Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection
Abstract Background A westernized diet comprising a high caloric intake from animal fats is known to influence the development of pathological inflammatory conditions. However, there has been relatively little focus upon the implications of such diets for the progression of infectious disease. Here,...
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doaj-316c9f889e114a97a57c198b2b9cf2052020-11-25T00:46:15ZengBMCMicrobiome2049-26182019-01-017111210.1186/s40168-019-0621-xShort-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infectionVanessa Las Heras0Adam G. Clooney1Feargal J. Ryan2Raul Cabrera-Rubio3Pat G. Casey4Cara M. Hueston5Jorge Pinheiro6Justine K. Rudkin7Silvia Melgar8Paul D. Cotter9Colin Hill10Cormac G. M. Gahan11APC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkTeagasc Food Research CentreAPC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkAPC Microbiome Ireland, University College CorkAbstract Background A westernized diet comprising a high caloric intake from animal fats is known to influence the development of pathological inflammatory conditions. However, there has been relatively little focus upon the implications of such diets for the progression of infectious disease. Here, we investigated the influence of a high-fat (HF) diet upon parameters that influence Listeria monocytogenes infection in mice. Results We determined that short-term administration of a HF diet increases the number of goblet cells, a known binding site for the pathogen, in the gut and also induces profound changes to the microbiota and promotes a pro-inflammatory gene expression profile in the host. Host physiological changes were concordant with significantly increased susceptibility to oral L. monocytogenes infection in mice fed a HF diet relative to low fat (LF)- or chow-fed animals. Prior to Listeria infection, short-term consumption of HF diet elevated levels of Firmicutes including Coprococcus, Butyricicoccus, Turicibacter and Clostridium XIVa species. During active infection with L. monocytogenes, microbiota changes were further exaggerated but host inflammatory responses were significantly downregulated relative to Listeria-infected LF- or chow-fed groups, suggestive of a profound tempering of the host response influenced by infection in the context of a HF diet. The effects of diet were seen beyond the gut, as a HF diet also increased the sensitivity of mice to systemic infection and altered gene expression profiles in the liver. Conclusions We adopted a systems approach to identify the effects of HF diet upon L. monocytogenes infection through analysis of host responses and microbiota changes (both pre- and post-infection). Overall, the results indicate that short-term consumption of a westernized diet has the capacity to significantly alter host susceptibility to L. monocytogenes infection concomitant with changes to the host physiological landscape. The findings suggest that diet should be a consideration when developing models that reflect human infectious disease.http://link.springer.com/article/10.1186/s40168-019-0621-xDietInfectionMicrobiomeListeria monocytogenesMiceMurine |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Vanessa Las Heras Adam G. Clooney Feargal J. Ryan Raul Cabrera-Rubio Pat G. Casey Cara M. Hueston Jorge Pinheiro Justine K. Rudkin Silvia Melgar Paul D. Cotter Colin Hill Cormac G. M. Gahan |
spellingShingle |
Vanessa Las Heras Adam G. Clooney Feargal J. Ryan Raul Cabrera-Rubio Pat G. Casey Cara M. Hueston Jorge Pinheiro Justine K. Rudkin Silvia Melgar Paul D. Cotter Colin Hill Cormac G. M. Gahan Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection Microbiome Diet Infection Microbiome Listeria monocytogenes Mice Murine |
author_facet |
Vanessa Las Heras Adam G. Clooney Feargal J. Ryan Raul Cabrera-Rubio Pat G. Casey Cara M. Hueston Jorge Pinheiro Justine K. Rudkin Silvia Melgar Paul D. Cotter Colin Hill Cormac G. M. Gahan |
author_sort |
Vanessa Las Heras |
title |
Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection |
title_short |
Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection |
title_full |
Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection |
title_fullStr |
Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection |
title_full_unstemmed |
Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection |
title_sort |
short-term consumption of a high-fat diet increases host susceptibility to listeria monocytogenes infection |
publisher |
BMC |
series |
Microbiome |
issn |
2049-2618 |
publishDate |
2019-01-01 |
description |
Abstract Background A westernized diet comprising a high caloric intake from animal fats is known to influence the development of pathological inflammatory conditions. However, there has been relatively little focus upon the implications of such diets for the progression of infectious disease. Here, we investigated the influence of a high-fat (HF) diet upon parameters that influence Listeria monocytogenes infection in mice. Results We determined that short-term administration of a HF diet increases the number of goblet cells, a known binding site for the pathogen, in the gut and also induces profound changes to the microbiota and promotes a pro-inflammatory gene expression profile in the host. Host physiological changes were concordant with significantly increased susceptibility to oral L. monocytogenes infection in mice fed a HF diet relative to low fat (LF)- or chow-fed animals. Prior to Listeria infection, short-term consumption of HF diet elevated levels of Firmicutes including Coprococcus, Butyricicoccus, Turicibacter and Clostridium XIVa species. During active infection with L. monocytogenes, microbiota changes were further exaggerated but host inflammatory responses were significantly downregulated relative to Listeria-infected LF- or chow-fed groups, suggestive of a profound tempering of the host response influenced by infection in the context of a HF diet. The effects of diet were seen beyond the gut, as a HF diet also increased the sensitivity of mice to systemic infection and altered gene expression profiles in the liver. Conclusions We adopted a systems approach to identify the effects of HF diet upon L. monocytogenes infection through analysis of host responses and microbiota changes (both pre- and post-infection). Overall, the results indicate that short-term consumption of a westernized diet has the capacity to significantly alter host susceptibility to L. monocytogenes infection concomitant with changes to the host physiological landscape. The findings suggest that diet should be a consideration when developing models that reflect human infectious disease. |
topic |
Diet Infection Microbiome Listeria monocytogenes Mice Murine |
url |
http://link.springer.com/article/10.1186/s40168-019-0621-x |
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