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      Long noncoding RNAs in lipid metabolism: literature review and conservation analysis across species

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          Abstract

          Background

          Lipids are important for the cell and organism life since they are major components of membranes, energy reserves and are also signal molecules. The main organs for the energy synthesis and storage are the liver and adipose tissue, both in humans and in more distant species such as chicken. Long noncoding RNAs (lncRNAs) are known to be involved in many biological processes including lipid metabolism.

          Results

          In this context, this paper provides the most exhaustive list of lncRNAs involved in lipid metabolism with 60 genes identified after an in-depth analysis of the bibliography, while all “review” type articles list a total of 27 genes. These 60 lncRNAs are mainly described in human or mice and only a few of them have a precise described mode-of-action. Because these genes are still named in a non-standard way making such a study tedious, we propose a standard name for this list according to the rules dictated by the HUGO consortium. Moreover, we identified about 10% of lncRNAs which are conserved between mammals and chicken and 2% between mammals and fishes. Finally, we demonstrated that two lncRNA were wrongly considered as lncRNAs in the literature since they are 3′ extensions of the closest coding gene.

          Conclusions

          Such a lncRNAs catalogue can participate to the understanding of the lipid metabolism regulators; it can be useful to better understand the genetic regulation of some human diseases (obesity, hepatic steatosis) or traits of economic interest in livestock species (meat quality, carcass composition). We have no doubt that this first set will be rapidly enriched in coming years.

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          Most cited references81

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          PhyloCSF: a comparative genomics method to distinguish protein coding and non-coding regions

          Motivation: As high-throughput transcriptome sequencing provides evidence for novel transcripts in many species, there is a renewed need for accurate methods to classify small genomic regions as protein coding or non-coding. We present PhyloCSF, a novel comparative genomics method that analyzes a multispecies nucleotide sequence alignment to determine whether it is likely to represent a conserved protein-coding region, based on a formal statistical comparison of phylogenetic codon models. Results: We show that PhyloCSF's classification performance in 12-species Drosophila genome alignments exceeds all other methods we compared in a previous study. We anticipate that this method will be widely applicable as the transcriptomes of many additional species, tissues and subcellular compartments are sequenced, particularly in the context of ENCODE and modENCODE, and as interest grows in long non-coding RNAs, often initially recognized by their lack of protein coding potential rather than conserved RNA secondary structures. Availability and Implementation: The Objective Caml source code and executables for GNU/Linux and Mac OS X are freely available at http://compbio.mit.edu/PhyloCSF Contact: mlin@mit.edu; manoli@mit.edu
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            A steroid receptor coactivator, SRA, functions as an RNA and is present in an SRC-1 complex.

            Nuclear receptors play critical roles in the regulation of eukaryotic gene expression. We report the isolation and functional characterization of a novel transcriptional coactivator, termed steroid receptor RNA activator (SRA). SRA is selective for steroid hormone receptors and mediates transactivation via their amino-terminal activation function. We provide functional and mechanistic evidence that SRA acts as an RNA transcript; transfected SRA, unlike other steroid receptor coregulators, functions in the presence of cycloheximide, and SRA mutants containing multiple translational stop signals retain their ability to activate steroid receptor-dependent gene expression. Biochemical fractionation shows that SRA exists in distinct ribonucleoprotein complexes, one of which contains the nuclear receptor coactivator steroid receptor coactivator 1. We suggest that SRA may act to confer functional specificity upon multiprotein complexes recruited by liganded receptors during transcriptional activation.
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              A liver-enriched long non-coding RNA, lncLSTR, regulates systemic lipid metabolism in mice.

              Long non-coding RNAs (lncRNAs) constitute a significant portion of mammalian genome, yet the physiological importance of lncRNAs is largely unknown. Here, we identify a liver-enriched lncRNA in mouse that we term liver-specific triglyceride regulator (lncLSTR). Mice with a liver-specific depletion of lncLSTR exhibit a marked reduction in plasma triglyceride levels. We show that lncLSTR depletion enhances apoC2 expression, leading to robust lipoprotein lipase activation and increased plasma triglyceride clearance. We further demonstrate that the regulation of apoC2 expression occurs through an FXR-mediated pathway. LncLSTR forms a molecular complex with TDP-43 to regulate expression of Cyp8b1, a key enzyme in the bile acid synthesis pathway, and engenders an in vivo bile pool that induces apoC2 expression through FXR. Finally, we demonstrate that lncLSTR depletion can reduce triglyceride levels in a hyperlipidemia mouse model. Taken together, these data support a model in which lncLSTR regulates a TDP-43/FXR/apoC2-dependent pathway to maintain systemic lipid homeostasis.
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                Author and article information

                Contributors
                kevin.muret@hotmail.fr
                colette.desert@agrocampus-ouest.fr
                laetitia.lagoutte@inra.fr
                morgane.boutin@agrocampus-ouest.fr
                florence.gondret@inra.fr
                tatiana.zerjal@inra.fr
                sandrine.lagarrigue@agrocampus-ouest.fr
                Journal
                BMC Genomics
                BMC Genomics
                BMC Genomics
                BioMed Central (London )
                1471-2164
                21 November 2019
                21 November 2019
                2019
                : 20
                : 882
                Affiliations
                [1 ]ISNI 0000 0004 0497 3491, GRID grid.463756.5, PEGASE, INRA, AGROCAMPUS OUEST, ; 35590 Saint-Gilles, France
                [2 ]ISNI 0000 0001 2185 8223, GRID grid.417885.7, GABI INRA, AgroParisTech, Université Paris-Saclay, ; Domaine de Vilvert, 78352 Jouy-en-Josas, France
                Author information
                http://orcid.org/0000-0002-4887-7245
                Article
                6093
                10.1186/s12864-019-6093-3
                6868825
                31752679
                79a5da85-0788-4bb8-b75e-846adc62ac5f
                © The Author(s). 2019

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 11 March 2019
                : 10 September 2019
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: FatInteger Project, ANR-11-SVS7
                Award ID: ChickStress Project, ANR-13-ADAP
                Award Recipient :
                Categories
                Review
                Custom metadata
                © The Author(s) 2019

                Genetics
                lncrna,lipid metabolism,liver,evolution,synteny
                Genetics
                lncrna, lipid metabolism, liver, evolution, synteny

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