TY - JOUR
T1 - Lysine-specific demethylase 1 promotes brown adipose tissue thermogenesis via repressing glucocorticoid activation
AU - Zeng, Xing
AU - Jedrychowski, Mark P.
AU - Chen, Yi
AU - Serag, Sara
AU - Lavery, Gareth G.
AU - Gygi, Steve P.
AU - Spiegelman, Bruce M.
N1 - Funding Information:
We thank Stuart Orkin and Marc Kerenyi for generously sharing the lsd1flox animals, Yang Shi and Benoît Laurent for providing the LSD1 constructs and experimental advice, Zachary Herbert and the Molecular Biology Core Facilities at Dana Farber Cancer Institute for sequencing studies, the Rodent Histology Core at Harvard Medical School for histology studies, and the Nikon Imaging Center at Harvard Medical School for immunofluorescence studies. This study was supported by National Institutes of Health grant DK31405 to B.M.S., and an American Heart Association post-doctoral fellowship to X.Z.
Publisher Copyright:
© 2016 Georgilis and Gil; Published by Cold Spring Harbor Laboratory Press.
PY - 2016/8/15
Y1 - 2016/8/15
N2 - Brown adipocytes display phenotypic plasticity, as they can switch between the active states of fatty acid oxidation and energy dissipation versus a more dormant state. Cold exposure or β-adrenergic stimulation favors the active thermogenic state, whereas sympathetic denervation or glucocorticoid administration promotes more lipid accumulation. Our understanding of the molecular mechanisms underlying these switches is incomplete. Here we found that LSD1 (lysine-specific demethylase 1), a histone demethylase, regulates brown adipocyte metabolism in two ways. On the one hand, LSD1 associates with PRDM16 to repress expression of white fat-selective genes. On the other hand, LSD1 represses HSD11B1 (hydroxysteroid 11-β-dehydrogenase isozyme 1), a key glucocorticoid-activating enzyme, independently from PRDM16. Adipose-specific ablation of LSD1 impaired mitochondrial fatty acid oxidation capacity of the brown adipose tissue, reduced whole-body energy expenditure, and increased fat deposition, which can be significantly alleviated by simultaneously deleting HSD11B1. These findings establish a novel regulatory pathway connecting histone modification and hormone activation with mitochondrial oxidative capacity and whole-body energy homeostasis.
AB - Brown adipocytes display phenotypic plasticity, as they can switch between the active states of fatty acid oxidation and energy dissipation versus a more dormant state. Cold exposure or β-adrenergic stimulation favors the active thermogenic state, whereas sympathetic denervation or glucocorticoid administration promotes more lipid accumulation. Our understanding of the molecular mechanisms underlying these switches is incomplete. Here we found that LSD1 (lysine-specific demethylase 1), a histone demethylase, regulates brown adipocyte metabolism in two ways. On the one hand, LSD1 associates with PRDM16 to repress expression of white fat-selective genes. On the other hand, LSD1 represses HSD11B1 (hydroxysteroid 11-β-dehydrogenase isozyme 1), a key glucocorticoid-activating enzyme, independently from PRDM16. Adipose-specific ablation of LSD1 impaired mitochondrial fatty acid oxidation capacity of the brown adipose tissue, reduced whole-body energy expenditure, and increased fat deposition, which can be significantly alleviated by simultaneously deleting HSD11B1. These findings establish a novel regulatory pathway connecting histone modification and hormone activation with mitochondrial oxidative capacity and whole-body energy homeostasis.
KW - Brown adipose tissue
KW - HSD11B1
KW - LSD1
KW - Mitochondria
KW - PRDM16
KW - Thermogenesis
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U2 - 10.1101/gad.285312.116
DO - 10.1101/gad.285312.116
M3 - Article
C2 - 27566776
AN - SCOPUS:84986881095
SN - 0890-9369
VL - 30
SP - 1822
EP - 1836
JO - Genes and Development
JF - Genes and Development
IS - 16
ER -