against aerosolized anthrax spores. Proc. Natl Acad. Sci. USA101(37), 13601–13606 (2004).
   PubMed Web of Science ®Google Scholar
• Schneerson R, Kubler-Kielb J, Liu T-Y et al. Poly (γ-d-glutamic acid) protein conjugates induce IgG antibodies in mice to the capsule of Bacillus anthracis: A potential addition to the anthrax vaccine. Proc. Natl Acad. Sci. USA100(15), 8945–8950 (2003).
   PubMed Web of Science ®Google Scholar
• Wang TT, Fellows PF, Leighton TJ, Lucas AH. Induction of opsonic antibodies to the γ-d-glutamic acid capsule of Bacillus anthracis by immunization with a synthetic peptide-carrier protein conjugate. FEMS Immunol. Med. Microbiol.40, 231–237 (2004).
   PubMed Web of Science ®Google Scholar
• Cohen S, Mendelson I, Altboum Z et al. Attenuated nontoxinogenic and nonencapsulated recombinant Bacillus anthracis spore vaccines protect against anthrax. Infect. and Immun.68(8), 4549–4558 (2000).
   PubMed Web of Science ®Google Scholar
• Martinez-Palomo A. The science of Louis Pasteur: a reconsideration. Q. Rev. Biol.76(1), 37–45 (2001).
   Google Scholar
• Shlyakhov EN, Rubinstein E. Human live anthrax vaccine in the former USSR. Vaccine12(8), 727–728 (1994).
   PubMed Web of Science ®Google Scholar
• Jefferson T, Demicheli V, Deeks J et al. Vaccines for preventing anthrax. Cochrane Database Syst. Rev. CD000975, (1997).
   Google Scholar
• Fee E, Brown TM. Anthrax and the wool trade. Am. J. Pub. Health92(5), 754–757 (2002).
   Google Scholar
• Plotkin SA, Brachman PS, Utell M, Bumford FH, Atchison MM. An epidemic of inhalation anthrax, the first in the twentieth century. I. Clinical features. Amer. J. Med.29, 992–1001 (1960).
   PubMed Web of Science ®Google Scholar
• Belton FC, Strange RE. Studies on a protective antigen produced in vitro from Bacillus anthracis: medium and methods of production. Br. J. Exp. Pathol.35, 144–152 (1954).
   PubMed Web of Science ®Google Scholar
• Wright GG, Green TW Jr, Kanode RG. Studies on immunity in anthrax V: immunizing activity of alum-precipitated protective antigen. J. Immunol.73, 387–391 (1954).
   PubMed Web of Science ®Google Scholar
• Puziss M and Wright GG. Studies on immunity in anthrax X. Gel-adsorbed protective antigen for immunization of man. J. Bacteriol.85, 230–236 (1963).
   PubMed Web of Science ®Google Scholar
• Abramova FA, Grinberg LM, Yampolskaya OV, Walker DH. Pathology of inhalational anthrax in 42 cases from the Sverdlovsk outbreak of 1979. Proc. Natl Acad. Sci. USA90, 2291–2294 (1993).
   PubMed Web of Science ®Google Scholar
• Meselson M, Guillemin J, Hugh-Jones M et al. The Sverdlovsk anthrax outbreak of 1979. Science266, 1202–1208 (1994).
   PubMed Web of Science ®Google Scholar
• Pittman P, Kim-Ahn G, Pifat DY et al. Anthrax vaccine: immunogenicity and safety of a dose-reduction, route-change comparison study in humans. Vaccine20, 1412–1420 (2002).
   PubMed Web of Science ®Google Scholar
• Marano N, Babcock J, Keitel W et al. Interim analysis of anthrax vaccine human reactogenicity and immunogenicity clinical trial. Bacillus Act 200543 (2005).
   Google Scholar
• The Anthrax Vaccine: Is it safe? Does it work? LM Joellenbeck, LL Zwanziger, JS Durch, BL Strom (Eds). National Academy Press, WA, USA (2002).
   Google Scholar
• Bush LM, Abrams BH, Beall A, Johnson CC. Index case of fatal inhalational anthrax due to bioterrorism in the United States. N. Engl. J. Med.345(22), 1607–1611 (2001).
   PubMed Web of Science ®Google Scholar
• Perkins BA, Ashford DA. Bioterrorism-related public health Bacillus anthracis research priorities. Emerg. Infect. Dis.8(10), 1183 (2002).
   Google Scholar
• Friedlander AM, Welkos SL, Ivins BE. Anthrax vaccines. Curr. Top. Microbiol. Immunol.271, 33–60 (2002).
   PubMed Web of Science ®Google Scholar
• Friedlander AM, Pittman PR, Parker GW. Anthrax vaccine: evidence for safety and efficacy against inhalational anthrax. JAMA282 (22), 2104–2106 (1999).
   PubMed Web of Science ®Google Scholar
• Fowler RA, Sanders GD, Bravata DM et al. Cost–effectiveness of defending against bioterrorism: a comparison of vaccination and antibiotic prophylaxis against anthrax. Ann. Intern. Med.142 (8), 601–610 (2005).
   PubMed Web of Science ®Google Scholar
• Gwinn W, Zhang M, Mon S et al. Scalable purification of Bacillus anthracis protective antigen from Escherichia coli. Protein Expr. Purif.45, 30–36 (2006).
   PubMed Web of Science ®Google Scholar
• Hepler RW, Kelly R, McNeely TB et al. A recombinant 63-kDa form of Bacillus anthracis protective antigen produced in the yeast Saccharomyces cerevisiae provides protection in rabbit and primate inhalational challenge models of anthrax infection. Vaccine24, 1501–1514 (2006).
   PubMed Web of Science ®Google Scholar
• Flick-Smith H, Walker N, Gibson P et al. A recombinant carboxy-terminal domain of the protective antigen of Bacillus anthracis protects mice against anthrax infection. Infect. Immun.70, 1653–1656 (2002).
   PubMed Web of Science ®Google Scholar
• Oggioni MR, Ciabattini A, Cuppone AM, Pozzi G. Bacillus spores for vaccine delivery. Vaccine21 (Suppl. 2), 96–101 (2003).
   PubMed Web of Science ®Google Scholar
• Hashimoto M, Boyer JL, Hackett NR, Wilson JM, Crystal RG. Induction of protective immunity to anthrax lethal toxin with a nonhuman primate adenovirus-based vaccine in the presence of preexisting anti-human adenovirus immunity. Infect. Immun.73(10), 6885–6891 (2005).
   PubMed Web of Science ®Google Scholar
• Gu Mi-Li, Leppla SH, Klinman DM. Protection against anthrax toxin by vaccination with a DNA plasmid encoding anthrax protective antigen. Vaccine17, 340–344 (1999).
   PubMed Web of Science ®Google Scholar
• Gaur R, Gupta PK, Banerjea AC, Singh Y. Effect of nasal immunization with protective antigen of Bacillus anthracis on protective immune response against anthrax toxin. Vaccine20, 2836–2839 (2002).
   PubMed Web of Science ®Google Scholar
• Boyaka PN, Tafaro A, Fischer R et al. Effective mucosal immunity to anthrax: neutralizing antibodies and Th cell responses following nasal immunization with protective antigen. J. Immunol.170(11), 5636–5643 (2003).
   PubMed Web of Science ®Google Scholar
• Kenney RT, Yu J, Guebre-Xabier M et al. Induction of protective immunity against lethal anthrax challenge with a patch. J. Infect. Dis.190, 774–781 (2004).
   PubMed Web of Science ®Google Scholar
• Mikszta JA, Sullivan VJ, Dean C et al. Protective immunization against inhalational anthrax: a comparison of minimally invasive delivery platforms. J. Infect. Dis.191, 278–288 (2005).
   PubMed Web of Science ®Google Scholar
• Rynkiewicz D, Rathkopf M, Ransom J et al. Marked enhancement of antibody response to anthrax vaccine adsorbed with CPG 7909 in healthy volunteers.
   Google Scholar
• Campbell JD, Kotloff KL, Chrisley L, Wasserman SS, Levine MM. Phase I recombinant protective antigen (rPA) anthrax vaccine trial.42nd Annual Meeting of Infectious Diseases Society of America, Boston, USA, September 30–October 3 (2004) Abstract 748.
   Google Scholar
• Keitel W, Treanor J, El-Sahly H et al. A Phase I, double-blind, dosage-escalating clinical trial to evaluate safety and immunogenicity of prophylactic anthrax DNA vaccine in healthy adults. 42nd Annual Meeting of Infectious Diseases Society of America. CA, USA, (2005).
   Google Scholar
• Gorse GJ, Keitel W, Keyserling H et al. Immunogenicity and tolerance of ascending doses of a recombinant protective antigen (rPA102) anthrax vaccine: a randomized, double-blinded, controlled, multicenter trial. Vaccine24(33–34), 5950–5959 (2006).
   PubMed Web of Science ®Google Scholar
• Leppla SH, Robbins JB, Schneerson R, Shiloach J. Development of an improved vaccine for anthrax. J. Clin. Invest.110(2), 141–144 (2002).
   PubMed Web of Science ®Google Scholar
• Scobie HM, Thomas D, Marlett JM et al. A soluble receptor decoy protects rats against anthrax lethal toxin challenge. J. Infect. Dis.192, 1047–1051 (2005).
   PubMed Web of Science ®Google Scholar
• Subramanian GM, Cronin PW, Poley G et al. A Phase I study of PAmAb, a fully human monoclonal antibody against Bacillus anthracis protective antigen, in healthy volunteers. Clin. Infect. Dis.41, 12–20 (2005).
   PubMed Web of Science ®Google Scholar
• Vodkin MH, Leppla SH. Cloning of the protective antigen gene of Bacillus anthracis. Cell34(2), 693–697 (1983).
   PubMed Web of Science ®Google Scholar
• Ivins BE, Welkos SL. Cloning and Expression of the Bacillus anthracis protective antigen gene in Bacillus subtilis. Infect. Immun.54(2), 537–542 (1986).
   PubMed Web of Science ®Google Scholar
• Worsham PL, Sowers MR. Isolation of an asporogenic (spoOA) protective antigen-producing strain of Bacillus anthracis. Can. J. Microbiol.45(1), 1–8 (1999).
   PubMed Web of Science ®Google Scholar
• Farchaus JW, Ribot WJ, Jendrek S, Little SF. Fermentation, purification, and characterization of protective antigen from a recombinant avirulent strain of Bacillus anthracis. Appl Environ. Microbiol.64(3), 982–991 (1998).
   PubMed Web of Science ®Google Scholar
• Ribot WJ, Powell BS, Ivins BE et al. Comparative vaccine efficacy of different isoforms of recombinant protective antigen against Bacillus anthracis spore challenge in rabbits. Vaccine24, 3469–3476 (2006)
   PubMed Web of Science ®Google Scholar
• Food and Drug Administration, HHS. New drug and biological drug products; evidence needed to demonstrate effectiveness of new drugs when human efficacy studies are not ethical or feasible. Federal Register67(105), 37988–37998 (2002).
   PubMedGoogle Scholar
• Phipps AJ, Premanandan C, Barnewall RE, Lairmore MD. Rabbit and nonhuman primate models of toxin-targeting human anthrax vaccines. Microbiol. Mol. Biol. Rev.68(4), 617–629 (2004).
   PubMed Web of Science ®Google Scholar