Expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of Drosophila melanogaster.

Paraoxonases (PON) are a family of proteins (PON1, 2 and 3) with multiple enzymatic activities. PON1 interferes with homoserine lactone-mediated quorum sensing in bacteria and with reactive oxygen species (ROS) in humans and mice. PON1 gene mutations have been linked to multiple traits, including ag...

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Main Authors: Alejandro A Pezzulo, Emma E Hornick, Michael V Rector, Miriam Estin, Anna C Reisetter, Peter J Taft, Stephen C Butcher, A Brent Carter, J Robert Manak, David A Stoltz, Joseph Zabner
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS ONE
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22952763/?tool=EBI
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author Alejandro A Pezzulo
Emma E Hornick
Michael V Rector
Miriam Estin
Anna C Reisetter
Peter J Taft
Stephen C Butcher
A Brent Carter
J Robert Manak
David A Stoltz
Joseph Zabner
author_facet Alejandro A Pezzulo
Emma E Hornick
Michael V Rector
Miriam Estin
Anna C Reisetter
Peter J Taft
Stephen C Butcher
A Brent Carter
J Robert Manak
David A Stoltz
Joseph Zabner
author_sort Alejandro A Pezzulo
collection DOAJ
description Paraoxonases (PON) are a family of proteins (PON1, 2 and 3) with multiple enzymatic activities. PON1 interferes with homoserine lactone-mediated quorum sensing in bacteria and with reactive oxygen species (ROS) in humans and mice. PON1 gene mutations have been linked to multiple traits, including aging, and diseases of the cardiovascular, nervous and gastrointestinal system. The overlapping enzymatic activities in the PON family members and high linkage disequilibrium rates within their polymorphisms confound animal and human studies of PON1 function. In contrast, arthropods such as Drosophila melanogaster have no PON homologs, resulting in an ideal model to study interactions between PON genotype and host phenotypes. We hypothesized that expression of PON1 in D. melanogaster would alter ROS. We found that PON1 alters expression of multiple oxidative stress genes and decreases superoxide anion levels in normal and germ-free D. melanogaster. We also found differences in the composition of the gut microbiota, with a remarkable increase in levels of Lactobacillus plantarum and associated changes in expression of antimicrobial and cuticle-related genes. PON1 expression directly decreased superoxide anion levels and altered bacterial colonization of the gut and its gene expression profile, highlighting the complex nature of the interaction between host genotype and gut microbiota. We speculate that the interaction between some genotypes and human diseases may be mediated by the presence of certain gut bacteria that can induce specific immune responses in the gut and other host tissues.
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spelling doaj.art-cef0308d5eca4bdf8db408f3208677772022-12-21T22:42:24ZengPublic Library of Science (PLoS)PLoS ONE1932-62032012-01-0178e4377710.1371/journal.pone.0043777Expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of Drosophila melanogaster.Alejandro A PezzuloEmma E HornickMichael V RectorMiriam EstinAnna C ReisetterPeter J TaftStephen C ButcherA Brent CarterJ Robert ManakDavid A StoltzJoseph ZabnerParaoxonases (PON) are a family of proteins (PON1, 2 and 3) with multiple enzymatic activities. PON1 interferes with homoserine lactone-mediated quorum sensing in bacteria and with reactive oxygen species (ROS) in humans and mice. PON1 gene mutations have been linked to multiple traits, including aging, and diseases of the cardiovascular, nervous and gastrointestinal system. The overlapping enzymatic activities in the PON family members and high linkage disequilibrium rates within their polymorphisms confound animal and human studies of PON1 function. In contrast, arthropods such as Drosophila melanogaster have no PON homologs, resulting in an ideal model to study interactions between PON genotype and host phenotypes. We hypothesized that expression of PON1 in D. melanogaster would alter ROS. We found that PON1 alters expression of multiple oxidative stress genes and decreases superoxide anion levels in normal and germ-free D. melanogaster. We also found differences in the composition of the gut microbiota, with a remarkable increase in levels of Lactobacillus plantarum and associated changes in expression of antimicrobial and cuticle-related genes. PON1 expression directly decreased superoxide anion levels and altered bacterial colonization of the gut and its gene expression profile, highlighting the complex nature of the interaction between host genotype and gut microbiota. We speculate that the interaction between some genotypes and human diseases may be mediated by the presence of certain gut bacteria that can induce specific immune responses in the gut and other host tissues.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22952763/?tool=EBI
spellingShingle Alejandro A Pezzulo
Emma E Hornick
Michael V Rector
Miriam Estin
Anna C Reisetter
Peter J Taft
Stephen C Butcher
A Brent Carter
J Robert Manak
David A Stoltz
Joseph Zabner
Expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of Drosophila melanogaster.
PLoS ONE
title Expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of Drosophila melanogaster.
title_full Expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of Drosophila melanogaster.
title_fullStr Expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of Drosophila melanogaster.
title_full_unstemmed Expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of Drosophila melanogaster.
title_short Expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of Drosophila melanogaster.
title_sort expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of drosophila melanogaster
url https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22952763/?tool=EBI
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