Citrobacter rodentium–host–microbiota interactions: immunity, bioenergetics and metabolism

Citrobacter rodentium is an extracellular enteric mouse-specific pathogen used to model infections with human pathogenic Escherichia coli and inflammatory bowel disease. C. rodentium injects type III secretion system effectors into intestinal epithelial cells (IECs) to target inflammatory, metabolic...

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Published inNature reviews. Microbiology Vol. 17; no. 11; pp. 701 - 715
Main Authors Mullineaux-Sanders, Caroline, Sanchez-Garrido, Julia, Hopkins, Eve G. D., Shenoy, Avinash R., Barry, Rachael, Frankel, Gad
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.11.2019
Nature Publishing Group
Subjects
631/326/41/2531
631/326/41/2533
631/326/421
Adaptive Immunity
Aerobiosis
Anaerobes
Analysis
Animals
Bioenergetics
Biomedical and Life Sciences
Cell survival
Cholesterol
Citrobacter
Citrobacter rodentium - growth & development
Citrobacter rodentium - immunology
Citrobacter rodentium - metabolism
E coli
Efflux
Energy Metabolism
Epithelial cells
Epithelial Cells - immunology
Epithelial Cells - pathology
Epithelium
Gastrointestinal Tract - immunology
Gastrointestinal Tract - microbiology
Glycolysis
Host Microbial Interactions
Host-bacteria relationships
Immune clearance
Immunity, Innate
Infectious Diseases
Inflammatory bowel diseases
Intestinal microflora
Intestinal Mucosa - immunology
Intestinal Mucosa - microbiology
Intestine
Life Sciences
Medical Microbiology
Metabolic pathways
Metabolism
Mice
Microbiology
Microbiota
Microbiota (Symbiotic organisms)
Mucosa
Oxygenation
Parasitology
Pathogenesis
Pathogenic microorganisms
Review Article
Signal transduction
Type III Secretion Systems - metabolism
Virology
Virulence Factors - metabolism
United Kingdom
Online AccessGet full text

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Abstract Citrobacter rodentium is an extracellular enteric mouse-specific pathogen used to model infections with human pathogenic Escherichia coli and inflammatory bowel disease. C. rodentium injects type III secretion system effectors into intestinal epithelial cells (IECs) to target inflammatory, metabolic and cell survival pathways and establish infection. While the host responds to infection by activating innate and adaptive immune signalling, required for clearance, the IECs respond by rapidly shifting bioenergetics to aerobic glycolysis, which leads to oxygenation of the epithelium, an instant expansion of mucosal-associated commensal Enterobacteriaceae and a decline of obligate anaerobes. Moreover, infected IECs reprogramme intracellular metabolic pathways, characterized by simultaneous activation of cholesterol biogenesis, import and efflux, leading to increased serum and faecal cholesterol levels. In this Review we summarize recent advances highlighting the intimate relationship between C. rodentium pathogenesis, metabolism and the gut microbiota. Citrobacter rodentium , an extracellular mouse-specific enteric pathogen, provides a robust model for the study of physiological host–pathogen–microbiota interactions. In this Review, Frankel and colleagues highlight how the C. rodentium model has advanced our understanding of enteric infections and inflammatory bowel disease, in particular changes to host metabolism and inflammation.
AbstractList Citrobacter rodentium is an extracellular enteric mouse-specific pathogen used to model infections with human pathogenic Escherichia coli and inflammatory bowel disease. C. rodentium injects type III secretion system effectors into intestinal epithelial cells (IECs) to target inflammatory, metabolic and cell survival pathways and establish infection. While the host responds to infection by activating innate and adaptive immune signalling, required for clearance, the IECs respond by rapidly shifting bioenergetics to aerobic glycolysis, which leads to oxygenation of the epithelium, an instant expansion of mucosal-associated commensal Enterobacteriaceae and a decline of obligate anaerobes. Moreover, infected IECs reprogramme intracellular metabolic pathways, characterized by simultaneous activation of cholesterol biogenesis, import and efflux, leading to increased serum and faecal cholesterol levels. In this Review we summarize recent advances highlighting the intimate relationship between C. rodentium pathogenesis, metabolism and the gut microbiota. Citrobacter rodentium, an extracellular mouse-specific enteric pathogen, provides a robust model for the study of physiological host-pathogen-microbiota interactions. In this Review, Frankel and colleagues highlight how the C. rodentium model has advanced our understanding of enteric infections and inflammatory bowel disease, in particular changes to host metabolism and inflammation.
Citrobacter rodentium is an extracellular enteric mouse-specific pathogen used to model infections with human pathogenic Escherichia coli and inflammatory bowel disease. C. rodentium injects type III secretion system effectors into intestinal epithelial cells (IECs) to target inflammatory, metabolic and cell survival pathways and establish infection. While the host responds to infection by activating innate and adaptive immune signalling, required for clearance, the IECs respond by rapidly shifting bioenergetics to aerobic glycolysis, which leads to oxygenation of the epithelium, an instant expansion of mucosal-associated commensal Enterobacteriaceae and a decline of obligate anaerobes. Moreover, infected IECs reprogramme intracellular metabolic pathways, characterized by simultaneous activation of cholesterol biogenesis, import and efflux, leading to increased serum and faecal cholesterol levels. In this Review we summarize recent advances highlighting the intimate relationship between C. rodentium pathogenesis, metabolism and the gut microbiota.
Citrobacter rodentium is an extracellular enteric mouse-specific pathogen used to model infections with human pathogenic Escherichia coli and inflammatory bowel disease. C. rodentium injects type III secretion system effectors into intestinal epithelial cells (IECs) to target inflammatory, metabolic and cell survival pathways and establish infection. While the host responds to infection by activating innate and adaptive immune signalling, required for clearance, the IECs respond by rapidly shifting bioenergetics to aerobic glycolysis, which leads to oxygenation of the epithelium, an instant expansion of mucosal-associated commensal Enterobacteriaceae and a decline of obligate anaerobes. Moreover, infected IECs reprogramme intracellular metabolic pathways, characterized by simultaneous activation of cholesterol biogenesis, import and efflux, leading to increased serum and faecal cholesterol levels. In this Review we summarize recent advances highlighting the intimate relationship between C. rodentium pathogenesis, metabolism and the gut microbiota. Citrobacter rodentium , an extracellular mouse-specific enteric pathogen, provides a robust model for the study of physiological host–pathogen–microbiota interactions. In this Review, Frankel and colleagues highlight how the C. rodentium model has advanced our understanding of enteric infections and inflammatory bowel disease, in particular changes to host metabolism and inflammation.
Citrobacter rodentium is an extracellular enteric mouse-specific pathogen used to model infections with human pathogenic Escherichia coli and inflammatory bowel disease. C. rodentium injects type III secretion system effectors into intestinal epithelial cells (IECs) to target inflammatory, metabolic and cell survival pathways and establish infection. While the host responds to infection by activating innate and adaptive immune signalling, required for clearance, the IECs respond by rapidly shifting bioenergetics to aerobic glycolysis, which leads to oxygenation of the epithelium, an instant expansion of mucosal-associated commensal Enterobacteriaceae and a decline of obligate anaerobes. Moreover, infected IECs reprogramme intracellular metabolic pathways, characterized by simultaneous activation of cholesterol biogenesis, import and efflux, leading to increased serum and faecal cholesterol levels. In this Review we summarize recent advances highlighting the intimate relationship between C. rodentium pathogenesis, metabolism and the gut microbiota.
Audience Academic
Author Barry, Rachael
Hopkins, Eve G. D.
Sanchez-Garrido, Julia
Shenoy, Avinash R.
Frankel, Gad
Mullineaux-Sanders, Caroline
Author_xml – sequence: 1
  givenname: Caroline
  surname: Mullineaux-Sanders
  fullname: Mullineaux-Sanders, Caroline
  organization: MRC Centre for Molecular Bacteriology and Infection, Department of Life Sciences, Imperial College London
– sequence: 2
  givenname: Julia
  surname: Sanchez-Garrido
  fullname: Sanchez-Garrido, Julia
  organization: MRC Centre for Molecular Bacteriology and Infection, Department of Life Sciences, Imperial College London
– sequence: 3
  givenname: Eve G. D.
  surname: Hopkins
  fullname: Hopkins, Eve G. D.
  organization: MRC Centre for Molecular Bacteriology and Infection, Department of Life Sciences, Imperial College London
– sequence: 4
  givenname: Avinash R.
  orcidid: 0000-0001-6228-9303
  surname: Shenoy
  fullname: Shenoy, Avinash R.
  organization: MRC Centre for Molecular Bacteriology and Infection, Department of Infectious Disease, Imperial College London
– sequence: 5
  givenname: Rachael
  surname: Barry
  fullname: Barry, Rachael
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  givenname: Gad
  orcidid: 0000-0002-0046-1363
  surname: Frankel
  fullname: Frankel, Gad
  email: g.frankel@imperial.ac.uk
  organization: MRC Centre for Molecular Bacteriology and Infection, Department of Life Sciences, Imperial College London
BackLink https://www.ncbi.nlm.nih.gov/pubmed/31541196$$D View this record in MEDLINE/PubMed
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Snippet Citrobacter rodentium is an extracellular enteric mouse-specific pathogen used to model infections with human pathogenic Escherichia coli and inflammatory...
Citrobacter rodentium is an extracellular enteric mouse-specific pathogen used to model infections with human pathogenic Escherichia coli and inflammatory...
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SubjectTerms 631/326/41/2531
631/326/41/2533
631/326/421
Adaptive Immunity
Aerobiosis
Anaerobes
Analysis
Animals
Bioenergetics
Biomedical and Life Sciences
Cell survival
Cholesterol
Citrobacter
Citrobacter rodentium - growth & development
Citrobacter rodentium - immunology
Citrobacter rodentium - metabolism
E coli
Efflux
Energy Metabolism
Epithelial cells
Epithelial Cells - immunology
Epithelial Cells - pathology
Epithelium
Gastrointestinal Tract - immunology
Gastrointestinal Tract - microbiology
Glycolysis
Host Microbial Interactions
Host-bacteria relationships
Immune clearance
Immunity, Innate
Infectious Diseases
Inflammatory bowel diseases
Intestinal microflora
Intestinal Mucosa - immunology
Intestinal Mucosa - microbiology
Intestine
Life Sciences
Medical Microbiology
Metabolic pathways
Metabolism
Mice
Microbiology
Microbiota
Microbiota (Symbiotic organisms)
Mucosa
Oxygenation
Parasitology
Pathogenesis
Pathogenic microorganisms
Review Article
Signal transduction
Type III Secretion Systems - metabolism
Virology
Virulence Factors - metabolism
Title Citrobacter rodentium–host–microbiota interactions: immunity, bioenergetics and metabolism
URI https://link.springer.com/article/10.1038/s41579-019-0252-z
https://www.ncbi.nlm.nih.gov/pubmed/31541196
https://www.proquest.com/docview/2305536067
https://search.proquest.com/docview/2295487138
Volume 17
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