Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase
Infiltration of various immune cell types into the fat tissue and liver has been implicated in obesity-induced insulin resistance. Jerry Olefsky and his colleagues now show that neutrophils are one of the earliest immune cells to arrive in these tissues, that they release the protease neutrophil ela...
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| Published in | Nature medicine Vol. 18; no. 9; pp. 1407 - 1412 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
New York
Nature Publishing Group US
01.09.2012
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Infiltration of various immune cell types into the fat tissue and liver has been implicated in obesity-induced insulin resistance. Jerry Olefsky and his colleagues now show that neutrophils are one of the earliest immune cells to arrive in these tissues, that they release the protease neutrophil elastase and that this enzyme degrades IRS-1, a key member of the insulin signaling pathway. These results show that neutrophils contribute to insulin resistance and how they may do so.
Chronic low-grade adipose tissue and liver inflammation is a major cause of systemic insulin resistance and is a key component of the low degree of insulin sensitivity that exists in obesity and type 2 diabetes
1
,
2
. Immune cells, such as macrophages, T cells, B cells, mast cells and eosinophils, have all been implicated as having a role in this process
3
,
4
,
5
,
6
,
7
,
8
. Neutrophils are typically the first immune cells to respond to inflammation and can exacerbate the chronic inflammatory state by helping to recruit macrophages and by interacting with antigen-presenting cells
9
,
10
,
11
. Neutrophils secrete several proteases, one of which is neutrophil elastase, which can promote inflammatory responses in several disease models
12
. Here we show that treatment of hepatocytes with neutrophil elastase causes cellular insulin resistance and that deletion of neutrophil elastase in high-fat-diet–induced obese (DIO) mice leads to less tissue inflammation that is associated with lower adipose tissue neutrophil and macrophage content. These changes are accompanied by improved glucose tolerance and increased insulin sensitivity. Taken together, we show that neutrophils can be added to the extensive repertoire of immune cells that participate in inflammation-induced metabolic disease. |
|---|---|
| AbstractList | Chronic low-grade adipose tissue and liver inflammation is a major cause of systemic insulin resistance and is a key component of the low degree of insulin sensitivity that exists in obesity and type 2 diabetes. Immune cells, such as macrophages, T cells, B cells, mast cells and eosinophils, have all been implicated as having a role in this process. Neutrophils are typically the first immune cells to respond to inflammation and can exacerbate the chronic inflammatory state by helping to recruit macrophages and by interacting with antigen-presenting cells. Neutrophils secrete several proteases, one of which is neutrophil elastase, which can promote inflammatory responses in several disease models. Here we show that treatment of hepatocytes with neutrophil elastase causes cellular insulin resistance and that deletion of neutrophil elastase in high-fat-diet–induced obese (DIO) mice leads to less tissue inflammation that is associated with lower adipose tissue neutrophil and macrophage content. These changes are accompanied by improved glucose tolerance and increased insulin sensitivity. Taken together, we show that neutrophils can be added to the extensive repertoire of immune cells that participate in inflammation-induced metabolic disease.Chronic low-grade adipose tissue and liver inflammation is a major cause of systemic insulin resistance and is a key component of the low degree of insulin sensitivity that exists in obesity and type 2 diabetes. Immune cells, such as macrophages, T cells, B cells, mast cells and eosinophils, have all been implicated as having a role in this process. Neutrophils are typically the first immune cells to respond to inflammation and can exacerbate the chronic inflammatory state by helping to recruit macrophages and by interacting with antigen-presenting cells. Neutrophils secrete several proteases, one of which is neutrophil elastase, which can promote inflammatory responses in several disease models. Here we show that treatment of hepatocytes with neutrophil elastase causes cellular insulin resistance and that deletion of neutrophil elastase in high-fat-diet–induced obese (DIO) mice leads to less tissue inflammation that is associated with lower adipose tissue neutrophil and macrophage content. These changes are accompanied by improved glucose tolerance and increased insulin sensitivity. Taken together, we show that neutrophils can be added to the extensive repertoire of immune cells that participate in inflammation-induced metabolic disease. Chronic low-grade adipose tissue and liver inflammation is a major cause of systemic insulin resistance and is a key component of the low degree of insulin sensitivity that exists in obesity and type 2 diabetes. Immune cells, such as macrophages, T cells, B cells, mast cells and eosinophils, have all been implicated as having a role in this process. Neutrophils are typically the first immune cells to respond to inflammation and can exacerbate the chronic inflammatory state by helping to recruit macrophages and by interacting with antigen-presenting cells. Neutrophils secrete several proteases, one of which is neutrophil elastase, which can promote inflammatory responses in several disease models. Here we show that treatment of hepatocytes with neutrophil elastase causes cellular insulin resistance and that deletion of neutrophil elastase in high-fat-diet–induced obese (DIO) mice leads to less tissue inflammation that is associated with lower adipose tissue neutrophil and macrophage content. These changes are accompanied by improved glucose tolerance and increased insulin sensitivity. Taken together, we show that neutrophils can be added to the extensive repertoire of immune cells that participate in inflammation-induced metabolic disease. Chronic low-grade adipose tissue and liver inflammation is a major cause of systemic insulin resistance and is a key component of the low degree of insulin sensitivity that exists in obesity and type 2 diabetes. Immune cells, such as macrophages, T cells, B cells, mast cells and eosinophils, have all been implicated as having a role in this process. Neutrophils are typically the first immune cells to respond to inflammation and can exacerbate the chronic inflammatory state by helping to recruit macrophages and by interacting with antigen-presenting cells. Neutrophils secrete several proteases, one of which is neutrophil elastase, which can promote inflammatory responses in several disease models. Here we show that treatment of hepatocytes with neutrophil elastase causes cellular insulin resistance and that deletion of neutrophil elastase in high-fat-diet-induced obese (DIO) mice leads to less tissue inflammation that is associated with lower adipose tissue neutrophil and macrophage content. These changes are accompanied by improved glucose tolerance and increased insulin sensitivity. Taken together, we show that neutrophils can be added to the extensive repertoire of immune cells that participate in inflammation-induced metabolic disease. [PUBLICATION ABSTRACT] Infiltration of various immune cell types into the fat tissue and liver has been implicated in obesity-induced insulin resistance. Jerry Olefsky and his colleagues now show that neutrophils are one of the earliest immune cells to arrive in these tissues, that they release the protease neutrophil elastase and that this enzyme degrades IRS-1, a key member of the insulin signaling pathway. These results show that neutrophils contribute to insulin resistance and how they may do so. Chronic low-grade adipose tissue and liver inflammation is a major cause of systemic insulin resistance and is a key component of the low degree of insulin sensitivity that exists in obesity and type 2 diabetes 1 , 2 . Immune cells, such as macrophages, T cells, B cells, mast cells and eosinophils, have all been implicated as having a role in this process 3 , 4 , 5 , 6 , 7 , 8 . Neutrophils are typically the first immune cells to respond to inflammation and can exacerbate the chronic inflammatory state by helping to recruit macrophages and by interacting with antigen-presenting cells 9 , 10 , 11 . Neutrophils secrete several proteases, one of which is neutrophil elastase, which can promote inflammatory responses in several disease models 12 . Here we show that treatment of hepatocytes with neutrophil elastase causes cellular insulin resistance and that deletion of neutrophil elastase in high-fat-diet–induced obese (DIO) mice leads to less tissue inflammation that is associated with lower adipose tissue neutrophil and macrophage content. These changes are accompanied by improved glucose tolerance and increased insulin sensitivity. Taken together, we show that neutrophils can be added to the extensive repertoire of immune cells that participate in inflammation-induced metabolic disease. |
| Author | Li, Dongmei Yan, Qingyun Ofrecio, Jachelle Lu, Min Zhu, Yimin Oh, Da Young Brenner, Martin B McNelis, Joanne Li, Pingping Lin, Michael Xu, Jianfeng Talukdar, Saswata Bandyopadhyay, Gautam Olefsky, Jerrold M |
| Author_xml | – sequence: 1 givenname: Saswata surname: Talukdar fullname: Talukdar, Saswata organization: Department of Medicine, University of California, San Diego, Present address: Pfizer, CVMED–Diabetes Prevention and Remission, Cambridge, Massachusetts, USA – sequence: 2 givenname: Da Young surname: Oh fullname: Oh, Da Young organization: Department of Medicine, University of California, San Diego – sequence: 3 givenname: Gautam surname: Bandyopadhyay fullname: Bandyopadhyay, Gautam organization: Department of Medicine, University of California, San Diego – sequence: 4 givenname: Dongmei surname: Li fullname: Li, Dongmei organization: Pfizer, Cardiovascular, Metabolic and Endocrine Diseases (CVMED)–Diabetes Prevention and Remission – sequence: 5 givenname: Jianfeng surname: Xu fullname: Xu, Jianfeng organization: Department of Medicine, University of California, San Diego – sequence: 6 givenname: Joanne surname: McNelis fullname: McNelis, Joanne organization: Department of Medicine, University of California, San Diego – sequence: 7 givenname: Min surname: Lu fullname: Lu, Min organization: Department of Medicine, University of California, San Diego – sequence: 8 givenname: Pingping surname: Li fullname: Li, Pingping organization: Department of Medicine, University of California, San Diego – sequence: 9 givenname: Qingyun surname: Yan fullname: Yan, Qingyun organization: Pfizer, Cardiovascular, Metabolic and Endocrine Diseases (CVMED)–Diabetes Prevention and Remission – sequence: 10 givenname: Yimin surname: Zhu fullname: Zhu, Yimin organization: Pfizer, Cardiovascular, Metabolic and Endocrine Diseases (CVMED)–Diabetes Prevention and Remission – sequence: 11 givenname: Jachelle surname: Ofrecio fullname: Ofrecio, Jachelle organization: Department of Medicine, University of California, San Diego – sequence: 12 givenname: Michael surname: Lin fullname: Lin, Michael organization: Department of Medicine, University of California, San Diego – sequence: 13 givenname: Martin B surname: Brenner fullname: Brenner, Martin B organization: Pfizer, Cardiovascular, Metabolic and Endocrine Diseases (CVMED)–Diabetes Prevention and Remission – sequence: 14 givenname: Jerrold M surname: Olefsky fullname: Olefsky, Jerrold M email: jolefsky@ucsd.edu organization: Department of Medicine, University of California, San Diego |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22863787$$D View this record in MEDLINE/PubMed |
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| Snippet | Infiltration of various immune cell types into the fat tissue and liver has been implicated in obesity-induced insulin resistance. Jerry Olefsky and his... Chronic low-grade adipose tissue and liver inflammation is a major cause of systemic insulin resistance and is a key component of the low degree of insulin... |
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| SubjectTerms | 631/250/2504/223/1699 631/250/256 692/699/2743/393 Adipose tissue Animals Antigen presentation Biomedical and Life Sciences Biomedicine Blotting, Western Body fat Body Weight - drug effects Cancer Research Densitometry Diet Diet, High-Fat Flow Cytometry Hepatocytes - drug effects Immune system Infectious Diseases Inflammation - etiology Inflammation - immunology Insulin resistance Insulin Resistance - immunology letter Liver diseases Metabolic Diseases Metabolic disorders Mice Molecular Medicine Neurosciences Neutrophils - immunology Neutrophils - secretion Obesity Obesity - complications Pancreatic Elastase - pharmacology Pancreatic Elastase - secretion Real-Time Polymerase Chain Reaction |
| Title | Neutrophils mediate insulin resistance in mice fed a high-fat diet through secreted elastase |
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