Energy Metabolism Regulating Mammalian Oocyte Maturation

Songsasen, Nucharin

doi:10.5772/33752

Cited by 10 publications

(7 citation statements)

References 93 publications

(166 reference statements)

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“…Oocyte developmental competence depends in part on the capacity to increase intracellular energy storage because the early embryo cleavages rely on stored lipid [ 3 , 13 ]. To increase its lipid stock, the oocyte may increase ACACA expression and thus FA synthesis.…”

Section: Resultsmentioning

confidence: 99%

“…Ovarian cells can use multiple metabolic substrates including glucose, amino acids and lipids; the flexibility of the metabolic pathways available for energy production during oocyte growth and maturation seems to be a key to high developmental competence of the oocyte [ 2 , 3 ]. Folliculogenesis and final oocyte maturation are regulated at the endocrine and paracrine levels and are strongly influenced by dietary fat supplementation in cows [ 4 ] and humans [ 5 ].…”

Section: Introductionmentioning

confidence: 99%

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MALDI Mass Spectrometry Imaging of Lipids and Gene Expression Reveals Differences in Fatty Acid Metabolism between Follicular Compartments in Porcine Ovaries

Uzbekova

Elis

Teixeira-Gomes

et al. 2015

Biology

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In mammals, oocytes develop inside the ovarian follicles; this process is strongly supported by the surrounding follicular environment consisting of cumulus, granulosa and theca cells, and follicular fluid. In the antral follicle, the final stages of oogenesis require large amounts of energy that is produced by follicular cells from substrates including glucose, amino acids and fatty acids (FAs). Since lipid metabolism plays an important role in acquiring oocyte developmental competence, the aim of this study was to investigate site-specificity of lipid metabolism in ovaries by comparing lipid profiles and expression of FA metabolism-related genes in different ovarian compartments. Using MALDI Mass Spectrometry Imaging, images of porcine ovary sections were reconstructed from lipid ion signals for the first time. Cluster analysis of ion spectra revealed differences in spatial distribution of lipid species among ovarian compartments, notably between the follicles and interstitial tissue. Inside the follicles analysis differentiated follicular fluid, granulosa, theca and the oocyte-cumulus complex. Moreover, by transcript quantification using real time PCR, we showed that expression of five key genes in FA metabolism significantly varied between somatic follicular cells (theca, granulosa and cumulus) and the oocyte. In conclusion, lipid metabolism differs between ovarian and follicular compartments.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

MALDI Mass Spectrometry Imaging of Lipids and Gene Expression Reveals Differences in Fatty Acid Metabolism between Follicular Compartments in Porcine Ovaries

Uzbekova

Elis

Teixeira-Gomes

et al. 2015

Biology

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“…These observations hypothesized that Tribbles in follicular cells may have a role during the final stages of folliculogenesis and oocyte maturation. It is well established that MAPKs along with energy metabolism in follicular cells, are essential for proper maturation of the enclosed oocyte and for subsequent fertilization [ 14 - 16 ]. Indeed the oocyte needs energy to perform maturation including meiosis resumption from prophase-I to the metaphase-II stage.…”

Section: Introductionmentioning

confidence: 99%

Tribbles expression in cumulus cells is related to oocyte maturation and fatty acid metabolism

et al. 2014

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BackgroundIn mammals, the Tribbles family includes widely expressed serine-threonine kinase-like proteins (TRIB1, TRIB2 and TRIB3) that are involved in multiple biological processes including cell proliferation and fatty acid (FA) metabolism. Our recent studies highlighted the importance of FA metabolism in cumulus cells (CC) during oocyte maturation in vertebrates and reported a higher TRIB1 expression in CC surrounding in vivo mature oocytes as compared to immature ooocytes in mice and cows. The objective was to investigate Tribbles expression patterns in bovine CC during in vitro maturation (IVM) and to examine their roles in the cumulus-oocyte complex.MethodsTribbles gene expression was analyzed in bovine and murine CC using quantitative RT-PCR. Proteins were detected using Western blot and intracellular localization was assessed by immunofluorescence. Bovine COCs were treated with etomoxir, an inhibitor of FA oxidation (FAO) which blocks CPT1 activity, during 6 h and 18 h IVM. Oocyte meiotic stage was assessed and expression of Tribbles and lipid metabolism genes was quantified in CC.Results and discussionTRIB1 and TRIB3 were more strongly expressed whereas TRIB2 was less expressed in CC surrounding the oocytes from preovulatory follicles than in CC of immature ones. In CC, Tribbles were located in the cytoplasm and nucleus; in mitotic cells TRIB2 and TRIB3 were detected in the spindle. In the oocyte, Tribbles proteins were detected in the ooplasm; also TRIB2 and TRIB3 were more accumulated in the germinal vesicle. In bovine CC, expression of TRIB1 and TRIB3 was transiently increased at a time preceding oocyte meiosis resumption in vitro. Treatment with etomoxir (150 μM) during IVM resulted in a significant reduction of oocyte maturation rate and decreased MAPK3/1 phosphorylation in the oocytes. In CC, 18 h IVM of etomoxir treatment significantly increased expression of TRIB1, TRIB3, CPTA1 (enzyme regulating FA entry in mitochondria for FAO) and CD36 (thrombospondin receptor involved in FA transport). Under the same conditions, expression of TRIB2 and ACACA (Acetyl coenzyme A carboxylase involved in FA synthesis) decreased in CC.All considered, Tribbles family members may be involved in cell proliferation and in FAO signaling in CC and participate in oocyte meiotic resumption regulation.

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“…Energy metabolism is crucial for oocyte maturation because progression through all the dynamic processes involved requires a lot of energy from various substrates including carbohydrates, amino acids and lipids 14 15 . Studies have suggested beneficial effects of glucose metabolism on oocyte maturation 16 17 18 19 20 21 22 .…”

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confidence: 99%

Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes

Xie

Wang

Jiao

et al. 2016

Sci Rep

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Although there are many reports on the effect of glucose metabolism on oocyte nuclear maturation, there are few studies on its effect on ooplasmic maturation. By manipulating glucose metabolism pathways using a maturation medium that could support oocyte nuclear maturation but only a limited blastocyst formation without glucose, this study determined effects of glucose metabolism pathways on ooplasmic maturation. During maturation of cumulus-oocyte-complexes (COCs) with glucose, the presence of PPP inhibitor, DHEA or glycolysis inhibitor, iodoacetate significantly decreased blastocyst rates, intraoocyte glutathione and ATP. While blastocyst rates, GSH/GSSG ratio and NADPH were higher, ROS was lower significantly in COCs matured with iodoacetate than with DHEA. Fructose-6-phosphate overcame the inhibitory effect of DHEA on PPP. During maturation of COCs with pyruvate, electron transport inhibitor, rotenone or monocarboxylate transfer inhibitor, 4-CIN significantly decreased blastocyst rates. Cumulus-denuded oocytes had a limited capacity to use glucose or lactate, but they could use pyruvate to support maturation. In conclusion, whereas glycolysis promoted ooplasmic maturation mainly by supplying energy, PPP facilitated ooplasmic maturation to a greater extent by both reducing oxidative stress and supplying energy through providing fructose-6-phosphate for glycolysis. Pyruvate was transferred by monocarboxylate transporters and utilized through mitochondrial electron transport to sustain ooplasmic maturation.

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Energy Metabolism Regulating Mammalian Oocyte Maturation

Cited by 10 publications

References 93 publications

MALDI Mass Spectrometry Imaging of Lipids and Gene Expression Reveals Differences in Fatty Acid Metabolism between Follicular Compartments in Porcine Ovaries

MALDI Mass Spectrometry Imaging of Lipids and Gene Expression Reveals Differences in Fatty Acid Metabolism between Follicular Compartments in Porcine Ovaries

Tribbles expression in cumulus cells is related to oocyte maturation and fatty acid metabolism

Effects of glucose metabolism during in vitro maturation on cytoplasmic maturation of mouse oocytes

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