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 journalArticle

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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 languageEnglish
Pages (from-to)2720-2737
Number of pages18
JournalCell Reports
Volume26
Issue number10
Early online date5 Mar 2019
DOIs
Publication statusPublished - 5 Mar 2019

Fingerprint

White Adipose Tissue
Brown Adipose Tissue
Thermogenesis
Microbiota
Tissue
Butyrates
Body Temperature
Metabolites
Homeostasis
Anti-Bacterial Agents
Temperature
Gastrointestinal Microbiome
Proteins

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)

Cite this

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 journalArticle

Li, B, Li, L, Li, M, Lam, SM, Wang, G, Wu, Y, Zhang, H, Niu, C, Zhang, X, Liu, X, Hambly, C, Jin, W, Shui, G & Speakman, JR 2019, 'Microbiota Depletion Impairs Thermogenesis of Brown Adipose Tissue and Browning of White Adipose Tissue', Cell Reports, vol. 26, no. 10, pp. 2720-2737. https://doi.org/10.1016/j.celrep.2019.02.015
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. / Microbiota Depletion Impairs Thermogenesis of Brown Adipose Tissue and Browning of White Adipose Tissue. In: Cell Reports. 2019 ; Vol. 26, No. 10. pp. 2720-2737.
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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.",
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AU - Li, Baoguo

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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

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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.

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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.

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KW - brite adipocytes

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