637
Views
36
CrossRef citations to date
0
Altmetric
Review

The exceptionally broad-based potential of active and passive vaccination targeting the conserved microbial surface polysaccharide PNAG

, &
Pages 1041-1053 | Received 04 Jan 2016, Accepted 24 Feb 2016, Published online: 16 Mar 2016

References

  • Achievements in Public Health. 1900-1999: control of infectious diseases. MMWR Morb Mort Wkly Rep. 1999;48(29):621–629.
  • Makela PH. Conjugate vaccines–a breakthrough in vaccine development. SE Asian J Trop Med Public Health. 2003;34(2):249–253.
  • Houser K, Subbarao K. Influenza vaccines: challenges and solutions. Cell Host Microbe. 2015;17(3):295–300.
  • Rubens M, Ramamoorthy V, Saxena A, et al.. HIV vaccine: Recent advances, current roadblocks, and future directions. J Immunol Res. 2015;2015:560347.
  • Sinha S, Medhi B, Sehgal R. Challenges of drug-resistant malaria. Parasite. 2014;21:61.
  • Cywes-Bentley C, Skurnik D, Zaidi T, et al. Antibody to a conserved antigenic target is protective against diverse prokaryotic and eukaryotic pathogens. Proc Natl Acad Sci USA. 2013;110(24):E2209–2218.
  • Gening ML, Maira-Litran T, Kropec A, et al. Synthetic β-(1->6)-linked N-acetylated and nonacetylated oligoglucosamines used to produce conjugate vaccines for bacterial pathogens. Infect Immun. 2012;78(2):764–772.
  • Kelly-Quintos C, Kropec A, Briggs S, et al. The role of epitope specificity in the human opsonic antibody response to the staphylococcal surface polysaccharide poly N-acetyl glucosamine. J Infect Dis. 2012-2019;192(11):2005.
  • Maira-Litran T, Kropec A, Goldmann DA, et al. Comparative opsonic and protective activities of Staphylococcus aureus conjugate vaccines containing native or deacetylated Staphylococcal Poly-N-acetyl-beta-(1-6)-glucosamine. Infect Immun. 2005;73(10):6752–6762.
  • Pozzi C, Wilk K, Lee JC, et al. Opsonic and protective properties of antibodies raised to conjugate vaccines targeting six Staphylococcus aureus antigens. Plos One. 2012;7(10):e46648.
  • Vlock D, Lee JC, Kropec-Huebner A, et al. Pre-clinical and initial phase i evaluations of a fully human monoclonal antibody directed against the PNAG surface polysaccharide on Staphylococcus aureus. Abstracts of the 50th ICAAC 2010; ASM Press; Abstract G1-1654/329;,2010.
  • Tojo M, Yamashita N, Goldmann DA, et al. Isolation and characterization of a capsular polysaccharide adhesin from Staphylococcus epidermidis. J Infect Dis. 1988;157(4):713–722.
  • Mack D, Fischer W, Krokotsch A, et al. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol. 1996;178(1):175–183.
  • McKenney D, Hubner J, Muller E, et al. The ica locus of Staphylococcus epidermidis encodes production of the capsular polysaccharide/adhesin. Infect Immun. 1998;66(10):4711–4720.
  • McKenney D, Pouliot KL, Wang Y, et al. Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science. 1999;284(5419):1523–1527.
  • Cramton SE, Gerke C, Schnell NF, et al. The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun. 1999;67(10):5427–5433.
  • Baldassarri L, Donnelli G, Gelosia A, et al. Purification and characterization of the staphylococcal slime-associated antigen and its occurrence among Staphylococcus epidermis clinical isolates. Infect Immun. 1996;64(8):3410–3415.
  • Muller E, Hübner J, Gutierrez N, et al. Isolation and characterization of transposon mutants of Staphylococcus epidermidis deficient in capsular polysaccharide/adhesin and slime. Infect Immun. 1993;61(2):551–558.
  • Maira-Litran T, Kropec A, Abeygunawardana C, et al. Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect Immun. 2002;70(8):4433–4440.
  • Joyce JG, Abeygunawardana C, Xu Q, et al. Isolation, structural characterization, and immunological evaluation of a high-molecular-weight exopolysaccharide from Staphylococcus aureus. Carbohydr Res. 2003;338(9):903–922.
  • O’Gara JP. ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett. 2007;270(2):179–188.
  • Wang X, Preston JF 3rd, Romeo T. The pgaABCD locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol. 2004;186(9):2724–2734.
  • Choi AHK, Slamti L, Avci FY, et al. The pgaABCD locus of Acinetobacter baumannii encodes the production of poly-beta-1-6-N-acetylglucosamine, which is critical for biofilm formation. J Bacteriol. 2009;191(19):5953–5963.
  • Skurnik D, Davis MR Jr., Benedetti D, et al. Targeting pan-resistant bacteria with antibodies to a broadly conserved surface polysaccharide expressed during infection. J Infect Dis. 1709-1718;205(11):2012.
  • Chen K-M, Chiang M-K, Wang M, et al. The role of pgaC in Klebsiella pneumoniae virulence and biofilm formation. Microb Pathog. 2014;77:89–99.
  • Parise G, Mishra M, Itoh Y, et al. Role of a putative polysaccharide locus in Bordetella biofilm development. J Bacteriol. 2006;189(3):750–760.
  • Roux D, Cywes-Bentley C, Zhang YF, et al. Identification of poly-N-acetylglucosamine as a major polysaccharide component of the Bacillus subtilis biofilm matrix. J Biol Chem. 2015;290(31):19261–19272.
  • Kropec A, Maira-Litran T, Jefferson KK, et al. Poly-N-acetylglucosamine production in Staphylococcus aureus is essential for virulence in murine models of systemic infection. Infect Immun. 2005;73(10):6868–6876.
  • Subashchandrabose S, Smith SN, Spurbeck RR, et al. Genome-wide detection of fitness genes in uropathogenic Escherichia coli during systemic infection. PLoS Pathog. 2013;9(12):e1003788.
  • Cerca N, Jefferson KK, Oliveira R, et al. Comparative antibody-mediated phagocytosis of Staphylococcus epidermidis cells grown in a biofilm or in the planktonic state. Infect Immun. 2006;74(8):4849–4855.
  • Heilmann C, Schweitzer O, Gerke C, et al. Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol. 1996;20(5):1083–1091.
  • Gerke C, Kraft A, Süssmuth R, et al. Characterization of the N-acetylglucosaminyltransferase activity involved in the biosynthesis of the Staphylococcus epidermidis polysaccharide intercellular adhesin. J Biol Chem. 1998;273(29):18586–18593.
  • Bobrov AG, Kirillina O, Forman S, et al. Insights into Yersinia pestis biofilm development: topology and co-interaction of Hms inner membrane proteins involved in exopolysaccharide production. Environ Microbiol. 2008;10(6):1419–1432.
  • Skurnik D, Roux D, Pons S, et al. Extended spectrum antibodies protective against carbapenemase producing Enterobacteriaceae. J Antimicrob Chemother. 2016 Jan 7. pii: dkv448. [Epub ahead of print]
  • Whitfield GB, Marmont LS, Howell PL. Enzymatic modifications of exopolysaccharides enhance bacterial persistence. Front Microbiol. 2015;6:471.
  • Bentancor LV, O’Malley JM, Bozkurt-Guzel C, et al. Poly-N-acetyl-beta-(1-6)-glucosamine is a target for protective immunity against Acinetobacter baumannii infections. Infect Immun. 2012;80(2):651–656.
  • Yoong P, Cywes-Bentley C, Pier GB. Poly-N-acetylglucosamine expression by wild-type Yersinia pestis is maximal at mammalian, not flea, temperatures. MBio. 2012;3(4):e00217–00212.
  • Kelly-Quintos C, Cavacini LA, Posner MR, et al. Characterization of the opsonic and protective activity against Staphylococcus aureus of fully human monoclonal antibodies specific for the bacterial surface polysaccharide poly-N-acetylglucosamine. Infect Immun. 2006;74(5):2742–2750.
  • Cerca N, Maira-Litrán T, Jefferson KK, et al. Protection against Escherichia coli infection by antibody to the Staphylococcus aureus poly-N-acetylglucosamine surface polysaccharide. Proc Natl Acad Sci USA. 2007;104(18):7528–7533.
  • Kaplan JB, Velliyagounder K, Ragunath C, et al. Genes involved in the synthesis and degradation of matrix polysaccharide in Actinobacillus actinomycetemcomitans and Actinobacillus pleuropneumoniae biofilms. J Bacteriol. 2004;186(24):8213–8220.
  • Ramasubbu N, Thomas LM, Ragunath C, et al. Structural analysis of Dispersin B, a biofilm-releasing glycoside hydrolase from the periodontopathogen Actinobacillus actinomycetemcomitans. J Mol Biol. 2005;349(3):475–486.
  • Skurnik D, Kropec A, Roux D, et al. Natural antibodies in normal human serum inhibit Staphylococcus aureus capsular polysaccharide vaccine efficacy. Clin Infect Dis. 2012;55(9):1188–1197.
  • Skurnik D, Merighi M, Grout M, et al. Animal and human antibodies to distinct Staphylococcus aureus antigens mutually neutralize opsonic killing and protection in mice. J Clin Invest. 2010;120(9):3220–3233.
  • Grachev AA, Gerbst AG, Gening ML, et al. NMR and conformational studies of linear and cyclic oligo-(1–>6)-beta-D-glucosamines. Carbohydr Res. 2011;346(15):2499–2510.
  • Verdier I, Durand G, Bes M, et al. Identification of the capsular polysaccharides in Staphylococcus aureus clinical isolates by PCR and agglutination tests. J Clin Microbiol. 2007;45(3):725–729.
  • Shinefield H, Black S, Fattom A, et al. Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N Engl J Med. 2002;346(7):491–496.
  • Daum RS, Spellberg B. Progress toward a Staphylococcus aureus vaccine. Clin Infect Dis. 2012;54(4):560–567.
  • Kojima Y, Tojo M, Goldmann DA, et al. Antibody to the capsular polysaccharide/adhesin protects rabbits against catheter-related bacteremia due to coagulase-negative staphylococci. J Infect Dis. 1990;162(2):435–441.
  • Takeda S, Pier GB, Kojima Y, et al. Protection against endocarditis due to Staphylococcus epidermidis by immunization with capsular polysaccharide/adhesin. Circulation. 1991;84(6):2539–2546.
  • Farrell PM, Collins J, Broderick LS, et al. Association between mucoid Pseudomonas infection and bronchiectasis in children with cystic fibrosis. Radiology. 2009;252(2):534–543.
  • Li Z, Kosorok MR, Farrell PM, et al. Longitudinal development of mucoid Pseudomonas aeruginosa infection and lung disease progression in children with cystic fibrosis. Jama. 2005;293(5):581–588.
  • Lu X, Skurnik D, Pozzi C, et al. A poly-N-acetylglucosamine-Shiga toxin broad-spectrum conjugate vaccine for Shiga toxin-producing Escherichia coli. Mbio. 2014;5(2):e00974-00914-e00974-00914.
  • Wallis R, Mitchell DA, Schmid R, et al. Paths reunited: Initiation of the classical and lectin pathways of complement activation. Immunobiol. 2010;215(1):1–11.
  • Brouwer N, Dolman KM, Van Houdt M, et al. Mannose-binding lectin (MBL) facilitates opsonophagocytosis of yeasts but not of bacteria despite MBL binding. J Immunol. 4124-4132;180(6):2008.
  • Garrett WS, Lord GM, Punit S, et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell. 2007;131(1):33–45.
  • Perez MM, Prenafeta A, Valle J, et al. Protection from Staphylococcus aureus mastitis associated with poly-N-acetyl beta-1,6 glucosamine specific antibody production using biofilm-embedded bacteria. Vaccine. 2009;27(17):2379–2386.
  • Cerca N, Jefferson KK, Maira-Litran T, et al. Molecular basis for preferential protective efficacy of antibodies directed to the poorly acetylated form of staphylococcal poly-N-acetyl-beta-(1-6)-glucosamine. Infect Immun. 2007;75(7):3406–3413.
  • Lukacova M, Barak I, Kazar J. Role of structural variations of polysaccharide antigens in the pathogenicity of Gram-negative bacteria. Clin Microbiol Infect. 2008;14(3):200–206.
  • Samuel G, Reeves P. Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr Res. 2503-2519;338(23):2003.
  • Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem. 2006;75:39–68.
  • Nordmann P, Cuzon G, Naas T. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet. 2009;9(4):228–236.
  • Poirel L, Pitout JD, Nordmann P. Carbapenemases: molecular diversity and clinical consequences. Future Microbiol. 2007;2(5):501–512.
  • Rasheed JK, Kitchel B, Zhu W, et al. New Delhi metallo-beta-lactamase-producing Enterobacteriaceae, United States. Emerg Infect Dis. 2013;19(6):870–878.
  • Darton TC, Blohmke CJ, Moorthy VS, et al. Design, recruitment, and microbiological considerations in human challenge studies. Lancet. 2015;15(7):840–851.
  • Hobbs MM, Sparling PF, Cohen MS, et al. Experimental gonococcal infection in male volunteers: cumulative experience with Neisseria gonorrhoeae strains FA1090 and MS11mkC. Front Microbiol. 2011;2:123.
  • Laurens MB, Billingsley P, Richman A, et al. Successful human infection with P. falciparum using three aseptic Anopheles stephensi mosquitoes: A new model for controlled human malaria infection. Plos One. 2013;8(7):e68969.
  • Labandeira-Rey M, Dodd D, Fortney KR, et al. A Haemophilus ducreyi CpxR deletion mutant is virulent in human volunteers. J Infect Dis. 2011;203(12):1859–1865.
  • Pollard AJ, Savulescu J, Oxford J, et al. Human microbial challenge: the ultimate animal model. Lancet. 2012;12(12):903–905.
  • Waddington CS, Darton TC, Jones C, et al. An outpatient, ambulant-design, controlled human infection model using escalating doses of Salmonella typhi challenge delivered in sodium bicarbonate solution. Clin Infect Dis. 2014;58(9):1230–1240.
  • Little DJ, Bamford NC, Pokrovskaya V, et al. Structural basis for the de-N-acetylation of poly-beta-1,6-N-acetyl-D-glucosamine in Gram-positive bacteria. J Biol Chem. 2014;289(52):35907–35917.
  • Little DJ, Li G, Ing C, et al. Modification and periplasmic translocation of the biofilm exopolysaccharide poly-beta-1,6-N-acetyl-D-glucosamine. Proc Natl Acad Sci USA. 2014;111(30):11013–11018.
  • Nissen M, Marshall H, Richmond P, et al. A randomized phase I study of the safety and immunogenicity of three ascending dose levels of a 3-antigen Staphylococcus aureus vaccine (SA3Ag) in healthy adults. Vaccine. 2015;33(15):1846–1854.
  • Lattar SM, Noto Llana M, Denoel P, et al. Protein antigens increase the protective efficacy of a capsule-based vaccine against Staphylococcus aureus in a rat model of osteomyelitis. Infect Immun. 2014;82(1):83–91.
  • Taylor A, Foo SS, Bruzzone R, et al. Fc receptors in antibody-dependent enhancement of viral infections. Immunol Rev. 2015;268(1):340–364.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.