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      Lipid Identification and Transcriptional Analysis of Controlling Enzymes in Bovine Ovarian Follicle

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          Abstract

          Ovarian follicle provides a favorable environment for enclosed oocytes, which acquire their competence in supporting embryo development in tight communications with somatic follicular cells and follicular fluid (FF). Although steroidogenesis in theca (TH) and granulosa cells (GC) is largely studied, and the molecular mechanisms of fatty acid (FA) metabolism in cumulus cells (CC) and oocytes are emerging, little data is available regarding lipid metabolism regulation within ovarian follicles. In this study, we investigated lipid composition and the transcriptional regulation of FA metabolism in 3–8 mm ovarian follicles in bovine. Using liquid chromatography and mass spectrometry (MS), 438 and 439 lipids were identified in FF and follicular cells, respectively. From the MALDI-TOF MS lipid fingerprints of FF, TH, GC, CC, and oocytes, and the MS imaging of ovarian sections, we identified 197 peaks and determined more abundant lipids in each compartment. Transcriptomics revealed lipid metabolism-related genes, which were expressed constitutively or more specifically in TH, GC, CC, or oocytes. Coupled with differential lipid composition, these data suggest that the ovarian follicle contains the metabolic machinery that is potentially capable of metabolizing FA from nutrient uptake, degrading and producing lipoproteins, performing de novo lipogenesis, and accumulating lipid reserves, thus assuring oocyte energy supply, membrane synthesis, and lipid-mediated signaling to maintain follicular homeostasis.

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          Most cited references73

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          Liver lipid metabolism.

          The liver plays a key role in lipid metabolism. Depending on species it is, more or less, the hub of fatty acid synthesis and lipid circulation through lipoprotein synthesis. Eventually the accumulation of lipid droplets into the hepatocytes results in hepatic steatosis, which may develop as a consequence of multiple dysfunctions such as alterations in beta-oxidation, very low density lipoprotein secretion, and pathways involved in the synthesis of fatty acids. In addition an increased circulating pool of non-esterified fatty acid may also to be a major determinant in the pathogenesis fatty liver disease. This review also focuses on transcription factors such as sterol-regulatory-element-binding protein-1c and peroxisome proliferator-activated receptor alpha, which promote either hepatic fatty acid synthesis or oxidation.
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            Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality.

            Oocyte quality is a key limiting factor in female fertility, yet we have a poor understanding of what constitutes oocyte quality or the mechanisms governing it. The ovarian follicular microenvironment and maternal signals, mediated primarily through granulosa cells (GCs) and cumulus cells (CCs), are responsible for nurturing oocyte growth, development and the gradual acquisition of oocyte developmental competence. However, oocyte-GC/CC communication is bidirectional with the oocyte secreting potent growth factors that act locally to direct the differentiation and function of CCs. Two important oocyte-secreted factors (OSFs) are growth-differentiation factor 9 and bone morphogenetic protein 15, which activate signaling pathways in CCs to regulate key genes and cellular processes required for CC differentiation and for CCs to maintain their distinctive phenotype. Hence, oocytes appear to tightly control their neighboring somatic cells, directing them to perform functions required for appropriate development of the oocyte. This oocyte-CC regulatory loop and the capacity of oocytes to regulate their own microenvironment by OSFs may constitute important components of oocyte quality. In support of this notion, it has recently been demonstrated that supplementing oocyte in vitro maturation (IVM) media with exogenous OSFs improves oocyte developmental potential, as evidenced by enhanced pre- and post-implantation embryo development. This new perspective on oocyte-CC interactions is improving our knowledge of the processes regulating oocyte quality, which is likely to have a number of applications, including improving the efficiency of clinical IVM and thereby providing new options for the treatment of infertility.
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              Expanding roles for SREBP in metabolism.

              Sterol regulatory element-binding protein (SREBP) transcription factors regulate cellular lipogenesis and lipid homeostasis. Recent studies reveal expanding roles for SREBPs with the description of new regulatory mechanisms, the identification of unexpected transcriptional targets, and the discovery of functions for SREBPs in type II diabetes, cancer, immunity, neuroprotection, and autophagy. Copyright © 2012 Elsevier Inc. All rights reserved.
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                Author and article information

                Journal
                Int J Mol Sci
                Int J Mol Sci
                ijms
                International Journal of Molecular Sciences
                MDPI
                1422-0067
                20 October 2018
                October 2018
                : 19
                : 10
                : 3261
                Affiliations
                [1 ]UMR PRC, INRA 85, CNRS 7247, Université de Tours, IFCE, 37380 Nouzilly, France; priscila.bertevello@ 123456inra.fr (P.S.B.); anais.carvalho@ 123456hotmail.fr (A.V.C.); valerie.labas@ 123456inra.fr (V.L.); marie-claire.blache@ 123456inra.fr (M.-C.B.); Charles.Banliat@ 123456inra.fr (C.B.); Luiz-Augusto.Viera-Cordeiro@ 123456inra.fr (L.A.V.C.); pascal.papillier@ 123456inra.fr (P.P.); virginie.maillard@ 123456inra.fr (V.M.); sebastien.elis@ 123456inra.fr (S.E.)
                [2 ]UMR ISP, INRA 1282, Université de Tours, 37380 Nouzilly, France; ana-paula.teixeira@ 123456inra.fr
                [3 ]UMR BDR, ENVA, INRA, Université Paris-Saclay, 78350 Jouy-en-Josas, France; veronique.duranthon@ 123456inra.fr
                [4 ]PAIB (Pôle d’Analyse et d’Imagerie des Biomolécules), Plate-forme CIRE (Chirurgie et Imagerie pour la Recherche et l’Enseignement, INRA, Université de Tours, CHRU de Tours, 37380 Nouzilly, France
                [5 ]Profilomic SA, F-92100 Boulogne-Billancourt, France; alexandre.seyer@ 123456medday-pharma.com
                Author notes
                [* ]Correspondence: svetlana.uzbekova@ 123456inra.fr ; Tel.: +33-247-427-951
                Article
                ijms-19-03261
                10.3390/ijms19103261
                6214003
                30347829
                0e179fe8-f2bf-4c8c-92b6-30ce2626bc92
                © 2018 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 September 2018
                : 18 October 2018
                Categories
                Article

                Molecular biology
                ovarian follicle,lipids,mass spectrometry imaging,maldi ms profiling,gene expression,oocyte,granulosa,theca,follicular fluid,bovine

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