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Petrus, Paul; Lecoutre, Simon; Dollet, Lucile; Wiel, Clotilde; Sulen, André; Gao, Hui; Tavira, Beatriz; Laurencikiene, Jurga; Rooyackers, Olav; Checa, Antonio; Douagi, Iyadh; Wheelock, Craig E.; Arner, Peter; McCarthy, Mark; Bergo, Martin O.; Edgar, Laurienne; Choudhury, Robin P.; Aouadi, Myriam; Krook, Anna; Rydén, Mikael
Cell metabolism, 02/2020, Letnik: 31, Številka: 2Journal Article
While obesity and associated metabolic complications are linked to inflammation of white adipose tissue (WAT), the causal factors remain unclear. We hypothesized that the local metabolic environment could be an important determinant. To this end, we compared metabolites released from WAT of 81 obese and non-obese women. This identified glutamine to be downregulated in obesity and inversely associated with a pernicious WAT phenotype. Glutamine administration in vitro and in vivo attenuated both pro-inflammatory gene and protein levels in adipocytes and WAT and macrophage infiltration in WAT. Metabolomic and bioenergetic analyses in human adipocytes suggested that glutamine attenuated glycolysis and reduced uridine diphosphate N-acetylglucosamine (UDP-GlcNAc) levels. UDP-GlcNAc is the substrate for the post-translational modification O-linked β-N-acetylglucosamine (O-GlcNAc) mediated by the enzyme O-GlcNAc transferase. Functional studies in human adipocytes established a mechanistic link between reduced glutamine, O-GlcNAcylation of nuclear proteins, and a pro-inflammatory transcriptional response. Altogether, glutamine metabolism is linked to WAT inflammation in obesity. Display omitted •Human adipose glutamine levels correlate inversely with fat mass and inflammation•Glutamine administration to mice attenuates adipose tissue inflammation•High glutamine reduces glycolysis and inflammation in human fat cells in vitro•Nuclear O-GlcNAcylation links glutamine to inflammation in adipose tissue Obesity is linked to white adipose tissue inflammation, but the causal factors remain unclear. Based on data obtained from clinical cohorts, mouse models, and cell cultures, Petrus et al. show that a reduction of adipose tissue glutamine levels in obesity leads to increased nuclear O-GlcNAcylation in adipocytes, which induces transcriptional activity of pro-inflammatory pathways.
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