Microbiota Depletion Impairs Thermogenesis of Brown Adipose Tissue and Browning of White Adipose Tissue

Baoguo Li; Li Li; Min Li; Sin Man Lam; Guanlin Wang; Yingga Wu; Hanlin Zhang; Chaoqun Niu; Xueying Zhang; Xue Liu; Catherine Hambly; Wanzhu Jin; Guanghou Shui; John R Speakman

doi:10.1016/j.celrep.2019.02.015

Microbiota Depletion Impairs Thermogenesis of Brown Adipose Tissue and Browning of White Adipose Tissue

Baoguo Li, Li Li, Min Li, Sin Man Lam, Guanlin Wang, Yingga Wu, Hanlin Zhang, Chaoqun Niu, Xueying Zhang, Xue Liu, Catherine Hambly, Wanzhu Jin, Guanghou Shui, John R Speakman

Research output: Contribution to journal › Article

26 Citations (Scopus)

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Abstract

The relation between gut microbiota and the host has been suggested to benefit metabolic homeostasis. Brown adipose tissue (BAT) and beige adipocytes facilitate thermogenesis to maintain host core body temperature during cold exposure. However, the potential impact of gut microbiota on the thermogenic process is confused. Here, we evaluated how BAT and white adipose tissue (WAT) responded to temperature challenges in mice lacking gut microbiota. We found that microbiota depletion via treatment with different cocktails of antibiotics (ABX) or in germ-free (GF) mice impaired the thermogenic capacity of BAT by blunting the increase in the expression of uncoupling protein 1 (UCP1) and reducing the browning process of WAT. Gavage of the bacterial metabolite butyrate increased the thermogenic capacity of ABX-treated mice, reversing the deficit. Our results indicate that gut microbiota contributes to upregulated thermogenesis in the cold environment and that this may be partially mediated via butyrate.

Original language	English
Pages (from-to)	2720-2737
Number of pages	18
Journal	Cell Reports
Volume	26
Issue number	10
Early online date	5 Mar 2019
DOIs	https://doi.org/10.1016/j.celrep.2019.02.015
Publication status	Published - 5 Mar 2019

Keywords

brown adipose tissue
beige adipocytes
brite adipocytes
white adipose tissue
hermogenesis
UCP1
gut microbiota
butyrate
antibiotics
germ free mice
macrophage
IL-4
CELLS
COMMENSAL BACTERIA
CATECHOLAMINES
GUT MICROBIOTA
DIET-INDUCED OBESITY
ALTERNATIVELY ACTIVATED MACROPHAGES
ENERGY-EXPENDITURE
DEACETYLATION
METABOLISM
SODIUM-BUTYRATE

ASJC Scopus subject areas

Biochemistry, Genetics and Molecular Biology(all)

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Microbiota Depletion Impairs Thermogenesis of Brown Adipose Tissue and Browning of White Adipose Tissue
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John Speakman

Biological Sciences (Research Theme)
Biological Sciences, Aberdeen Centre For Environmental Sustainability - Chair in Zoology

Person: Academic

Cite this

Li, B., Li, L., Li, M., Lam, S. M., Wang, G., Wu, Y., Zhang, H., Niu, C., Zhang, X., Liu, X., Hambly, C., Jin, W., Shui, G., & Speakman, J. R. (2019). Microbiota Depletion Impairs Thermogenesis of Brown Adipose Tissue and Browning of White Adipose Tissue. Cell Reports, 26(10), 2720-2737. https://doi.org/10.1016/j.celrep.2019.02.015

Microbiota Depletion Impairs Thermogenesis of Brown Adipose Tissue and Browning of White Adipose Tissue. / Li, Baoguo; Li, Li; Li, Min; Lam, Sin Man; Wang, Guanlin; Wu, Yingga; Zhang, Hanlin; Niu, Chaoqun; Zhang, Xueying; Liu, Xue; Hambly, Catherine; Jin, Wanzhu; Shui, Guanghou; Speakman, John R.

In: Cell Reports, Vol. 26, No. 10, 05.03.2019, p. 2720-2737.

Research output: Contribution to journal › Article

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title = "Microbiota Depletion Impairs Thermogenesis of Brown Adipose Tissue and Browning of White Adipose Tissue",

abstract = "The relation between gut microbiota and the host has been suggested to benefit metabolic homeostasis. Brown adipose tissue (BAT) and beige adipocytes facilitate thermogenesis to maintain host core body temperature during cold exposure. However, the potential impact of gut microbiota on the thermogenic process is confused. Here, we evaluated how BAT and white adipose tissue (WAT) responded to temperature challenges in mice lacking gut microbiota. We found that microbiota depletion via treatment with different cocktails of antibiotics (ABX) or in germ-free (GF) mice impaired the thermogenic capacity of BAT by blunting the increase in the expression of uncoupling protein 1 (UCP1) and reducing the browning process of WAT. Gavage of the bacterial metabolite butyrate increased the thermogenic capacity of ABX-treated mice, reversing the deficit. Our results indicate that gut microbiota contributes to upregulated thermogenesis in the cold environment and that this may be partially mediated via butyrate.",

keywords = "brown adipose tissue, beige adipocytes, brite adipocytes, white adipose tissue, hermogenesis, UCP1, gut microbiota, butyrate, antibiotics, germ free mice, macrophage, IL-4, CELLS, COMMENSAL BACTERIA, CATECHOLAMINES, GUT MICROBIOTA, DIET-INDUCED OBESITY, ALTERNATIVELY ACTIVATED MACROPHAGES, ENERGY-EXPENDITURE, DEACETYLATION, METABOLISM, SODIUM-BUTYRATE",

author = "Baoguo Li and Li Li and Min Li and Lam, {Sin Man} and Guanlin Wang and Yingga Wu and Hanlin Zhang and Chaoqun Niu and Xueying Zhang and Xue Liu and Catherine Hambly and Wanzhu Jin and Guanghou Shui and Speakman, {John R}",

note = "This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB13030000) and Natural Science Foundation of China (NSFC; 91649108), the Chinese Academy of Sciences-Novo Nordisk Foundation, as well as grants from the Chinese Academy of Sciences “1000 Talents” recruitment program and a “Great-Wall Professorship” from the Chinese Academy of Sciences-Novo Nordisk Foundation. J.R.S. was also supported by a Wolfson merit professorship from The UK Royal Society. We are grateful to all of the members of the Molecular Energetics Group for their support and discussion of the results. We would like to thank Dr. Jia and Dr. Sun from the Core Facility for Protein Research from the Institute of Biophysics, Chinese Academy of Sciences for flow cytometry, and Peter Thomson and Marina Samatiou for technical assistance with the DLW measurements. ",

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AU - Li, Baoguo

AU - Li, Li

AU - Li, Min

AU - Lam, Sin Man

AU - Wang, Guanlin

AU - Wu, Yingga

AU - Zhang, Hanlin

AU - Niu, Chaoqun

AU - Zhang, Xueying

AU - Liu, Xue

AU - Hambly, Catherine

AU - Jin, Wanzhu

AU - Shui, Guanghou

AU - Speakman, John R

N1 - This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB13030000) and Natural Science Foundation of China (NSFC; 91649108), the Chinese Academy of Sciences-Novo Nordisk Foundation, as well as grants from the Chinese Academy of Sciences “1000 Talents” recruitment program and a “Great-Wall Professorship” from the Chinese Academy of Sciences-Novo Nordisk Foundation. J.R.S. was also supported by a Wolfson merit professorship from The UK Royal Society. We are grateful to all of the members of the Molecular Energetics Group for their support and discussion of the results. We would like to thank Dr. Jia and Dr. Sun from the Core Facility for Protein Research from the Institute of Biophysics, Chinese Academy of Sciences for flow cytometry, and Peter Thomson and Marina Samatiou for technical assistance with the DLW measurements.

PY - 2019/3/5

Y1 - 2019/3/5

N2 - The relation between gut microbiota and the host has been suggested to benefit metabolic homeostasis. Brown adipose tissue (BAT) and beige adipocytes facilitate thermogenesis to maintain host core body temperature during cold exposure. However, the potential impact of gut microbiota on the thermogenic process is confused. Here, we evaluated how BAT and white adipose tissue (WAT) responded to temperature challenges in mice lacking gut microbiota. We found that microbiota depletion via treatment with different cocktails of antibiotics (ABX) or in germ-free (GF) mice impaired the thermogenic capacity of BAT by blunting the increase in the expression of uncoupling protein 1 (UCP1) and reducing the browning process of WAT. Gavage of the bacterial metabolite butyrate increased the thermogenic capacity of ABX-treated mice, reversing the deficit. Our results indicate that gut microbiota contributes to upregulated thermogenesis in the cold environment and that this may be partially mediated via butyrate.

AB - The relation between gut microbiota and the host has been suggested to benefit metabolic homeostasis. Brown adipose tissue (BAT) and beige adipocytes facilitate thermogenesis to maintain host core body temperature during cold exposure. However, the potential impact of gut microbiota on the thermogenic process is confused. Here, we evaluated how BAT and white adipose tissue (WAT) responded to temperature challenges in mice lacking gut microbiota. We found that microbiota depletion via treatment with different cocktails of antibiotics (ABX) or in germ-free (GF) mice impaired the thermogenic capacity of BAT by blunting the increase in the expression of uncoupling protein 1 (UCP1) and reducing the browning process of WAT. Gavage of the bacterial metabolite butyrate increased the thermogenic capacity of ABX-treated mice, reversing the deficit. Our results indicate that gut microbiota contributes to upregulated thermogenesis in the cold environment and that this may be partially mediated via butyrate.

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KW - beige adipocytes

KW - brite adipocytes

KW - white adipose tissue

KW - hermogenesis

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KW - germ free mice

KW - macrophage

KW - IL-4

KW - CELLS

KW - COMMENSAL BACTERIA

KW - CATECHOLAMINES

KW - GUT MICROBIOTA

KW - DIET-INDUCED OBESITY

KW - ALTERNATIVELY ACTIVATED MACROPHAGES

KW - ENERGY-EXPENDITURE

KW - DEACETYLATION

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KW - SODIUM-BUTYRATE

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