High Incidence of Metabolically Active Brown Adipose Tissue in Healthy Adult Humans

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Abstract

OBJECTIVE

The significant roles of brown adipose tissue (BAT) in the regulation of energy expenditure and adiposity are established in small rodents but have been controversial in humans. The objective is to examine the prevalence of metabolically active BAT in healthy adult humans and to clarify the effects of cold exposure and adiposity.

RESEARCH DESIGN AND METHODS

In vivo 2-[ ¹⁸F]fluoro-2-deoxyglucose (FDG) uptake into adipose tissue was measured in 56 healthy volunteers (31 male and 25 female subjects) aged 23–65 years by positron emission tomography (PET) combined with X-ray computed tomography (CT).

RESULTS

When exposed to cold (19°C) for 2 h, 17 of 32 younger subjects (aged 23–35 years) and 2 of 24 elderly subjects (aged 38–65 years) showed a substantial FDG uptake into adipose tissue of the supraclavicular and paraspinal regions, whereas they showed no detectable uptake when kept warm (27°C). Histological examinations confirmed the presence of brown adipocytes in these regions. The cold-activated FDG uptake was increased in winter compared with summer ( P < 0.001) and was inversely related to BMI ( P < 0.001) and total ( P < 0.01) and visceral ( P < 0.001) fat areas estimated from CT image at the umbilical level.

CONCLUSIONS

Our findings, being against the conventional view, indicate the high incidence of metabolically active BAT in adult humans and suggest a role in the control of body temperature and adiposity.

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Most cited references 16

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The adipose organ.

S Cinti (2005)

In mammals, the adipose tissues are contained in a multi-depot organ: the adipose organ. It consists of several subcutaneous and visceral depots. Some areas of these depots are brown and correspond to brown adipose tissue, while many are white and correspond to white adipose tissue. The organ is rich of vessels and parenchymal nerve fibers, but their density is higher in the brown areas. White areas contain a variable amount of brown adipocytes and their number varies with age, strain and environmental conditions. All adipocytes of the adipose organ express a specific adrenoceptor: ss3AR. Recent data have stressed the plasticity of the adipose organ in adult animals, and in parallel with the cytological variations there are also vascular as well as neural variations. Of note, treatment of genetically and diet induced obese rats with ss3 adrenoceptor agonists ameliorate their pathological condition and this is accompanied by the appearance of brown adipocytes in white areas of the adipose organ. This drug-induced modification of the anatomy of the organ is also obtained by the treatment with PPARgamma agonists in rats and dogs. We have previously shown that the transformation of white adipose tissue into brown adipose tissue in rats treated with ss3 adrenoceptor agonists is due to a direct transformation of differentiated unilocular adipocytes (transdifferentiation). We recently also showed that the absence of ss3 adrenoceptors strongly depress this type of plasticity in the adipose organ. All together these experiments strongly suggest the possibility to modulate the plasticity of the adipose organ with therapeutic implications for obesity and related disorders.

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UCP1 deficiency increases susceptibility to diet-induced obesity with age.

Masahiro Saito, Y Wang, Zhijun Wang … (2005)

Loss of nonshivering thermogenesis in mice by inactivation of the mitochondrial uncoupling protein gene (Ucp1-/- mice) causes increased sensitivity to cold and unexpected resistance to diet-induced obesity at a young age. To clarify the role of UCP1 in body weight regulation throughout life and influence of UCP1 deficiency on longevity, we longitudinally analyzed the phenotypes of Ucp1-/- mice maintained in a room at 23 degrees C. There was no difference in body weight and lifespan between genotypes under the standard chow diet condition, whereas the mutant mice developed obesity with age under the high-fat (HF) diet condition. Compared with Ucp1+/+ mice, Ucp1-/- mice showed increased expression of genes related to thermogenesis and fatty acid metabolism, such as beta3-adrenergic receptor, in adipose tissues of the 3-month-old mutants; however, the augmented expression was reduced in Ucp1+/+ mice in 11-month-old Ucp1-/- mice fed the HF diet. Likewise, the increased levels of UCP3 and cAMP-dependent protein kinase in the brown adipose tissue of Ucp1-/- mice given the standard diet were decreased significantly in that of Ucp1-/- mice fed the HF diet, which animals showed impaired norepinephrine-induced lipolysis in their adipose tissues. These results suggest profound attenuation of beta-adrenergic responsiveness and fatty acid utilization in Ucp1-/- mice fed the HF diet, bringing them to late-onset obesity. Our findings provide evidence that UCP1 is neither essential for body weight regulation nor for longevity under conditions of standard diet and normal housing temperature, but deficiency increases susceptibility to obesity with age in combination with HF diet.

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Uncoupling protein 1 is necessary for norepinephrine-induced glucose utilization in brown adipose tissue.

Kazuhiro Kimura, Chitoku Toda, Yuko Okamatsu … (2005)

Sympathetic stimulation activates glucose utilization in parallel with fatty acid oxidation and thermogenesis in brown adipose tissue (BAT) through the beta-adrenergic receptors. To clarify the roles of the principal thermogenic molecule mitochondrial uncoupling protein 1 (UCP1) in the sympathetically stimulated glucose utilization, we investigated the uptake of 2-deoxyglucose (2-DG) into BAT and some other tissues of UCP1-knockout (KO) mice in vivo. In wild-type (WT) mice, administration of norepinephrine (NE) accelerated the disappearance of plasma 2-DG and increased 2-DG uptake into BAT and heart without any rise of plasma insulin level. In UCP1-KO mice, the stimulatory effect of NE on 2-DG uptake into BAT, but not into heart, disappeared completely. Insulin administration increased 2-DG uptake into BAT and also heart similarly in WT and UCP1-KO mice. NE also increased the activity of AMP-activated protein kinase (AMP kinase) in BAT of WT but not UCP1-KO mice. Our results, together with reports that the activation of AMP kinase increases glucose transport in myocytes, suggest that the sympathetically stimulated glucose utilization in BAT is due to the serial activation of UCP1 and AMP kinase.

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Author and article information

Journal

Journal ID (nlm-ta): Diabetes

Journal ID (hwp): diabetes

Journal ID (pmc): diabetes

Journal ID (publisher-id): Diabetes

Title: Diabetes

Publisher: American Diabetes Association

ISSN (Print): 0012-1797

ISSN (Electronic): 1939-327X

Publication date (Print): July 2009

Publication date (Electronic): 28 April 2009

Volume: 58

Issue: 7

Pages: 1526-1531

Affiliations

[1] ¹Department of Nutrition, School of Nursing and Nutrition, Tenshi College, Sapporo, Japan;

[2] ²Department of Biomedical Sciences, Graduate School of Veterinary Medicine, Hokkaido University, Sapporo, Japan;

[3] ³Graduate School of Medicine, Hokkdaido University, Sapporo, Japan;

[4] ⁴PET Center, Ehime Hospital, Matsuyama, Japan;

[5] ⁵LSI Sapporo Clinic, Sapporo, Japan.

Author notes

Corresponding author: Masayuki Saito, saito@ 123456tenshi.ac.jp .

Article

Publisher ID: 0530

DOI: 10.2337/db09-0530

PMC ID: 2699872

PubMed ID: 19401428

SO-VID: 5e76385b-f49b-4105-b6ce-fc131cf4f0e9

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Readers may use this article as long as the work is properly cited, the use is educational and not for profit, and the work is not altered. See http://creativecommons.org/licenses/by-nc-nd/3.0/ for details.

High Incidence of Metabolically Active Brown Adipose Tissue in Healthy Adult Humans : Effects of Cold Exposure and Adiposity

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Abstract

OBJECTIVE

RESEARCH DESIGN AND METHODS

RESULTS

CONCLUSIONS

Related collections

Society for Endocrinology

Most cited references 16

The adipose organ.

UCP1 deficiency increases susceptibility to diet-induced obesity with age.

Uncoupling protein 1 is necessary for norepinephrine-induced glucose utilization in brown adipose tissue.

Author and article information

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