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

Xie, Hong-Li; Wang, Yan‐Bo; Jiao, Guiai; Kong, De-Ling; Li, Qing; Li, Hong; Zheng, Libing; Tan, Jing-He

doi:10.1038/srep20764

Cited by 64 publications

(72 citation statements)

References 52 publications

(63 reference statements)

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“…In a variety of mammals, glucose metabolism and pyruvate play an important role in oocyte maturation and subsequent early embryonic development [1–3]. In an in vitro oocyte culture system, a decrease in glucose concentration was shown to significantly inhibit meiotic divisions, subcapsular maturation, and subsequent embryonic development in bubaline and bovine oocytes[4, 5].…”

Section: Introductionmentioning

confidence: 99%

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The Role of Glucose Metabolism on Porcine Oocyte Cytoplasmic Maturation and Its Possible Mechanisms

et al. 2016

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In the present study, we investigated the potential role of glucose and pyruvate in the cytoplasmic maturation of porcine oocytes by investigating the effect of glucose and/or pyruvate supplementation, in the presence or absence of 10% porcine follicular fluid (PFF), on meiotic maturation and subsequent embryo development. In the absence of 10% PFF, without exogenous addition of glucose and pyruvate, the medium seemed unable to support maturation. In the presence of 10% PFF, the addition of 5.6 mM glucose and/or 2 mM pyruvate during in vitro maturation of cumulus enclosed oocytes increased MII oocyte and blastocyst rates. In contrast, oocytes denuded of cumulus cells were not able to take full advantage of the glucose in the medium, as only pyruvate was able to increase the MII rate and the subsequent early embryo developmental ability. Treatment of cumulus enclosed oocytes undergoing maturation with 200 μM dehydroepiandrosterone (DHEA), a pentose phosphate pathway inhibitor, or 2 μM iodoacetate (IA), a glycolysis inhibitor, significantly reduced GHS, intra-oocyte ATP, maternal gene expression, and MPF activity levels. DHEA was also able to increase ROS and reduce the levels of NADPH. Moreover, blastocysts of the DHEA- or IA-treated groups presented higher apoptosis rates and markedly lower cell proliferation cell rates than those of the non-treated group. In conclusion, our results suggest that oocytes maturing in the presence of 10% PFF can make full use of energy sources through glucose metabolism only when they are accompanied by cumulus cells, and that pentose phosphate pathway (PPP) and glycolysis promote porcine oocyte cytoplasmic maturation by supplying energy, regulating maternal gene expression, and controlling MPF activity.

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Section: Introductionmentioning

confidence: 99%

“…Mammalian oocytes metabolize glucose primarily through glycolysis, PPP, and the tricarboxylic acid cycle (TAC) [1, 9]. PPP and/or glycolysis appear to play a key role in the resumption of meiosis in mouse oocytes [1, 10].…”

Section: Introductionmentioning

confidence: 99%

The Role of Glucose Metabolism on Porcine Oocyte Cytoplasmic Maturation and Its Possible Mechanisms

et al. 2016

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“…Glucose metabolism affected both oocyte maturation and following development of oocytes after fertilization and oocyte aging89. Glucose metabolism in cumulus cells prevented oocyte aging by producing pyruvate and NADPH through glycolysis and pentose phosphate pathway (PPP).…”

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confidence: 99%

Oocyte aging-induced Neuronatin (NNAT) hypermethylation affects oocyte quality by impairing glucose transport in porcine

Gao

Chen

Wang

et al. 2016

Sci Rep

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DNA methylation plays important roles in regulating many physiological behaviors; however, few studies were focused on the changes of DNA methylation during oocyte aging. Early studies showed that some imprinted genes’ DNA methylation had been changed in aged mouse oocytes. In this study, we used porcine oocytes to test the hypothesis that oocyte aging would alter DNA methylation pattern of genes and disturb their expression in age oocytes, which affected the developmental potential of oocytes. We compared several different types of genes and found that the expression and DNA methylation of Neuronatin (NNAT) were disturbed in aged oocytes significantly. Additional experiments demonstrated that glucose transport was impaired in aged oocytes and injection of NNAT antibody into fresh oocytes led to the same effects on glucose transport. These results suggest that the expression of NNAT was declined by elevating DNA methylation, which affected oocyte quality by decreasing the ability of glucose transport in aged oocytes.

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“…These results suggest that proper levels of cellular ATP in MII oocytes is one of the key factors determining fertilization and early embryo development, and Gas6 is associated with ATP production and HS production. When mitochondria produce excessive ATP, they also release ROS, and ROS oxidatively damage mitochondrial DNA (mtDNA), impair mitochondrial function, and contribute to free radical formation [38,50]. In the current study, excessive mitochondrial ATP production in MII oocytes by Gas6 RNAi led to the generation of ROS.…”

Section: Discussionmentioning

confidence: 75%

“…Cytoplasmic maturation is composed of various changes within oocytes, including accumulation of mRNA and proteins, reorganization of cytoskeleton and organelles, and changes in metabolism [38]. We have previously shown that Gas6 is a mammalian maternal effect gene and is critical for cytoplasmic maturation and normal fertilization, especially Ca 2+ excitability, cortical granule exocytosis, SCD and PN formation [8].…”

Section: Discussionmentioning

confidence: 99%

Oocyte Cytoplasmic Gas6 and Heparan Sulfate (HS) are Required to Establish the Open Chromatin State in Nuclei During Remodeling and Reprogramming

Kim

Lee

et al. 2017

Cell Physiol Biochem

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Background/Aims: Previously, we found that silencing of growth arrest-specific gene 6 (Gas6) in oocytes impaired cytoplasmic maturation, resulting in failure of sperm chromatin decondensation (SCD) and pronuclear (PN) formation after fertilization. Thus, we conducted this study to determine the effect of Gas6 RNAi on downstream genes and to elucidate the working mechanism of Gas6 on oocyte cytoplasmic maturation and SCD. Methods: Using RT-PCR, Western blot and immunofluorescence, the expression levels of various target genes and the localization of heparan sulfate (HS) were analyzed after Gas6 RNAi. The roles of Gas6 in HS biosynthesis, production of ATP and GSH, ROS generation and ΔΨm were also investigated. SCD and micrococcal nuclease (MNase) analyses were used to examine the effects of HS on the open chromatin state in sperm and somatic cell nuclei, respectively. Results: Disruption of Gas6 expression led to the inhibition of HS biosynthesis through the reduction of several HS biosynthetic enzymes. The rescue experiment, HS treatment in vitro, significantly recovered SCD and PN formation, confirming that HS had the ability to induce sperm head remodeling during fertilization. Interestingly, excessive mitochondrial activation in Gas6-depleted MII oocytes caused ROS generation and glutathione (GSH) degradation via mitochondrial activation, such as elevated ΔΨm and ATP production. Indeed, HS-treated NIH3T3 cell nuclei showed an open chromatin state, as determined by diffuse DAPI staining and increased sensitivity to MNase. Conclusion: We propose that the addition of HS to sperm and/or oocyte maturation would improve the efficiency of in vitro fertilization and somatic cell nuclear transfer (SCNT) reprogramming.

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

Cited by 64 publications

References 52 publications

The Role of Glucose Metabolism on Porcine Oocyte Cytoplasmic Maturation and Its Possible Mechanisms

The Role of Glucose Metabolism on Porcine Oocyte Cytoplasmic Maturation and Its Possible Mechanisms

Oocyte aging-induced Neuronatin (NNAT) hypermethylation affects oocyte quality by impairing glucose transport in porcine

Oocyte Cytoplasmic Gas6 and Heparan Sulfate (HS) are Required to Establish the Open Chromatin State in Nuclei During Remodeling and Reprogramming

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