Human gut derived-organoids provide model to study gluten response and effects of microbiota-derived molecules in celiac disease

Celiac disease (CD) is an immune-mediated disorder triggered by gluten exposure. The contribution of the adaptive immune response to CD pathogenesis has been extensively studied, but the absence of valid experimental models has hampered our understanding of the early steps leading to loss of gluten...

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Published inScientific reports Vol. 9; no. 1; p. 7029
Main Authors Freire, Rachel, Ingano, Laura, Serena, Gloria, Cetinbas, Murat, Anselmo, Anthony, Sapone, Anna, Sadreyev, Ruslan I., Fasano, Alessio, Senger, Stefania
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 07.05.2019
Nature Publishing Group
Subjects
13/1
13/100
13/106
13/2
13/21
13/31
13/51
14/19
38/22
38/39
38/91
631/532/2437
692/4020/1503/1702/1357
Adaptive immunity
Adult
Aged
Autoimmune diseases
Celiac disease
Celiac Disease - genetics
Celiac Disease - microbiology
Celiac Disease - pathology
Cell Proliferation
Cytokines
Cytokines - metabolism
Digestive system
Duodenum - cytology
Duodenum - pathology
Dysbiosis - metabolism
Epithelium
Gastrointestinal Microbiome - genetics
Gastrointestinal Microbiome - physiology
Gastrointestinal tract
Gene Expression
Gliadin
Gliadin - metabolism
Gliadin - pharmacology
Gluten
Glutens - metabolism
Glutens - pharmacology
Humanities and Social Sciences
Humans
Immune response
Immunological tolerance
Inflammation
Innate immunity
Intestinal Mucosa - cytology
Intestinal Mucosa - drug effects
Intestinal Mucosa - pathology
Intestine
Lactic acid
Microbiota
Middle Aged
multidisciplinary
Organoids
Pathogenesis
Permeability
Polysaccharides
Reproducibility of Results
Ribonucleic acid
RNA
Science
Science (multidisciplinary)
Stem cells
Stem Cells - pathology
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Abstract Celiac disease (CD) is an immune-mediated disorder triggered by gluten exposure. The contribution of the adaptive immune response to CD pathogenesis has been extensively studied, but the absence of valid experimental models has hampered our understanding of the early steps leading to loss of gluten tolerance. Using intestinal organoids developed from duodenal biopsies from both non-celiac (NC) and celiac (CD) patients, we explored the contribution of gut epithelium to CD pathogenesis and the role of microbiota-derived molecules in modulating the epithelium’s response to gluten. When compared to NC, RNA sequencing of CD organoids revealed significantly altered expression of genes associated with gut barrier, innate immune response, and stem cell functions. Monolayers derived from CD organoids exposed to gliadin showed increased intestinal permeability and enhanced secretion of pro-inflammatory cytokines compared to NC controls. Microbiota-derived bioproducts butyrate, lactate, and polysaccharide A improved barrier function and reduced gliadin-induced cytokine secretion. We concluded that: (1) patient-derived organoids faithfully express established and newly identified molecular signatures characteristic of CD. (2) microbiota-derived bioproducts can be used to modulate the epithelial response to gluten. Finally, we validated the use of patient-derived organoids monolayers as a novel tool for the study of CD.
AbstractList Celiac disease (CD) is an immune-mediated disorder triggered by gluten exposure. The contribution of the adaptive immune response to CD pathogenesis has been extensively studied, but the absence of valid experimental models has hampered our understanding of the early steps leading to loss of gluten tolerance. Using intestinal organoids developed from duodenal biopsies from both non-celiac (NC) and celiac (CD) patients, we explored the contribution of gut epithelium to CD pathogenesis and the role of microbiota-derived molecules in modulating the epithelium’s response to gluten. When compared to NC, RNA sequencing of CD organoids revealed significantly altered expression of genes associated with gut barrier, innate immune response, and stem cell functions. Monolayers derived from CD organoids exposed to gliadin showed increased intestinal permeability and enhanced secretion of pro-inflammatory cytokines compared to NC controls. Microbiota-derived bioproducts butyrate, lactate, and polysaccharide A improved barrier function and reduced gliadin-induced cytokine secretion. We concluded that: (1) patient-derived organoids faithfully express established and newly identified molecular signatures characteristic of CD. (2) microbiota-derived bioproducts can be used to modulate the epithelial response to gluten. Finally, we validated the use of patient-derived organoids monolayers as a novel tool for the study of CD.
Celiac disease (CD) is an immune-mediated disorder triggered by gluten exposure. The contribution of the adaptive immune response to CD pathogenesis has been extensively studied, but the absence of valid experimental models has hampered our understanding of the early steps leading to loss of gluten tolerance. Using intestinal organoids developed from duodenal biopsies from both non-celiac (NC) and celiac (CD) patients, we explored the contribution of gut epithelium to CD pathogenesis and the role of microbiota-derived molecules in modulating the epithelium's response to gluten. When compared to NC, RNA sequencing of CD organoids revealed significantly altered expression of genes associated with gut barrier, innate immune response, and stem cell functions. Monolayers derived from CD organoids exposed to gliadin showed increased intestinal permeability and enhanced secretion of pro-inflammatory cytokines compared to NC controls. Microbiota-derived bioproducts butyrate, lactate, and polysaccharide A improved barrier function and reduced gliadin-induced cytokine secretion. We concluded that: (1) patient-derived organoids faithfully express established and newly identified molecular signatures characteristic of CD. (2) microbiota-derived bioproducts can be used to modulate the epithelial response to gluten. Finally, we validated the use of patient-derived organoids monolayers as a novel tool for the study of CD.Celiac disease (CD) is an immune-mediated disorder triggered by gluten exposure. The contribution of the adaptive immune response to CD pathogenesis has been extensively studied, but the absence of valid experimental models has hampered our understanding of the early steps leading to loss of gluten tolerance. Using intestinal organoids developed from duodenal biopsies from both non-celiac (NC) and celiac (CD) patients, we explored the contribution of gut epithelium to CD pathogenesis and the role of microbiota-derived molecules in modulating the epithelium's response to gluten. When compared to NC, RNA sequencing of CD organoids revealed significantly altered expression of genes associated with gut barrier, innate immune response, and stem cell functions. Monolayers derived from CD organoids exposed to gliadin showed increased intestinal permeability and enhanced secretion of pro-inflammatory cytokines compared to NC controls. Microbiota-derived bioproducts butyrate, lactate, and polysaccharide A improved barrier function and reduced gliadin-induced cytokine secretion. We concluded that: (1) patient-derived organoids faithfully express established and newly identified molecular signatures characteristic of CD. (2) microbiota-derived bioproducts can be used to modulate the epithelial response to gluten. Finally, we validated the use of patient-derived organoids monolayers as a novel tool for the study of CD.
ArticleNumber 7029
Author Freire, Rachel
Anselmo, Anthony
Sapone, Anna
Ingano, Laura
Sadreyev, Ruslan I.
Senger, Stefania
Serena, Gloria
Cetinbas, Murat
Fasano, Alessio
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  fullname: Serena, Gloria
  organization: Mucosal Immunology and Biology Research Center and Center for Celiac Research and Treatment, Department of Pediatrics, Massachusetts General Hospital, Harvard Medical School
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  surname: Fasano
  fullname: Fasano, Alessio
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Issue 1
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Snippet Celiac disease (CD) is an immune-mediated disorder triggered by gluten exposure. The contribution of the adaptive immune response to CD pathogenesis has been...
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Title Human gut derived-organoids provide model to study gluten response and effects of microbiota-derived molecules in celiac disease
URI https://link.springer.com/article/10.1038/s41598-019-43426-w
https://www.ncbi.nlm.nih.gov/pubmed/31065051
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https://pubmed.ncbi.nlm.nih.gov/PMC6505524
Volume 9
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