Lipopolysaccharide structure impacts the entry kinetics of bacterial outer membrane vesicles into host cells
Outer membrane vesicles are nano-sized microvesicles shed from the outer membrane of Gram-negative bacteria and play important roles in immune priming and disease pathogenesis. However, our current mechanistic understanding of vesicle-host cell interactions is limited by a lack of methods to study t...
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| Published in | PLoS pathogens Vol. 13; no. 11; p. e1006760 |
|---|---|
| Main Authors | , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.11.2017
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Outer membrane vesicles are nano-sized microvesicles shed from the outer membrane of Gram-negative bacteria and play important roles in immune priming and disease pathogenesis. However, our current mechanistic understanding of vesicle-host cell interactions is limited by a lack of methods to study the rapid kinetics of vesicle entry and cargo delivery to host cells. Here, we describe a highly sensitive method to study the kinetics of vesicle entry into host cells in real-time using a genetically encoded, vesicle-targeted probe. We found that the route of vesicular uptake, and thus entry kinetics and efficiency, are shaped by bacterial cell wall composition. The presence of lipopolysaccharide O antigen enables vesicles to bypass clathrin-mediated endocytosis, which enhances both their entry rate and efficiency into host cells. Collectively, our findings highlight the composition of the bacterial cell wall as a major determinant of secretion-independent delivery of virulence factors during Gram-negative infections. |
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| AbstractList | Outer membrane vesicles are nano-sized microvesicles shed from the outer membrane of Gram-negative bacteria and play important roles in immune priming and disease pathogenesis. However, our current mechanistic understanding of vesicle-host cell interactions is limited by a lack of methods to study the rapid kinetics of vesicle entry and cargo delivery to host cells. Here, we describe a highly sensitive method to study the kinetics of vesicle entry into host cells in real-time using a genetically encoded, vesicle-targeted probe. We found that the route of vesicular uptake, and thus entry kinetics and efficiency, are shaped by bacterial cell wall composition. The presence of lipopolysaccharide O antigen enables vesicles to bypass clathrin-mediated endocytosis, which enhances both their entry rate and efficiency into host cells. Collectively, our findings highlight the composition of the bacterial cell wall as a major determinant of secretion-independent delivery of virulence factors during Gram-negative infections. Outer membrane vesicles are nano-sized microvesicles shed from the outer membrane of Gram-negative bacteria and play important roles in immune priming and disease pathogenesis. However, our current mechanistic understanding of vesicle-host cell interactions is limited by a lack of methods to study the rapid kinetics of vesicle entry and cargo delivery to host cells. Here, we describe a highly sensitive method to study the kinetics of vesicle entry into host cells in real-time using a genetically encoded, vesicle-targeted probe. We found that the route of vesicular uptake, and thus entry kinetics and efficiency, are shaped by bacterial cell wall composition. The presence of lipopolysaccharide O antigen enables vesicles to bypass clathrin-mediated endocytosis, which enhances both their entry rate and efficiency into host cells. Collectively, our findings highlight the composition of the bacterial cell wall as a major determinant of secretion-independent delivery of virulence factors during Gram-negative infections. All Gram negative species of bacteria, including those that cause significant disease, release small vesicles from their cell membrane. These vesicles deliver toxins and other virulence factors to host cells during infection. Current methods for studying host cell entry are limited due to the nanometer size and rapid uptake kinetics of vesicles. Here we developed a method to monitor the rapid vesicle entry into host cells in real-time. This method highlighted differences in kinetics and entry route of vesicles into host cells, which varied with the bacterial cell wall composition and thus, the vesicle surface. Increased understanding of vesicular entry mechanisms could identify targets which may allow us to combat infections by inhibiting delivery of vesicle-associated toxins to host cells. |
| Author | O'Donoghue, Eloise J Browning, Douglas F Alderwick, Luke Bielska, Ewa Hadis, Mohammed Jabbari, Sara Fernandez-Trillo, Francisco Krachler, Anne Marie Sirisaengtaksin, Natalie |
| AuthorAffiliation | The University of Texas at Austin, UNITED STATES 4 School of Mathematics, University of Birmingham, Edgbaston, Birmingham, United Kingdom 2 Department of Microbiology and Molecular Genetics, University of Texas McGovern Medical School at Houston, Houston, Texas, United States of America 1 Institute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom 3 Institute of Microbiology and Infection, School of Chemistry, University of Birmingham, Edgbaston, Birmingham, United Kingdom |
| AuthorAffiliation_xml | – name: 1 Institute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom – name: 2 Department of Microbiology and Molecular Genetics, University of Texas McGovern Medical School at Houston, Houston, Texas, United States of America – name: 3 Institute of Microbiology and Infection, School of Chemistry, University of Birmingham, Edgbaston, Birmingham, United Kingdom – name: The University of Texas at Austin, UNITED STATES – name: 4 School of Mathematics, University of Birmingham, Edgbaston, Birmingham, United Kingdom |
| Author_xml | – sequence: 1 givenname: Eloise J orcidid: 0000-0002-3991-1165 surname: O'Donoghue fullname: O'Donoghue, Eloise J organization: Institute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom – sequence: 2 givenname: Natalie orcidid: 0000-0002-8791-722X surname: Sirisaengtaksin fullname: Sirisaengtaksin, Natalie organization: Department of Microbiology and Molecular Genetics, University of Texas McGovern Medical School at Houston, Houston, Texas, United States of America – sequence: 3 givenname: Douglas F orcidid: 0000-0003-4672-3514 surname: Browning fullname: Browning, Douglas F organization: Institute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom – sequence: 4 givenname: Ewa orcidid: 0000-0002-3138-4719 surname: Bielska fullname: Bielska, Ewa organization: Institute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom – sequence: 5 givenname: Mohammed surname: Hadis fullname: Hadis, Mohammed organization: Institute of Microbiology and Infection, School of Chemistry, University of Birmingham, Edgbaston, Birmingham, United Kingdom – sequence: 6 givenname: Francisco orcidid: 0000-0002-6680-5683 surname: Fernandez-Trillo fullname: Fernandez-Trillo, Francisco organization: Institute of Microbiology and Infection, School of Chemistry, University of Birmingham, Edgbaston, Birmingham, United Kingdom – sequence: 7 givenname: Luke surname: Alderwick fullname: Alderwick, Luke organization: Institute of Microbiology and Infection, School of Biosciences, University of Birmingham, Edgbaston, Birmingham, United Kingdom – sequence: 8 givenname: Sara orcidid: 0000-0001-5235-0406 surname: Jabbari fullname: Jabbari, Sara organization: School of Mathematics, University of Birmingham, Edgbaston, Birmingham, United Kingdom – sequence: 9 givenname: Anne Marie orcidid: 0000-0002-0936-0016 surname: Krachler fullname: Krachler, Anne Marie organization: Department of Microbiology and Molecular Genetics, University of Texas McGovern Medical School at Houston, Houston, Texas, United States of America |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/29186191$$D View this record in MEDLINE/PubMed |
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| Copyright | 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: O’Donoghue EJ, Sirisaengtaksin N, Browning DF, Bielska E, Hadis M, Fernandez-Trillo F, et al. (2017) Lipopolysaccharide structure impacts the entry kinetics of bacterial outer membrane vesicles into host cells. PLoS Pathog 13(11): e1006760. https://doi.org/10.1371/journal.ppat.1006760 2017 O’Donoghue et al 2017 O’Donoghue et al 2017 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: O’Donoghue EJ, Sirisaengtaksin N, Browning DF, Bielska E, Hadis M, Fernandez-Trillo F, et al. (2017) Lipopolysaccharide structure impacts the entry kinetics of bacterial outer membrane vesicles into host cells. PLoS Pathog 13(11): e1006760. https://doi.org/10.1371/journal.ppat.1006760 |
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| SubjectTerms | Antigens Bacteria Bacterial infections Bacterial vesicles Biology and Life Sciences Cell interactions Cell Wall - chemistry Cell Wall - metabolism Cell walls Clathrin Coding E coli Endocytosis Escherichia coli Funding Genetic code Gram-negative bacteria Gram-Negative Bacteria - chemistry Gram-Negative Bacteria - metabolism Gram-Negative Bacterial Infections - metabolism Gram-Negative Bacterial Infections - microbiology Host-Pathogen Interactions Humans Infections Kinetics Lipopolysaccharides Lipopolysaccharides - chemistry Lipopolysaccharides - metabolism Medicine and Health Sciences Membrane vesicles Methods O antigen Pathogenesis Priming Research and Analysis Methods Salmonella Toxins Transport Vesicles - metabolism Transport Vesicles - microbiology Vesicles Virulence Virulence factors Virulence Factors - metabolism |
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| Title | Lipopolysaccharide structure impacts the entry kinetics of bacterial outer membrane vesicles into host cells |
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