Opsonic and Protective Properties of Antibodies Raised to Conjugate Vaccines Targeting Six Staphylococcus aureus Antigens

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Pozzi, Clarissa ^a   Wilk, Katarzyna ^a   Lee, Jean C ^a   Gening, Marina ^b   Nifantiev, Nikolay ^b   Pier, Gerald B ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b N D ZELINSKY INSTITUTE OF ORGANIC CHEMISTRY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BACTERIAL ANTIGEN; CAPSULAR POLYSACCHARIDE TYPE 5 CLUMPING FACTOR B VACCINE; CAPSULAR POLYSACCHARIDE TYPE 8 IRON SURFACE DETERMINANT B VACCINE; GLUCOSAMINE ALPHA HEMOLYSIN VACCINE; STAPHYLOCOCCUS VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL LOAD; BACTERICIDAL ACTIVITY; CONTROLLED STUDY; DRUG CONJUGATION; IMMUNITY; IN VITRO STUDY; MOUSE; NONHUMAN; OPSONIC KILLING ACTIVITY; SKIN ABSCESS; STAPHYLOCOCCAL PNEUMONIA; STAPHYLOCOCCUS AUREUS;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, BACTERIAL; BACTERIAL ADHESION; BACTERIAL VACCINES; BASE SEQUENCE; DNA PRIMERS; ENZYME-LINKED IMMUNOSORBENT ASSAY; MICE; NOSE; STAPHYLOCOCCUS AUREUS;

EID: 84867546402     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0046648     Document Type: Article

References (68)

1. Kluytmans J, Struelens M, (2009) Methicillin resistant Staphylococcus aureus in the hospital. BMJ 338: b364.
2. Gerber J, Coffin S, Smathers S, Zaoutis T, (2009) Trends in the incidence of methicillin resistant Staphylococcus aureus infection in children's hospitals in the United States. Clin Infect Dis 49: 65-71.
3. Shinefield H, Black S, Fattom A, Horwith G, Rasgon S, et al. (2002) Use of a Staphylococcus aureus conjugate vaccine in patients receiving hemodialysis. N Engl J Med 346: 491-496.
4. Kuklin NA, Clark DJ, Secore S, Cook J, Cope LD, et al. (2006) A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model. Infect Immun 74: 2215-2223.
5. Harro C, Betts R, Orenstein W, Kwak EJ, Greenberg HE, et al. (2010) Safety and Immunogenicity of a Novel Staphylococcus aureus Vaccine: Results from a First-in-Human Dose-Ranging Study. Clin Vaccine Immunol 17: 1868-1874.
6. DeJonge M, Burchfield D, Bloom B, Duenas M, Walker W, et al. (2007) Clinical trial of safety and efficacy of INH-A21 for the prevention of nosocomial staphylococcal bloodstream infection in premature infants. J Pediatr 151: 260-265.
7. Proctor RA, (2012) Challenges for a universal Staphylococcus aureus vaccine. Clin Infect Dis 54: 1179-1186.
8. Verkaik NJ, van Wamel WJ, van Belkum A, (2011) Immunotherapeutic approaches against Staphylococcus aureus. Immunotherapy 3: 1063-1073.
9. McKenney D, Pouliot KL, Wang Y, Murthy V, Ulrich M, et al. (1999) Broadly protective vaccine for Staphylococcus aureus based on an in vivo-expressed antigen. Science 284: 1523-1527.
10. Maira-Litran T, Kropec A, Goldmann DA, Pier GB, (2005) Comparative opsonic and protective activities of Staphylococcus aureus conjugate vaccines containing native or deacetylated staphylococcal poly-N-acetyl-β-(1-6)-glucosamine. Infect Immun 73: 6752-6762.
11. Cerca N, Maira-Litran T, Jefferson KK, Grout M, Goldmann DA, et al. (2007) Protection against Escherichia coli infection by antibody to the Staphylococcus aureus poly-N-acetylglucosamine surface polysaccharide. Proc Natl Acad Sci U S A 104: 7528-7533.
12. Choi AHK, Slamti L, Avci FY, Pier GB, Maira-Litrán T, (2009) The pgaABCD locus of Acinetobacter baumannii encodes the production of poly-β-1-6-N-acetyl glucosamine which is critical for biofilm formation. J Bacteriol 191: 5953-5963.
13. Skurnik D, Davis MR Jr, Benedetti D, Moravec KL, Cywes-Bentley C, et al. (2012) Targeting pan-resistant bacteria with antibodies to a broadly conserved surface polysaccharide expressed during infection. J Infect Dis 205: 1709-1718.
14. Kelly-Quintos C, Cavacini LA, Posner MR, Goldmann D, Pier GB, (2006) 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 74: 2742-2750.
15. Skurnik D, Merighi M, Grout M, Gadjeva M, Maira-Litran T, et al. (2010) Animal and human antibodies to distinct Staphylococcus aureus antigens mutually neutralize opsonic killing and protection in mice. J Clin Invest 9: 3220-3233.
16. Schaffer AC, Solinga RM, Cocchiaro J, Portoles M, Kiser KB, et al. (2006) Immunization with Staphylococcus aureus clumping factor B, a major determinant in nasal carriage, reduces nasal colonization in a murine model. Infect Immun 74: 2145-2153.
17. Stranger-Jones YK, Bae T, Schneewind O, (2006) Vaccine assembly from surface proteins of Staphylococcus aureus. Proc Natl Acad Sci U S A 103: 16942-16947.
18. Josefsson E, Hartford O, O'Brien L, Patti JM, Foster T, (2001) Protection against experimental Staphylococcus aureus arthritis by vaccination with clumping factor A, a novel virulence determinant. J Infect Dis 184: 1572-1580.
19. Menzies BE, Kernodle DS, (1994) Site-directed mutagenesis of the alpha-toxin gene of Staphylococcus aureus: role of histidines in toxin activity in vitro and in a murine model. Infect Immun 62: 1843-1847.
20. Menzies BE, Kernodle DS, (1996) Passive immunization with antiserum to a nontoxic alpha-toxin mutant from Staphylococcus aureus is protective in a murine model. Infect Immun 64: 1839-1841.
21. Wardenburg JB, Schneewind O, (2008) Vaccine protection against Staphylococcus aureus pneumonia. J Exp Med 205: 287-294.
22. Kernodle DS, (2011) Expectations regarding vaccines and immune therapies directed against Staphylococcus aureus α-Hemolysin. J Infect Dis 203: 1692-1693.
23. Kreiswirth BN, Lofdahl S, Betley MJ, O'Reilly M, Schlievert PM, et al. (1983) The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305: 709-712.
24. Baba T, Bae T, Schneewind O, Takeuchi F, Hiramatsu K, (2008) Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands. J Bacteriol 190: 300-310.
25. Miller LG, Perdreau-Remington F, Rieg G, Mehdi S, Perlroth J, et al. (2005) Necrotizing fasciitis caused by community-associated methicillin-resistant Staphylococcus aureus in Los Angeles. N Engl J Med 352: 1445-1453.
26. Mempel M, Schmidt T, Weidinger S, Schnopp C, Foster T, et al. (1998) Role of Staphylococcus aureus surface-associated proteins in the attachment to cultured HaCaT keratinocytes in a new adhesion assay. J Invest Dermatol 111: 452-456.
27. McAleese FM, Walsh EJ, Sieprawska M, Potempa J, Foster TJ, (2001) Loss of clumping factor B fibrinogen binding activity by Staphylococcus aureus involves cessation of transcription, shedding and cleavage by metalloprotease. J Biol Chem 276: 29969-29978.
28. Mazmanian SK, Skaar EP, Gaspar AH, Humayun M, Gornicki P, et al. (2003) Passage of heme-iron across the envelope of Staphylococcus aureus. Science 299: 906-909.
29. Mazmanian SK, Ton-That H, Su K, Schneewind O, (2002) An iron-regulated sortase anchors a class of surface protein during Staphylococcus aureus pathogenesis. Proc Natl Acad Sci U S A 99: 2293-2298.
30. Sau S, Bhasin N, Wann ER, Lee JC, Foster TJ, et al. (1997) The Staphylococcus aureus allelic genetic loci for serotype 5 and 8 capsule expression contain the type-specific genes flanked by common genes. Microbiol 143: 2395-2405.
31. Lee CY, Buranen SL, Ye ZH, (1991) Construction of single-copy integration vectors for Staphylococcus aureus. Gene 103: 101-105.
32. Watts A, Ke D, Wang Q, Pillay A, Nicholson-Weller A, et al. (2005) Staphylococcus aureus strains that express serotype 5 or serotype 8 capsular polysaccharides differ in virulence. Infect Immun 73: 3502-3511.
33. Kiser KB, Cantey-Kiser JM, Lee JC, (1999) Development and characterization of a Staphylococcus aureus nasal colonization model in mice. Infect Immun 67: 5001-5006.
34. Gening ML, Maira-Litran T, Kropec A, Skurnik D, Grout M, et al. (2010) Synthetic β-(1->6)-linked N-acetylated and nonacetylated oligoglucosamines used to produce conjugate vaccines for bacterial pathogens. Infect Immun 78: 764-772.
35. Bartlett AH, Foster TJ, Hayashida A, Park PW, (2008) α-Toxin Facilitates the generation of cxc chemokine gradients and stimulates neutrophil homing in Staphylococcus aureus pneumonia. J Infect Dis 198: 1529-1535.
36. Miajlovic H, Zapotoczna M, Geoghegan JA, Kerrigan SW, Speziale P, et al. (2010) Direct interaction of iron-regulated surface determinant IsdB of Staphylococcus aureus with the GPIIb/IIIa receptor on platelets. Microbiology 156: 920-928.
37. O'Connell DP, Nanavaty T, McDevitt D, Gurusiddappa S, Hook M, et al. (1998) The fibrinogen-binding MSCRAMM (clumping factor) of Staphylococcus aureus has a Ca2+-dependent inhibitory site. J Biol Chem 273: 6821-6829.
38. Smith RL, Gilkerson E, (1979) Quantitation of glycosaminoglycan hexosamine using 3-methyl-2- benzothiazolone hydrazone hydrochloride. Anal Biochem 98: 478-480.
39. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
40. Maira-Litran T, Kropec A, Abeygunawardana C, Joyce J, Mark G 3rd, et al. (2002) Immunochemical properties of the staphylococcal poly-N-acetylglucosamine surface polysaccharide. Infect Immun 70: 4433-4440.
41. Collins SJ, Ruscetti FW, Gallagher RE, Gallo RC, (1978) Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proc Natl Acad Sci U S A 75: 2458-2462.
42. Breitman TR, Selonick SE, Collins SJ, (1980) Induction of differentiation of the human promyelocytic leukemia cell line (HL-60) by retinoic acid. Proc Natl Acad Sci U S A 77: 2936-2940.
43. Martinez JE, Romero-Steiner S, Pilishvili T, Barnard S, Schinsky J, et al. (1999) A flow cytometric opsonophagocytic assay for measurement of functional antibodies elicited after vaccination with the 23-valent pneumococcal polysaccharide vaccine. Clin Diagn Lab Immunol 6: 581-586.
44. Romero-Steiner S, Frasch C, Concepcion N, Goldblatt D, Kayhty H, et al. (2003) Multilaboratory evaluation of a viability assay for measurement of opsonophagocytic antibodies specific to the capsular polysaccharides of Streptococcus pneumoniae. Clin Diagn Lab Immunol 10: 1019-1024.
45. Romero-Steiner S, Libutti D, Pais LB, Dykes J, Anderson P, et al. (1997) Standardization of an opsonophagocytic assay for the measurement of functional antibody activity against Streptococcus pneumoniae using differentiated HL-60 cells. Clin Diagn Lab Immunol 4: 415-422.
46. Wolz C, McDevitt D, Foster TJ, Cheung AL, (1996) Influence of agr on fibrinogen binding in Staphylococcus aureus Newman. Infect Immun 64: 3142-3147.
47. Kaiser AB, Kernodle DS, Parker RA, (1992) Low-inoculum model of surgical wound infection. J Infect Dis 166: 393-399.
48. Ni Eidhin D, Perkins S, Francois P, Vaudaux P, Hook M, et al. (1998) Clumping factor B (ClfB), a new surface-located fibrinogen-binding adhesin of Staphylococcus aureus. Mol Microbiol 30: 245-257.
49. O'Riordan K, Lee JC, (2004) Staphylococcus aureus capsular polysaccharides. Clin Microbiol Rev 17: 218-234.
50. Nilsson IM, Patti JM, Bremell T, Hook M, Tarkowski A, (1998) Vaccination with a recombinant fragment of collagen adhesin provides protection against Staphylococcus aureus-mediated septic death. J Clin Invest 101: 2640-2649.
51. Hall AE, Domanski PJ, Patel PR, Vernachio JH, Syribeys PJ, et al. (2003) Characterization of a protective monoclonal antibody recognizing Staphylococcus aureus MSCRAMM protein clumping factor A. Infect Immun 71: 6864-6870.
52. Weisman LE, Thackray HM, Steinhorn RH, Walsh WF, Lassiter HA, et al. (2011) A Randomized study of a monoclonal antibody (Pagibaximab) to prevent staphylococcal sepsis. Pediatrics 128: 271-279.
53. Trotter CL, McVernon J, Ramsay ME, Whitney CG, Mulholland EK, et al. (2008) Optimising the use of conjugate vaccines to prevent disease caused by Haemophilus influenzae type b, Neisseria meningitidis and Streptococcus pneumoniae. Vaccine 26: 4434-4445.
54. Swingler G, Fransman D, Hussey G, (2003) Conjugate vaccines for preventing Haemophilus influenzae type b infections. Cochrane Database Syst Rev pp. CD001729.
55. Parise G, Mishra M, Itoh Y, Romeo T, Deora R, (2006) Role of a putative polysaccharide locus in Bordetella biofilm development. J Bacteriol 189: 750-760.
56. Sloan GP, Love CF, Sukumar N, Mishra M, Deora R, (2007) The Bordetella Bps polysaccharide is critical for biofilm development in the mouse respiratory tract. J Bacteriol 189: 8270-8276.
57. Matthysse AG, Deora R, Mishra M, Torres AG, (2008) Polysaccharides cellulose, poly-beta-1,6-n-acetyl-D-glucosamine, and colanic acid are required for optimal binding of Escherichia coli O157:H7 strains to alfalfa sprouts and K-12 strains to plastic but not for binding to epithelial cells. Appl Environ Microbiol 74: 2384-2390.
58. Erickson DL, Jarrett CO, Callison JA, Fischer ER, Hinnebusch BJ, (2008) Loss of a biofilm-inhibiting glycosyl hydrolase during the emergence of Yersinia pestis. J Bacteriol 190: 8163-8170.
59. Hinnebusch BJ, Erickson DL, (2008) Yersinia pestis biofilm in the flea vector and its role in the transmission of plague. Curr Top Microbiol Immunol 322: 229-248.
60. Avci FY, Li X, Tsuji M, Kasper DL, (2011) A mechanism for glycoconjugate vaccine activation of the adaptive immune system and its implications for vaccine design. Nat Med 17: 1602-1609.
61. Ragle BE, Bubeck Wardenburg J, (2009) Anti-alpha-hemolysin monoclonal antibodies mediate protection against Staphylococcus aureus pneumonia. Infect Immun 77: 2712-2718.
62. Kennedy AD, Bubeck Wardenburg J, Gardner DJ, Long D, Whitney AR, et al. (2010) Targeting of alpha-hemolysin by active or passive immunization decreases severity of USA300 skin infection in a mouse model. J Infect Dis 202: 1050-1058.
63. Kim HK, DeDent A, Cheng AG, McAdow M, Bagnoli F, et al. (2010) IsdA and IsdB antibodies protect mice against Staphylococcus aureus abscess formation and lethal challenge. Vaccine 28: 6382-6392.
64. Fowler VG, Allen KB, Turnbull BW, Moreira ED, Moustafa M, et al. (2012) Efficacy and safety of V710, a Staphylococcus aureus vaccine, in preventing bacteraemia and/or deep sternal wound infections in patients undergoing cardiac surgery. Abstracts of the ECMID 2012 Conference. Abstract O164.
65. Broughan J, Anderson R, Anderson AS, (2011) Strategies for and advances in the development of Staphylococcus aureus prophylactic vaccines. Expert Rev Vaccines 10: 695-708.
66. Spellberg B, Daum R, (2012) Development of a vaccine against Staphylococcus aureus. Semin Immunopathol 34: 335-348.
67. Spellberg B, Ibrahim AS, Yeaman MR, Lin L, Fu Y, et al. (2008) The antifungal vaccine derived from the recombinant N terminus of Als3p protects mice against the bacterium Staphylococcus aureus. Infect Immun 76: 4574-4580.
68. Guide SV, Stock F, Gill VJ, Anderson VL, Malech HL, et al. (2003) Reinfection, rather than persistent infection, in patients with chronic granulomatous disease. J Infect Dis 187: 845-853.