Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.

Phagocytosis is a key process of the immune system. The human pathogen Klebsiella pneumoniae is a well known example of a pathogen highly resistant to phagocytosis. A wealth of evidence demonstrates that the capsule polysaccharide (CPS) plays a crucial role in resistance to phagocytosis. The amoeba...

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Autores principales: Catalina March, Victoria Cano, David Moranta, Enrique Llobet, Camino Pérez-Gutiérrez, Juan M Tomás, Teresa Suárez, Junkal Garmendia, José A Bengoechea
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spelling oai:doaj.org-article:1a97845a55a84df99050fe0bfb9818772021-11-18T07:57:16ZRole of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.1932-620310.1371/journal.pone.0056847https://doaj.org/article/1a97845a55a84df99050fe0bfb9818772013-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23457627/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203Phagocytosis is a key process of the immune system. The human pathogen Klebsiella pneumoniae is a well known example of a pathogen highly resistant to phagocytosis. A wealth of evidence demonstrates that the capsule polysaccharide (CPS) plays a crucial role in resistance to phagocytosis. The amoeba Dictyostelium discoideum shares with mammalian macrophages the ability to phagocytose and kill bacteria. The fact that K. pneumoniae is ubiquitous in nature and, therefore, should avoid predation by amoebae, poses the question whether K. pneumoniae employs similar means to counteract amoebae and mammalian phagocytes. Here we developed an assay to evaluate K. pneumoniae-D. discoideum interaction. The richness of the growth medium affected the threshold at which the cps mutant was permissive for Dictyostelium and only at lower nutrient concentrations the cps mutant was susceptible to predation by amoebae. Given the critical role of bacterial surface elements on host-pathogen interactions, we explored the possible contribution of the lipopolysaccharide (LPS) and outer membrane proteins (OMPs) to combat phagoyctosis by D. discoideum. We uncover that, in addition to the CPS, the LPS O-polysaccharide and the first core sugar participate in Klebsiella resistance to predation by D. discoideum. K. pneumoniae LPS lipid A decorations are also necessary to avoid predation by amoebae although PagP-dependent palmitoylation plays a more important role than the lipid A modification with aminoarabinose. Mutants lacking OMPs OmpA or OmpK36 were also permissive for D. discoideium growth. Except the LPS O-polysaccharide mutants, all mutants were more susceptible to phagocytosis by mouse alveolar macrophages. Finally, we found a correlation between virulence, using the pneumonia mouse model, and resistance to phagocytosis. Altogether, this work reveals novel K. pneumoniae determinants involved in resistance to phagocytosis and supports the notion that Dictyostelium amoebae might be useful as host model to measure K. pneumoniae virulence and not only phagocytosis.Catalina MarchVictoria CanoDavid MorantaEnrique LlobetCamino Pérez-GutiérrezJuan M TomásTeresa SuárezJunkal GarmendiaJosé A BengoecheaPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 8, Iss 2, p e56847 (2013)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Catalina March
Victoria Cano
David Moranta
Enrique Llobet
Camino Pérez-Gutiérrez
Juan M Tomás
Teresa Suárez
Junkal Garmendia
José A Bengoechea
Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.
description Phagocytosis is a key process of the immune system. The human pathogen Klebsiella pneumoniae is a well known example of a pathogen highly resistant to phagocytosis. A wealth of evidence demonstrates that the capsule polysaccharide (CPS) plays a crucial role in resistance to phagocytosis. The amoeba Dictyostelium discoideum shares with mammalian macrophages the ability to phagocytose and kill bacteria. The fact that K. pneumoniae is ubiquitous in nature and, therefore, should avoid predation by amoebae, poses the question whether K. pneumoniae employs similar means to counteract amoebae and mammalian phagocytes. Here we developed an assay to evaluate K. pneumoniae-D. discoideum interaction. The richness of the growth medium affected the threshold at which the cps mutant was permissive for Dictyostelium and only at lower nutrient concentrations the cps mutant was susceptible to predation by amoebae. Given the critical role of bacterial surface elements on host-pathogen interactions, we explored the possible contribution of the lipopolysaccharide (LPS) and outer membrane proteins (OMPs) to combat phagoyctosis by D. discoideum. We uncover that, in addition to the CPS, the LPS O-polysaccharide and the first core sugar participate in Klebsiella resistance to predation by D. discoideum. K. pneumoniae LPS lipid A decorations are also necessary to avoid predation by amoebae although PagP-dependent palmitoylation plays a more important role than the lipid A modification with aminoarabinose. Mutants lacking OMPs OmpA or OmpK36 were also permissive for D. discoideium growth. Except the LPS O-polysaccharide mutants, all mutants were more susceptible to phagocytosis by mouse alveolar macrophages. Finally, we found a correlation between virulence, using the pneumonia mouse model, and resistance to phagocytosis. Altogether, this work reveals novel K. pneumoniae determinants involved in resistance to phagocytosis and supports the notion that Dictyostelium amoebae might be useful as host model to measure K. pneumoniae virulence and not only phagocytosis.
format article
author Catalina March
Victoria Cano
David Moranta
Enrique Llobet
Camino Pérez-Gutiérrez
Juan M Tomás
Teresa Suárez
Junkal Garmendia
José A Bengoechea
author_facet Catalina March
Victoria Cano
David Moranta
Enrique Llobet
Camino Pérez-Gutiérrez
Juan M Tomás
Teresa Suárez
Junkal Garmendia
José A Bengoechea
author_sort Catalina March
title Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.
title_short Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.
title_full Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.
title_fullStr Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.
title_full_unstemmed Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes.
title_sort role of bacterial surface structures on the interaction of klebsiella pneumoniae with phagocytes.
publisher Public Library of Science (PLoS)
publishDate 2013
url https://doaj.org/article/1a97845a55a84df99050fe0bfb981877
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