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Title: Membrane insertion for the detection of lipopolysaccharides: Exploring the dynamics of amphiphile-in-lipid assays

Abstract

Shiga toxin-producing Escherichia coli is an important cause of foodborne illness, with cases attributable to beef, fresh produce and other sources. Many serotypes of the pathogen cause disease, and differentiating one serotype from another requires specific identification of the O antigen located on the lipopolysaccharide (LPS) molecule. The amphiphilic structure of LPS poses a challenge when using classical detection methods, which do not take into account its lipoglycan biochemistry. Typically, detection of LPS requires heat or chemical treatment of samples and relies on bioactivity assays for the conserved lipid A portion of the molecule. Our goal was to develop assays to facilitate the direct and discriminative detection of the entire LPS molecule and its O antigen in complex matrices using minimal sample processing. To perform serogroup identification of LPS, we used a method called membrane insertion on a waveguide biosensor, and tested three serogroups of LPS. The membrane insertion technique allows for the hydrophobic association of LPS with a lipid bilayer, where the exposed O antigen can be targeted for specific detection. Samples of beef lysate were spiked with LPS to perform O antigen specific detection of LPS from E. coli O157. To validate assay performance, we evaluated the biophysicalmore » interactions of LPS with lipid bilayers both in- and outside of a flow cell using fluorescence microscopy and fluorescently doped lipids. Our results indicate that membrane insertion allows for the qualitative and reliable identification of amphiphilic LPS in complex samples like beef homogenates. In addition, we also demonstrated that LPS-induced hole formation does not occur under the conditions of the membrane insertion assays. Together, these findings describe for the first time the serogroup-specific detection of amphiphilic LPS in complex samples using a membrane insertion assay, and highlight the importance of LPS molecular conformations in detection architectures.« less

Authors:
 [1];  [2];  [2];  [3];  [4];  [2];  [1];  [5]
+ Show Author Affiliations
  1. Univ. of New Mexico, Albuquerque, NM (United States); Los Alamos National Lab. (LANL), Los Alamos, NM (United States); The New Mexico Consortium, Los Alamos, NM (United States)
  2. Los Alamos National Lab. (LANL), Los Alamos, NM (United States)
  3. Univ. of Nebraska-Lincoln, Lincoln, NE (United States)
  4. Univ. of New Mexico, Albuquerque, NM (United States); The New Mexico Consortium, Los Alamos, NM (United States)
  5. Consejo Superior de Investigaciones Cientificas (Spain)
Publication Date:
Research Org.:
Los Alamos National Laboratory (LANL), Los Alamos, NM (United States); Energy Frontier Research Centers (EFRC) (United States). Photosynthetic Antenna Research Center (PARC)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1321771
Report Number(s):
LA-UR-15-29061
Journal ID: ISSN 1932-6203
Grant/Contract Number:  
AC52-06NA25396; SC0001035
Resource Type:
Accepted Manuscript
Journal Name:
PLoS ONE
Additional Journal Information:
Journal Volume: 11; Journal Issue: 5; Journal ID: ISSN 1932-6203
Publisher:
Public Library of Science
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; biological science; lipopolysaccharide; amphiphile; waveguide; membrane insertion; membrane dynamics; beef; lipid bilayer; lipids; fluorescence imaging; lipid signaling; laboratory glassware; biomarkers; endotoxins

Citation Formats

Stromberg, Loreen R., Hengartner, Nicolas W., Swingle, Kirstie L., Moxley, Rodney A., Graves, Steven W., Montano, Gabriel A., Mukundan, Harshini, and Gasset, Maria. Membrane insertion for the detection of lipopolysaccharides: Exploring the dynamics of amphiphile-in-lipid assays. United States: N. p., 2016. Web. doi:10.1371/journal.pone.0156295.
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Stromberg, Loreen R., Hengartner, Nicolas W., Swingle, Kirstie L., Moxley, Rodney A., Graves, Steven W., Montano, Gabriel A., Mukundan, Harshini, & Gasset, Maria. Membrane insertion for the detection of lipopolysaccharides: Exploring the dynamics of amphiphile-in-lipid assays. United States. https://doi.org/10.1371/journal.pone.0156295
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Stromberg, Loreen R., Hengartner, Nicolas W., Swingle, Kirstie L., Moxley, Rodney A., Graves, Steven W., Montano, Gabriel A., Mukundan, Harshini, and Gasset, Maria. Thu . "Membrane insertion for the detection of lipopolysaccharides: Exploring the dynamics of amphiphile-in-lipid assays". United States. https://doi.org/10.1371/journal.pone.0156295. https://www.osti.gov/servlets/purl/1321771.
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@article{osti_1321771,
title = {Membrane insertion for the detection of lipopolysaccharides: Exploring the dynamics of amphiphile-in-lipid assays},
author = {Stromberg, Loreen R. and Hengartner, Nicolas W. and Swingle, Kirstie L. and Moxley, Rodney A. and Graves, Steven W. and Montano, Gabriel A. and Mukundan, Harshini and Gasset, Maria},
abstractNote = {Shiga toxin-producing Escherichia coli is an important cause of foodborne illness, with cases attributable to beef, fresh produce and other sources. Many serotypes of the pathogen cause disease, and differentiating one serotype from another requires specific identification of the O antigen located on the lipopolysaccharide (LPS) molecule. The amphiphilic structure of LPS poses a challenge when using classical detection methods, which do not take into account its lipoglycan biochemistry. Typically, detection of LPS requires heat or chemical treatment of samples and relies on bioactivity assays for the conserved lipid A portion of the molecule. Our goal was to develop assays to facilitate the direct and discriminative detection of the entire LPS molecule and its O antigen in complex matrices using minimal sample processing. To perform serogroup identification of LPS, we used a method called membrane insertion on a waveguide biosensor, and tested three serogroups of LPS. The membrane insertion technique allows for the hydrophobic association of LPS with a lipid bilayer, where the exposed O antigen can be targeted for specific detection. Samples of beef lysate were spiked with LPS to perform O antigen specific detection of LPS from E. coli O157. To validate assay performance, we evaluated the biophysical interactions of LPS with lipid bilayers both in- and outside of a flow cell using fluorescence microscopy and fluorescently doped lipids. Our results indicate that membrane insertion allows for the qualitative and reliable identification of amphiphilic LPS in complex samples like beef homogenates. In addition, we also demonstrated that LPS-induced hole formation does not occur under the conditions of the membrane insertion assays. Together, these findings describe for the first time the serogroup-specific detection of amphiphilic LPS in complex samples using a membrane insertion assay, and highlight the importance of LPS molecular conformations in detection architectures.},
doi = {10.1371/journal.pone.0156295},
journal = {PLoS ONE},
number = 5,
volume = 11,
place = {United States},
year = {Thu May 26 00:00:00 EDT 2016},
month = {Thu May 26 00:00:00 EDT 2016}
}
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https://doi.org/10.1371/journal.pone.0156295
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Spontaneous insertion of lipopolysaccharide into lipid membranes from aqueous solution
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Bacterial endotoxins: extraordinary lipids that activate eucaryotic signal transduction.
journal, September 1993

Aggregation behavior and size of lipopolysaccharide from Escherichia coli O55:B5
journal, November 2006

The immunopathogenesis of sepsis
journal, December 2002

Development and evaluation of an enzyme-linked immunosorbent assay for endotoxin in milk
journal, September 1988

Purification and characterization of lipopolysaccharides from six strains of non-O157 Shiga toxin-producing Escherichia coli
journal, September 2015

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In vivo protection against endotoxin by plasma high density lipoprotein.
journal, December 1993

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Structural Requirements of Lipid a for Endotoxicity and Other Biological Activities
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Structure and function of lipopolysaccharides
journal, July 2002

Short-range interactions between lipid bilayers measured by X-ray diffraction
journal, August 2000

Shiga toxin-producing Escherichia coli: An overview1
journal, March 2007

Microcantilever array biosensors for detection and recognition of Gram-negative bacterial endotoxins
journal, July 2014

  • Nieradka, Konrad; Kapczyńska, Katarzyna; Rybka, Jacek
  • Sensors and Actuators B: Chemical, Vol. 198
  • DOI: 10.1016/j.snb.2014.03.023

Spontaneous insertion of lipopolysaccharide into lipid membranes from aqueous solution
journal, February 2011

Lipopolysaccharide Identification with Functionalized Polydiacetylene Liposome Sensors
journal, April 2004

  • Rangin, Marianne; Basu, Amit
  • Journal of the American Chemical Society, Vol. 126, Issue 16
  • DOI: 10.1021/ja039822x

Optimizing a Waveguide-Based Sandwich Immunoassay for Tumor Biomarkers: Evaluating Fluorescent Labels and Functional Surfaces
journal, February 2009

  • Mukundan, Harshini; Xie, Hongzhi; Anderson, Aaron S.
  • Bioconjugate Chemistry, Vol. 20, Issue 2, p. 222-230
  • DOI: 10.1021/bc800283e

Exploiting lipopolysaccharide-induced deformation of lipid bilayers to modify membrane composition and generate two-dimensional geometric membrane array patterns
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Planar optical waveguide-based biosensor for the quantitative detection of tumor markers
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  • Sensors and Actuators B: Chemical, Vol. 138, Issue 2
  • DOI: 10.1016/j.snb.2009.01.073

Detection of stealthy small amphiphilic biomarkers
journal, August 2014

  • Sakamuri, Rama Murthy; Capek, Petr; Dickerson, Tobin J.
  • Journal of Microbiological Methods, Vol. 103
  • DOI: 10.1016/j.mimet.2014.05.012

Understanding the interaction of Lipoarabinomannan with membrane mimetic architectures
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Rapid Estimation of Microbial Numbers in Fresh Ground Beef by Use of the Limulus Test
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Novel optical strategies for biodetection
conference, September 2013

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Pathogen detection using single mode planar optical waveguides
journal, January 2005

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  • Journal of Materials Chemistry, Vol. 15, Issue 43, p. 4639-4647
  • DOI: 10.1039/b502329g

Recognition of pathogen-associated molecular patterns by TLR family
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Methods of Endotoxin Detection
journal, August 2015

Quantitative Multiplex Detection of Pathogen Biomarkers on Multichannel Waveguides
journal, January 2010

  • Mukundan, Harshini; Xie, Hongzhi; Price, Dominique
  • Analytical Chemistry, Vol. 82, Issue 1
  • DOI: 10.1021/ac901497g

A mutant of Escherichia coli defective in the first step of endotoxin biosynthesis.
journal, April 1990

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    Works referencing / citing this record:

    Developing and Deploying Universal Diagnostic Platforms for One-Health Biosurveillance
    journal, May 2018

    Detection of Lipid and Amphiphilic Biomarkers for Disease Diagnostics
    journal, July 2017

    • Kubicek-Sutherland, Jessica; Vu, Dung; Mendez, Heather
    • Biosensors, Vol. 7, Issue 4
    • DOI: 10.3390/bios7030025

    Direct detection of bacteremia by exploiting host-pathogen interactions of lipoteichoic acid and lipopolysaccharide
    journal, April 2019

    • Kubicek-Sutherland, Jessica Z.; Vu, Dung M.; Noormohamed, Aneesa
    • Scientific Reports, Vol. 9, Issue 1
    • DOI: 10.1038/s41598-019-42502-5

    Direct detection of bacteremia by exploiting host-pathogen interactions of lipoteichoic acid and lipopolysaccharide
    journal, April 2019

    • Kubicek-Sutherland, Jessica Z.; Vu, Dung M.; Noormohamed, Aneesa
    • Scientific Reports, Vol. 9, Issue 1
    • DOI: 10.1038/s41598-019-42502-5
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