Proteomic View of Interactions of Shiga Toxin-Producing Escherichia coli with the Intestinal Environment in Gnotobiotic Piglets

Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer's patches and formation of attachment/effacement (A/E) lesions. These lesions trigger leukocyte infiltration followed by inflammation and intestinal hemorrhage. Systems bio...

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Published inPloS one Vol. 8; no. 6; p. e66462
Main Authors Pieper, Rembert, Zhang, Quanshun, Clark, David J, Parmar, Prashanth P, Alami, Hamid, Suh, Moo-Jin, Kuntumalla, Srilatha, Braisted, John C, Huang, Shih-Ting, Tzipori, Saul
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 19.06.2013
Public Library of Science (PLoS)
Subjects
Abundance
Acid resistance
Acidification
Acyltransferase
Adaptation
Ammonia
Analysis
Animals
Bacteria
Biofilms
Biology
Biosynthesis
Cell surface
Chromatography, Liquid
Coliforms
Colonization
Crosstalk
E coli
Electrophoresis, Gel, Two-Dimensional
Epidemics
Escherichia coli
Escherichia coli Proteins - biosynthesis
Gastrointestinal diseases
Gene expression
Genomes
Germ-Free Life
Glutamate decarboxylase
Gnotobiotic
Hemorrhage
Homeostasis
Immunity
In vivo methods and tests
Infection
Infections
Infectious diseases
Infiltration
Inflammatory bowel disease
Innate immunity
Intestine
Intestines - microbiology
Intracellular
Lesions
Leukocytes
Lipopolysaccharides
Lysates
Metabolism
Mitogens
NADP
Nutrients
Oxygen
Pathogenesis
Pathogens
Pattern recognition
Phosphates
Physiological aspects
Proteins
Proteomics
Pyridine
Pyridine nucleotide transhydrogenase
Pyridines
Reactive Nitrogen Species - metabolism
Reactive Oxygen Species - metabolism
Secretions
Shiga toxin
Shiga Toxin - biosynthesis
Shiga-Toxigenic Escherichia coli - metabolism
Shigella
Shigella dysenteriae
Signal transduction
Stationary phase
Stress response
Swine
Tandem Mass Spectrometry
Trefoil factor
Two dimensional analysis
Veterinary colleges
Veterinary medicine
United States > US
Maryland
Massachusetts
Online AccessGet full text

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Abstract Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer's patches and formation of attachment/effacement (A/E) lesions. These lesions trigger leukocyte infiltration followed by inflammation and intestinal hemorrhage. Systems biology, which explores the crosstalk of Stx-producing Escherichia coli with the in vivo host environment, may elucidate novel molecular pathogenesis aspects. Enterohemorrhagic E. coli strain 86-24 produces Shiga toxin-2 and belongs to the serotype O157:H7. Bacterial cells were scrapped from stationary phase cultures (the in vitro condition) and used to infect gnotobiotic piglets via intestinal lavage. Bacterial cells isolated from the piglets' guts constituted the in vivo condition. Cell lysates were subjected to quantitative 2D gel and shotgun proteomic analyses, revealing metabolic shifts towards anaerobic energy generation, changes in carbon utilization, phosphate and ammonia starvation, and high activity of a glutamate decarboxylase acid resistance system in vivo. Increased abundance of pyridine nucleotide transhydrogenase (PntA and PntB) suggested in vivo shortage of intracellular NADPH. Abundance changes of proteins implicated in lipopolysaccharide biosynthesis (LpxC, ArnA, the predicted acyltransferase L7029) and outer membrane (OM) assembly (LptD, MlaA, MlaC) suggested bacterial cell surface modulation in response to activated host defenses. Indeed, there was evidence for interactions of innate immunity-associated proteins secreted into the intestines (GP340, REG3-γ, resistin, lithostathine, and trefoil factor 3) with the bacterial cell envelope. Proteomic analysis afforded insights into system-wide adaptations of strain 86-24 to a hostile intestinal milieu, including responses to limited nutrients and cofactor supplies, intracellular acidification, and reactive nitrogen and oxygen species-mediated stress. Protein and lipopolysaccharide compositions of the OM were altered. Enhanced expression of type III secretion system effectors correlated with a metabolic shift back to a more aerobic milieu in vivo. Apparent pathogen pattern recognition molecules from piglet intestinal secretions adhered strongly to the bacterial cell surface.
AbstractList Background Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer’s patches and formation of attachment/effacement (A/E) lesions. These lesions trigger leukocyte infiltration followed by inflammation and intestinal hemorrhage. Systems biology, which explores the crosstalk of Stx-producing Escherichia coli with the in vivo host environment, may elucidate novel molecular pathogenesis aspects. Methodology/Principal Findings Enterohemorrhagic E. coli strain 86–24 produces Shiga toxin-2 and belongs to the serotype O157:H7. Bacterial cells were scrapped from stationary phase cultures (the in vitro condition) and used to infect gnotobiotic piglets via intestinal lavage. Bacterial cells isolated from the piglets’ guts constituted the in vivo condition. Cell lysates were subjected to quantitative 2D gel and shotgun proteomic analyses, revealing metabolic shifts towards anaerobic energy generation, changes in carbon utilization, phosphate and ammonia starvation, and high activity of a glutamate decarboxylase acid resistance system in vivo. Increased abundance of pyridine nucleotide transhydrogenase (PntA and PntB) suggested in vivo shortage of intracellular NADPH. Abundance changes of proteins implicated in lipopolysaccharide biosynthesis (LpxC, ArnA, the predicted acyltransferase L7029) and outer membrane (OM) assembly (LptD, MlaA, MlaC) suggested bacterial cell surface modulation in response to activated host defenses. Indeed, there was evidence for interactions of innate immunity-associated proteins secreted into the intestines (GP340, REG3-γ, resistin, lithostathine, and trefoil factor 3) with the bacterial cell envelope. Significance Proteomic analysis afforded insights into system-wide adaptations of strain 86–24 to a hostile intestinal milieu, including responses to limited nutrients and cofactor supplies, intracellular acidification, and reactive nitrogen and oxygen species-mediated stress. Protein and lipopolysaccharide compositions of the OM were altered. Enhanced expression of type III secretion system effectors correlated with a metabolic shift back to a more aerobic milieu in vivo. Apparent pathogen pattern recognition molecules from piglet intestinal secretions adhered strongly to the bacterial cell surface.
Background Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer’s patches and formation of attachment/effacement (A/E) lesions. These lesions trigger leukocyte infiltration followed by inflammation and intestinal hemorrhage. Systems biology, which explores the crosstalk of Stx-producing Escherichia coli with the in vivo host environment, may elucidate novel molecular pathogenesis aspects. Methodology/Principal Findings Enterohemorrhagic E. coli strain 86–24 produces Shiga toxin-2 and belongs to the serotype O157:H7. Bacterial cells were scrapped from stationary phase cultures (the in vitro condition) and used to infect gnotobiotic piglets via intestinal lavage. Bacterial cells isolated from the piglets’ guts constituted the in vivo condition. Cell lysates were subjected to quantitative 2D gel and shotgun proteomic analyses, revealing metabolic shifts towards anaerobic energy generation, changes in carbon utilization, phosphate and ammonia starvation, and high activity of a glutamate decarboxylase acid resistance system in vivo. Increased abundance of pyridine nucleotide transhydrogenase (PntA and PntB) suggested in vivo shortage of intracellular NADPH. Abundance changes of proteins implicated in lipopolysaccharide biosynthesis (LpxC, ArnA, the predicted acyltransferase L7029) and outer membrane (OM) assembly (LptD, MlaA, MlaC) suggested bacterial cell surface modulation in response to activated host defenses. Indeed, there was evidence for interactions of innate immunity-associated proteins secreted into the intestines (GP340, REG3-γ, resistin, lithostathine, and trefoil factor 3) with the bacterial cell envelope. Significance Proteomic analysis afforded insights into system-wide adaptations of strain 86–24 to a hostile intestinal milieu, including responses to limited nutrients and cofactor supplies, intracellular acidification, and reactive nitrogen and oxygen species-mediated stress. Protein and lipopolysaccharide compositions of the OM were altered. Enhanced expression of type III secretion system effectors correlated with a metabolic shift back to a more aerobic milieu in vivo. Apparent pathogen pattern recognition molecules from piglet intestinal secretions adhered strongly to the bacterial cell surface.
Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer's patches and formation of attachment/effacement (A/E) lesions. These lesions trigger leukocyte infiltration followed by inflammation and intestinal hemorrhage. Systems biology, which explores the crosstalk of Stx-producing Escherichia coli with the in vivo host environment, may elucidate novel molecular pathogenesis aspects. Enterohemorrhagic E. coli strain 86-24 produces Shiga toxin-2 and belongs to the serotype O157:H7. Bacterial cells were scrapped from stationary phase cultures (the in vitro condition) and used to infect gnotobiotic piglets via intestinal lavage. Bacterial cells isolated from the piglets' guts constituted the in vivo condition. Cell lysates were subjected to quantitative 2D gel and shotgun proteomic analyses, revealing metabolic shifts towards anaerobic energy generation, changes in carbon utilization, phosphate and ammonia starvation, and high activity of a glutamate decarboxylase acid resistance system in vivo. Increased abundance of pyridine nucleotide transhydrogenase (PntA and PntB) suggested in vivo shortage of intracellular NADPH. Abundance changes of proteins implicated in lipopolysaccharide biosynthesis (LpxC, ArnA, the predicted acyltransferase L7029) and outer membrane (OM) assembly (LptD, MlaA, MlaC) suggested bacterial cell surface modulation in response to activated host defenses. Indeed, there was evidence for interactions of innate immunity-associated proteins secreted into the intestines (GP340, REG3-[gamma], resistin, lithostathine, and trefoil factor 3) with the bacterial cell envelope. Proteomic analysis afforded insights into system-wide adaptations of strain 86-24 to a hostile intestinal milieu, including responses to limited nutrients and cofactor supplies, intracellular acidification, and reactive nitrogen and oxygen species-mediated stress. Protein and lipopolysaccharide compositions of the OM were altered. Enhanced expression of type III secretion system effectors correlated with a metabolic shift back to a more aerobic milieu in vivo. Apparent pathogen pattern recognition molecules from piglet intestinal secretions adhered strongly to the bacterial cell surface.
Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer's patches and formation of attachment/effacement (A/E) lesions. These lesions trigger leukocyte infiltration followed by inflammation and intestinal hemorrhage. Systems biology, which explores the crosstalk of Stx-producing Escherichia coli with the in vivo host environment, may elucidate novel molecular pathogenesis aspects.Enterohemorrhagic E. coli strain 86-24 produces Shiga toxin-2 and belongs to the serotype O157:H7. Bacterial cells were scrapped from stationary phase cultures (the in vitro condition) and used to infect gnotobiotic piglets via intestinal lavage. Bacterial cells isolated from the piglets' guts constituted the in vivo condition. Cell lysates were subjected to quantitative 2D gel and shotgun proteomic analyses, revealing metabolic shifts towards anaerobic energy generation, changes in carbon utilization, phosphate and ammonia starvation, and high activity of a glutamate decarboxylase acid resistance system in vivo. Increased abundance of pyridine nucleotide transhydrogenase (PntA and PntB) suggested in vivo shortage of intracellular NADPH. Abundance changes of proteins implicated in lipopolysaccharide biosynthesis (LpxC, ArnA, the predicted acyltransferase L7029) and outer membrane (OM) assembly (LptD, MlaA, MlaC) suggested bacterial cell surface modulation in response to activated host defenses. Indeed, there was evidence for interactions of innate immunity-associated proteins secreted into the intestines (GP340, REG3-γ, resistin, lithostathine, and trefoil factor 3) with the bacterial cell envelope.Proteomic analysis afforded insights into system-wide adaptations of strain 86-24 to a hostile intestinal milieu, including responses to limited nutrients and cofactor supplies, intracellular acidification, and reactive nitrogen and oxygen species-mediated stress. Protein and lipopolysaccharide compositions of the OM were altered. Enhanced expression of type III secretion system effectors correlated with a metabolic shift back to a more aerobic milieu in vivo. Apparent pathogen pattern recognition molecules from piglet intestinal secretions adhered strongly to the bacterial cell surface.
Background Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer's patches and formation of attachment/effacement (A/E) lesions. These lesions trigger leukocyte infiltration followed by inflammation and intestinal hemorrhage. Systems biology, which explores the crosstalk of Stx-producing Escherichia coli with the in vivo host environment, may elucidate novel molecular pathogenesis aspects. Methodology/Principal Findings Enterohemorrhagic E. coli strain 86-24 produces Shiga toxin-2 and belongs to the serotype O157:H7. Bacterial cells were scrapped from stationary phase cultures (the in vitro condition) and used to infect gnotobiotic piglets via intestinal lavage. Bacterial cells isolated from the piglets' guts constituted the in vivo condition. Cell lysates were subjected to quantitative 2D gel and shotgun proteomic analyses, revealing metabolic shifts towards anaerobic energy generation, changes in carbon utilization, phosphate and ammonia starvation, and high activity of a glutamate decarboxylase acid resistance system in vivo. Increased abundance of pyridine nucleotide transhydrogenase (PntA and PntB) suggested in vivo shortage of intracellular NADPH. Abundance changes of proteins implicated in lipopolysaccharide biosynthesis (LpxC, ArnA, the predicted acyltransferase L7029) and outer membrane (OM) assembly (LptD, MlaA, MlaC) suggested bacterial cell surface modulation in response to activated host defenses. Indeed, there was evidence for interactions of innate immunity-associated proteins secreted into the intestines (GP340, REG3-[gamma], resistin, lithostathine, and trefoil factor 3) with the bacterial cell envelope. Significance Proteomic analysis afforded insights into system-wide adaptations of strain 86-24 to a hostile intestinal milieu, including responses to limited nutrients and cofactor supplies, intracellular acidification, and reactive nitrogen and oxygen species-mediated stress. Protein and lipopolysaccharide compositions of the OM were altered. Enhanced expression of type III secretion system effectors correlated with a metabolic shift back to a more aerobic milieu in vivo. Apparent pathogen pattern recognition molecules from piglet intestinal secretions adhered strongly to the bacterial cell surface.
Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer's patches and formation of attachment/effacement (A/E) lesions. These lesions trigger leukocyte infiltration followed by inflammation and intestinal hemorrhage. Systems biology, which explores the crosstalk of Stx-producing Escherichia coli with the in vivo host environment, may elucidate novel molecular pathogenesis aspects. Enterohemorrhagic E. coli strain 86-24 produces Shiga toxin-2 and belongs to the serotype O157:H7. Bacterial cells were scrapped from stationary phase cultures (the in vitro condition) and used to infect gnotobiotic piglets via intestinal lavage. Bacterial cells isolated from the piglets' guts constituted the in vivo condition. Cell lysates were subjected to quantitative 2D gel and shotgun proteomic analyses, revealing metabolic shifts towards anaerobic energy generation, changes in carbon utilization, phosphate and ammonia starvation, and high activity of a glutamate decarboxylase acid resistance system in vivo. Increased abundance of pyridine nucleotide transhydrogenase (PntA and PntB) suggested in vivo shortage of intracellular NADPH. Abundance changes of proteins implicated in lipopolysaccharide biosynthesis (LpxC, ArnA, the predicted acyltransferase L7029) and outer membrane (OM) assembly (LptD, MlaA, MlaC) suggested bacterial cell surface modulation in response to activated host defenses. Indeed, there was evidence for interactions of innate immunity-associated proteins secreted into the intestines (GP340, REG3-γ, resistin, lithostathine, and trefoil factor 3) with the bacterial cell envelope. Proteomic analysis afforded insights into system-wide adaptations of strain 86-24 to a hostile intestinal milieu, including responses to limited nutrients and cofactor supplies, intracellular acidification, and reactive nitrogen and oxygen species-mediated stress. Protein and lipopolysaccharide compositions of the OM were altered. Enhanced expression of type III secretion system effectors correlated with a metabolic shift back to a more aerobic milieu in vivo. Apparent pathogen pattern recognition molecules from piglet intestinal secretions adhered strongly to the bacterial cell surface.
Audience Academic
Author Alami, Hamid
Braisted, John C
Zhang, Quanshun
Tzipori, Saul
Kuntumalla, Srilatha
Pieper, Rembert
Huang, Shih-Ting
Clark, David J
Suh, Moo-Jin
Parmar, Prashanth P
AuthorAffiliation 1 J. Craig Venter Institute, Rockville, Maryland, United States of America
2 Division of Infectious Diseases, Cummings School of Veterinary Medicine, Tufts University, North Grafton, Massachusetts, United States of America
Charité-University Medicine Berlin, Germany
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– name: Charité-University Medicine Berlin, Germany
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/23840478$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
2013 Pieper et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2013 Pieper et al 2013 Pieper et al
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– notice: 2013 Pieper et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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Notes Competing Interests: The authors have declared that no competing interests exist.
Conceived and designed the experiments: RP ST. Performed the experiments: QZ DJC HA PPP MS. Analyzed the data: RP QZ STH JCB. Contributed reagents/materials/analysis tools: STH SK JCB. Wrote the paper: RP. Manuscript review, pathogenesis: QZ ST.
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SSID ssj0053866
Score 2.2053683
Snippet Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer's patches and formation of...
Background Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer's patches and formation...
Background Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer’s patches and formation...
Background Shiga toxin (Stx)-producing Escherichia coli cause severe intestinal infections involving colonization of epithelial Peyer’s patches and formation...
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SourceType Open Website
Open Access Repository
Aggregation Database
Index Database
StartPage e66462
SubjectTerms Abundance
Acid resistance
Acidification
Acyltransferase
Adaptation
Ammonia
Analysis
Animals
Bacteria
Biofilms
Biology
Biosynthesis
Cell surface
Chromatography, Liquid
Coliforms
Colonization
Crosstalk
E coli
Electrophoresis, Gel, Two-Dimensional
Epidemics
Escherichia coli
Escherichia coli Proteins - biosynthesis
Gastrointestinal diseases
Gene expression
Genomes
Germ-Free Life
Glutamate decarboxylase
Gnotobiotic
Hemorrhage
Homeostasis
Immunity
In vivo methods and tests
Infection
Infections
Infectious diseases
Infiltration
Inflammatory bowel disease
Innate immunity
Intestine
Intestines - microbiology
Intracellular
Lesions
Leukocytes
Lipopolysaccharides
Lysates
Metabolism
Mitogens
NADP
Nutrients
Oxygen
Pathogenesis
Pathogens
Pattern recognition
Phosphates
Physiological aspects
Proteins
Proteomics
Pyridine
Pyridine nucleotide transhydrogenase
Pyridines
Reactive Nitrogen Species - metabolism
Reactive Oxygen Species - metabolism
Secretions
Shiga toxin
Shiga Toxin - biosynthesis
Shiga-Toxigenic Escherichia coli - metabolism
Shigella
Shigella dysenteriae
Signal transduction
Stationary phase
Stress response
Swine
Tandem Mass Spectrometry
Trefoil factor
Two dimensional analysis
Veterinary colleges
Veterinary medicine
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Title Proteomic View of Interactions of Shiga Toxin-Producing Escherichia coli with the Intestinal Environment in Gnotobiotic Piglets
URI https://www.ncbi.nlm.nih.gov/pubmed/23840478
https://www.proquest.com/docview/1369824959
https://pubmed.ncbi.nlm.nih.gov/PMC3686733
https://doaj.org/article/38fbf8c6c63849529148c2e0a753a2fb
http://dx.doi.org/10.1371/journal.pone.0066462
Volume 8
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