Neutrophil activation by Escherichia coli isolates from human intestine: effects of bacterial hydroperoxidase activity and surface hydrophobicity

Successful colonization of the intestine requires that bacteria interact with the innate immune system and, in particular, neutrophils. Progression of inflammatory bowel diseases (IBD) is associated with alterations in gut microbiota, and dysbiosis in Crohn’s disease (CD) patients is often associate...

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Main Authors: Mariam Moshkovskaya, Tatyana Vakhrusheva, Daria Rakitina, Julia Baykova, Oleg Panasenko, Lilia Basyreva, Sergey Gusev, Alexander Gusev, Elena Mikhalchik, Natalia Smolina, Gennadiy Dobretsov, Petr Scherbakov, Asfold Parfenov, Nina Fadeeva, Olga Pobeguts, Vadim Govorun
Format: Article
Language:English
Published: Wiley 2020-03-01
Series:FEBS Open Bio
Subjects:
Online Access:https://doi.org/10.1002/2211-5463.12796
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spelling doaj-b26383d1d4544f44b252c7e0b937492c2020-11-25T03:59:05ZengWileyFEBS Open Bio2211-54632020-03-0110341442610.1002/2211-5463.12796Neutrophil activation by Escherichia coli isolates from human intestine: effects of bacterial hydroperoxidase activity and surface hydrophobicityMariam Moshkovskaya0Tatyana Vakhrusheva1Daria Rakitina2Julia Baykova3Oleg Panasenko4Lilia Basyreva5Sergey Gusev6Alexander Gusev7Elena Mikhalchik8Natalia Smolina9Gennadiy Dobretsov10Petr Scherbakov11Asfold Parfenov12Nina Fadeeva13Olga Pobeguts14Vadim Govorun15Federal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaMoscow Clinical Scientific Center Central Scientific Institute of Gastroenterology Moscow RussiaMoscow Clinical Scientific Center Central Scientific Institute of Gastroenterology Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaFederal Research and Clinical Center of Physical‐Chemical Medicine of FMBA Moscow RussiaSuccessful colonization of the intestine requires that bacteria interact with the innate immune system and, in particular, neutrophils. Progression of inflammatory bowel diseases (IBD) is associated with alterations in gut microbiota, and dysbiosis in Crohn’s disease (CD) patients is often associated with an expansion of Escherichia coli. Here, we investigated the ability of such E. coli isolates to avoid neutrophil activation and to utilize reactive oxygen species. Neutrophil activation was detected in vitro in normal human blood via luminol chemiluminescence (CL) induced by reactive oxygen and halogen species generated by neutrophils. No significant difference in neutrophil activation in vitro was detected between isolates from inflamed (23 isolates) vs healthy intestines (5 isolates), with 10‐fold variation within both groups (2.9–61.2 mV). CL activity of isolates from the same patient differed by 1.5–5 times. Twenty‐four isolates from ileal aspirate, biopsy, and feces of seven patients with CD and one patient with no intestine inflammation were tested for extracellular peroxidase and catalase activity and cell surface hydrophobicity. Average values between patients varied from 26 ± 3 to 73 ± 18 µmol·g−1 of air dry weight for peroxidase activity, from 15 ± 2 to 189 ± 56 mmol·g−1 of air dry weight for catalase activity, and from 5 ± 3 to 105 ± 9 a.u. for the hydrophobic probe fluorescence. Extracellular peroxidase activity and hydrophobicity of bacterial cell surface correlated negatively with stimulated neutrophil CL. The ability of some isolates to avoid neutrophil activation and to utilize reactive oxygen species may provide a strategy to survive assault by the innate immune system.https://doi.org/10.1002/2211-5463.12796chemiluminescenceCrohn’s diseaseE. colifluorescent probesneutrophil activationperoxidase
collection DOAJ
language English
format Article
sources DOAJ
author Mariam Moshkovskaya
Tatyana Vakhrusheva
Daria Rakitina
Julia Baykova
Oleg Panasenko
Lilia Basyreva
Sergey Gusev
Alexander Gusev
Elena Mikhalchik
Natalia Smolina
Gennadiy Dobretsov
Petr Scherbakov
Asfold Parfenov
Nina Fadeeva
Olga Pobeguts
Vadim Govorun
spellingShingle Mariam Moshkovskaya
Tatyana Vakhrusheva
Daria Rakitina
Julia Baykova
Oleg Panasenko
Lilia Basyreva
Sergey Gusev
Alexander Gusev
Elena Mikhalchik
Natalia Smolina
Gennadiy Dobretsov
Petr Scherbakov
Asfold Parfenov
Nina Fadeeva
Olga Pobeguts
Vadim Govorun
Neutrophil activation by Escherichia coli isolates from human intestine: effects of bacterial hydroperoxidase activity and surface hydrophobicity
FEBS Open Bio
chemiluminescence
Crohn’s disease
E. coli
fluorescent probes
neutrophil activation
peroxidase
author_facet Mariam Moshkovskaya
Tatyana Vakhrusheva
Daria Rakitina
Julia Baykova
Oleg Panasenko
Lilia Basyreva
Sergey Gusev
Alexander Gusev
Elena Mikhalchik
Natalia Smolina
Gennadiy Dobretsov
Petr Scherbakov
Asfold Parfenov
Nina Fadeeva
Olga Pobeguts
Vadim Govorun
author_sort Mariam Moshkovskaya
title Neutrophil activation by Escherichia coli isolates from human intestine: effects of bacterial hydroperoxidase activity and surface hydrophobicity
title_short Neutrophil activation by Escherichia coli isolates from human intestine: effects of bacterial hydroperoxidase activity and surface hydrophobicity
title_full Neutrophil activation by Escherichia coli isolates from human intestine: effects of bacterial hydroperoxidase activity and surface hydrophobicity
title_fullStr Neutrophil activation by Escherichia coli isolates from human intestine: effects of bacterial hydroperoxidase activity and surface hydrophobicity
title_full_unstemmed Neutrophil activation by Escherichia coli isolates from human intestine: effects of bacterial hydroperoxidase activity and surface hydrophobicity
title_sort neutrophil activation by escherichia coli isolates from human intestine: effects of bacterial hydroperoxidase activity and surface hydrophobicity
publisher Wiley
series FEBS Open Bio
issn 2211-5463
publishDate 2020-03-01
description Successful colonization of the intestine requires that bacteria interact with the innate immune system and, in particular, neutrophils. Progression of inflammatory bowel diseases (IBD) is associated with alterations in gut microbiota, and dysbiosis in Crohn’s disease (CD) patients is often associated with an expansion of Escherichia coli. Here, we investigated the ability of such E. coli isolates to avoid neutrophil activation and to utilize reactive oxygen species. Neutrophil activation was detected in vitro in normal human blood via luminol chemiluminescence (CL) induced by reactive oxygen and halogen species generated by neutrophils. No significant difference in neutrophil activation in vitro was detected between isolates from inflamed (23 isolates) vs healthy intestines (5 isolates), with 10‐fold variation within both groups (2.9–61.2 mV). CL activity of isolates from the same patient differed by 1.5–5 times. Twenty‐four isolates from ileal aspirate, biopsy, and feces of seven patients with CD and one patient with no intestine inflammation were tested for extracellular peroxidase and catalase activity and cell surface hydrophobicity. Average values between patients varied from 26 ± 3 to 73 ± 18 µmol·g−1 of air dry weight for peroxidase activity, from 15 ± 2 to 189 ± 56 mmol·g−1 of air dry weight for catalase activity, and from 5 ± 3 to 105 ± 9 a.u. for the hydrophobic probe fluorescence. Extracellular peroxidase activity and hydrophobicity of bacterial cell surface correlated negatively with stimulated neutrophil CL. The ability of some isolates to avoid neutrophil activation and to utilize reactive oxygen species may provide a strategy to survive assault by the innate immune system.
topic chemiluminescence
Crohn’s disease
E. coli
fluorescent probes
neutrophil activation
peroxidase
url https://doi.org/10.1002/2211-5463.12796
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