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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Autores principales: 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
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Publicado: Public Library of Science (PLoS) 2012
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Acceso en línea:https://doaj.org/article/cef0308d5eca4bdf8db408f320867777
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spelling oai:doaj.org-article:cef0308d5eca4bdf8db408f3208677772021-11-18T07:07:03ZExpression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of Drosophila melanogaster.1932-620310.1371/journal.pone.0043777https://doaj.org/article/cef0308d5eca4bdf8db408f3208677772012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22952763/?tool=EBIhttps://doaj.org/toc/1932-6203Paraoxonases (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.Alejandro A PezzuloEmma E HornickMichael V RectorMiriam EstinAnna C ReisetterPeter J TaftStephen C ButcherA Brent CarterJ Robert ManakDavid A StoltzJoseph ZabnerPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 8, p e43777 (2012)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
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.
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.
format article
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
title 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_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_sort expression of human paraoxonase 1 decreases superoxide levels and alters bacterial colonization in the gut of drosophila melanogaster.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/cef0308d5eca4bdf8db408f320867777
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