Human intestinal lipid storage through sequential meals reveals faster dinner appearance is associated with hyperlipidemia

Background It is increasingly recognized that intestinal cells can store lipids after a meal, yet the effect of this phenomenon on lipid absorption patterns in insulin resistance remains unknown.Methods The kinetics of meal fat appearance were measured in insulin-sensitive (IS, n = 8) and insulin-re...

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Main Authors: Miriam Jacome-Sosa, Qiong Hu, Camila M. Manrique-Acevedo, Robert D. Phair, Elizabeth J. Parks
Format: Article
Language:English
Published: American Society for Clinical investigation 2021-08-01
Series:JCI Insight
Subjects:
Online Access:https://doi.org/10.1172/jci.insight.148378
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author Miriam Jacome-Sosa
Qiong Hu
Camila M. Manrique-Acevedo
Robert D. Phair
Elizabeth J. Parks
author_facet Miriam Jacome-Sosa
Qiong Hu
Camila M. Manrique-Acevedo
Robert D. Phair
Elizabeth J. Parks
author_sort Miriam Jacome-Sosa
collection DOAJ
description Background It is increasingly recognized that intestinal cells can store lipids after a meal, yet the effect of this phenomenon on lipid absorption patterns in insulin resistance remains unknown.Methods The kinetics of meal fat appearance were measured in insulin-sensitive (IS, n = 8) and insulin-resistant (IR, n = 8) subjects after sequential, isotopically labeled lunch and dinner meals. Plasma dynamics on triacylglycerol-rich (TAG-rich) lipoproteins and plasma hormones were analyzed using a nonlinear, non–steady state kinetic model.Results At the onset of dinner, IS subjects showed an abrupt plasma appearance of lunch lipid consistent with the “second-meal effect,” followed by slower appearance of dinner fat in plasma, resulting in reduced accumulation of dinner TAG of 48% compared with lunch. By contrast, IR subjects exhibited faster meal TAG appearance rates after both lunch and dinner. This effect of lower enterocyte storage between meals was associated with greater nocturnal and next-morning hyperlipidemia. The biochemical data and the kinetic analysis of second-meal effect dynamics are consistent with rapid secretion of stored TAG bypassing lipolysis and resynthesis. In addition, the data are consistent with a role for the diurnal pattern of plasma leptin in regulating the processing of dietary lipid.Conclusion These data support the concept that intestinal lipid storage may be physiologically beneficial in IS subjects.Trial registration ClinicalTrials.gov NCT02020343.Funding This study was supported by a grant from the American Diabetes Association (grant 1-13-TS-12).
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spelling doaj.art-30cd366a60a64a838072b83ec280b7c12022-12-22T02:41:12ZengAmerican Society for Clinical investigationJCI Insight2379-37082021-08-01615Human intestinal lipid storage through sequential meals reveals faster dinner appearance is associated with hyperlipidemiaMiriam Jacome-SosaQiong HuCamila M. Manrique-AcevedoRobert D. PhairElizabeth J. ParksBackground It is increasingly recognized that intestinal cells can store lipids after a meal, yet the effect of this phenomenon on lipid absorption patterns in insulin resistance remains unknown.Methods The kinetics of meal fat appearance were measured in insulin-sensitive (IS, n = 8) and insulin-resistant (IR, n = 8) subjects after sequential, isotopically labeled lunch and dinner meals. Plasma dynamics on triacylglycerol-rich (TAG-rich) lipoproteins and plasma hormones were analyzed using a nonlinear, non–steady state kinetic model.Results At the onset of dinner, IS subjects showed an abrupt plasma appearance of lunch lipid consistent with the “second-meal effect,” followed by slower appearance of dinner fat in plasma, resulting in reduced accumulation of dinner TAG of 48% compared with lunch. By contrast, IR subjects exhibited faster meal TAG appearance rates after both lunch and dinner. This effect of lower enterocyte storage between meals was associated with greater nocturnal and next-morning hyperlipidemia. The biochemical data and the kinetic analysis of second-meal effect dynamics are consistent with rapid secretion of stored TAG bypassing lipolysis and resynthesis. In addition, the data are consistent with a role for the diurnal pattern of plasma leptin in regulating the processing of dietary lipid.Conclusion These data support the concept that intestinal lipid storage may be physiologically beneficial in IS subjects.Trial registration ClinicalTrials.gov NCT02020343.Funding This study was supported by a grant from the American Diabetes Association (grant 1-13-TS-12).https://doi.org/10.1172/jci.insight.148378Metabolism
spellingShingle Miriam Jacome-Sosa
Qiong Hu
Camila M. Manrique-Acevedo
Robert D. Phair
Elizabeth J. Parks
Human intestinal lipid storage through sequential meals reveals faster dinner appearance is associated with hyperlipidemia
JCI Insight
Metabolism
title Human intestinal lipid storage through sequential meals reveals faster dinner appearance is associated with hyperlipidemia
title_full Human intestinal lipid storage through sequential meals reveals faster dinner appearance is associated with hyperlipidemia
title_fullStr Human intestinal lipid storage through sequential meals reveals faster dinner appearance is associated with hyperlipidemia
title_full_unstemmed Human intestinal lipid storage through sequential meals reveals faster dinner appearance is associated with hyperlipidemia
title_short Human intestinal lipid storage through sequential meals reveals faster dinner appearance is associated with hyperlipidemia
title_sort human intestinal lipid storage through sequential meals reveals faster dinner appearance is associated with hyperlipidemia
topic Metabolism
url https://doi.org/10.1172/jci.insight.148378
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