Central IKKβ inhibition prevents air pollution mediated peripheral inflammation and exaggeration of type II diabetes

Abstract Background Prior experimental and epidemiologic data support a link between exposure to fine ambient particulate matter (<2.5 μm in aerodynamic diameter, PM2.5) and development of insulin resistance/Type II diabetes mellitus (Type II DM). We investigated the role of hypothalamic inflamma...

Full description

Saved in:
Bibliographic Details
Main Authors: Cuiqing Liu, Laura K Fonken, Aixia Wang, Andrei Maiseyeu, Yuntao Bai, Tse-Yao Wang, Santosh Maurya, Yi-An Ko, Muthu Periasamy, Timothy Dvonch, Masako Morishita, Robert D Brook, Jack Harkema, Zhekang Ying, Bhramar Mukherjee, Qinghua Sun, Randy J Nelson, Sanjay Rajagopalan
Format: Article
Language:English
Published: BMC 2014-10-01
Series:Particle and Fibre Toxicology
Subjects:
Online Access:https://doi.org/10.1186/s12989-014-0053-5
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849326000566960128
author Cuiqing Liu
Laura K Fonken
Aixia Wang
Andrei Maiseyeu
Yuntao Bai
Tse-Yao Wang
Santosh Maurya
Yi-An Ko
Muthu Periasamy
Timothy Dvonch
Masako Morishita
Robert D Brook
Jack Harkema
Zhekang Ying
Bhramar Mukherjee
Qinghua Sun
Randy J Nelson
Sanjay Rajagopalan
author_facet Cuiqing Liu
Laura K Fonken
Aixia Wang
Andrei Maiseyeu
Yuntao Bai
Tse-Yao Wang
Santosh Maurya
Yi-An Ko
Muthu Periasamy
Timothy Dvonch
Masako Morishita
Robert D Brook
Jack Harkema
Zhekang Ying
Bhramar Mukherjee
Qinghua Sun
Randy J Nelson
Sanjay Rajagopalan
author_sort Cuiqing Liu
collection DOAJ
description Abstract Background Prior experimental and epidemiologic data support a link between exposure to fine ambient particulate matter (<2.5 μm in aerodynamic diameter, PM2.5) and development of insulin resistance/Type II diabetes mellitus (Type II DM). We investigated the role of hypothalamic inflammation in PM2.5-mediated diabetes development. Methods KKay mice, a genetically susceptible model of Type II DM, were assigned to either concentrated PM2.5 or filtered air (FA) for 4–8 weeks via a versatile aerosol concentrator and exposure system, or administered intra-cerebroventricular with either IKKβ inhibitor (IMD-0354) or TNFα antibody (infliximab) for 4–5 weeks simultaneously with PM2.5 exposure. Glucose tolerance, insulin sensitivity, oxygen consumption and heat production were evaluated. At euthanasia, blood, spleen, visceral adipose tissue and hypothalamus were collected to measure inflammatory cells using flow cytometry. Standard immunohistochemical methods and quantitative PCR were used to assess targets of interest. Results PM2.5 exposure led to hyperglycemia and insulin resistance, which was accompanied by increased hypothalamic IL-6, TNFα, and IKKβ mRNA expression and microglial/astrocyte reactivity. Targeting the NFκB pathway with intra-cerebroventricular administration of an IKKβ inhibitor [IMD-0354, n = 8 for each group)], but not TNFα blockade with infliximab [(n = 6 for each group], improved glucose tolerance, insulin sensitivity, rectified energy homeostasis (O2 consumption, CO2 production, respiratory exchange ratio and heat generation) and reduced peripheral inflammation in response to PM2.5. Conclusions Central inhibition of IKKβ prevents PM2.5 mediated peripheral inflammation and exaggeration of type II diabetes. These results provide novel insights into how air pollution may mediate susceptibility to insulin resistance and Type II DM.
format Article
id doaj-art-d36eaed32ab64f6fa6e0c2042d00be8b
institution Kabale University
issn 1743-8977
language English
publishDate 2014-10-01
publisher BMC
record_format Article
series Particle and Fibre Toxicology
spelling doaj-art-d36eaed32ab64f6fa6e0c2042d00be8b2025-08-20T03:48:15ZengBMCParticle and Fibre Toxicology1743-89772014-10-0111111610.1186/s12989-014-0053-5Central IKKβ inhibition prevents air pollution mediated peripheral inflammation and exaggeration of type II diabetesCuiqing Liu0Laura K Fonken1Aixia Wang2Andrei Maiseyeu3Yuntao Bai4Tse-Yao Wang5Santosh Maurya6Yi-An Ko7Muthu Periasamy8Timothy Dvonch9Masako Morishita10Robert D Brook11Jack Harkema12Zhekang Ying13Bhramar Mukherjee14Qinghua Sun15Randy J Nelson16Sanjay Rajagopalan17Department of Physiology, Hangzhou Normal UniversityWexner Medical Center, The Ohio State UniversityWexner Medical Center, The Ohio State UniversityDivision of Cardiovascular Medicine, University of MarylandWexner Medical Center, The Ohio State UniversityWexner Medical Center, The Ohio State UniversityWexner Medical Center, The Ohio State UniversityDepartment of Biostatistics, University of MichiganWexner Medical Center, The Ohio State UniversityDepartment of Environmental Health Sciences, University of MichiganDepartment of Environmental Health Sciences, University of MichiganDepartment of Environmental Health Sciences, University of MichiganCenter for Integrative Toxicology, Michigan State UniversityDivision of Cardiovascular Medicine, University of MarylandDepartment of Biostatistics, University of MichiganWexner Medical Center, The Ohio State UniversityWexner Medical Center, The Ohio State UniversityDivision of Cardiovascular Medicine, University of MarylandAbstract Background Prior experimental and epidemiologic data support a link between exposure to fine ambient particulate matter (<2.5 μm in aerodynamic diameter, PM2.5) and development of insulin resistance/Type II diabetes mellitus (Type II DM). We investigated the role of hypothalamic inflammation in PM2.5-mediated diabetes development. Methods KKay mice, a genetically susceptible model of Type II DM, were assigned to either concentrated PM2.5 or filtered air (FA) for 4–8 weeks via a versatile aerosol concentrator and exposure system, or administered intra-cerebroventricular with either IKKβ inhibitor (IMD-0354) or TNFα antibody (infliximab) for 4–5 weeks simultaneously with PM2.5 exposure. Glucose tolerance, insulin sensitivity, oxygen consumption and heat production were evaluated. At euthanasia, blood, spleen, visceral adipose tissue and hypothalamus were collected to measure inflammatory cells using flow cytometry. Standard immunohistochemical methods and quantitative PCR were used to assess targets of interest. Results PM2.5 exposure led to hyperglycemia and insulin resistance, which was accompanied by increased hypothalamic IL-6, TNFα, and IKKβ mRNA expression and microglial/astrocyte reactivity. Targeting the NFκB pathway with intra-cerebroventricular administration of an IKKβ inhibitor [IMD-0354, n = 8 for each group)], but not TNFα blockade with infliximab [(n = 6 for each group], improved glucose tolerance, insulin sensitivity, rectified energy homeostasis (O2 consumption, CO2 production, respiratory exchange ratio and heat generation) and reduced peripheral inflammation in response to PM2.5. Conclusions Central inhibition of IKKβ prevents PM2.5 mediated peripheral inflammation and exaggeration of type II diabetes. These results provide novel insights into how air pollution may mediate susceptibility to insulin resistance and Type II DM.https://doi.org/10.1186/s12989-014-0053-5DiabetesParticulate matterHypothalamusInflammationIKKβ
spellingShingle Cuiqing Liu
Laura K Fonken
Aixia Wang
Andrei Maiseyeu
Yuntao Bai
Tse-Yao Wang
Santosh Maurya
Yi-An Ko
Muthu Periasamy
Timothy Dvonch
Masako Morishita
Robert D Brook
Jack Harkema
Zhekang Ying
Bhramar Mukherjee
Qinghua Sun
Randy J Nelson
Sanjay Rajagopalan
Central IKKβ inhibition prevents air pollution mediated peripheral inflammation and exaggeration of type II diabetes
Particle and Fibre Toxicology
Diabetes
Particulate matter
Hypothalamus
Inflammation
IKKβ
title Central IKKβ inhibition prevents air pollution mediated peripheral inflammation and exaggeration of type II diabetes
title_full Central IKKβ inhibition prevents air pollution mediated peripheral inflammation and exaggeration of type II diabetes
title_fullStr Central IKKβ inhibition prevents air pollution mediated peripheral inflammation and exaggeration of type II diabetes
title_full_unstemmed Central IKKβ inhibition prevents air pollution mediated peripheral inflammation and exaggeration of type II diabetes
title_short Central IKKβ inhibition prevents air pollution mediated peripheral inflammation and exaggeration of type II diabetes
title_sort central ikkβ inhibition prevents air pollution mediated peripheral inflammation and exaggeration of type ii diabetes
topic Diabetes
Particulate matter
Hypothalamus
Inflammation
IKKβ
url https://doi.org/10.1186/s12989-014-0053-5
work_keys_str_mv AT cuiqingliu centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT laurakfonken centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT aixiawang centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT andreimaiseyeu centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT yuntaobai centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT tseyaowang centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT santoshmaurya centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT yianko centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT muthuperiasamy centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT timothydvonch centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT masakomorishita centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT robertdbrook centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT jackharkema centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT zhekangying centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT bhramarmukherjee centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT qinghuasun centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT randyjnelson centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes
AT sanjayrajagopalan centralikkbinhibitionpreventsairpollutionmediatedperipheralinflammationandexaggerationoftypeiidiabetes