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      Lipid classes in adipose tissues and liver differ between Shetland ponies and Warmblood horses

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          Abstract

          Fatty acids, as key components of cellular membranes and complex lipids, may play a central role in endocrine signalling and the function of adipose tissue and liver. Thus, the lipid fatty acid composition may play a role in health status in the equine. This study aimed to investigate the fatty acid composition of different tissues and liver lipid classes by comparing Warmblood horses and Shetland ponies under defined conditions. We hypothesized that ponies show different lipid patterns than horses in adipose tissue, liver and plasma. Six Warmblood horses and six Shetland ponies were housed and fed under identical conditions. Tissue and blood sampling were performed following a standardized protocol. A one-step lipid extraction, methylation and trans-esterification method with subsequent gas chromatography was used to analyse the total lipid content and fatty acid profile of retroperitoneal, mesocolon and subcutaneous adipose tissue, liver and plasma. Fatty acids were grouped according to their degree of saturation and their conjugated double bond into the respective lipid classes. In the adipose tissues, saturated fatty acids (SFAs) and n-9 monounsaturated fatty acids (n-9 MUFAs) were most present in ponies and horses. N-6 polyunsaturated fatty acids (n-6 PUFAs), followed by SFAs, were most frequently found in liver tissue and plasma in all animals. Horses, in comparison to ponies, had significantly higher n-6 PUFA levels in all tissues and plasma. In liver tissue, horses had significantly lower hepatic iso-branched-chain fatty acids (iso-BCFAs) than ponies. The hepatic fatty acid composition of selected lipid classes was different between horses and ponies. In the polar PL fraction, horses had low n-9 MUFA and n-3 PUFA contents but higher n-6 PUFA contents than ponies. Furthermore, iso-BCFAs are absent in several hepatic lipid fractions of horses but not ponies. The differences in fatty acid lipid classes between horses and ponies provide key information on the species- and location-specific regulation of FA metabolism, thus affecting health status such as inflammatory responses.

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          Most cited references51

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          Structure, function, and dietary regulation of delta6, delta5, and delta9 desaturases.

          Fatty acid desaturases introduce a double bond in a specific position of long-chain fatty acids, and are conserved across kingdoms. Degree of unsaturation of fatty acids affects physical properties of membrane phospholipids and stored triglycerides. In addition, metabolites of polyunsaturated fatty acids are used as signaling molecules in many organisms. Three desaturases, Delta9, Delta6, and Delta5, are present in humans. Delta-9 catalyzes synthesis of monounsaturated fatty acids. Oleic acid, a main product of Delta9 desaturase, is the major fatty acid in mammalian adipose triglycerides, and is also used for phospholipid and cholesteryl ester synthesis. Delta-6 and Delta5 desaturases are required for the synthesis of highly unsaturated fatty acids (HUFAs), which are mainly esterified into phospholipids and contribute to maintaining membrane fluidity. While HUFAs may be required for cold tolerance in plants and fish, the primary role of HUFAs in mammals is cell signaling. Arachidonic acid is required as substrates for eicosanoid synthesis, while docosahexaenoic acid is required in visual and neuronal functions. Desaturases in mammals are regulated at the transcriptional level. Reflecting overlapping functions, three desaturases share a common mechanism of a feedback regulation to maintain products in membrane phospholipids. At the same time, regulation of Delta9 desaturase differs from Delta6 and Delta5 desaturases because its products are incorporated into more diverse lipid groups. Combinations of multiple transcription factors achieve this sophisticated differential regulation.
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            Habitual dietary intake of n-3 and n-6 fatty acids in relation to inflammatory markers among US men and women.

            Polyunsaturated fatty acid intake favorably affects chronic inflammatory-related diseases such as cardiovascular disease; however, high intake of n-6 fatty acids may attenuate the known beneficial effects of n-3 fatty acids. We investigated habitual dietary n-3 fatty acid intake and its interaction with n-6 fatty acids in relation to the plasma inflammatory markers C-reactive protein, interleukin 6, and soluble tumor necrosis factor receptors 1 and 2 (sTNF-R1 and R2) among 405 healthy men and 454 healthy women. After adjustment for other predictors of inflammation, intake of the n-3 fatty acids eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) was inversely associated with plasma levels of sTNF-R1 and sTNF-R2 (P=0.03 and P<0.001, respectively) and somewhat less so for C-reactive protein (P=0.08). n-3 alpha-linolenic acid and n-6 cis-linoleic acid were not significantly related to the inflammatory markers. We found little if any association between n-3 fatty acid (EPA+DHA) intake and tumor necrosis factor receptors among participants with low intake of n-6 but a strong inverse association among those with high n-6 intake (P=0.04 and 0.002 for interaction of n-3 with n-6 on sTNF-R1 and sTNF-R2, respectively). These results suggest that n-6 fatty acids do not inhibit the antiinflammatory effects of n-3 fatty acids and that the combination of both types of fatty acids is associated with the lowest levels of inflammation. The inhibition of inflammatory cytokines may be one possible mechanism for the observed beneficial effects of these fatty acids on chronic inflammatory-related diseases.
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              Genetic variants of the FADS1 FADS2 gene cluster are associated with altered (n-6) and (n-3) essential fatty acids in plasma and erythrocyte phospholipids in women during pregnancy and in breast milk during lactation.

              The enzymes encoded by fatty acid desaturase (FADS) 1 and FADS2 are rate-limiting enzymes in the desaturation of linoleic acid [LA; 18:2(n-6)] to arachidonic acid [ARA; 20:4(n-6)], and alpha-linolenic acid [ALA; 18:3(n-3)] to eicosapentaenoic acid [EPA; 20:5(n-3)] and docosahexaenoic acid [DHA; 22:6(n-3)]. ARA, EPA, and DHA play central roles in infant growth, neural development, and immune function. The maternal ARA, EPA, and DHA status in gestation influences maternal-to-infant transfer and breast milk provides fatty acids for infants after birth. We determined if single nucleotide polymorphisms in FADS1 and FADS2 influence plasma phospholipid and erythrocyte ethanolamine phosphoglyceride (EPG) (n-6) and (n-3) fatty acids of women in pregnancy or their breast milk during lactation. We genotyped rs174553, rs99780, rs174575, and rs174583 in the FADS1 FADS2 gene cluster and analyzed plasma and erythrocyte fatty acids and dietary intake for 69 pregnant women and breast milk for a subset of 54 women exclusively breast-feeding at 1 mo postpartum. Minor allele homozygotes of rs174553(GG), rs99780(TT), and rs174583(TT) had lower ARA but higher LA in plasma phospholipids and erythrocyte EPG and decreased (n-6) and (n-3) fatty acid product:precursor ratios at 16 and 36 wk of gestation. Breast milk fatty acids were influenced by genotype, with significantly lower 14:0, ARA, and EPA but higher 20:2(n-6) in the minor allele homozygotes of rs174553(GG), rs99780(TT), and rs174583(TT) and lower ARA, EPA, 22:5(n-3), and DHA in the minor allele homozygotes G/G of rs174575. We showed that genetic variants of FADS1 and FADS2 influence blood lipid and breast milk essential fatty acids in pregnancy and lactation.
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                Author and article information

                Contributors
                Role: Formal analysisRole: Writing – original draftRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: ResourcesRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                21 March 2019
                2019
                : 14
                : 3
                : e0207568
                Affiliations
                [1 ] Institute of Animal Nutrition, Nutrition Diseases and Dietetics, Faculty of Veterinary Medicine, University of Leipzig, Leipzig, Germany
                [2 ] Institute of Biochemistry, Faculty of Veterinary Medicine, University of Leipzig, Leipzig, Germany
                [3 ] University Equine Hospital, formerly Large Animal Clinic for Surgery, Faculty of Veterinary Medicine, University of Leipzig, Leipzig, Germany
                University of Illinois, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-7641-3336
                http://orcid.org/0000-0001-7151-0751
                Article
                PONE-D-18-31443
                10.1371/journal.pone.0207568
                6428305
                30897169
                d4057589-edaf-4549-ae26-c5e580aae40a
                © 2019 Adolph et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 31 October 2018
                : 1 March 2019
                Page count
                Figures: 1, Tables: 4, Pages: 18
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: VE 225/9-1
                Award Recipient :
                This study was funded by the German Research Foundation (VE 225/9-1) and the University of Leipzig within the program of Open Access Publishing. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Equines
                Horses
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Mammals
                Equines
                Ponies
                Biology and Life Sciences
                Biochemistry
                Lipids
                Fatty Acids
                Biology and Life Sciences
                Biochemistry
                Lipids
                Biology and Life Sciences
                Biochemistry
                Lipids
                Fats
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Blood
                Blood Plasma
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Blood
                Blood Plasma
                Biology and Life Sciences
                Physiology
                Body Fluids
                Blood
                Blood Plasma
                Medicine and Health Sciences
                Physiology
                Body Fluids
                Blood
                Blood Plasma
                Medicine and Health Sciences
                Endocrinology
                Diabetic Endocrinology
                Insulin
                Biology and Life Sciences
                Biochemistry
                Hormones
                Insulin
                Biology and Life Sciences
                Cell Biology
                Cellular Structures and Organelles
                Cell Membranes
                Membrane Metabolism
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files ( S1 Dataset).

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                Uncategorized

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