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Pneumococcal interactions with epithelial cells are crucial for optimal biofilm formation and colonization in vitro and in vivo

Marks, Laura R; Parameswaran, G Iyer and Hakansson, Anders P LU (2012) In Infection and Immunity 80(8). p.60-2744
Abstract

The human nasopharynx is the main reservoir for Streptococcus pneumoniae (the pneumococcus) and the source for both horizontal spread and transition to infection. Some clinical evidence indicates that nasopharyngeal carriage is harder to eradicate with antibiotics than is pneumococcal invasive disease, which may suggest that colonizing pneumococci exist in biofilm communities that are more resistant to antibiotics. While pneumococcal biofilms have been observed during symptomatic infection, their role in colonization and the role of host factors in this process have been less studied. Here, we show for the first time that pneumococci form highly structured biofilm communities during colonization of the murine nasopharynx that display... (More)

The human nasopharynx is the main reservoir for Streptococcus pneumoniae (the pneumococcus) and the source for both horizontal spread and transition to infection. Some clinical evidence indicates that nasopharyngeal carriage is harder to eradicate with antibiotics than is pneumococcal invasive disease, which may suggest that colonizing pneumococci exist in biofilm communities that are more resistant to antibiotics. While pneumococcal biofilms have been observed during symptomatic infection, their role in colonization and the role of host factors in this process have been less studied. Here, we show for the first time that pneumococci form highly structured biofilm communities during colonization of the murine nasopharynx that display increased antibiotic resistance. Furthermore, pneumococcal biofilms grown on respiratory epithelial cells exhibited phenotypes similar to those observed during colonization in vivo, whereas abiotic surfaces produced less ordered and more antibiotic-sensitive biofilms. The importance of bacterial-epithelial cell interactions during biofilm formation was shown using both clinical strains with variable colonization efficacies and pneumococcal mutants with impaired colonization characteristics in vivo. In both cases, the ability of strains to form biofilms on epithelial cells directly correlated with their ability to colonize the nasopharynx in vivo, with colonization-deficient strains forming less structured and more antibiotic-sensitive biofilms on epithelial cells, an association that was lost when grown on abiotic surfaces. Thus, these studies emphasize the importance of host-bacterial interactions in pneumococcal biofilm formation and provide the first experimental data to explain the high resistance of pneumococcal colonization to eradication by antibiotics.

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author
organization
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type
Contribution to journal
publication status
published
subject
keywords
Animals, Anti-Bacterial Agents, Bacterial Adhesion, Biofilms, Biomass, Carrier State, Cell Line, Tumor, Cells, Cultured, Drug Resistance, Bacterial, Epithelial Cells, Female, Humans, Mice, Mice, Inbred BALB C, Microscopy, Electron, Scanning, Nasopharynx, Pneumococcal Infections, Respiratory Mucosa, Streptococcus pneumoniae
in
Infection and Immunity
volume
80
issue
8
pages
17 pages
publisher
American Society for Microbiology
external identifiers
  • scopus:84864569507
ISSN
1098-5522
DOI
10.1128/IAI.00488-12
language
English
LU publication?
yes
id
7b4be066-920e-4043-a78e-91b5b700b09f
date added to LUP
2016-05-21 10:50:05
date last changed
2017-07-23 05:14:41
@article{7b4be066-920e-4043-a78e-91b5b700b09f,
  abstract     = {<p>The human nasopharynx is the main reservoir for Streptococcus pneumoniae (the pneumococcus) and the source for both horizontal spread and transition to infection. Some clinical evidence indicates that nasopharyngeal carriage is harder to eradicate with antibiotics than is pneumococcal invasive disease, which may suggest that colonizing pneumococci exist in biofilm communities that are more resistant to antibiotics. While pneumococcal biofilms have been observed during symptomatic infection, their role in colonization and the role of host factors in this process have been less studied. Here, we show for the first time that pneumococci form highly structured biofilm communities during colonization of the murine nasopharynx that display increased antibiotic resistance. Furthermore, pneumococcal biofilms grown on respiratory epithelial cells exhibited phenotypes similar to those observed during colonization in vivo, whereas abiotic surfaces produced less ordered and more antibiotic-sensitive biofilms. The importance of bacterial-epithelial cell interactions during biofilm formation was shown using both clinical strains with variable colonization efficacies and pneumococcal mutants with impaired colonization characteristics in vivo. In both cases, the ability of strains to form biofilms on epithelial cells directly correlated with their ability to colonize the nasopharynx in vivo, with colonization-deficient strains forming less structured and more antibiotic-sensitive biofilms on epithelial cells, an association that was lost when grown on abiotic surfaces. Thus, these studies emphasize the importance of host-bacterial interactions in pneumococcal biofilm formation and provide the first experimental data to explain the high resistance of pneumococcal colonization to eradication by antibiotics.</p>},
  author       = {Marks, Laura R and Parameswaran, G Iyer and Hakansson, Anders P},
  issn         = {1098-5522},
  keyword      = {Animals,Anti-Bacterial Agents,Bacterial Adhesion,Biofilms,Biomass,Carrier State,Cell Line, Tumor,Cells, Cultured,Drug Resistance, Bacterial,Epithelial Cells,Female,Humans,Mice,Mice, Inbred BALB C,Microscopy, Electron, Scanning,Nasopharynx,Pneumococcal Infections,Respiratory Mucosa,Streptococcus pneumoniae},
  language     = {eng},
  number       = {8},
  pages        = {60--2744},
  publisher    = {American Society for Microbiology},
  series       = {Infection and Immunity},
  title        = {Pneumococcal interactions with epithelial cells are crucial for optimal biofilm formation and colonization in vitro and in vivo},
  url          = {http://dx.doi.org/10.1128/IAI.00488-12},
  volume       = {80},
  year         = {2012},
}