Abstract
Metabolic syndrome is a group of obesity-related metabolic abnormalities that increase an individual's risk of developing type 2 diabetes and cardiovascular disease. Here, we show that mice genetically deficient in Toll-like receptor 5 (TLR5), a component of the innate immune system that is expressed in the gut mucosa and that helps defend against infection, exhibit hyperphagia and develop hallmark features of metabolic syndrome, including hyperlipidemia, hypertension, insulin resistance, and increased adiposity. These metabolic changes correlated with changes in the composition of the gut microbiota, and transfer of the gut microbiota from TLR5-deficient mice to wild-type germ-free mice conferred many features of metabolic syndrome to the recipients. Food restriction prevented obesity, but not insulin resistance, in the TLR5-deficient mice. These results support the emerging view that the gut microbiota contributes to metabolic disease and suggest that malfunction of the innate immune system may promote the development of metabolic syndrome.
MeSH Terms
Animals
Bacterial Physiological Phenomena
Blood Glucose/analysis
Body Fat Distribution
Body Weight
Caloric Restriction
Dietary Fats/administration & dosage
Female
Germ-Free Life
Hyperphagia/etiology
Immunity, Innate
Insulin Resistance
Intestinal Mucosa/immunology
Intestines/microbiology
Male
Metabolic Syndrome/etiology,immunology,microbiology
Mice
Mice, Knockout
Obesity/etiology,immunology,microbiology,prevention & control
Toll-Like Receptor 5/deficiency,genetics,metabolism
Chemicals
Blood Glucose
Dietary Fats
Toll-Like Receptor 5
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Vijay-Kumar Matam
Department of Pathology, Emory University, Atlanta, GA 30322, USA.
Aitken Jesse D
Carvalho Frederic A
Cullender Tyler C
Mwangi Simon
Srinivasan Shanthi
Sitaraman Shanthi V
Knight Rob
Ley Ruth E
Gewirtz Andrew T
References (16)
16 references, click to expand
-
Deletion of TLR5 results in spontaneous colitis in mice.
J Clin Invest. 2007 Dec;117(12):3909-21
PMID: 18008007
-
The gut microbiota as an environmental factor that regulates fat storage.
Proc Natl Acad Sci U S A. 2004 Nov 2;101(44):15718-23
PMID: 15505215
-
Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system.
Cell. 2007 Oct 5;131(1):33-45
PMID: 17923086
-
Obesity alters gut microbial ecology.
Proc Natl Acad Sci U S A. 2005 Aug 2;102(31):11070-5
PMID: 16033867
-
An obesity-associated gut microbiome with increased capacity for energy harvest.
Nature. 2006 Dec 21;444(7122):1027-31
PMID: 17183312
-
TLR4 links innate immunity and fatty acid-induced insulin resistance.
J Clin Invest. 2006 Nov;116(11):3015-25
PMID: 17053832
-
Chronic intracerebroventricular infusion of insulin reduces food intake and body weight of baboons.
Nature. 1979 Nov 29;282(5738):503-5
PMID: 116135
-
Will all Americans become overweight or obese? estimating the progression and cost of the US obesity epidemic.
Obesity (Silver Spring). 2008 Oct;16(10):2323-30
PMID: 18719634
-
Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice.
Diabetes. 2008 Jun;57(6):1470-81
PMID: 18305141
-
Nutrient sensing and inflammation in metabolic diseases.
Nat Rev Immunol. 2008 Dec;8(12):923-34
PMID: 19029988
-
Microbial ecology: human gut microbes associated with obesity.
Nature. 2006 Dec 21;444(7122):1022-3
PMID: 17183309
-
The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice.
Sci Transl Med. 2009 Nov 11;1(6):6ra14
PMID: 20368178
-
UniFrac: a new phylogenetic method for comparing microbial communities.
Appl Environ Microbiol. 2005 Dec;71(12):8228-35
PMID: 16332807
-
Innate and adaptive immunity cooperate flexibly to maintain host-microbiota mutualism.
Science. 2009 Jul 31;325(5940):617-20
PMID: 19644121
-
The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance.
Diabetes. 2007 Oct;56(10 ):2533-40
PMID: 17639021
-
A core gut microbiome in obese and lean twins.
Nature. 2009 Jan 22;457(7228):480-4
PMID: 19043404