Secreted proteins from the helminth Fasciola hepatica inhibit the initiation of autoreactive T cell responses and prevent diabetes in the NOD mouse

Infections with helminth parasites prevent/attenuate auto-inflammatory disease. Here we show that molecules secreted by a helminth parasite could prevent Type 1 Diabetes (T1D) in nonobese diabetic (NOD) mice. When delivered at 4 weeks of age (coincident with the initiation of autoimmunity), the excr...

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Published inPloS one Vol. 9; no. 1; p. e86289
Main Authors Lund, Maria E, O'Brien, Bronwyn A, Hutchinson, Andrew T, Robinson, Mark W, Simpson, Ann M, Dalton, John P, Donnelly, Sheila
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 21.01.2014
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Abstract Infections with helminth parasites prevent/attenuate auto-inflammatory disease. Here we show that molecules secreted by a helminth parasite could prevent Type 1 Diabetes (T1D) in nonobese diabetic (NOD) mice. When delivered at 4 weeks of age (coincident with the initiation of autoimmunity), the excretory/secretory products of Fasciola hepatica (FhES) prevented the onset of T1D, with 84% of mice remaining normoglycaemic and insulitis-free at 30 weeks of age. Disease protection was associated with suppression of IFN-γ secretion from autoreactive T cells and a switch to the production of a regulatory isotype (from IgG2a to IgG1) of autoantibody. Following FhES injection, peritoneal macrophages converted to a regulatory M2 phenotype, characterised by increased expression levels of Ym1, Arg-1, TGFβ and PD-L1. Expression of these M2 genetic markers increased in the pancreatic lymph nodes and the pancreas of FhES-treated mice. In vitro, FhES-stimulated M2 macrophages induced the differentiation of Tregs from splenocytes isolated from naïve NOD mice. Collectively, our data shows that FhES contains immune-modulatory molecules that mediate protection from autoimmune diabetes via the induction and maintenance of a regulatory immune environment.
AbstractList Infections with helminth parasites prevent/attenuate auto-inflammatory disease. Here we show that molecules secreted by a helminth parasite could prevent Type 1 Diabetes (T1D) in nonobese diabetic (NOD) mice. When delivered at 4 weeks of age (coincident with the initiation of autoimmunity), the excretory/secretory products of Fasciola hepatica (FhES) prevented the onset of T1D, with 84% of mice remaining normoglycaemic and insulitis-free at 30 weeks of age. Disease protection was associated with suppression of IFN-γ secretion from autoreactive T cells and a switch to the production of a regulatory isotype (from IgG2a to IgG1) of autoantibody. Following FhES injection, peritoneal macrophages converted to a regulatory M2 phenotype, characterised by increased expression levels of Ym1, Arg-1, TGFβ and PD-L1. Expression of these M2 genetic markers increased in the pancreatic lymph nodes and the pancreas of FhES-treated mice. In vitro, FhES-stimulated M2 macrophages induced the differentiation of Tregs from splenocytes isolated from naïve NOD mice. Collectively, our data shows that FhES contains immune-modulatory molecules that mediate protection from autoimmune diabetes via the induction and maintenance of a regulatory immune environment.
Infections with helminth parasites prevent/attenuate auto-inflammatory disease. Here we show that molecules secreted by a helminth parasite could prevent Type 1 Diabetes (T1D) in nonobese diabetic (NOD) mice. When delivered at 4 weeks of age (coincident with the initiation of autoimmunity), the excretory/secretory products of Fasciola hepatica (FhES) prevented the onset of T1D, with 84% of mice remaining normoglycaemic and insulitis-free at 30 weeks of age. Disease protection was associated with suppression of IFN-[gamma] secretion from autoreactive T cells and a switch to the production of a regulatory isotype (from IgG2a to IgG1) of autoantibody. Following FhES injection, peritoneal macrophages converted to a regulatory M2 phenotype, characterised by increased expression levels of Ym1, Arg-1, TGF[beta] and PD-L1. Expression of these M2 genetic markers increased in the pancreatic lymph nodes and the pancreas of FhES-treated mice. In vitro, FhES-stimulated M2 macrophages induced the differentiation of Tregs from splenocytes isolated from naïve NOD mice. Collectively, our data shows that FhES contains immune-modulatory molecules that mediate protection from autoimmune diabetes via the induction and maintenance of a regulatory immune environment.
Infections with helminth parasites prevent/attenuate auto-inflammatory disease. Here we show that molecules secreted by a helminth parasite could prevent Type 1 Diabetes (T1D) in nonobese diabetic (NOD) mice. When delivered at 4 weeks of age (coincident with the initiation of autoimmunity), the excretory/secretory products of Fasciola hepatica (FhES) prevented the onset of T1D, with 84% of mice remaining normoglycaemic and insulitis-free at 30 weeks of age. Disease protection was associated with suppression of IFN-γ secretion from autoreactive T cells and a switch to the production of a regulatory isotype (from IgG2a to IgG1) of autoantibody. Following FhES injection, peritoneal macrophages converted to a regulatory M2 phenotype, characterised by increased expression levels of Ym1, Arg-1, TGFβ and PD-L1. Expression of these M2 genetic markers increased in the pancreatic lymph nodes and the pancreas of FhES-treated mice. In vitro , FhES-stimulated M2 macrophages induced the differentiation of Tregs from splenocytes isolated from naïve NOD mice. Collectively, our data shows that FhES contains immune-modulatory molecules that mediate protection from autoimmune diabetes via the induction and maintenance of a regulatory immune environment.
Audience Academic
Author Hutchinson, Andrew T
Dalton, John P
Simpson, Ann M
Donnelly, Sheila
Lund, Maria E
O'Brien, Bronwyn A
Robinson, Mark W
AuthorAffiliation 2 School of Biological Sciences, Queen's University Belfast, Belfast, Northern Ireland
3 Institute of Parasitology, McDonald Campus, McGill University, St. Anne de Bellevue, Quebec, Canada
1 School of Medical and Molecular Biosciences, University of Technology Sydney, New South Wales, Australia
Université Paris Descartes, France
4 The i3 Institute, University of Technology Sydney, New South Wales, Australia
AuthorAffiliation_xml – name: 4 The i3 Institute, University of Technology Sydney, New South Wales, Australia
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/24466007$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2014 Public Library of Science
2014 Lund et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://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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– notice: 2014 Lund et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://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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Competing Interests: The authors have declared that no competing interests exist.
Conceived and designed the experiments: MEL BAO JPD SD. Performed the experiments: MEL BAO ATH SD. Analyzed the data: MEL BAO ATH MWR AS JPD SD. Contributed reagents/materials/analysis tools: MWR JPD SD. Wrote the paper: MEL BAO ATH MWR AS JPD SD.
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SSID ssj0053866
Score 2.4201412
Snippet Infections with helminth parasites prevent/attenuate auto-inflammatory disease. Here we show that molecules secreted by a helminth parasite could prevent Type...
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SubjectTerms Animals
Antigens
Autoantibodies
Autoantibodies - immunology
Autoimmune diseases
Autoimmunity
Autoimmunity - immunology
B cells
B7-H1 Antigen - immunology
beta-N-Acetylhexosaminidases - immunology
Biology
Cell Differentiation - immunology
Cytokines
Diabetes
Diabetes mellitus
Diabetes Mellitus, Experimental - immunology
Diabetes Mellitus, Experimental - parasitology
Diabetes Mellitus, Type 1 - immunology
Diabetes Mellitus, Type 1 - parasitology
Disease
Environmental law
Fasciola hepatica
Fasciola hepatica - immunology
Female
Gene expression
Genetic markers
Health aspects
Helminths - immunology
Immunoglobulin G
Immunomodulation
Infections
Inflammatory diseases
Insulin
Insulitis
Interferon
Interferon-gamma - immunology
Lectins - immunology
Lymph nodes
Lymph Nodes - immunology
Lymph Nodes - parasitology
Lymphocytes
Lymphocytes T
Macrophages
Macrophages, Peritoneal - immunology
Macrophages, Peritoneal - parasitology
Mammals
Medicine
Mice
Mice, Inbred NOD
Pancreas
Pancreas - immunology
Parasites
PD-L1 protein
Peritoneum
Prevention
Proteins
Rodents
Schistosoma mansoni
Splenocytes
Studies
T cells
T-Lymphocytes, Regulatory - immunology
T-Lymphocytes, Regulatory - parasitology
Transforming Growth Factor beta - immunology
Type 1 diabetes
γ-Interferon
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Title Secreted proteins from the helminth Fasciola hepatica inhibit the initiation of autoreactive T cell responses and prevent diabetes in the NOD mouse
URI https://www.ncbi.nlm.nih.gov/pubmed/24466007
https://www.proquest.com/docview/1490992821
https://search.proquest.com/docview/1492691113
https://pubmed.ncbi.nlm.nih.gov/PMC3897667
https://doaj.org/article/caff9c70f6774635b63afd1dd98d17d6
http://dx.doi.org/10.1371/journal.pone.0086289
Volume 9
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