Blocking IL-6 trans-Signaling Prevents High-Fat Diet-Induced Adipose Tissue Macrophage Recruitment but Does Not Improve Insulin Resistance

Interleukin-6 (IL-6) plays a paradoxical role in inflammation and metabolism. The pro-inflammatory effects of IL-6 are mediated via IL-6 “trans-signaling,” a process where the soluble form of the IL-6 receptor (sIL-6R) binds IL-6 and activates signaling in inflammatory cells that express the gp130 b...

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Published inCell metabolism Vol. 21; no. 3; pp. 403 - 416
Main Authors Kraakman, Michael J., Kammoun, Helene L., Allen, Tamara L., Deswaerte, Virginie, Henstridge, Darren C., Estevez, Emma, Matthews, Vance B., Neill, Bronwyn, White, David A., Murphy, Andrew J., Peijs, Lone, Yang, Christine, Risis, Steve, Bruce, Clinton R., Du, Xiao-Jun, Bobik, Alex, Lee-Young, Robert S., Kingwell, Bronwyn A., Vasanthakumar, Ajithkumar, Shi, Wei, Kallies, Axel, Lancaster, Graeme I., Rose-John, Stefan, Febbraio, Mark A.
Format Journal Article
LanguageEnglish
Published United States Elsevier Inc 03.03.2015
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Abstract Interleukin-6 (IL-6) plays a paradoxical role in inflammation and metabolism. The pro-inflammatory effects of IL-6 are mediated via IL-6 “trans-signaling,” a process where the soluble form of the IL-6 receptor (sIL-6R) binds IL-6 and activates signaling in inflammatory cells that express the gp130 but not the IL-6 receptor. Here we show that trans-signaling recruits macrophages into adipose tissue (ATM). Moreover, blocking trans-signaling with soluble gp130Fc protein prevents high-fat diet (HFD)-induced ATM accumulation, but does not improve insulin action. Importantly, however, blockade of IL-6 trans-signaling, unlike complete ablation of IL-6 signaling, does not exacerbate obesity-induced weight gain, liver steatosis, or insulin resistance. Our data identify the sIL-6R as a critical chemotactic signal for ATM recruitment and suggest that selectively blocking IL-6 trans-signaling may be a more favorable treatment option for inflammatory diseases, compared with current treatments that completely block the action of IL-6 and negatively impact upon metabolic homeostasis. [Display omitted] •IL-6 trans-signaling recruits macrophages to adipose tissue in HFD-induced obesity•Blocking IL-6 trans-signaling with sgp130Fc prevents HFD-induced ATM accumulation•Prevention of ATM accumulation in obesity does not rescue insulin resistance•Blocking IL-6 trans-signaling does not exacerbate HFD-induced insulin resistance Macrophage recruitment to adipose tissue is a hallmark of obesity and can contribute to insulin resistance. Kraakman et al. show that IL-6 trans-signaling is responsible for macrophage recruitment to adipose tissue in obesity, a process that can be blocked by treatment with a soluble gp130Fc protein.
AbstractList Interleukin-6 (IL-6) plays a paradoxical role in inflammation and metabolism. The pro-inflammatory effects of IL-6 are mediated via IL-6 "trans-signaling," a process where the soluble form of the IL-6 receptor (sIL-6R) binds IL-6 and activates signaling in inflammatory cells that express the gp130 but not the IL-6 receptor. Here we show that trans-signaling recruits macrophages into adipose tissue (ATM). Moreover, blocking trans-signaling with soluble gp130Fc protein prevents high-fat diet (HFD)-induced ATM accumulation, but does not improve insulin action. Importantly, however, blockade of IL-6 trans-signaling, unlike complete ablation of IL-6 signaling, does not exacerbate obesity-induced weight gain, liver steatosis, or insulin resistance. Our data identify the sIL-6R as a critical chemotactic signal for ATM recruitment and suggest that selectively blocking IL-6 trans-signaling may be a more favorable treatment option for inflammatory diseases, compared with current treatments that completely block the action of IL-6 and negatively impact upon metabolic homeostasis.
Interleukin-6 (IL-6) plays a paradoxical role in inflammation and metabolism. The pro-inflammatory effects of IL-6 are mediated via IL-6 “trans-signaling,” a process where the soluble form of the IL-6 receptor (sIL-6R) binds IL-6 and activates signaling in inflammatory cells that express the gp130 but not the IL-6 receptor. Here we show that trans-signaling recruits macrophages into adipose tissue (ATM). Moreover, blocking trans-signaling with soluble gp130Fc protein prevents high-fat diet (HFD)-induced ATM accumulation, but does not improve insulin action. Importantly, however, blockade of IL-6 trans-signaling, unlike complete ablation of IL-6 signaling, does not exacerbate obesity-induced weight gain, liver steatosis, or insulin resistance. Our data identify the sIL-6R as a critical chemotactic signal for ATM recruitment and suggest that selectively blocking IL-6 trans-signaling may be a more favorable treatment option for inflammatory diseases, compared with current treatments that completely block the action of IL-6 and negatively impact upon metabolic homeostasis. [Display omitted] •IL-6 trans-signaling recruits macrophages to adipose tissue in HFD-induced obesity•Blocking IL-6 trans-signaling with sgp130Fc prevents HFD-induced ATM accumulation•Prevention of ATM accumulation in obesity does not rescue insulin resistance•Blocking IL-6 trans-signaling does not exacerbate HFD-induced insulin resistance Macrophage recruitment to adipose tissue is a hallmark of obesity and can contribute to insulin resistance. Kraakman et al. show that IL-6 trans-signaling is responsible for macrophage recruitment to adipose tissue in obesity, a process that can be blocked by treatment with a soluble gp130Fc protein.
Author Kammoun, Helene L.
Lee-Young, Robert S.
Shi, Wei
Neill, Bronwyn
Allen, Tamara L.
Murphy, Andrew J.
Peijs, Lone
Febbraio, Mark A.
Kallies, Axel
Lancaster, Graeme I.
Risis, Steve
Kingwell, Bronwyn A.
Bobik, Alex
Du, Xiao-Jun
Matthews, Vance B.
Bruce, Clinton R.
Henstridge, Darren C.
Kraakman, Michael J.
Vasanthakumar, Ajithkumar
Estevez, Emma
White, David A.
Yang, Christine
Deswaerte, Virginie
Rose-John, Stefan
Author_xml – sequence: 1
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  surname: Kraakman
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  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 2
  givenname: Helene L.
  surname: Kammoun
  fullname: Kammoun, Helene L.
  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 3
  givenname: Tamara L.
  surname: Allen
  fullname: Allen, Tamara L.
  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 4
  givenname: Virginie
  surname: Deswaerte
  fullname: Deswaerte, Virginie
  organization: Vascular Biology and Atherosclerosis Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 5
  givenname: Darren C.
  surname: Henstridge
  fullname: Henstridge, Darren C.
  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
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  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
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  surname: White
  fullname: White, David A.
  organization: Experimental Cardiology Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 10
  givenname: Andrew J.
  surname: Murphy
  fullname: Murphy, Andrew J.
  organization: Haematopoiesis and Leukocyte Biology Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 11
  givenname: Lone
  surname: Peijs
  fullname: Peijs, Lone
  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 12
  givenname: Christine
  surname: Yang
  fullname: Yang, Christine
  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 13
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  surname: Risis
  fullname: Risis, Steve
  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
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  givenname: Clinton R.
  surname: Bruce
  fullname: Bruce, Clinton R.
  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 15
  givenname: Xiao-Jun
  surname: Du
  fullname: Du, Xiao-Jun
  organization: Experimental Cardiology Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
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  organization: Vascular Biology and Atherosclerosis Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
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  surname: Lee-Young
  fullname: Lee-Young, Robert S.
  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 18
  givenname: Bronwyn A.
  surname: Kingwell
  fullname: Kingwell, Bronwyn A.
  organization: Metabolic and Vascular Physiology Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
– sequence: 19
  givenname: Ajithkumar
  surname: Vasanthakumar
  fullname: Vasanthakumar, Ajithkumar
  organization: Walter & Eliza Hall Institute of Medical Research, Parkville, VIC 3052, Australia
– sequence: 20
  givenname: Wei
  surname: Shi
  fullname: Shi, Wei
  organization: Walter & Eliza Hall Institute of Medical Research, Parkville, VIC 3052, Australia
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  surname: Kallies
  fullname: Kallies, Axel
  organization: Walter & Eliza Hall Institute of Medical Research, Parkville, VIC 3052, Australia
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  surname: Lancaster
  fullname: Lancaster, Graeme I.
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  givenname: Stefan
  surname: Rose-John
  fullname: Rose-John, Stefan
  organization: Department of Biochemistry, Christian-Albrechts-Universität zu Kiel, 24098 Kiel, Germany
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  givenname: Mark A.
  surname: Febbraio
  fullname: Febbraio, Mark A.
  email: mark.febbraio@bakeridi.edu.au
  organization: Cellular and Molecular Metabolism Laboratory, BakerIDI Heart & Diabetes Institute, Melbourne, VIC 3004, Australia
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25738456$$D View this record in MEDLINE/PubMed
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SSID ssj0036393
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Snippet Interleukin-6 (IL-6) plays a paradoxical role in inflammation and metabolism. The pro-inflammatory effects of IL-6 are mediated via IL-6 “trans-signaling,” a...
Interleukin-6 (IL-6) plays a paradoxical role in inflammation and metabolism. The pro-inflammatory effects of IL-6 are mediated via IL-6 "trans-signaling," a...
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SubjectTerms Adipose Tissue - metabolism
Adipose Tissue - physiology
Animals
Cytokine Receptor gp130 - metabolism
Diet, High-Fat - adverse effects
Insulin Resistance - physiology
Interleukin-6 - metabolism
Macrophages - metabolism
Macrophages - physiology
Mice
Mice, Inbred C57BL
Mice, Transgenic
Receptors, Interleukin-6 - metabolism
Signal Transduction - physiology
Title Blocking IL-6 trans-Signaling Prevents High-Fat Diet-Induced Adipose Tissue Macrophage Recruitment but Does Not Improve Insulin Resistance
URI https://dx.doi.org/10.1016/j.cmet.2015.02.006
https://www.ncbi.nlm.nih.gov/pubmed/25738456
https://search.proquest.com/docview/1661335288
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