Staphylococcus epidermidis uses distinct mechanisms of biofilm formation to interfere with phagocytosis and activation of mouse macrophage-like cells 774A.1.

TY - JOUR

T1 - Staphylococcus epidermidis uses distinct mechanisms of biofilm formation to interfere with phagocytosis and activation of mouse macrophage-like cells 774A.1.

AU - Schommer, Nina

AU - Christner, Martin

AU - Hentschke, Moritz

AU - Ruckdeschel, Klaus

AU - Aepfelbacher, Martin

AU - Rohde, Holger

PY - 2011

Y1 - 2011

N2 - Assembly of adherent biofilms is the key mechanism involved in Staphylococcus epidermidis virulence during device-associated infections. Aside from polysaccharide intercellular adhesin (PIA), the accumulation-associated protein Aap and the extracellular matrix binding protein Embp act as intercellular adhesins, mediating S. epidermidis cell aggregation and biofilm accumulation. The aim of this study was to investigate structural features of PIA-, Aap-, and Embp-mediated S. epidermidis biofilms in more detail and to evaluate their specific contributions to biofilm-related S. epidermidis immune escape. PIA-, Embp-, and Aap-mediated biofilms exhibited substantial morphological differences. Basically, PIA synthesis induced formation of macroscopically visible, rough cell clusters, whereas Aap- and Embp-dependent biofilms preferentially displayed a smooth layer of aggregated bacteria. On the microscopic level, PIA was found to form a string-like organized extracellular matrix connecting the bacteria, while Embp produced small deposits of intercellular matrix and Aap was strictly localized to the bacterial surface. Despite marked differences, S. epidermidis strains using PIA, Aap, or Embp for biofilm formation were protected from uptake by J774A.1 macrophages, with similarly efficiencies. In addition, compared to biofilm-negative S. epidermidis strains, isogenic biofilm-forming S. epidermidis induced only a diminished inflammatory J774A.1 macrophage response, leading to significantly (88.2 to 88.7%) reduced NF-?B activation and 68.8 to 83% reduced interleukin-1? (IL-1?) production. Mechanical biofilm dispersal partially restored induction of NF-?B activation, although bacterial cell surfaces remained decorated with the respective intercellular adhesins. Our results demonstrate that distinct S. epidermidis biofilm morphotypes are similarly effective at protecting S. epidermidis from phagocytic uptake and at counteracting macrophage activation, providing novel insights into mechanisms that could contribute to the chronic and persistent course of biofilm-related S. epidermidis foreign material infections.

AB - Assembly of adherent biofilms is the key mechanism involved in Staphylococcus epidermidis virulence during device-associated infections. Aside from polysaccharide intercellular adhesin (PIA), the accumulation-associated protein Aap and the extracellular matrix binding protein Embp act as intercellular adhesins, mediating S. epidermidis cell aggregation and biofilm accumulation. The aim of this study was to investigate structural features of PIA-, Aap-, and Embp-mediated S. epidermidis biofilms in more detail and to evaluate their specific contributions to biofilm-related S. epidermidis immune escape. PIA-, Embp-, and Aap-mediated biofilms exhibited substantial morphological differences. Basically, PIA synthesis induced formation of macroscopically visible, rough cell clusters, whereas Aap- and Embp-dependent biofilms preferentially displayed a smooth layer of aggregated bacteria. On the microscopic level, PIA was found to form a string-like organized extracellular matrix connecting the bacteria, while Embp produced small deposits of intercellular matrix and Aap was strictly localized to the bacterial surface. Despite marked differences, S. epidermidis strains using PIA, Aap, or Embp for biofilm formation were protected from uptake by J774A.1 macrophages, with similarly efficiencies. In addition, compared to biofilm-negative S. epidermidis strains, isogenic biofilm-forming S. epidermidis induced only a diminished inflammatory J774A.1 macrophage response, leading to significantly (88.2 to 88.7%) reduced NF-?B activation and 68.8 to 83% reduced interleukin-1? (IL-1?) production. Mechanical biofilm dispersal partially restored induction of NF-?B activation, although bacterial cell surfaces remained decorated with the respective intercellular adhesins. Our results demonstrate that distinct S. epidermidis biofilm morphotypes are similarly effective at protecting S. epidermidis from phagocytic uptake and at counteracting macrophage activation, providing novel insights into mechanisms that could contribute to the chronic and persistent course of biofilm-related S. epidermidis foreign material infections.

KW - Animals

KW - Cells, Cultured

KW - Mice

KW - Enzyme-Linked Immunosorbent Assay

KW - Fluorescent Antibody Technique

KW - Microscopy, Confocal

KW - NF-kappa B/metabolism

KW - Adhesins, Bacterial/physiology

KW - Biofilms/growth & development

KW - Interleukin-1beta/metabolism

KW - Macrophage Activation/immunology

KW - Macrophages/immunology

KW - Phagocytosis/immunology

KW - Staphylococcal Infections/immunology/microbiology

KW - Staphylococcus epidermidis/immunology/physiology

KW - Animals

KW - Cells, Cultured

KW - Mice

KW - Enzyme-Linked Immunosorbent Assay

KW - Fluorescent Antibody Technique

KW - Microscopy, Confocal

KW - NF-kappa B/metabolism

KW - Adhesins, Bacterial/physiology

KW - Biofilms/growth & development

KW - Interleukin-1beta/metabolism

KW - Macrophage Activation/immunology

KW - Macrophages/immunology

KW - Phagocytosis/immunology

KW - Staphylococcal Infections/immunology/microbiology

KW - Staphylococcus epidermidis/immunology/physiology

M3 - SCORING: Journal article

VL - 79

SP - 2267

EP - 2276

JO - INFECT IMMUN

JF - INFECT IMMUN

SN - 0019-9567

IS - 6

M1 - 6

ER -