Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection

Vanessa Las Heras, Adam G. Clooney, Feargal 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

Research output: Contribution to journalArticle

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.

LanguageEnglish
Article number7
JournalMicrobiome
Volume7
Issue number1
DOIs
Publication statusPublished - 18 Jan 2019

Keywords

  • Diet
  • Goblet cell
  • Immunity
  • Infection
  • Listeria monocytogenes
  • Mice
  • Microbiome
  • Murine

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

Cite this

Heras, V. L., Clooney, A. G., Ryan, F., Cabrera-Rubio, R., Casey, P. G., Hueston, C. M., ... Gahan, C. G. M. (2019). Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection. Microbiome, 7(1), [7]. https://doi.org/10.1186/s40168-019-0621-x
Heras, Vanessa Las ; Clooney, Adam G. ; Ryan, Feargal ; Cabrera-Rubio, Raul ; Casey, Pat G. ; Hueston, Cara M. ; Pinheiro, Jorge ; Rudkin, Justine K. ; Melgar, Silvia ; Cotter, Paul D. ; Hill, Colin ; Gahan, Cormac G.M. / Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection. In: Microbiome. 2019 ; Vol. 7, No. 1.
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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.",
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Heras, VL, Clooney, AG, Ryan, F, Cabrera-Rubio, R, Casey, PG, Hueston, CM, Pinheiro, J, Rudkin, JK, Melgar, S, Cotter, PD, Hill, C & Gahan, CGM 2019, 'Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection', Microbiome, vol. 7, no. 1, 7. https://doi.org/10.1186/s40168-019-0621-x

Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection. / Heras, Vanessa Las; Clooney, Adam G.; Ryan, Feargal; Cabrera-Rubio, Raul; Casey, Pat G.; Hueston, Cara M.; Pinheiro, Jorge; Rudkin, Justine K.; Melgar, Silvia; Cotter, Paul D.; Hill, Colin; Gahan, Cormac G.M.

In: Microbiome, Vol. 7, No. 1, 7, 18.01.2019.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Short-term consumption of a high-fat diet increases host susceptibility to Listeria monocytogenes infection

AU - Heras, Vanessa Las

AU - Clooney, Adam G.

AU - Ryan, Feargal

AU - Cabrera-Rubio, Raul

AU - Casey, Pat G.

AU - Hueston, Cara M.

AU - Pinheiro, Jorge

AU - Rudkin, Justine K.

AU - Melgar, Silvia

AU - Cotter, Paul D.

AU - Hill, Colin

AU - Gahan, Cormac G.M.

PY - 2019/1/18

Y1 - 2019/1/18

N2 - 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.

AB - 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.

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KW - Goblet cell

KW - Immunity

KW - Infection

KW - Listeria monocytogenes

KW - Mice

KW - Microbiome

KW - Murine

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U2 - 10.1186/s40168-019-0621-x

DO - 10.1186/s40168-019-0621-x

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T2 - Microbiome

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