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      Relationship between mitochondrial DNA Copy Number and SIRT1 Expression in Porcine Oocytes

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          Abstract

          The present study assessed the effect of resveratrol on the expression of SIRT1 and mitochondrial quality and quantity in porcine oocytes. Supplementing the maturation medium with 20 µM resveratrol increased the expression of SIRT1, and enhanced mitochondrial functions, as observed from the increased ATP content and mitochondrial membrane potential. Addition of resveratrol also improved the ability of oocytes to develop into the blastocyst stage following activation. The effects of resveratrol on mitochondrial number were examined by comparing the mitochondrial DNA copy number (Mt number) between group of oocytes collected from the same donor gilt ovaries. Supplementing the maturation medium with only resveratrol did not affect the Mt number in the oocytes. However, supplementing the maturation medium with 10 µM MG132, a proteasome inhibitor, significantly increased the amount of ubiquitinated proteins and Mt number by 12 and 14%, respectively. In addition, when resveratrol was added to the medium containing MG132, the Mt number increased significantly by 39%, this effect was diminished by the addition of the SIRT1 inhibitor EX527. Furthermore, supplementing the medium with MG132 and EX527 did not affect Mt number. The mean SIRT1 expression in 20 oocytes was significantly and positively correlated with the Mt number in oocytes collected from the same donor. This study suggests that the expression of SIRT1 is associated with the Mt number in oocytes. In addition, activation of SIRT1 by resveratrol enhances the biosynthesis and degradation of mitochondria in oocytes, thereby replenishing and improving mitochondrial function and the developmental ability of oocytes.

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          Most cited references 22

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          Mammalian SIRT1 represses forkhead transcription factors.

          The NAD-dependent deacetylase SIR2 and the forkhead transcription factor DAF-16 regulate lifespan in model organisms, such as yeast and C. elegans. Here we show that the mammalian SIR2 ortholog SIRT1 deacetylates and represses the activity of the forkhead transcription factor Foxo3a and other mammalian forkhead factors. This regulation appears to be in the opposite direction from the genetic interaction of SIR2 with forkhead in C. elegans. By restraining mammalian forkhead proteins, SIRT1 also reduces forkhead-dependent apoptosis. The inhibition of forkhead activity by SIRT1 parallels the effect of this deacetylase on the tumor suppressor p53. We speculate how down-regulating these two classes of damage-responsive mammalian factors may favor long lifespan under certain environmental conditions, such as calorie restriction.
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            New insights into the role of mitochondria in aging: mitochondrial dynamics and more.

            A decline in mitochondrial function plays a key role in the aging process and increases the incidence of age-related disorders. A deeper understanding of the intricate nature of mitochondrial dynamics, which is described as the balance between mitochondrial fusion and fission, has revealed that functional and structural alterations in mitochondrial morphology are important factors in several key pathologies associated with aging. Indeed, a recent wave of studies has demonstrated the pleiotropic role of fusion and fission proteins in numerous cellular processes, including mitochondrial metabolism, redox signaling, the maintenance of mitochondrial DNA and cell death. Additionally, mitochondrial fusion and fission, together with autophagy, have been proposed to form a quality-maintenance mechanism that facilitates the removal of damaged mitochondria from the cell, a process that is particularly important to forestall aging. Thus, dysfunctional regulation of mitochondrial dynamics might be one of the intrinsic causes of mitochondrial dysfunction, which contributes to oxidative stress and cell death during the aging process. In this Commentary, we discuss recent studies that have converged at a consensus regarding the involvement of mitochondrial dynamics in key cellular processes, and introduce a possible link between abnormal mitochondrial dynamics and aging.
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              Mitochondrial content reflects oocyte variability and fertilization outcome.

              To determine the content of mitochondrial DNA (mtDNA) in oocytes from a range of patients with fertilization success and failure. Analysis of mtDNA content in fertilized and unfertilized oocytes and embryos by real-time polymerase chain reaction (PCR). University hospital infertility and research center. Fifty-four women seeking treatment for infertility. None. A total of 142 fertilized and unfertilized oocytes were classified into three main groups. Group I consisted of 35 fertilized oocytes from 21 patients; group II, 65 unfertilized oocytes from 36 patients; and group III, 42 degenerate oocytes from 23 patients. Mitochondrial DNA content was determined by SYBR Green real-time PCR-based assay. The mean mtDNA copy number for the fertilized oocytes was 250,454, whereas for the unfertilized group it was 163,698. There were significant differences for mtDNA copy number between the male factor and female factor infertility unfertilized oocytes and between the unexplained infertility and female factor infertility groups. The mean copy number for the degenerate oocyte group was 44,629, which was significantly different from the other subdivisions in this group. Mitochondrial DNA content is critical to fertilization outcome and serves as an important marker of oocyte quality, explaining some cases of fertilization failure.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                18 April 2014
                : 9
                : 4
                Affiliations
                Tokyo University of Agriculture, Funako, Atugi City, Japan
                RIKEN Advanced Science Institute, Japan
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: HI. Performed the experiments: DS HT NI ST HI. Analyzed the data: DS HT NI ST TK HI. Contributed reagents/materials/analysis tools: DS HI. Wrote the paper: DS HI.

                Article
                PONE-D-14-02124
                10.1371/journal.pone.0094488
                3991605
                24747689

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Page count
                Pages: 8
                Funding
                Grant-in-Aid for Scientic Research C (KAKENHI, grant number: 25450400). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Biophysics
                Developmental Biology
                Embryology
                Fertilization
                Molecular Development

                Uncategorized

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