Structural insight into host recognition by aggregative adherence fimbriae of enteroaggregative Escherichia coli.
Enteroaggregative Escherichia coli (EAEC) is a leading cause of acute and persistent diarrhea worldwide. A recently emerged Shiga-toxin-producing strain of EAEC resulted in significant mortality and morbidity due to progressive development of hemolytic-uremic syndrome. The attachment of EAEC to the...
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2014
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oai:doaj.org-article:2fd6baa77f094eb08a903919a04007e92021-11-25T05:46:02ZStructural insight into host recognition by aggregative adherence fimbriae of enteroaggregative Escherichia coli.1553-73661553-737410.1371/journal.ppat.1004404https://doaj.org/article/2fd6baa77f094eb08a903919a04007e92014-09-01T00:00:00Zhttps://doi.org/10.1371/journal.ppat.1004404https://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Enteroaggregative Escherichia coli (EAEC) is a leading cause of acute and persistent diarrhea worldwide. A recently emerged Shiga-toxin-producing strain of EAEC resulted in significant mortality and morbidity due to progressive development of hemolytic-uremic syndrome. The attachment of EAEC to the human intestinal mucosa is mediated by aggregative adherence fimbria (AAF). Using X-ray crystallography and NMR structures, we present new atomic resolution insight into the structure of AAF variant I from the strain that caused the deadly outbreak in Germany in 2011, and AAF variant II from archetype strain 042, and propose a mechanism for AAF-mediated adhesion and biofilm formation. Our work shows that major subunits of AAF assemble into linear polymers by donor strand complementation where a single minor subunit is inserted at the tip of the polymer by accepting the donor strand from the terminal major subunit. Whereas the minor subunits of AAF have a distinct conserved structure, AAF major subunits display large structural differences, affecting the overall pilus architecture. These structures suggest a mechanism for AAF-mediated adhesion and biofilm formation. Binding experiments using wild type and mutant subunits (NMR and SPR) and bacteria (ELISA) revealed that despite the structural differences AAF recognize a common receptor, fibronectin, by employing clusters of basic residues at the junction between subunits in the pilus. We show that AAF-fibronectin attachment is based primarily on electrostatic interactions, a mechanism not reported previously for bacterial adhesion to biotic surfaces.Andrea A BerryYi YangNatalia PakharukovaJames A GarnettWei-chao LeeErnesto CotaJan MarchantSaumendra RoyMinna TuittilaBing LiuKeith G InmanFernando Ruiz-PerezInacio MandomandoJames P NataroAnton V ZavialovSteve MatthewsPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 10, Iss 9, p e1004404 (2014) |
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| topic |
Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 |
| spellingShingle |
Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Andrea A Berry Yi Yang Natalia Pakharukova James A Garnett Wei-chao Lee Ernesto Cota Jan Marchant Saumendra Roy Minna Tuittila Bing Liu Keith G Inman Fernando Ruiz-Perez Inacio Mandomando James P Nataro Anton V Zavialov Steve Matthews Structural insight into host recognition by aggregative adherence fimbriae of enteroaggregative Escherichia coli. |
| description |
Enteroaggregative Escherichia coli (EAEC) is a leading cause of acute and persistent diarrhea worldwide. A recently emerged Shiga-toxin-producing strain of EAEC resulted in significant mortality and morbidity due to progressive development of hemolytic-uremic syndrome. The attachment of EAEC to the human intestinal mucosa is mediated by aggregative adherence fimbria (AAF). Using X-ray crystallography and NMR structures, we present new atomic resolution insight into the structure of AAF variant I from the strain that caused the deadly outbreak in Germany in 2011, and AAF variant II from archetype strain 042, and propose a mechanism for AAF-mediated adhesion and biofilm formation. Our work shows that major subunits of AAF assemble into linear polymers by donor strand complementation where a single minor subunit is inserted at the tip of the polymer by accepting the donor strand from the terminal major subunit. Whereas the minor subunits of AAF have a distinct conserved structure, AAF major subunits display large structural differences, affecting the overall pilus architecture. These structures suggest a mechanism for AAF-mediated adhesion and biofilm formation. Binding experiments using wild type and mutant subunits (NMR and SPR) and bacteria (ELISA) revealed that despite the structural differences AAF recognize a common receptor, fibronectin, by employing clusters of basic residues at the junction between subunits in the pilus. We show that AAF-fibronectin attachment is based primarily on electrostatic interactions, a mechanism not reported previously for bacterial adhesion to biotic surfaces. |
| format |
article |
| author |
Andrea A Berry Yi Yang Natalia Pakharukova James A Garnett Wei-chao Lee Ernesto Cota Jan Marchant Saumendra Roy Minna Tuittila Bing Liu Keith G Inman Fernando Ruiz-Perez Inacio Mandomando James P Nataro Anton V Zavialov Steve Matthews |
| author_facet |
Andrea A Berry Yi Yang Natalia Pakharukova James A Garnett Wei-chao Lee Ernesto Cota Jan Marchant Saumendra Roy Minna Tuittila Bing Liu Keith G Inman Fernando Ruiz-Perez Inacio Mandomando James P Nataro Anton V Zavialov Steve Matthews |
| author_sort |
Andrea A Berry |
| title |
Structural insight into host recognition by aggregative adherence fimbriae of enteroaggregative Escherichia coli. |
| title_short |
Structural insight into host recognition by aggregative adherence fimbriae of enteroaggregative Escherichia coli. |
| title_full |
Structural insight into host recognition by aggregative adherence fimbriae of enteroaggregative Escherichia coli. |
| title_fullStr |
Structural insight into host recognition by aggregative adherence fimbriae of enteroaggregative Escherichia coli. |
| title_full_unstemmed |
Structural insight into host recognition by aggregative adherence fimbriae of enteroaggregative Escherichia coli. |
| title_sort |
structural insight into host recognition by aggregative adherence fimbriae of enteroaggregative escherichia coli. |
| publisher |
Public Library of Science (PLoS) |
| publishDate |
2014 |
| url |
https://doaj.org/article/2fd6baa77f094eb08a903919a04007e9 |
| work_keys_str_mv |
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| _version_ |
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