Staphylococcus aureus surface attachment selectively influences tolerance against charged antibiotics
Andrew HaylesRichard BrightNgoc Huu NguyenVi Khanh TruongJitraporn VongsvivutJonathan WoodStephen P. KiddKrasimir Vasilev
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Abstract:
The threat of infection during implant placement surgery remains a considerable burden for millions of patients worldwide. To combat this threat, clinicians employ a range of anti-infective strategies and practices. One of the most common interventions is the use of prophylactic antibiotic treatment during implant placement surgery. However, these practices can be detrimental by promoting the resilience of biofilm-forming bacteria and enabling them to persist throughout treatment and re-emerge later, causing a life-threatening infection. Thus, it is of the utmost importance to elucidate the events occurring during the initial stages of bacterial surface attachment and determine whether any biological processes may be targeted to improve surgical outcomes. Using gene expression analysis, we identified a cellular mechanism of S. aureus which modifies its cell surface charge following attachment to a medical grade titanium surface. We determined the upregulation of two systems involved in the D-alanylation of teichoic acids and the lysylation of phosphatidylglycerol. We supported these molecular findings by utilizing synchrotron-sourced attenuated total reflection Fourier-transform infrared microspectroscopy to analyze the biomolecular properties of the S. aureus cell surface following attachment. As a direct consequence, S. aureus quickly becomes substantially more tolerant to the positively charged vancomycin, but not the negatively charged cefazolin. The present study can assist clinicians in rationally selecting the most potent antibiotic in prophylaxis treatments. Furthermore, it highlights a cellular process that could potentially be targeted by novel technologies and strategies to improve the outcome of antibiotic prophylaxis during implant placement surgery. The antibiotic tolerance of bacteria in biofilm is a well-established phenomenon. However, the physiological adaptations employed by Staphylococcus aureus to increase its antibiotic tolerance during the early stages of surface attachment are poorly understood. Using multiple techniques, including gene expression analysis and synchrotron-sourced Fourier-transform infrared microspectroscopy, we generated insights into the physiological response of S. aureus following attachment to a medical grade titanium surface. We showed that this phenotypic transition enables S. aureus to better tolerate the positively charged vancomycin, but not the negatively charged cefazolin. These findings shed light on the antibiotic tolerance mechanisms employed by S. aureus to survive prophylactically administered antibiotics and can help clinicians to protect patients from infections.Keywords:
Cefazolin
Teichoic acid
The effect of teichoic acid from Staphylococcus aureus Wood 46 on DC maturation in vitro was investigated. It was shown that treatment of immature DC with teichoic acid resulted in increasing of DC maturation. Treated with teichoic acid DC demonstrated the high level of HLA-DR and CD80, CD86 markers expression. Treatment of immature DC with 2 mkg/ ml of teichoic acid caused increase of its ability to stimulate allogenic lym teichoic acid caused increase of its ability to stimulate allogenic lymphocyte proliferation in vitro.
Teichoic acid
Lipoteichoic acid
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Both the wall ribitol teichoic acid and the membrane glycerol teichoic acid (lipoteichoic acid) from Lactobacillus plantarum NCIB 7220 have α- d -glucosyl substituents. Antisera to the ribitol teichoic acid were obtained by injecting whole or disintegrated organisms, the antigenicity of the wall teichoic acid apparently depending on its association with protein. It was necessary to inject disintegrated organisms or purified lipoteichoic acid to ensure the production of antibodies to the glycerol teichoic acid; these antibodies did not react with ribitol teichoic acid. The specificity of antibodies to the wall ribitol teichoic acid depends primarily on the α- d -glucosyl substituents, as the antibodies cross-react with α- d -glucosyl-substituted glycerol teichoic acids but not with an unsubstituted ribitol teichoic acid. The specificity of antibodies to the membrane glycerol teichoic acid may be directed against either the glucose or glycerol components, depending on the preparation injected.
Teichoic acid
Ribitol
Lipoteichoic acid
Antigenicity
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An enzyme-linked immunosorbent assay was used to evaluate the immunoglobulin G (IgG) response to Staphylococcus aureus crude teichoic acid (TA) and peptidoglycan (PG) in both rabbits and patients with osteomyelitis. In rabbits with experimental S. aureus osteomyelitis, elevated levels of IgG to TA were present in 13/18 (72%) of the serum samples obtained at 4 and 10 weeks postinfection. In contrast, only 5/18 (28%) of these sera were found to be positive for antibodies to PG. Of a total of 39 patients with confirmed S. aureus osteomyelitis (11 acute, 28 chronic), IgG to TA was elevated in 17 (44%), whereas antibodies to PG were found to be increased in only 1 (3%). Cross-reacting antibodies to S. aureus TA were detected in only 1/18 (6%) of the patients with osteomyelitis caused by organisms other than S. aureus. These studies indicate that IgG to TA is more prevalent than IgG to PG in patients with staphylococcal osteomyelitis. Although these results are encouraging, a larger number of patients is required for an adequate evaluation of the TA enzyme-linked immunosorbent assay for the diagnosis and management of suspected S. aureus osteomyelitis.
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Human sera were found to contain antibodies precipitating with each of two samples of teichoic acid of Staphylococcus aureus prior to immunization; these antibodies were probably formed as a result of contact or infection with this microorganism. Injection of teichoic acid into two individuals resulted in a rise in circulating antibody to teichoic acid; a third subject probably had a primary response to alpha-teichoic acid. Quantitative precipitin and agar diffusion studies revealed the presence of two distinct antibodies in the sera and showed that each specimen of teichoic acid was a mixture of two polymers an alpha-linked N-acetylglucosaminyl-ribitol polymer and a beta-linked N-acetylglucosaminyl-ribitol polymer, termed alpha- and beta-teichoic acids respectively. The alpha-teichoic acid anti-alpha-teichoic acid system was inhibited best by alpha-linked glucosaminides and the beta-anti-beta-teichoic acid system was inhibited best by a beta-linked glucosaminide. The alpha- and (beta-teichoic acids could be separated from each other by specific precipitation under appropriate conditions and recovered from the washed specific precipitates. The existence of two distinct teichoic acid polymers raises important questions as to cell wall structure and the biosynthesis of the teichoic acids.
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Precipitin
Lipoteichoic acid
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Teichoic acid
Gram-Positive Bacteria
Cell envelope
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The molecular interactions between staphylococcal phages and host cell surfaces are poorly understood. Employing Staphylococcus aureus teichoic acid mutants, we demonstrate that wall teichoic acid (WTA), but not lipoteichoic acid, serves as a receptor for staphylococcal siphovirus and myovirus, while only the siphovirus requires glycosylated WTA.
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Lipoteichoic acid
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Summary: Both wall and membrane teichoic acids from Lactobacillus helveticus ncib8025 are glycerol phosphate polymers partially substituted with α-d-glucosyl residues. The membrane teichoic acid, isolated as a complex with lipid (lipoteichoic acid), was antigenic when injected into rabbits with Freund’s adjuvant. The α-d-glucosyl substituents are primarily responsible for the serological specificity of the membrane antigen, and account for the reaction of wall teichoic acid with antisera to the membrane teichoic acid. Glycerol teichoic acids either differing in or lacking sugar substitution may cross-react and the significance of these observations is discussed.
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Lipoteichoic acid
Lactobacillus helveticus
Sugar phosphates
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The distribution of a pulse of teichoic acid-specific radiolabel between wall and membrane teichoic acids in pneumococci was constant over a subsequent chase period, suggesting that wall and membrane teichoic acids are biosynthesized simultaneously and independently.
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Lipoteichoic acid
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Teichoic acid
Chemical structure
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SUMMARY: The walls and cell contents of a number of lactobacilli were prepared by mechanical disruption of the organisms followed by differential centrifugation. The nature of the teichoic acid present in the separated fractions was determined by extracting it with dilute trichloroacetic acid, precipitating with ethanol and identifying the precipitated polymer by hydrolysis to ribitol or glycerol phosphates and other recognizable degradation products. All the organisms contained a glycerol teichoic acid within the cell. This and similar observations with other bacteria indicates that glycerol teichoic acids play an important part in cellular metabolism. Both glycerol and ribitol teichoic acids occur in walls. The presence and type of teichoic acid in the walls correlate with the serological behaviour of lactobacilli and provide a useful means of classification. It is suggested that teichoic acids themselves may possess antigenic properties.
Teichoic acid
Ribitol
Muramic acid
Trichloroacetic acid
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