Intradermal Immunization with Wall Teichoic Acid (WTA) Elicits and Augments an Anti-WTA IgG Response that Protects Mice from Methicillin-Resistant Staphylococcus aureus Infection Independent of Mannose-Binding Lectin Status

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Takahashi, Kazue ^a   Kurokawa, Kenji ^b   Moyo, Patience ^a   Jung, Dong Jun ^b   An, Jang Hyun ^b   Chigweshe, Lorencia ^a   Paul, Elahna ^a   Lee, Bok Luel ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b Pusan National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VACCINE; COMPLEMENT COMPONENT C4; COMPLEMENT COMPONENT C4C; IMMUNOGLOBULIN G ANTIBODY; MANNOSE BINDING LECTIN; UNCLASSIFIED DRUG; WALL TEICHOIC ACID;

ABSCESS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL GROWTH; BACTERIAL STRAIN; COMMUNITY ASSOCIATED METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; COMPLEMENT ACTIVATION; CONTROLLED STUDY; GROWTH INHIBITION; HEALTHCARE ASSOCIATED METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; IMMUNOPROPHYLAXIS; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; INFECTION RESISTANCE; INFECTION SENSITIVITY; KNOCKOUT MOUSE; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; METHICILLIN SUSCEPTIBLE STAPHYLOCOCCUS AUREUS; MOUSE; NONHUMAN; WILD TYPE;

ANIMALS; ANTIBODIES, ANTI-IDIOTYPIC; CELL WALL; COMPLEMENT ACTIVATION; FEMALE; IMMUNIZATION; IMMUNOGLOBULIN G; INJECTIONS, INTRADERMAL; MANNOSE-BINDING LECTIN; MANNOSE-BINDING LECTINS; METABOLISM, INBORN ERRORS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; STAPHYLOCOCCAL INFECTIONS; TEICHOIC ACIDS;

EID: 84880977020     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069739     Document Type: Article

References (46)

1. Lowy FD, (1998) Staphylococcus aureus infections. N Engl J Med 339: 520-532.
2. Cosgrove SE, Qi Y, Kaye KS, Harbarth S, Karchmer AW, et al. (2005) The impact of methicillin resistance in Staphylococcus aureus bacteremia on patient outcomes: mortality, length of stay, and hospital charges. [see comment]. Infection Control & Hospital Epidemiology 26: 166-174.
3. Creech CB 2nd, Kernodle DS, Alsentzer A, Wilson C, Edwards KM, (2005) Increasing rates of nasal carriage of methicillin-resistant Staphylococcus aureus in healthy children. Pediatric Infectious Disease Journal 24: 617-621.
4. Weidenmaier C, Peschel A, (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat Rev Microbiol 6: 276-287.
5. Navarre WW, Schneewind O, (1999) Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol Mol Biol Rev 63: 174-229.
6. Swoboda JG, Campbell J, Meredith TC, Walker S, (2010) Wall teichoic acid function, biosynthesis, and inhibition. Chembiochem 11: 35-45.
7. Weidenmaier C, Peschel A, Xiong YQ, Kristian SA, Dietz K, et al. (2005) Lack of wall teichoic acids in Staphylococcus aureus leads to reduced interactions with endothelial cells and to attenuated virulence in a rabbit model of endocarditis. J Infect Dis 191: 1771-1777.
8. Kohler T, Weidenmaier C, Peschel A, (2009) Wall teichoic acid protects Staphylococcus aureus against antimicrobial fatty acids from human skin. J Bacteriol 191: 4482-4484.
9. Weidenmaier C, Kokai-Kun JF, Kristian SA, Chanturiya T, Kalbacher H, et al. (2004) Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. [see comment]. Nature Medicine 10: 243-245.
10. Weidenmaier C, McLoughlin RM, Lee JC, (2010) The zwitterionic cell wall teichoic acid of Staphylococcus aureus provokes skin abscesses in mice by a novel CD4+ T-cell-dependent mechanism. PLoS One 5: e13227.
11. Takahashi K, Ip WE, Michelow IC, Ezekowitz RA, (2006) The mannose-binding lectin: a prototypic pattern recognition molecule. Curr Opin Immunol 18: 16-23.
12. Shi L, Takahashi K, Dundee J, Shahroor-Karni S, Thiel S, et al. (2004) Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J Exp Med 199: 1379-1390.
13. Eisen DP, Dean MM, Boermeester MA, Fidler KJ, Gordon AC, et al. (2008) Low serum mannose-binding lectin level increases the risk of death due to pneumococcal infection. Clin Infect Dis 47: 510-516.
14. Smithson A, Perello R, Horcajada JP, Nicolas JM, Lozano F, (2008) Is mannose-binding lectin deficiency associated with infection due to Gram-positive bacteria? Clin Infect Dis 47: 1492-1493; author reply 1493.
15. Takahashi K, Ezekowitz RA, (2005) The role of the mannose-binding lectin in innate immunity. Clin Infect Dis 41 (Suppl 7):: S440-444.
16. Baldwin SL, Bertholet S, Kahn M, Zharkikh I, Ireton GC, et al. (2009) Intradermal immunization improves protective efficacy of a novel TB vaccine candidate. Vaccine 27: 3063-3071.
17. Firbas C, Boehm T, Buerger V, Schuller E, Sabarth N, et al. (2010) Immunogenicity and safety of different injection routes and schedules of IC41, a Hepatitis C virus (HCV) peptide vaccine. Vaccine 28: 2397-2407.
18. Mohanan D, Slutter B, Henriksen-Lacey M, Jiskoot W, Bouwstra JA, et al. (2010) Administration routes affect the quality of immune responses: A cross-sectional evaluation of particulate antigen-delivery systems. J Control Release 147: 342-349.
19. Romani N, Thurnher M, Idoyaga J, Steinman RM, Flacher V, (2010) Targeting of antigens to skin dendritic cells: possibilities to enhance vaccine efficacy. Immunol Cell Biol 88: 424-430.
20. Kurokawa K, Lee H, Roh KB, Asanuma M, Kim YS, et al. (2009) The Triacylated ATP Binding Cluster Transporter Substrate-binding Lipoprotein of Staphylococcus aureus Functions as a Native Ligand for Toll-like Receptor 2. J Biol Chem 284: 8406-8411.
21. Park KH, Kurokawa K, Zheng L, Jung DJ, Tateishi K, et al. (2010) Human serum mannose-binding lectin senses wall teichoic acid Glycopolymer of Staphylococcus aureus, which is restricted in infancy. J Biol Chem 285: 27167-27175.
22. Jung DJ, An JH, Kurokawa K, Jung YC, Kim MJ, et al. (2012) Specific Serum Ig Recognizing Staphylococcal Wall Teichoic Acid Induces Complement-Mediated Opsonophagocytosis against Staphylococcus aureus. J Immunol.
23. Gaikwad S, Deodhar LP, (1984) Experimental foreign body infection in mice by Staphylococcus epidermidis. J Postgrad Med 30: 229-231.
24. Bubeck Wardenburg J, Williams WA, Missiakas D, (2006) Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc Natl Acad Sci U S A 103: 13831-13836.
25. Park JW, Kim CH, Kim JH, Je BR, Roh KB, et al. (2007) Clustering of peptidoglycan recognition protein-SA is required for sensing lysine-type peptidoglycan in insects. Proc Natl Acad Sci U S A 104: 6602-6607.
26. Moller-Kristensen M, Hamblin MR, Thiel S, Jensenius JC, Takahashi K, (2007) Burn injury reveals altered phenotype in mannan-binding lectin-deficient mice. J Invest Dermatol 127: 1524-1531.
27. Guttormsen HK, Stuart LM, Shi L, Carroll MC, Chen J, et al. (2009) Deficiency of mannose-binding lectin greatly increases antibody response in a mouse model of vaccination. Clin Immunol 130: 264-271.
28. Ruseva M, Kolev M, Dagnaes-Hansen F, Hansen SB, Takahashi K, et al. (2009) Mannan-binding lectin deficiency modulates the humoral immune response dependent on the genetic environment. Immunology 127: 279-288.
29. Chang WC, Hartshorn KL, White MR, Moyo P, Michelow IC, et al. (2011) Recombinant chimeric lectins consisting of mannose-binding lectin and L-ficolin are potent inhibitors of influenza A virus compared with mannose-binding lectin. Biochem Pharmacol 81: 388-395.
30. Berek C, Berger A, Apel M, (1991) Maturation of the immune response in germinal centers. Cell 67: 1121-1129.
31. Stein KE, (1992) Thymus-independent and thymus-dependent responses to polysaccharide antigens. J Infect Dis 165 (Suppl 1):: S49-52.
32. Schmaler M, Jann NJ, Ferracin F, Landolt LZ, Biswas L, et al. (2009) Lipoproteins in Staphylococcus aureus mediate inflammation by TLR2 and iron-dependent growth in vivo. J Immunol 182: 7110-7118.
33. Ip WK, Takahashi K, Moore KJ, Stuart LM, Ezekowitz RA, (2008) Mannose-binding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome. J Exp Med 205: 169-181.
34. Romani N, Flacher V, Tripp CH, Sparber F, Ebner S, et al. (2012) Targeting skin dendritic cells to improve intradermal vaccination. Curr Top Microbiol Immunol 351: 113-138.
35. Teunissen MB, Haniffa M, Collin MP, (2012) Insight into the immunobiology of human skin and functional specialization of skin dendritic cell subsets to innovate intradermal vaccination design. Curr Top Microbiol Immunol 351: 25-76.
36. Combadiere B, Liard C, (2011) Transcutaneous and intradermal vaccination. Hum Vaccin 7: 811-827.
37. Hoal-Van Helden EG, Epstein J, Victor TC, Hon D, Lewis LA, et al. (1999) Mannose-binding protein B allele confers protection against tuberculous meningitis. Pediatr Res 45: 459-464.
38. Santos IK, Costa CH, Krieger H, Feitosa MF, Zurakowski D, et al. (2001) Mannan-binding lectin enhances susceptibility to visceral leishmaniasis. Infect Immun 69: 5212-5215.
39. Turner MW, (2003) The role of mannose-binding lectin in health and disease. Mol Immunol 40: 423-429.
40. Edwards AM, Potts JR, Josefsson E, Massey RC, (2010) Staphylococcus aureus host cell invasion and virulence in sepsis is facilitated by the multiple repeats within FnBPA. PLoS Pathog 6: e1000964.
41. Edwards AM, Massey RC, (2011) How does Staphylococcus aureus escape the bloodstream? Trends Microbiol 19: 184-190.
42. Howden BP, Davies JK, Johnson PD, Stinear TP, Grayson ML, (2010) Reduced vancomycin susceptibility in Staphylococcus aureus, including vancomycin-intermediate and heterogeneous vancomycin-intermediate strains: resistance mechanisms, laboratory detection, and clinical implications. Clin Microbiol Rev 23: 99-139.
43. Ding Y, Onodera Y, Lee JC, Hooper DC, (2008) NorB, an efflux pump in Staphylococcus aureus strain MW2, contributes to bacterial fitness in abscesses. J Bacteriol 190: 7123-7129.
44. Ehlert K, (1999) Methicillin-resistance in Staphylococcus aureus- molecular basis, novel targets and antibiotic therapy. Curr Pharm Des 5: 45-55.
45. Trotonda MP, Xiong YQ, Memmi G, Bayer AS, Cheung AL, (2009) Role of mgrA and sarA in methicillin-resistant Staphylococcus aureus autolysis and resistance to cell wall-active antibiotics. J Infect Dis 199: 209-218.
46. Gill SR, Fouts DE, Archer GL, Mongodin EF, Deboy RT, et al. (2005) Insights on evolution of virulence and resistance from the complete genome analysis of an early methicillin-resistant Staphylococcus aureus strain and a biofilm-producing methicillin-resistant Staphylococcus epidermidis strain. J Bacteriol 187: 2426-2438.