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...
Main Authors: | , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Frontiers Media S.A.
2020-09-01
|
Series: | Frontiers in Immunology |
Subjects: | |
Online Access: | https://www.frontiersin.org/article/10.3389/fimmu.2020.572056/full |
id |
doaj-c627e211dcd54f54bef6a472fc0e6eed |
---|---|
record_format |
Article |
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 |
work_keys_str_mv |
AT lenareiske interkingdomcrosstalkintimesofstresssalmonellatyphimuriumgrowninthepresenceofcatecholaminesinhibitsporcineimmunefunctionalityinvitro AT sonjasschmucker interkingdomcrosstalkintimesofstresssalmonellatyphimuriumgrowninthepresenceofcatecholaminesinhibitsporcineimmunefunctionalityinvitro AT juliasteuber interkingdomcrosstalkintimesofstresssalmonellatyphimuriumgrowninthepresenceofcatecholaminesinhibitsporcineimmunefunctionalityinvitro AT charlottetoulouse interkingdomcrosstalkintimesofstresssalmonellatyphimuriumgrowninthepresenceofcatecholaminesinhibitsporcineimmunefunctionalityinvitro AT birgitpfaffinger interkingdomcrosstalkintimesofstresssalmonellatyphimuriumgrowninthepresenceofcatecholaminesinhibitsporcineimmunefunctionalityinvitro AT volkerstefanski interkingdomcrosstalkintimesofstresssalmonellatyphimuriumgrowninthepresenceofcatecholaminesinhibitsporcineimmunefunctionalityinvitro |
_version_ |
1724643899230650368 |