Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro

In stressful situations, catecholamines modulate mammalian immune function, and in addition, they can be sensed by many bacteria. Catecholamine sensing was also found in the zoonotic gut pathogen Salmonella Typhimurium, probably contributing to the stress-induced increased risk of salmonellosis. Vir...

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Main Authors: Lena Reiske, Sonja S. Schmucker, Julia Steuber, Charlotte Toulouse, Birgit Pfaffinger, Volker Stefanski
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-09-01
Series:Frontiers in Immunology
Subjects:
pig
Online Access:https://www.frontiersin.org/article/10.3389/fimmu.2020.572056/full
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spelling doaj-c627e211dcd54f54bef6a472fc0e6eed2020-11-25T03:14:13ZengFrontiers Media S.A.Frontiers in Immunology1664-32242020-09-011110.3389/fimmu.2020.572056572056Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitroLena Reiske0Sonja S. Schmucker1Julia Steuber2Charlotte Toulouse3Birgit Pfaffinger4Volker Stefanski5Behavioral Physiology of Livestock, Institute of Animal Science, University of Hohenheim, Stuttgart, GermanyBehavioral Physiology of Livestock, Institute of Animal Science, University of Hohenheim, Stuttgart, GermanyCellular Microbiology, Institute of Biology, University of Hohenheim, Stuttgart, GermanyCellular Microbiology, Institute of Biology, University of Hohenheim, Stuttgart, GermanyBehavioral Physiology of Livestock, Institute of Animal Science, University of Hohenheim, Stuttgart, GermanyBehavioral Physiology of Livestock, Institute of Animal Science, University of Hohenheim, Stuttgart, GermanyIn stressful situations, catecholamines modulate mammalian immune function, and in addition, they can be sensed by many bacteria. Catecholamine sensing was also found in the zoonotic gut pathogen Salmonella Typhimurium, probably contributing to the stress-induced increased risk of salmonellosis. Virulence traits such as proliferation and invasiveness are promoted upon bacterial catecholamine sensing, but it is unknown whether S. Typhimurium may also inhibit mammalian immune function in stressful situations. We thus investigated whether supernatants from S. Typhimurium grown in the presence of catecholamines modulate porcine mitogen-induced lymphocyte proliferation. Lymphocyte proliferation was reduced by supernatants from catecholamine-exposed Salmonella in a dose-dependent manner. We further examined whether adrenaline oxidation to adrenochrome, which is promoted by bacteria, could be responsible for the observed effect, but this molecule either enhanced lymphocyte functionality or had no effect. We could thereby exclude adrenochrome as a potential immunomodulating agent produced by S. Typhimurium. This study is the first to demonstrate that bacteria grown in the presence of catecholamine stress hormones alter their growth environment, probably by producing immunomodulating substances, in a way that host immune response is suppressed. These findings add a new dimension to interkingdom signaling and provide novel clues to explain the increased susceptibility of a stressed host to Salmonella infection.https://www.frontiersin.org/article/10.3389/fimmu.2020.572056/fullSalmonella Typhimuriumcatecholaminesadrenalineadrenochromepigstress
collection DOAJ
language English
format Article
sources DOAJ
author Lena Reiske
Sonja S. Schmucker
Julia Steuber
Charlotte Toulouse
Birgit Pfaffinger
Volker Stefanski
spellingShingle Lena Reiske
Sonja S. Schmucker
Julia Steuber
Charlotte Toulouse
Birgit Pfaffinger
Volker Stefanski
Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro
Frontiers in Immunology
Salmonella Typhimurium
catecholamines
adrenaline
adrenochrome
pig
stress
author_facet Lena Reiske
Sonja S. Schmucker
Julia Steuber
Charlotte Toulouse
Birgit Pfaffinger
Volker Stefanski
author_sort Lena Reiske
title Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro
title_short Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro
title_full Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro
title_fullStr Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro
title_full_unstemmed Interkingdom Cross-Talk in Times of Stress: Salmonella Typhimurium Grown in the Presence of Catecholamines Inhibits Porcine Immune Functionality in vitro
title_sort interkingdom cross-talk in times of stress: salmonella typhimurium grown in the presence of catecholamines inhibits porcine immune functionality in vitro
publisher Frontiers Media S.A.
series Frontiers in Immunology
issn 1664-3224
publishDate 2020-09-01
description In stressful situations, catecholamines modulate mammalian immune function, and in addition, they can be sensed by many bacteria. Catecholamine sensing was also found in the zoonotic gut pathogen Salmonella Typhimurium, probably contributing to the stress-induced increased risk of salmonellosis. Virulence traits such as proliferation and invasiveness are promoted upon bacterial catecholamine sensing, but it is unknown whether S. Typhimurium may also inhibit mammalian immune function in stressful situations. We thus investigated whether supernatants from S. Typhimurium grown in the presence of catecholamines modulate porcine mitogen-induced lymphocyte proliferation. Lymphocyte proliferation was reduced by supernatants from catecholamine-exposed Salmonella in a dose-dependent manner. We further examined whether adrenaline oxidation to adrenochrome, which is promoted by bacteria, could be responsible for the observed effect, but this molecule either enhanced lymphocyte functionality or had no effect. We could thereby exclude adrenochrome as a potential immunomodulating agent produced by S. Typhimurium. This study is the first to demonstrate that bacteria grown in the presence of catecholamine stress hormones alter their growth environment, probably by producing immunomodulating substances, in a way that host immune response is suppressed. These findings add a new dimension to interkingdom signaling and provide novel clues to explain the increased susceptibility of a stressed host to Salmonella infection.
topic Salmonella Typhimurium
catecholamines
adrenaline
adrenochrome
pig
stress
url https://www.frontiersin.org/article/10.3389/fimmu.2020.572056/full
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