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      Analysis of porcine adipose tissue transcriptome reveals differences in de novo fatty acid synthesis in pigs with divergent muscle fatty acid composition

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          Abstract

          Background

          In pigs, adipose tissue is one of the principal organs involved in the regulation of lipid metabolism. It is particularly involved in the overall fatty acid synthesis with consequences in other lipid-target organs such as muscles and the liver. With this in mind, we have used massive, parallel high-throughput sequencing technologies to characterize the porcine adipose tissue transcriptome architecture in six Iberian x Landrace crossbred pigs showing extreme phenotypes for intramuscular fatty acid composition (three per group).

          Results

          High-throughput RNA sequencing was used to generate a whole characterization of adipose tissue (backfat) transcriptome. A total of 4,130 putative unannotated protein-coding sequences were identified in the 20% of reads which mapped in intergenic regions. Furthermore, 36% of the unmapped reads were represented by interspersed repeats, SINEs being the most abundant elements. Differential expression analyses identified 396 candidate genes among divergent animals for intramuscular fatty acid composition. Sixty-two percent of these genes (247/396) presented higher expression in the group of pigs with higher content of intramuscular SFA and MUFA, while the remaining 149 showed higher expression in the group with higher content of PUFA. Pathway analysis related these genes to biological functions and canonical pathways controlling lipid and fatty acid metabolisms. In concordance with the phenotypic classification of animals, the major metabolic pathway differentially modulated between groups was de novo lipogenesis, the group with more PUFA being the one that showed lower expression of lipogenic genes.

          Conclusions

          These results will help in the identification of genetic variants at loci that affect fatty acid composition traits. The implications of these results range from the improvement of porcine meat quality traits to the application of the pig as an animal model of human metabolic diseases.

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          Most cited references42

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          Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism.

          Dysregulation of lipid metabolism in individual tissues leads to systemic disruption of insulin action and glucose metabolism. Utilizing quantitative lipidomic analyses and mice deficient in adipose tissue lipid chaperones aP2 and mal1, we explored how metabolic alterations in adipose tissue are linked to whole-body metabolism through lipid signals. A robust increase in de novo lipogenesis rendered the adipose tissue of these mice resistant to the deleterious effects of dietary lipid exposure. Systemic lipid profiling also led to identification of C16:1n7-palmitoleate as an adipose tissue-derived lipid hormone that strongly stimulates muscle insulin action and suppresses hepatosteatosis. Our data reveal a lipid-mediated endocrine network and demonstrate that adipose tissue uses lipokines such as C16:1n7-palmitoleate to communicate with distant organs and regulate systemic metabolic homeostasis.
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            Fatty acid synthesis and its regulation.

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              Role for stearoyl-CoA desaturase-1 in leptin-mediated weight loss.

              Leptin elicits a metabolic response that cannot be explained by its anorectic effects alone. To examine the mechanism underlying leptin's metabolic actions, we used transcription profiling to identify leptin-regulated genes in ob/ob liver. Leptin was found to specifically repress RNA levels and enzymatic activity of hepatic stearoyl-CoA desaturase-1 (SCD-1), which catalyzes the biosynthesis of monounsaturated fatty acids. Mice lacking SCD-1 were lean and hypermetabolic. ob/ob mice with mutations in SCD-1 were significantly less obese than ob/ob controls and had markedly increased energy expenditure. ob/ob mice with mutations in SCD-1 had histologically normal livers with significantly reduced triglyceride storage and VLDL (very low density lipoprotein) production. These findings suggest that down-regulation of SCD-1 is an important component of leptin's metabolic actions.
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                Author and article information

                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central
                1471-2164
                2013
                1 December 2013
                : 14
                : 843
                Affiliations
                [1 ]Centre de Recerca en Agrigenòmica (Consorci CSIC-IRTA-UAB-UB), Edifici CRAG, Campus UAB, Bellaterra, 08193 Barcelona, Spain
                [2 ]Departament de Ciència Animal i dels Aliments, Facultat de Veterinària, Campus UAB, Bellaterra, 08193 Barcelona, Spain
                [3 ]INRA, UMR 1313 Génétique Animale et Biologie Intégrative (GABI), Equipe Génétique Immunité Santé, Jouy-en-Josas F-78352 France
                [4 ]AgroParisTech, UMR 1313 GABI, Jouy-en-Josas F-78352 France
                [5 ]CEA, DSV/iRCM/SREIT/LREG, Jouy-en-Josas F-78352 France
                [6 ]Departamento de Mejora Genética Animal, INIA, Ctra. de la Coruña km. 7, 28040 Madrid, Spain
                [7 ]Genètica i Millora Animal, IRTA Lleida, 25198 Lleida, Spain
                Article
                1471-2164-14-843
                10.1186/1471-2164-14-843
                3879068
                24289474
                6534429e-6d4e-4566-bab7-74deff5364f9
                Copyright © 2013 Corominas et al.; licensee BioMed Central Ltd.

                This is an open access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 7 June 2013
                : 25 November 2013
                Categories
                Research Article

                Genetics
                rna-seq,de novo lipogenesis,transcriptome,adipose tissue,pork
                Genetics
                rna-seq, de novo lipogenesis, transcriptome, adipose tissue, pork

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