Olive- and Coconut-Oil-Enriched Diets Decreased Secondary Bile Acids and Regulated Metabolic and Transcriptomic Markers of Brain Injury in the Frontal Cortexes of NAFLD Pigs

The objective of this study was to investigate the effect of dietary fatty acid (FA) saturation and carbon chain length on brain bile acid (BA) metabolism and neuronal number in a pig model of pediatric NAFLD. Thirty 20-day-old Iberian pigs, pair-housed in pens, were randomly assigned to receive one...

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Main Authors: Magdalena A. Maj, Tanvi R. Gehani, Chad Immoos, Mikaelah S. Medrano, Rob K. Fanter, Christine R. Strand, Hunter Glanz, Brian D. Piccolo, Mohammed K. Abo-Ismail, Michael R. La Frano, Rodrigo Manjarín
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Language:English
Published: MDPI AG 2022-09-01
Series:Brain Sciences
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Online Access:https://www.mdpi.com/2076-3425/12/9/1193
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author Magdalena A. Maj
Tanvi R. Gehani
Chad Immoos
Mikaelah S. Medrano
Rob K. Fanter
Christine R. Strand
Hunter Glanz
Brian D. Piccolo
Mohammed K. Abo-Ismail
Michael R. La Frano
Rodrigo Manjarín
author_facet Magdalena A. Maj
Tanvi R. Gehani
Chad Immoos
Mikaelah S. Medrano
Rob K. Fanter
Christine R. Strand
Hunter Glanz
Brian D. Piccolo
Mohammed K. Abo-Ismail
Michael R. La Frano
Rodrigo Manjarín
author_sort Magdalena A. Maj
collection DOAJ
description The objective of this study was to investigate the effect of dietary fatty acid (FA) saturation and carbon chain length on brain bile acid (BA) metabolism and neuronal number in a pig model of pediatric NAFLD. Thirty 20-day-old Iberian pigs, pair-housed in pens, were randomly assigned to receive one of three hypercaloric diets for 10 weeks: (1) lard-enriched (LAR; <i>n</i> = 5 pens), (2) olive-oil-enriched (OLI, <i>n</i> = 5), and (3) coconut-oil-enriched (COC; <i>n</i> = 5). Pig behavior and activity were analyzed throughout the study. All animals were euthanized on week 10 and frontal cortex (FC) samples were collected for immunohistochemistry, metabolomic, and transcriptomic analyses. Data were analyzed by multivariate and univariate statistics. No differences were observed in relative brain weight, neuronal number, or cognitive functioning between diets. Pig activity and FC levels of neuroprotective secondary BAs and betaine decreased in the COC and OLI groups compared with LAR, and paralleled the severity of NAFLD. In addition, OLI-fed pigs showed downregulation of genes involved in neurotransmission, synaptic transmission, and nervous tissue development. Similarly, COC-fed pigs showed upregulation of neurogenesis and myelin repair genes, which caused the accumulation of medium-chain acylcarnitines in brain tissue. In conclusion, our results indicate that secondary BA levels in the FCs of NAFLD pigs are affected by dietary FA composition and are associated with metabolic and transcriptomic markers of brain injury. Dietary interventions that aim to replace saturated FAs by medium-chain or monounsaturated FAs in high-fat hypercaloric diets may have a negative effect on brain health in NAFLD patients.
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spelling doaj.art-16494241450f4f88a996fbccb785adfc2023-11-23T15:20:48ZengMDPI AGBrain Sciences2076-34252022-09-01129119310.3390/brainsci12091193Olive- and Coconut-Oil-Enriched Diets Decreased Secondary Bile Acids and Regulated Metabolic and Transcriptomic Markers of Brain Injury in the Frontal Cortexes of NAFLD PigsMagdalena A. Maj0Tanvi R. Gehani1Chad Immoos2Mikaelah S. Medrano3Rob K. Fanter4Christine R. Strand5Hunter Glanz6Brian D. Piccolo7Mohammed K. Abo-Ismail8Michael R. La Frano9Rodrigo Manjarín10Department of Biological Sciences, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USADepartment of Biomedical Engineering, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USADepartment of Chemistry and Biochemistry, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USADepartment of Chemistry and Biochemistry, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USACollege of Agriculture, Food and Environmental Sciences, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USADepartment of Biological Sciences, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USADepartment of Statistics, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USAUSDA-ARS Arkansas Children’s Nutrition Center, 1120 Marshall St. SLOT 512-20B, Little Rock, AR 72202, USADepartment of Animal Science, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USACal Poly Metabolomics Service Center, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USADepartment of Animal Science, California Polytechnic State University, 1 Grand Ave., San Luis Obispo, CA 93407, USAThe objective of this study was to investigate the effect of dietary fatty acid (FA) saturation and carbon chain length on brain bile acid (BA) metabolism and neuronal number in a pig model of pediatric NAFLD. Thirty 20-day-old Iberian pigs, pair-housed in pens, were randomly assigned to receive one of three hypercaloric diets for 10 weeks: (1) lard-enriched (LAR; <i>n</i> = 5 pens), (2) olive-oil-enriched (OLI, <i>n</i> = 5), and (3) coconut-oil-enriched (COC; <i>n</i> = 5). Pig behavior and activity were analyzed throughout the study. All animals were euthanized on week 10 and frontal cortex (FC) samples were collected for immunohistochemistry, metabolomic, and transcriptomic analyses. Data were analyzed by multivariate and univariate statistics. No differences were observed in relative brain weight, neuronal number, or cognitive functioning between diets. Pig activity and FC levels of neuroprotective secondary BAs and betaine decreased in the COC and OLI groups compared with LAR, and paralleled the severity of NAFLD. In addition, OLI-fed pigs showed downregulation of genes involved in neurotransmission, synaptic transmission, and nervous tissue development. Similarly, COC-fed pigs showed upregulation of neurogenesis and myelin repair genes, which caused the accumulation of medium-chain acylcarnitines in brain tissue. In conclusion, our results indicate that secondary BA levels in the FCs of NAFLD pigs are affected by dietary FA composition and are associated with metabolic and transcriptomic markers of brain injury. Dietary interventions that aim to replace saturated FAs by medium-chain or monounsaturated FAs in high-fat hypercaloric diets may have a negative effect on brain health in NAFLD patients.https://www.mdpi.com/2076-3425/12/9/1193transcriptomicsmetabolomicsIberian pigsbrainpediatric modelneurodegeneration
spellingShingle Magdalena A. Maj
Tanvi R. Gehani
Chad Immoos
Mikaelah S. Medrano
Rob K. Fanter
Christine R. Strand
Hunter Glanz
Brian D. Piccolo
Mohammed K. Abo-Ismail
Michael R. La Frano
Rodrigo Manjarín
Olive- and Coconut-Oil-Enriched Diets Decreased Secondary Bile Acids and Regulated Metabolic and Transcriptomic Markers of Brain Injury in the Frontal Cortexes of NAFLD Pigs
Brain Sciences
transcriptomics
metabolomics
Iberian pigs
brain
pediatric model
neurodegeneration
title Olive- and Coconut-Oil-Enriched Diets Decreased Secondary Bile Acids and Regulated Metabolic and Transcriptomic Markers of Brain Injury in the Frontal Cortexes of NAFLD Pigs
title_full Olive- and Coconut-Oil-Enriched Diets Decreased Secondary Bile Acids and Regulated Metabolic and Transcriptomic Markers of Brain Injury in the Frontal Cortexes of NAFLD Pigs
title_fullStr Olive- and Coconut-Oil-Enriched Diets Decreased Secondary Bile Acids and Regulated Metabolic and Transcriptomic Markers of Brain Injury in the Frontal Cortexes of NAFLD Pigs
title_full_unstemmed Olive- and Coconut-Oil-Enriched Diets Decreased Secondary Bile Acids and Regulated Metabolic and Transcriptomic Markers of Brain Injury in the Frontal Cortexes of NAFLD Pigs
title_short Olive- and Coconut-Oil-Enriched Diets Decreased Secondary Bile Acids and Regulated Metabolic and Transcriptomic Markers of Brain Injury in the Frontal Cortexes of NAFLD Pigs
title_sort olive and coconut oil enriched diets decreased secondary bile acids and regulated metabolic and transcriptomic markers of brain injury in the frontal cortexes of nafld pigs
topic transcriptomics
metabolomics
Iberian pigs
brain
pediatric model
neurodegeneration
url https://www.mdpi.com/2076-3425/12/9/1193
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