Glycan surface antigens from Bacillus anthracis as vaccine targets: current status and future perspectives

References

• Hanna P. Anthrax pathogenesis and host response. Curr Top Microbiol Immunol 1998;225:13-35
   PubMed Web of Science ®Google Scholar
• Wang JY, Roehrl MH. Anthrax vaccine design: strategies to achieve comprehensive protection against spore, bacillus, and toxin. Med Immunol 2005;4:4
   PubMedGoogle Scholar
• Friedlander AM, Welkos SL, Pitt ML, et al. Postexposure prophylaxis against experimental inhalation anthrax. J Infect Dis 1993;167:1239-43
   PubMed Web of Science ®Google Scholar
• Lane HC, Montagne JL, Fauci AS. Bioterrorism: a clear and present danger. Nat Med 2001;7:1271-3
   PubMed Web of Science ®Google Scholar
• Bennett RL. Chemical or biological terrorist attacks: an analysis of the preparedness of hospitals for managing victims affected by chemical or biological weapons of mass destruction. Int J Environ Res Public Health 2006;3:67-75
   PubMedGoogle Scholar
• Bouzanias DG. Current and future medical approaches to combat the anthrax threat. J Med Chem 2010;53:4305-31
   PubMed Web of Science ®Google Scholar
• Webb G. Being prepared: modeling the response to an anthrax attack. Ann Intern Med 2005;142:667-8
   PubMed Web of Science ®Google Scholar
• Klinman DM, Yamamoto M, Tross D, et al. Anthrax prevention and treatment: utility of therapy combining antibiotic plus vaccine. Expert Opin Biol Ther 2009;9(12):1477-86
   PubMed Web of Science ®Google Scholar
• Berti F, Adamo R. Recent mechanistic insights on glycoconjugate vaccines and future perspectives. ACS Chem Biol 2013;8:1653-63
   Google Scholar
• Astronomo RD, Burton DR. Carbohydrate vaccines: developing sweet solutions to sticky situations? Nat Rev Drug Discov 2010;9:308-24
   PubMed Web of Science ®Google Scholar
• Meselson M, Guillemin J, Hugh-Jones M, et al. The Sverdlovsk anthrax outbreak of 1979;Science 1994;266:1202-8
   Google Scholar
• Spencer RC. Bacillus anthracis. J Clin Pathol 2003;56:182-7
   PubMed Web of Science ®Google Scholar
• Young JA, Collier RJ. Anthrax toxin: receptor binding, internalization, pore formation, and translocation. Annu Rev Biochem 2007;76:243-65
   PubMed Web of Science ®Google Scholar
• Candela T, Fouet A. Bacillus anthracis CapD, belonging to the g-glutamyltranspeptidase family, is required for the covalent anchoring of capsule to peptidoglycan. Mol Microbiol 2005;57:717-26
   PubMed Web of Science ®Google Scholar
• Bouzanias DG. Potential biological targets of Bacillus anthracis in anti-infective approaches against the threat of bioterrorism. Expert Rev Anti Infect Ther 2007;5:665-84
   PubMed Web of Science ®Google Scholar
• Bouzanias DG. Medical countermeasures to protect humans from anthrax bioterrorism. Trends Microbiol 2009;17:522-8
   PubMed Web of Science ®Google Scholar
• Brey RN. Molecular basis for improved anthrax vaccines. Adv Drug Deliv Rev 2005;57:1266-92
   PubMed Web of Science ®Google Scholar
• Baillie LW. Past, imminent and future human medical countermeasures for anthrax. J Appl Microbiol 2006;101:594-606
   PubMed Web of Science ®Google Scholar
• Wimer-Mackin S, Hinchcliffe M, Petrie CR, et al. An intranasal vaccine targeting both the Bacillus anthracis toxin and bacterium provides protection against aerosol spore challenge in rabbits. Vaccine 2006;24:3953-63
   PubMed Web of Science ®Google Scholar
• Chabot DJ, Scorpio A, Tobery SA, et al. Anthrax capsule vaccine protects against experimental infection. Vaccine 2004;23:43-7
   PubMed Web of Science ®Google Scholar
• Welkos S, Little S, Friedlander A, et al. The role of antibodies to Bacillus anthracis and anthrax toxin components in inhibiting the early stages of infection by anthrax spores. Microbiology 2001;147:1677-85
   PubMedGoogle Scholar
• Ducle H, Hong HA, Atkins HS, et al. Immunization against anthrax using Bacillus subtilis spores expressing the anthrax protective antigen. Vaccine 2007;25:346-55
   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 2005;73:5978-87
   PubMed Web of Science ®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. Vaccine 2006;33-4.5950-9
   Google Scholar
• Lipton E. US cancels order for 75 million doses of anthrax vaccine. N. Y. Times; 2006. No A23
   Google Scholar
• Fasanella A, Tonello F, Garofolo G, et al. Protective activity and immunogenicity of two recombinant anthrax vaccines for veterinary use. Vaccine 2008;26:5684-8
   PubMed Web of Science ®Google Scholar
• Joyce J, Cook J, Chabot D, et al. Immunogenicity and protective efficacy of Bacillus anthracis poly-gamma-D-glutamic acid capsule covalently coupled to a protein carrier using a novel triazine-based conjugation strategy. J Biol Chem 2006;281:4831-43
   PubMed Web of Science ®Google Scholar
• Rhie GE, Roehrl MH, Mourez M, et al. A dually active anthrax vaccine that confers protection against both bacilli and toxins. Proc Natl Acad Sci USA 2003;100:10925-30
   PubMed Web of Science ®Google Scholar
• Aulinger BA, Roehrl MH, Mekalanos JJ, et al. Combining anthrax vaccine and therapy: a dominant negative inhibitor of anthrax toxin is also a potent and safe immunogen for vaccines. Infect Immun 2005;73:3408-14
   PubMed Web of Science ®Google Scholar
• Kaur M, Singh S, Bhatnagar R. Anthrax vaccines: present status and future prospects. Expert Rev Vaccines 2013;12:955-70
   PubMed Web of Science ®Google Scholar
• Klinman DM. CpG oligonucleotides accelerate and boost the immune response elicited by AVA, the licensed anthrax vaccine. Expert Rev Vaccines 2006;5:365-9
   PubMed Web of Science ®Google Scholar
• Costantino P, Rappuoli R, Berti F. The design of semi-synthetic and synthetic glycoconjugate vaccines. Expert Opin Drug Discov 2011;6:1045-67
   PubMed Web of Science ®Google Scholar
• Baddiley J. Teichoic acids in walls and the molecular structure of bacterial walls. Proc R Soc Lond B Biol Sci 1968;170:331-48
   PubMed Web of Science ®Google Scholar
• Coley J, Duckworth M, Baddiley J. The occurrence of lipoteichoic acids in the membranes of Gram-positive bacteria. J Gen Microbiol 1972;73:587-91
   PubMedGoogle Scholar
• Gründling A, Schneewind O. Synthesis of glycerol phosphate lipoteichoic acid in Staphylococcus aureus. Proc Natl Acad Sci USA 2007;104:8478-83
   PubMed Web of Science ®Google Scholar
• Garufi G, Hendrickx AP, Beeri K, et al. Synthesis of lipoteichoic acids in Bacillus anthracis. J Bacteriol 2012;194:4312-21
   PubMed Web of Science ®Google Scholar
• Robert A, Samuelson P, Andreoni C, et al. Surface display on staphylococci: a comparative study. FEBS Lett 1996;390:327-33
   PubMed Web of Science ®Google Scholar
• Kuo LM, Davies HC, Smith L. Monoclonal antibodies to cytochrome c from paracoccus denitrificans: effects on electron transport reactions. Biochim Biophys Acta 1985;809:388-95
   PubMedGoogle Scholar
• Sorensen UB, Henrichsen J, Chen HC, Szu SC. Covalent linkage between the capsular polysaccharide and the cell wall peptidoglycan of Streptococcus pneumoniae revealed by immunochemical methods. Microb Pathog 1990;8:325-34
   PubMed Web of Science ®Google Scholar
• He LM, Neu MP, Vanderberg LA. Bacillus licheniformis γ −glutamyl exopolymer: physicochemical characterization and U(VI) interaction. Environ Sci Technol 2000;34:1694-701
   Web of Science ®Google Scholar
• Barua S, Iver JK, Houghes MA, et al. Toxin inhibition of antimicrobial factors peptidoglycan in human blood induced by Bacillus anthracis. Infect Immun 2013;81:3693-702
   PubMed Web of Science ®Google Scholar
• Langer M, Malykhin A, Maeda K, et al. Bacillus anthracis peptidoglycan stimulates an inflammatory response in monocytes through the p38 mitogen-activated protein kinase pathway. PLoS One 2008;3:e3706
   Web of Science ®Google Scholar
• Sun D, Popescu NI, Raisley B, et al. RII and complement Bacillus anthracis peptidoglycan activates human platelets through Fcg. J Biol Chem 2013;122:571-9
   Google Scholar
• Qiu P, Li Y, Shiloach J, et al. Bacillus anthracis cell wall peptidoglycan but not Lethal or Edema toxins produces changes consistent with disseminated intravascular coagulation in a rat model. J Infect Dis 2013;208:978-89
   PubMed Web of Science ®Google Scholar
• S Schäffer C, Messner P. The structure of secondary cell wall polymers: how Gram-positive bacteria stick their cell walls together. Microbiology 2005;151:643-51
   PubMed Web of Science ®Google Scholar
• Mesnage S, Tosi-Couture E, Mock M, Fouet A. The S-layer homology domain as a means for anchoring heterologous proteins on the cell surface of Bacillus anthracis. J Appl Microbiol 1999;87:256-60
   PubMed Web of Science ®Google Scholar
• Kern J, Ryan C, Faull K, et al. Bacillus anthracis surface-layer proteins assemble by binding to the secondary cell wall polysaccharide in a manner that requires csaB and tagO. J Mol Biol 2010;401:757-75
   PubMed Web of Science ®Google Scholar
• Leoff C, Saile E, Rauvolfova J, et al. Secondary cell wall polysaccharides of Bacillus anthracis are antigens that contain specific epitopes which cross-react with three pathogenic Bacillus cereus strains that caused severe disease, and other epitopes common to all the Bacillus cereus strains tested. Glycobiology 2009;19:65-673
   Web of Science ®Google Scholar
• Choudhury B, Leoff C, Saile E, et al. Species-specific polysaccharide of Bacillus anthracis is the structure of the major cell wall. J Biol Chem 2006;281:27932-41
   PubMed Web of Science ®Google Scholar
• Oberli MA, Bindschadler P, Werz DB, et al. Synthesis of a hexasaccharide repeating unit from Bacillus anthracis vegetative cell walls. Org Lett 2008;10:905-8
   PubMed Web of Science ®Google Scholar
• Forsberg LS, Choudhury B, Leoff C, et al. Secondary cell wall polysaccharides from Bacillus cereus strains G9241, 03BB87 and 03BB102 causing fatal pneumonia share similar glycosyl structures with the polysaccharides from Bacillus anthracis. Glycobiology 2011;21:934-48
   PubMed Web of Science ®Google Scholar
• Ganguly J, Low LY, Kamal N, et al. The secondary cell wall polysaccharide of Bacillus anthracis provides the specific binding ligand for the C-terminal cell wall-binding domain of two phage endolysins, PlyL and PlyG. Glycobiology 2013;23:820-32
   PubMed Web of Science ®Google Scholar
• Mo K-F, Li X, Li H, et al. Endolysins of Bacillus anthracis bacteriophages recognize unique carbohydrate epitopes of vegetative cell wall polysaccharides with high affinity and selectivity. J Am Chem Soc 2012;134:15556-62
   PubMed Web of Science ®Google Scholar
• Vasan M, Rauvolfova J, Wolfert MA, et al. Chemical synthesis and immunological properties of oligosaccharides derived from the vegetative cell wall of Bacillus anthracis. ChemBioChem 2008;9:1716-20
   PubMed Web of Science ®Google Scholar
• Errington J. Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Microbiol Rev 1993;57:1-33
   PubMedGoogle Scholar
• G Gerhardt P. Cytology of Bacillus anthracis. Fed Proc 1967;26:1504-17
   PubMedGoogle Scholar
• Roels S, Losick R. Adjacent and divergently oriented operons under the control of the sporulation regulatory protein GerE in Bacillus subtilis. J Bacteriol 1995;177:6263-75
   PubMed Web of Science ®Google Scholar
• Steichen C, Chen P, Kearney JF, et al. Indentification of the immunodominant protein and other proteins of the Bacillus anthracis exosporium. J Bacteriol 2003;185:1903-10
   PubMed Web of Science ®Google Scholar
• Daubenspeck JM, Zeng H, Chen P, et al. Novel oligosaccharide side chains of the collagen-like region of BclA, the major glycoprotein of the Bacillus anthracis exosporium. J Biol Chem 2004;279:30945-53
   PubMed Web of Science ®Google Scholar
• Saksena R, Adamo R, Kováč P. Studies toward a conjugate vaccine for anthrax. Synthesis and characterization of anthrose [4,6-dideoxy-4-(3-hydroxy-3-methylbutanamido)-2-O-methyl-D-glucopyranose] and its methyl glycosides. Carbohydr Res 2005;340:1591-600
   PubMed Web of Science ®Google Scholar
• Werz DB, Seeberger PH. Total synthesis of antigen bacillus anthracis tetrasaccharide-creation of an anthrax vaccine candidate. Angew Chem Int Ed. Engl 2005;44:6315-18
   PubMed Web of Science ®Google Scholar
• Adamo R, Saksena R, Kováč P. Synthesis of the beta anomer of the spacer-equipped tetrasaccharide side chain of the major glycoprotein of the Bacillus anthracis exosporium. Carbohydr Res 2005;340:2579-82
   PubMed Web of Science ®Google Scholar
• Saksena R, Adamo R, Kováč P. Synthesis of the tetrasaccharide side chain of the major glycoprotein of the Bacillus anthracis exosporium. Bioorg Med Chem Lett 2006;16:615-17
   PubMed Web of Science ®Google Scholar
• Adamo R, Saksena R, Kováč P. Studies towards a conjugate vaccine for anthrax: synthesis of the tetrasaccharide side chain of the Bacillus anthracis exosporium. Helv Chim Acta 2006;89:1075-88
   Web of Science ®Google Scholar
• Saksena R, Adamo R, Kováč P. Immunogens related to the synthetic tetrasaccharide side chain of the Bacillus anthracis exosporium. Bioorg Med Chem 2007;15:4283-310
   PubMed Web of Science ®Google Scholar
• Mehta AS, Saile E, Zhong W, et al. Synthesis and antigenic analysis of the BclA glycoprotein oligosaccharide from the Bacillus anthracis exosporium. Chemistry 2006;12:9136-49
   PubMed Web of Science ®Google Scholar
• Crich D, Vinogradova O. Synthesis of the antigenic tetrasaccharide side chain from the major glycoprotein of Bacillus anthracis exosporium. J Org Chem 2007;72:6513-20
   PubMed Web of Science ®Google Scholar
• Milhomme O, Dhénin SGY, Djedaïni-Pilard F, et al. Synthetic studies toward the anthrax tetrasaccharide: alternative synthesis of this antigen. Carbohydr Res 2012;356:115-31
   PubMed Web of Science ®Google Scholar
• Guo H, O’Doherty GA. De novo asymmetric synthesis of the anthrax tetrasaccharide by a palladium-catalyzed glycosylation reaction. Angew Chem Int Ed Engl 2007;46:5206-8
   PubMed Web of Science ®Google Scholar
• Dhenin SG, Moreau V, Morel N, et al. Synthesis of an anthrose derivative and production of polyclonal antibodies for the detection of anthrax spores. Carbohydr Res 2008;343:2101-10
   PubMed Web of Science ®Google Scholar
• Hou S, Kovác P. A convenient synthesis of furanose-free D-Fucose per-O-acetates and a precursor for anthrose. Eur J Org Chem 2008;1947-52
   Web of Science ®Google Scholar
• Kováč P, Hou S. Conjugation-amenable tetrasaccharide of the side chain of the major glycoprotein of the Bacillus anthracis exosporium: a large-scale preparation. Synthesis 2009;2009:545-50
   Google Scholar
• Milhomme O, Grandjean C. Synthetic efforts towards glycoconjugate-based vaccines active against anthrax. Curr Org Synth 2014;18:291-311
   Google Scholar
• Oberli MA, Horlacher T, Werz DB, Seeberger PH. Synthetic oligosaccharide bacterial antigens to produce monoclonal antibodies for diagnosis and treatment of disease using Bacillus anthracis as a case study from anti carbohydrate antibodies, Chapter 2 In: Kosma P, Müller-Loennies S, editors. Molecular basis to clinical application. Springer; 2012. 37-54
   Google Scholar
• Werz DB, Adibekian A, Seeberger PH. Synthesis of a spore surface pentasaccharide of Bacillus anthracis. Eur J Org Chem 2007;2007:1976-82
   Web of Science ®Google Scholar
• Tamborrini M, Werz DB, Frey J, et al. Anti-carbohydrate antibodies for the detection of anthrax spores. Angew Chem Int Ed Engl 2006;45:6581-2
   PubMed Web of Science ®Google Scholar
• Wang D. Carbohydrate microarrays. Proteomics 2003;3:2167-75
   PubMed Web of Science ®Google Scholar
• Wang D, Carroll GT, Turro NJ, et al. Photogenerated glycan arrays identify immunogenic sugar moieties of Bacillus anthracis exosporium. Proteomics 2007;7:180-4
   PubMed Web of Science ®Google Scholar
• Oberli MA, Tamborrini M, Tsai Y-H, et al. Molecular analysis of carbohydrate-antibody interactions: case study using a Bacillus anthracis tetrasaccharide. J Am Chem Soc 2010;132:10239-102419
   PubMed Web of Science ®Google Scholar
• Kuehn A, Kovac P, Saksena R, et al. Development of antibodies against anthrose tetrasaccharide for specific detection of Bacillus anthracis spores. Clin Vaccine Immunol 2009;16:1728-37
   PubMed Web of Science ®Google Scholar
• Saile E, Boons GJ, Buskas T, et al. Antibody responses to a spore carbohydrate antigen as a marker of nonfatal inhalation anthrax in rhesus macaques. Clin Vaccine Immunol 2011;18:743-8
   PubMed Web of Science ®Google Scholar
• Tamborrini M, Holzer M, Seeberger PH, Schurch N and Pluschke G. Anthrax spore detection by a Luminex assay based on monoclonal antibodies that recognize anthrose-containing oligosaccharides. Clin Vaccine Immunol 2010;17:1446-51
   PubMedGoogle Scholar
• Milhomme O, Köhler SM, Ropartz D, et al. Synthesis and immunochemical evaluation of a non-methylated disaccharide analogue of the anthrax tetrasaccharide. Org Biomol Chem 2012;10:8524-32
   PubMed Web of Science ®Google Scholar
• Gauthier YP, Tournier J-N, Paucod J-C, et al. Efficacy of a vaccine based on Protective Antigen and killed spores against experimental inhalational anthrax. Infect Immune 2009;77:1197-207
   PubMed Web of Science ®Google Scholar
• Daniel WB, Seeberger PH, Tamborrini M, et al. Antibodies for the detection of Bacillus anthracis and vaccine against B. anthracis infections. From PCT Int Appl 2007; WO 2007125089 A2 20071108
   Google Scholar
• Bacillus anthracis oligosaccharide variant conjugates as vaccines against anthrax and kits comprising antibodies for diagnosis of anthrax. Russell CW, Boons GJ, Buskas T, et al. From U.S. Pat Appl Publ., US 2009; 20090246200 A1 20091001
   Google Scholar
• Raab CP. Passive Immunization. Prim Care 2011;38:681-91
   PubMed Web of Science ®Google Scholar
• Brahmbhatt TN, Darnell SC, Carvalho HM, et al. Recombinant exosporium protein BclA of Bacillus anthracis is effective as a booster for mice primed with suboptimal amounts of protective antigen. Infect Immun 2007;75:5240-7
   PubMed Web of Science ®Google Scholar
• Xia G, Kohler T, Peschel A. The wall teichoic acid and lipoteichoic acid polymers of Staphylococcus aureus. Int J Med Microbiol 2010;300:148-54
   PubMed Web of Science ®Google Scholar
• Capparelli R, Nocerino N, Medaglia C, et al. The Staphylococcus aureus peptidoglycan protects mice against the pathogen and eradicates experimentally induced infection. PLoS One 2011;6:e28377
   PubMed Web of Science ®Google Scholar
• Peachman KK, Li Q, Matyas GR, et al. Anthrax vaccine antigen-adjuvant formulations completely protect New Zealand white rabbits against challenge with Bacillus anthracis Ames strain spores. Clin Vaccine Immunol 2012;19:11-16
   PubMed Web of Science ®Google Scholar
• Rynkiewicz D, Rathkopf M, Sim I, et al. Marked enhancement of the immune response to BioThrax® (Anthrax Vaccine Adsorbed) by the TLR9 agonist CPG 7909 in healthy volunteers. Infect Immun 2011;29(37):6313-20
   Google Scholar
• Sloat BR, Cui Z. Nasal immunization with a dual antigen anthrax vaccine induced strong mucosal and systemic immune responses against toxins and bacilli. Vaccine 2006;24:6405-13
   PubMed Web of Science ®Google Scholar
• Devera TS, Joshi SK, Aye LM, et al. Regulation of anthrax toxin-specific antibody titers by natural killer T cell-derived IL-4 and IFNγ. PLoS One 2011;6:e23817
   Web of Science ®Google Scholar
• Merkel TJ, Perera PY, Kelly VK, et al. Development of a highly efficacious vaccinia-based dual vaccine against smallpox and anthrax, two important bioterror entities. Proc Natl Acad Sci USA 2010;107:18091-6
   PubMed Web of Science ®Google Scholar
• Flick-Smith HC, Eyles JE, Hebdon R, et al. Mucosal or parenteral administration of microsphere-associated Bacillus anthracis protective antigen protects against anthrax infection in mice. Infect Immun 2002;70:2022-8
   PubMed Web of Science ®Google Scholar
• Bielinska AU, Janczak KW, Landers JJ, et al. Mucosal immunization with a novel nanoemulsion-based recombinant anthrax protective antigen vaccine protects against Bacillus anthracis spore challenge. Infect Immun 2007;75:4020-9
   PubMed Web of Science ®Google Scholar
• Petersen LK, Phanse Y, Ramer-Tait AE, et al. Amphiphilic polyanhydride nanoparticles stabilize Bacillus anthracis protective antigen. Mol Pharm 2012;9:874-82
   PubMed Web of Science ®Google Scholar
• Liu TH, Oscherwitz J, Schnepp B, et al. Genetic vaccines for anthrax based on recombinant adeno-associated virus vectors. Mol Ther 2009;17:373-9
   PubMed Web of Science ®Google Scholar