Intestinal and Hepatic Uptake of Dietary Peroxidized Lipids and Their Decomposition Products, and Their Subsequent Effects on Apolipoprotein A1 and Paraoxonase1

Both pro- and antiatherosclerotic effects have been ascribed to dietary peroxidized lipids. Confusion on the role of peroxidized lipids in atherosclerotic cardiovascular disease is punctuated by a lack of understanding regarding the metabolic fate and potential physiological effects of dietary perox...

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Main Authors: Xueting Jiang, Pragney Deme, Rajat Gupta, Dmitry Litvinov, Kathryn Burge, Sampath Parthasarathy, Chandrakala Aluganti Narasimhulu
Format: Article
Language:English
Published: MDPI AG 2021-08-01
Series:Antioxidants
Subjects:
Online Access:https://www.mdpi.com/2076-3921/10/8/1258
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spelling doaj-b55f3f490f3847be800f57dd19532f3f2021-08-26T13:28:47ZengMDPI AGAntioxidants2076-39212021-08-01101258125810.3390/antiox10081258Intestinal and Hepatic Uptake of Dietary Peroxidized Lipids and Their Decomposition Products, and Their Subsequent Effects on Apolipoprotein A1 and Paraoxonase1Xueting Jiang0Pragney Deme1Rajat Gupta2Dmitry Litvinov3Kathryn Burge4Sampath Parthasarathy5Chandrakala Aluganti Narasimhulu6Burnett School of Biomedical Sciences, College of Medicine, University of Central Florida, Orlando, FL 32827, USABurnett School of Biomedical Sciences, College of Medicine, University of Central Florida, Orlando, FL 32827, USABurnett School of Biomedical Sciences, College of Medicine, University of Central Florida, Orlando, FL 32827, USABurnett School of Biomedical Sciences, College of Medicine, University of Central Florida, Orlando, FL 32827, USADepartment of Pediatrics, Division of Neonatology, University of Oklahoma Health Sciences Center, Oklahoma City, OK 73104, USABurnett School of Biomedical Sciences, College of Medicine, University of Central Florida, Orlando, FL 32827, USABurnett School of Biomedical Sciences, College of Medicine, University of Central Florida, Orlando, FL 32827, USABoth pro- and antiatherosclerotic effects have been ascribed to dietary peroxidized lipids. Confusion on the role of peroxidized lipids in atherosclerotic cardiovascular disease is punctuated by a lack of understanding regarding the metabolic fate and potential physiological effects of dietary peroxidized lipids and their decomposition products. This study sought to determine the metabolic fate and physiological ramifications of 13-hydroperoxyoctadecadienoic acid (13-HPODE) and 13-HODE (13-hydroxyoctadecadienoic acid) supplementation in intestinal and hepatic cell lines, as well as any effects resulting from 13-HPODE or 13-HODE degradation products. In the presence of Caco-2 cells, 13-HPODE was rapidly reduced to 13-HODE. Upon entering the cell, 13-HODE appears to undergo decomposition, followed by esterification. Moreover, 13-HPODE undergoes autodecomposition to produce aldehydes such as 9-oxononanoic acid (9-ONA). Results indicate that 9-ONA was oxidized to azelaic acid (AzA) rapidly in cell culture media, but AzA was poorly absorbed by intestinal cells and remained detectable in cell culture media for up to 18 h. An increased apolipoprotein A1 (ApoA1) secretion was observed in Caco-2 cells in the presence of 13-HPODE, 9-ONA, and AzA, whereas such induction was not observed in HepG2 cells. However, 13-HPODE treatments suppressed paraoxonase 1 (PON1) activity, suggesting the induction of ApoA1 secretion by 13-HPODE may not represent functional high-density lipoprotein (HDL) capable of reducing oxidative stress. Alternatively, AzA induced both ApoA1 secretion and PON1 activity while suppressing ApoB secretion in differentiated Caco-2 cells but not in HepG2. These results suggest oxidation of 9-ONA to AzA might be an important phenomenon, resulting in the accumulation of potentially beneficial dietary peroxidized lipid-derived aldehydes.https://www.mdpi.com/2076-3921/10/8/1258oxidized lipidslinoleic acidfree fatty acid peroxidesoxononanoic acidazelaic acidparaoxonase 1
collection DOAJ
language English
format Article
sources DOAJ
author Xueting Jiang
Pragney Deme
Rajat Gupta
Dmitry Litvinov
Kathryn Burge
Sampath Parthasarathy
Chandrakala Aluganti Narasimhulu
spellingShingle Xueting Jiang
Pragney Deme
Rajat Gupta
Dmitry Litvinov
Kathryn Burge
Sampath Parthasarathy
Chandrakala Aluganti Narasimhulu
Intestinal and Hepatic Uptake of Dietary Peroxidized Lipids and Their Decomposition Products, and Their Subsequent Effects on Apolipoprotein A1 and Paraoxonase1
Antioxidants
oxidized lipids
linoleic acid
free fatty acid peroxides
oxononanoic acid
azelaic acid
paraoxonase 1
author_facet Xueting Jiang
Pragney Deme
Rajat Gupta
Dmitry Litvinov
Kathryn Burge
Sampath Parthasarathy
Chandrakala Aluganti Narasimhulu
author_sort Xueting Jiang
title Intestinal and Hepatic Uptake of Dietary Peroxidized Lipids and Their Decomposition Products, and Their Subsequent Effects on Apolipoprotein A1 and Paraoxonase1
title_short Intestinal and Hepatic Uptake of Dietary Peroxidized Lipids and Their Decomposition Products, and Their Subsequent Effects on Apolipoprotein A1 and Paraoxonase1
title_full Intestinal and Hepatic Uptake of Dietary Peroxidized Lipids and Their Decomposition Products, and Their Subsequent Effects on Apolipoprotein A1 and Paraoxonase1
title_fullStr Intestinal and Hepatic Uptake of Dietary Peroxidized Lipids and Their Decomposition Products, and Their Subsequent Effects on Apolipoprotein A1 and Paraoxonase1
title_full_unstemmed Intestinal and Hepatic Uptake of Dietary Peroxidized Lipids and Their Decomposition Products, and Their Subsequent Effects on Apolipoprotein A1 and Paraoxonase1
title_sort intestinal and hepatic uptake of dietary peroxidized lipids and their decomposition products, and their subsequent effects on apolipoprotein a1 and paraoxonase1
publisher MDPI AG
series Antioxidants
issn 2076-3921
publishDate 2021-08-01
description Both pro- and antiatherosclerotic effects have been ascribed to dietary peroxidized lipids. Confusion on the role of peroxidized lipids in atherosclerotic cardiovascular disease is punctuated by a lack of understanding regarding the metabolic fate and potential physiological effects of dietary peroxidized lipids and their decomposition products. This study sought to determine the metabolic fate and physiological ramifications of 13-hydroperoxyoctadecadienoic acid (13-HPODE) and 13-HODE (13-hydroxyoctadecadienoic acid) supplementation in intestinal and hepatic cell lines, as well as any effects resulting from 13-HPODE or 13-HODE degradation products. In the presence of Caco-2 cells, 13-HPODE was rapidly reduced to 13-HODE. Upon entering the cell, 13-HODE appears to undergo decomposition, followed by esterification. Moreover, 13-HPODE undergoes autodecomposition to produce aldehydes such as 9-oxononanoic acid (9-ONA). Results indicate that 9-ONA was oxidized to azelaic acid (AzA) rapidly in cell culture media, but AzA was poorly absorbed by intestinal cells and remained detectable in cell culture media for up to 18 h. An increased apolipoprotein A1 (ApoA1) secretion was observed in Caco-2 cells in the presence of 13-HPODE, 9-ONA, and AzA, whereas such induction was not observed in HepG2 cells. However, 13-HPODE treatments suppressed paraoxonase 1 (PON1) activity, suggesting the induction of ApoA1 secretion by 13-HPODE may not represent functional high-density lipoprotein (HDL) capable of reducing oxidative stress. Alternatively, AzA induced both ApoA1 secretion and PON1 activity while suppressing ApoB secretion in differentiated Caco-2 cells but not in HepG2. These results suggest oxidation of 9-ONA to AzA might be an important phenomenon, resulting in the accumulation of potentially beneficial dietary peroxidized lipid-derived aldehydes.
topic oxidized lipids
linoleic acid
free fatty acid peroxides
oxononanoic acid
azelaic acid
paraoxonase 1
url https://www.mdpi.com/2076-3921/10/8/1258
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