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The Contribution of Neutrophils and NETs to the Development of Type 1 Diabetes

Type 1 diabetes (T1D) is an autoimmune disease resulting from the destruction of insulin-producing beta cells in pancreatic islets. T lymphocytes are the claimed pathogenic effectors but abnormalities of other immune cell types, including neutrophils, also characterize T1D development. During human...

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Autores principales: Petrelli, Alessandra, Popp, Sarah K., Fukuda, Riho, Parish, Christopher R., Bosi, Emanuele, Simeonovic, Charmaine J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9299437/
https://www.ncbi.nlm.nih.gov/pubmed/35874740
http://dx.doi.org/10.3389/fimmu.2022.930553
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author Petrelli, Alessandra
Popp, Sarah K.
Fukuda, Riho
Parish, Christopher R.
Bosi, Emanuele
Simeonovic, Charmaine J.
author_facet Petrelli, Alessandra
Popp, Sarah K.
Fukuda, Riho
Parish, Christopher R.
Bosi, Emanuele
Simeonovic, Charmaine J.
author_sort Petrelli, Alessandra
collection PubMed
description Type 1 diabetes (T1D) is an autoimmune disease resulting from the destruction of insulin-producing beta cells in pancreatic islets. T lymphocytes are the claimed pathogenic effectors but abnormalities of other immune cell types, including neutrophils, also characterize T1D development. During human T1D natural history, neutrophils are reduced in the circulation, while accumulate in the pancreas where release of neutrophil extracellular traps (NETs), or NETosis, is manifest. Recent-onset T1D patients also demonstrate activated circulating neutrophils, associated with a unique neutrophil gene signature. Neutrophils can bind to platelets, leading to the formation of platelet-neutrophil aggregates (PNAs). PNAs increase in the circulation during the development of human T1D and provide a mechanism for neutrophil activation and mobilization/recruitment to the pancreas. In non-obese diabetic or NOD mice, T1D autoimmunity is accompanied by dynamic changes in neutrophil numbers, activation state, PNAs and/or NETosis/NET proteins in the circulation, pancreas and/or islets. Such properties differ between stages of T1D disease and underpin potentially indirect and direct impacts of the innate immune system in T1D pathogenesis. Supporting the potential for a pathogenic role in T1D, NETs and extracellular histones can directly damage isolated islets in vitro, a toxicity that can be prevented by small polyanions. In human T1D, NET-related damage can target the whole pancreas, including both the endocrine and exocrine components, and contribute to beta cell destruction, providing evidence for a neutrophil-associated T1D endotype. Future intervention in T1D could therefore benefit from combined strategies targeting T cells and accessory destructive elements of activated neutrophils.
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spelling pubmed-92994372022-07-21 The Contribution of Neutrophils and NETs to the Development of Type 1 Diabetes Petrelli, Alessandra Popp, Sarah K. Fukuda, Riho Parish, Christopher R. Bosi, Emanuele Simeonovic, Charmaine J. Front Immunol Immunology Type 1 diabetes (T1D) is an autoimmune disease resulting from the destruction of insulin-producing beta cells in pancreatic islets. T lymphocytes are the claimed pathogenic effectors but abnormalities of other immune cell types, including neutrophils, also characterize T1D development. During human T1D natural history, neutrophils are reduced in the circulation, while accumulate in the pancreas where release of neutrophil extracellular traps (NETs), or NETosis, is manifest. Recent-onset T1D patients also demonstrate activated circulating neutrophils, associated with a unique neutrophil gene signature. Neutrophils can bind to platelets, leading to the formation of platelet-neutrophil aggregates (PNAs). PNAs increase in the circulation during the development of human T1D and provide a mechanism for neutrophil activation and mobilization/recruitment to the pancreas. In non-obese diabetic or NOD mice, T1D autoimmunity is accompanied by dynamic changes in neutrophil numbers, activation state, PNAs and/or NETosis/NET proteins in the circulation, pancreas and/or islets. Such properties differ between stages of T1D disease and underpin potentially indirect and direct impacts of the innate immune system in T1D pathogenesis. Supporting the potential for a pathogenic role in T1D, NETs and extracellular histones can directly damage isolated islets in vitro, a toxicity that can be prevented by small polyanions. In human T1D, NET-related damage can target the whole pancreas, including both the endocrine and exocrine components, and contribute to beta cell destruction, providing evidence for a neutrophil-associated T1D endotype. Future intervention in T1D could therefore benefit from combined strategies targeting T cells and accessory destructive elements of activated neutrophils. Frontiers Media S.A. 2022-07-06 /pmc/articles/PMC9299437/ /pubmed/35874740 http://dx.doi.org/10.3389/fimmu.2022.930553 Text en Copyright © 2022 Petrelli, Popp, Fukuda, Parish, Bosi and Simeonovic https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Petrelli, Alessandra
Popp, Sarah K.
Fukuda, Riho
Parish, Christopher R.
Bosi, Emanuele
Simeonovic, Charmaine J.
The Contribution of Neutrophils and NETs to the Development of Type 1 Diabetes
title The Contribution of Neutrophils and NETs to the Development of Type 1 Diabetes
title_full The Contribution of Neutrophils and NETs to the Development of Type 1 Diabetes
title_fullStr The Contribution of Neutrophils and NETs to the Development of Type 1 Diabetes
title_full_unstemmed The Contribution of Neutrophils and NETs to the Development of Type 1 Diabetes
title_short The Contribution of Neutrophils and NETs to the Development of Type 1 Diabetes
title_sort contribution of neutrophils and nets to the development of type 1 diabetes
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9299437/
https://www.ncbi.nlm.nih.gov/pubmed/35874740
http://dx.doi.org/10.3389/fimmu.2022.930553
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