Effect of sex on glucose handling by adipocytes isolated from rat subcutaneous, mesenteric and perigonadal adipose tissue

Background Adult rat epididymal adipocytes are able to convert large amounts of glucose to lactate and glycerol. However, fatty acid efflux is much lower than that expected from glycerol levels if they were the product of lipolysis. Use of glucose for lipogenesis is limited, in contrast with the act...

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Main Authors: Floriana Rotondo, Ana Cecilia Ho-Palma, Xavier Remesar, José Antonio Fernández-López, María del Mar Romero, Marià Alemany
Format: Article
Language:English
Published: PeerJ Inc. 2018-08-01
Series:PeerJ
Subjects:
Online Access:https://peerj.com/articles/5440.pdf
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author Floriana Rotondo
Ana Cecilia Ho-Palma
Xavier Remesar
José Antonio Fernández-López
María del Mar Romero
Marià Alemany
author_facet Floriana Rotondo
Ana Cecilia Ho-Palma
Xavier Remesar
José Antonio Fernández-López
María del Mar Romero
Marià Alemany
author_sort Floriana Rotondo
collection DOAJ
description Background Adult rat epididymal adipocytes are able to convert large amounts of glucose to lactate and glycerol. However, fatty acid efflux is much lower than that expected from glycerol levels if they were the product of lipolysis. Use of glucose for lipogenesis is limited, in contrast with the active glycolysis-derived lactate (and other 3-carbon substrates). In this study, we analyzed whether white adipose tissue (WAT) site and sex affect these processes. Methods Mature adipocytes from perigonadal, mesenteric and subcutaneous WAT of female and male rats were isolated, and incubated with 7 or 14 mM glucose during 1 or 2 days. Glucose consumption, metabolite efflux and gene expression of glycolytic and lipogenesis-related genes were measured. Results The effects of medium initial glucose concentration were minimal on most parameters studied. Sex-induced differences that were more extensive; however, the most marked, distinct, effects between WAT sites, were dependent on the time of incubation. In general, the production of lactate was maintained during the incubation, but glycerol release rates increased with time, shifting from a largely glycolytic origin to its triacylglycerol (TAG) lipolytic release. Glycerol incorporation was concurrent with increased TAG turnover: lipolytic glycerol was selectively secreted, while most fatty acids were recycled again into TAG. Fatty acid efflux increased with incubation, but was, nevertheless, minimal compared with that of glycerol. Production of lactate and glycerol from glucose were maximal in mesenteric WAT. Discussion Female rats showed a higher adipocyte metabolic activity than males. In mesenteric WAT, gene expression (and substrate efflux) data suggested that adipocyte oxidation of pyruvate to acetyl-CoA was higher in females than in males, with enhanced return of oxaloacetate to the cytoplasm for its final conversion to lactate. WAT site differences showed marked tissue specialization-related differences. Use of glucose for lipogenesis was seriously hampered over time, when TAG turnover-related lipolysis was activated. We postulate that these mechanisms may help decrease glycaemia and fat storage, producing, instead, a higher availability of less-regulated 3-carbon substrates, used for energy elsewhere.
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spelling doaj.art-d140042908714591ad95721f252691682023-12-03T10:26:59ZengPeerJ Inc.PeerJ2167-83592018-08-016e544010.7717/peerj.5440Effect of sex on glucose handling by adipocytes isolated from rat subcutaneous, mesenteric and perigonadal adipose tissueFloriana Rotondo0Ana Cecilia Ho-Palma1Xavier Remesar2José Antonio Fernández-López3 María del Mar Romero4Marià Alemany5Department of Biochemistry and Molecular Biomedicine, University of Barcelona, Faculty of Biology, Barcelona, SpainDepartment of Biochemistry and Molecular Biomedicine, University of Barcelona, Faculty of Biology, Barcelona, SpainDepartment of Biochemistry and Molecular Biomedicine, University of Barcelona, Faculty of Biology, Barcelona, SpainDepartment of Biochemistry and Molecular Biomedicine, University of Barcelona, Faculty of Biology, Barcelona, SpainDepartment of Biochemistry and Molecular Biomedicine, University of Barcelona, Faculty of Biology, Barcelona, SpainDepartment of Biochemistry and Molecular Biomedicine, University of Barcelona, Faculty of Biology, Barcelona, SpainBackground Adult rat epididymal adipocytes are able to convert large amounts of glucose to lactate and glycerol. However, fatty acid efflux is much lower than that expected from glycerol levels if they were the product of lipolysis. Use of glucose for lipogenesis is limited, in contrast with the active glycolysis-derived lactate (and other 3-carbon substrates). In this study, we analyzed whether white adipose tissue (WAT) site and sex affect these processes. Methods Mature adipocytes from perigonadal, mesenteric and subcutaneous WAT of female and male rats were isolated, and incubated with 7 or 14 mM glucose during 1 or 2 days. Glucose consumption, metabolite efflux and gene expression of glycolytic and lipogenesis-related genes were measured. Results The effects of medium initial glucose concentration were minimal on most parameters studied. Sex-induced differences that were more extensive; however, the most marked, distinct, effects between WAT sites, were dependent on the time of incubation. In general, the production of lactate was maintained during the incubation, but glycerol release rates increased with time, shifting from a largely glycolytic origin to its triacylglycerol (TAG) lipolytic release. Glycerol incorporation was concurrent with increased TAG turnover: lipolytic glycerol was selectively secreted, while most fatty acids were recycled again into TAG. Fatty acid efflux increased with incubation, but was, nevertheless, minimal compared with that of glycerol. Production of lactate and glycerol from glucose were maximal in mesenteric WAT. Discussion Female rats showed a higher adipocyte metabolic activity than males. In mesenteric WAT, gene expression (and substrate efflux) data suggested that adipocyte oxidation of pyruvate to acetyl-CoA was higher in females than in males, with enhanced return of oxaloacetate to the cytoplasm for its final conversion to lactate. WAT site differences showed marked tissue specialization-related differences. Use of glucose for lipogenesis was seriously hampered over time, when TAG turnover-related lipolysis was activated. We postulate that these mechanisms may help decrease glycaemia and fat storage, producing, instead, a higher availability of less-regulated 3-carbon substrates, used for energy elsewhere.https://peerj.com/articles/5440.pdfAdipose tissueGlycerolLactateGlycolysisAdipocyteGlycerogenesis
spellingShingle Floriana Rotondo
Ana Cecilia Ho-Palma
Xavier Remesar
José Antonio Fernández-López
María del Mar Romero
Marià Alemany
Effect of sex on glucose handling by adipocytes isolated from rat subcutaneous, mesenteric and perigonadal adipose tissue
PeerJ
Adipose tissue
Glycerol
Lactate
Glycolysis
Adipocyte
Glycerogenesis
title Effect of sex on glucose handling by adipocytes isolated from rat subcutaneous, mesenteric and perigonadal adipose tissue
title_full Effect of sex on glucose handling by adipocytes isolated from rat subcutaneous, mesenteric and perigonadal adipose tissue
title_fullStr Effect of sex on glucose handling by adipocytes isolated from rat subcutaneous, mesenteric and perigonadal adipose tissue
title_full_unstemmed Effect of sex on glucose handling by adipocytes isolated from rat subcutaneous, mesenteric and perigonadal adipose tissue
title_short Effect of sex on glucose handling by adipocytes isolated from rat subcutaneous, mesenteric and perigonadal adipose tissue
title_sort effect of sex on glucose handling by adipocytes isolated from rat subcutaneous mesenteric and perigonadal adipose tissue
topic Adipose tissue
Glycerol
Lactate
Glycolysis
Adipocyte
Glycerogenesis
url https://peerj.com/articles/5440.pdf
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