Identification of the Virulence Landscape Essential for Entamoeba histolytica Invasion of the Human Colon

Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent trophozoites start to destroy the muco-epithelial barrier by first crossing the mucus, then killing host cells, triggering inflammation and subseq...

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Published inPLoS pathogens Vol. 9; no. 12; p. e1003824
Main Authors Thibeaux, Roman, Weber, Christian, Hon, Chung-Chau, Dillies, Marie-Agnès, Avé, Patrick, Coppée, Jean-Yves, Labruyère, Elisabeth, Guillén, Nancy
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.12.2013
Public Library of Science (PLoS)
Subjects
Adult
Amino Acid Sequence
Animals
beta-Amylase - genetics
beta-Amylase - metabolism
Biochemistry, Molecular Biology
Cloning, Molecular
Colon
Colon (Anatomy)
Colon - parasitology
Colon - pathology
Cricetinae
Dysentery, Amebic - genetics
Dysentery, Amebic - parasitology
Entamoeba histolytica
Entamoeba histolytica - genetics
Entamoeba histolytica - growth & development
Entamoeba histolytica - pathogenicity
Gene expression
Genomics
Genotype & phenotype
Health aspects
Host-Parasite Interactions - genetics
Host-parasite relationships
Humans
Infections
Life Sciences
Male
Mesocricetus
Metabolites
Microbiological research
Microbiology and Parasitology
Models, Molecular
Molecular Sequence Data
Mortality
Ontology
Parasitology
Physiological aspects
Sequence Homology, Amino Acid
Virulence (Microbiology)
Virulence Factors - genetics
Virulence Factors - metabolism
France
Amino Acid Sequence
beta-Amylase
Cricetinae
Humans
Models, Molecular
Molecular Sequence Data
Entamoeba histolytica
Male
Virulence Factors
Sequence Homology, Amino Acid
Animals
Cloning, Molecular
Mesocricetus
Adult
Colon
Host-Parasite Interactions
Dysentery, Amebic
Online AccessGet full text
ISSN1553-7374
1553-7366
1553-7374
DOI10.1371/journal.ppat.1003824

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Abstract Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent trophozoites start to destroy the muco-epithelial barrier by first crossing the mucus, then killing host cells, triggering inflammation and subsequently causing dysentery. The main goal of this study was to analyse pathophysiology and gene expression changes related to virulent (i.e. HM1:IMSS) and non-virulent (i.e. Rahman) strains when they are in contact with the human colon. Transcriptome comparisons between the two strains, both in culture conditions and upon contact with human colon explants, provide a global view of gene expression changes that might contribute to the observed phenotypic differences. The most remarkable feature of the virulent phenotype resides in the up-regulation of genes implicated in carbohydrate metabolism and processing of glycosylated residues. Consequently, inhibition of gene expression by RNA interference of a glycoside hydrolase (β-amylase absent from humans) abolishes mucus depletion and tissue invasion by HM1:IMSS. In summary, our data suggest a potential role of carbohydrate metabolism in colon invasion by virulent E. histolytica.
AbstractList Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent trophozoites start to destroy the muco- epithelial barrier by first crossing the mucus, then killing host cells, triggering inflammation and subsequently causing dysentery. The main goal of this study was to analyse pathophysiology and gene expression changes related to virulent (i.e. HM1:IMSS) and non-virulent (i.e. Rahman) strains when they are in contact with the human colon. Transcriptome comparisons between the two strains, both in culture conditions and upon contact with human colon explants, provide a global view of gene expression changes that might contribute to the observed phenotypic differences. The most remarkable feature of the virulent phenotype resides in the up-regulation of genes implicated in carbohydrate metabolism and processing of glycosylated residues. Consequently, inhibition of gene expression by RNA interference of a glycoside hydrolase (β-amylase absent from humans) abolishes mucus depletion and tissue invasion by HM1:IMSS. In summary, our data suggest a potential role of carbohydrate metabolism in colon invasion by virulent E. histolytica.
  Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent trophozoites start to destroy the muco-epithelial barrier by first crossing the mucus, then killing host cells, triggering inflammation and subsequently causing dysentery. The main goal of this study was to analyse pathophysiology and gene expression changes related to virulent (i.e. HM1:IMSS) and non-virulent (i.e. Rahman) strains when they are in contact with the human colon. Transcriptome comparisons between the two strains, both in culture conditions and upon contact with human colon explants, provide a global view of gene expression changes that might contribute to the observed phenotypic differences. The most remarkable feature of the virulent phenotype resides in the up-regulation of genes implicated in carbohydrate metabolism and processing of glycosylated residues. Consequently, inhibition of gene expression by RNA interference of a glycoside hydrolase (β-amylase absent from humans) abolishes mucus depletion and tissue invasion by HM1:IMSS. In summary, our data suggest a potential role of carbohydrate metabolism in colon invasion by virulent E. histolytica.
Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent trophozoites start to destroy the muco-epithelial barrier by first crossing the mucus, then killing host cells, triggering inflammation and subsequently causing dysentery. The main goal of this study was to analyse pathophysiology and gene expression changes related to virulent (i.e. HM1:IMSS) and non-virulent (i.e. Rahman) strains when they are in contact with the human colon. Transcriptome comparisons between the two strains, both in culture conditions and upon contact with human colon explants, provide a global view of gene expression changes that might contribute to the observed phenotypic differences. The most remarkable feature of the virulent phenotype resides in the up-regulation of genes implicated in carbohydrate metabolism and processing of glycosylated residues. Consequently, inhibition of gene expression by RNA interference of a glycoside hydrolase (β-amylase absent from humans) abolishes mucus depletion and tissue invasion by HM1:IMSS. In summary, our data suggest a potential role of carbohydrate metabolism in colon invasion by virulent E. histolytica.Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent trophozoites start to destroy the muco-epithelial barrier by first crossing the mucus, then killing host cells, triggering inflammation and subsequently causing dysentery. The main goal of this study was to analyse pathophysiology and gene expression changes related to virulent (i.e. HM1:IMSS) and non-virulent (i.e. Rahman) strains when they are in contact with the human colon. Transcriptome comparisons between the two strains, both in culture conditions and upon contact with human colon explants, provide a global view of gene expression changes that might contribute to the observed phenotypic differences. The most remarkable feature of the virulent phenotype resides in the up-regulation of genes implicated in carbohydrate metabolism and processing of glycosylated residues. Consequently, inhibition of gene expression by RNA interference of a glycoside hydrolase (β-amylase absent from humans) abolishes mucus depletion and tissue invasion by HM1:IMSS. In summary, our data suggest a potential role of carbohydrate metabolism in colon invasion by virulent E. histolytica.
Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent trophozoites start to destroy the muco-epithelial barrier by first crossing the mucus, then killing host cells, triggering inflammation and subsequently causing dysentery. The main goal of this study was to analyse pathophysiology and gene expression changes related to virulent (i.e. HM1:IMSS) and non-virulent (i.e. Rahman) strains when they are in contact with the human colon. Transcriptome comparisons between the two strains, both in culture conditions and upon contact with human colon explants, provide a global view of gene expression changes that might contribute to the observed phenotypic differences. The most remarkable feature of the virulent phenotype resides in the up-regulation of genes implicated in carbohydrate metabolism and processing of glycosylated residues. Consequently, inhibition of gene expression by RNA interference of a glycoside hydrolase (β-amylase absent from humans) abolishes mucus depletion and tissue invasion by HM1:IMSS. In summary, our data suggest a potential role of carbohydrate metabolism in colon invasion by virulent E. histolytica . Entamoeba histolytica is an intestinal parasite which displays diverse phenotypes with respect to pathogenesis in the human colon. Trophozoites can remain as commensal, without causing evident intestinal damage, or they can destroy the colonic mucosa leading to amoebiasis. Using human colon explants and transcriptome analysis, we investigated the gene expression profile of two E. histolytica strains (virulent and non-virulent) during their contact with the intestinal mucus to gain insights into the molecular basis responsible for amoebic divergent phenotypes. Our results suggest that the virulent E. histolytica , when in contact with the intestinal barrier, specifically increases the rate of gene transcription for enzymes necessary to exploits the carbohydrate resources present in the human colon. Using RNA interference methodologies to knockdown gene expression, our data revealed the potential role of amoebic β-amylase (a glycosydase) in colon invasion and mucus depletion. Our data implies that the ability of an E. histolytica strain to exploit the carbohydrate resources might affect its ability to invasion the intestine.
Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent trophozoites start to destroy the muco-epithelial barrier by first crossing the mucus, then killing host cells, triggering inflammation and subsequently causing dysentery. The main goal of this study was to analyse pathophysiology and gene expression changes related to virulent (i.e. HM1:IMSS) and non-virulent (i.e. Rahman) strains when they are in contact with the human colon. Transcriptome comparisons between the two strains, both in culture conditions and upon contact with human colon explants, provide a global view of gene expression changes that might contribute to the observed phenotypic differences. The most remarkable feature of the virulent phenotype resides in the up-regulation of genes implicated in carbohydrate metabolism and processing of glycosylated residues. Consequently, inhibition of gene expression by RNA interference of a glycoside hydrolase (b-amylase absent from humans) abolishes mucus depletion and tissue invasion by HM1:IMSS. In summary, our data suggest a potential role of carbohydrate metabolism in colon invasion by virulent E. histolytica.
Audience Academic
Author Dillies, Marie-Agnès
Weber, Christian
Labruyère, Elisabeth
Thibeaux, Roman
Guillén, Nancy
Coppée, Jean-Yves
Avé, Patrick
Hon, Chung-Chau
AuthorAffiliation 2 INSERM U786, Paris, France
3 Université de Versailles Saint-Quentin-en-Yvelines, Versailles, France
5 Institut Pasteur, Unité Histopathologie Humaine et Modèles Animaux, Paris, France
4 Institut Pasteur, Transcriptome et Epigénome, Département Génomes et Génétique, Paris, France
1 Institut Pasteur, Unité Biologie Cellulaire du Parasitisme, Paris, France
University of Virginia Health System, United States of America
AuthorAffiliation_xml – name: 2 INSERM U786, Paris, France
– name: 4 Institut Pasteur, Transcriptome et Epigénome, Département Génomes et Génétique, Paris, France
– name: 5 Institut Pasteur, Unité Histopathologie Humaine et Modèles Animaux, Paris, France
– name: University of Virginia Health System, United States of America
– name: 1 Institut Pasteur, Unité Biologie Cellulaire du Parasitisme, Paris, France
– name: 3 Université de Versailles Saint-Quentin-en-Yvelines, Versailles, France
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ContentType Journal Article
Copyright COPYRIGHT 2013 Public Library of Science
Attribution
2013 Thibeaux et al 2013 Thibeaux et al
2013 Thibeaux et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Thibeaux R, Weber C, Hon C-C, Dillies M-A, Avé P, et al. (2013) Identification of the Virulence Landscape Essential for Entamoeba histolytica Invasion of the Human Colon. PLoS Pathog 9(12): e1003824. doi:10.1371/journal.ppat.1003824
Copyright_xml – notice: COPYRIGHT 2013 Public Library of Science
– notice: Attribution
– notice: 2013 Thibeaux et al 2013 Thibeaux et al
– notice: 2013 Thibeaux et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Thibeaux R, Weber C, Hon C-C, Dillies M-A, Avé P, et al. (2013) Identification of the Virulence Landscape Essential for Entamoeba histolytica Invasion of the Human Colon. PLoS Pathog 9(12): e1003824. doi:10.1371/journal.ppat.1003824
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Issue 12
Keywords Amino Acid Sequence
beta-Amylase
Cricetinae
Humans
Models, Molecular
Molecular Sequence Data
Entamoeba histolytica
Male
Virulence Factors
Sequence Homology, Amino Acid
Animals
Cloning, Molecular
Mesocricetus
Adult
Colon
Host-Parasite Interactions
Dysentery, Amebic
Language English
License Attribution: http://creativecommons.org/licenses/by
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
Creative Commons Attribution License
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content type line 23
PMCID: PMC3868522
Conceived and designed the experiments: RT CW CCH MAD EL NG. Performed the experiments: RT CW PA. Analyzed the data: RT CW CCH NG. Contributed reagents/materials/analysis tools: EL JYC. Wrote the paper: RT EL CCH NG.
The authors have declared that no competing interests exist.
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Snippet Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent...
Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent...
  Entamoeba histolytica is the pathogenic amoeba responsible for amoebiasis, an infectious disease targeting human tissues. Amoebiasis arises when virulent...
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SubjectTerms Adult
Amino Acid Sequence
Animals
beta-Amylase - genetics
beta-Amylase - metabolism
Biochemistry, Molecular Biology
Cloning, Molecular
Colon
Colon (Anatomy)
Colon - parasitology
Colon - pathology
Cricetinae
Dysentery, Amebic - genetics
Dysentery, Amebic - parasitology
Entamoeba histolytica
Entamoeba histolytica - genetics
Entamoeba histolytica - growth & development
Entamoeba histolytica - pathogenicity
Gene expression
Genomics
Genotype & phenotype
Health aspects
Host-Parasite Interactions - genetics
Host-parasite relationships
Humans
Infections
Life Sciences
Male
Mesocricetus
Metabolites
Microbiological research
Microbiology and Parasitology
Models, Molecular
Molecular Sequence Data
Mortality
Ontology
Parasitology
Physiological aspects
Sequence Homology, Amino Acid
Virulence (Microbiology)
Virulence Factors - genetics
Virulence Factors - metabolism
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Title Identification of the Virulence Landscape Essential for Entamoeba histolytica Invasion of the Human Colon
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