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      Dual effect of fetal bovine serum on early development depends on stage-specific reactive oxygen species demands in pigs

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          Abstract

          Despite the application of numerous supplements to improve in vitro culture (IVC) conditions of mammalian cells, studies regarding the effect of fetal bovine serum (FBS) on mammalian early embryogenesis, particularly in relation to redox homeostasis, are lacking. Herein, we demonstrated that early development of in vitro-produced (IVP) porcine embryos highly depends on the combination of FBS supplementation timing and embryonic reactive oxygen species (ROS) requirements. Interestingly, FBS significantly reduced intracellular ROS levels in parthenogenetically activated (PA) embryos regardless of the developmental stage. However, the beneficial effect of FBS on early embryogenesis was found only during the late phase (IVC 4–6 days) treatment group. In particular, developmental competence parameters, such as blastocyst formation rate, cellular survival, total cell number and trophectoderm proportion, were markedly increased by FBS supplementation during the late IVC phase. In addition, treatment with FBS elevated antioxidant transcript levels during the late IVC phase. In contrast, supplementation with FBS during the entire period (1–6 days) or during the early IVC phase (1–2 days) greatly impaired the developmental parameters. Consistent with the results from PA embryos, the developmental competence of in vitro fertilization (IVF) or somatic cell nuclear transfer (SCNT) embryos were markedly improved by treatment with FBS during the late IVC phase. Moreover, the embryonic stage-specific effects of FBS were reversed by the addition of an oxidant and were mimicked by treatment with an antioxidant. These findings may increase our understanding of redox-dependent early embryogenesis and contribute to the large-scale production of high-quality IVP embryos.

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          Most cited references63

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          Oxidative Stress, Mitochondrial Dysfunction, and Aging

          Aging is an intricate phenomenon characterized by progressive decline in physiological functions and increase in mortality that is often accompanied by many pathological diseases. Although aging is almost universally conserved among all organisms, the underlying molecular mechanisms of aging remain largely elusive. Many theories of aging have been proposed, including the free-radical and mitochondrial theories of aging. Both theories speculate that cumulative damage to mitochondria and mitochondrial DNA (mtDNA) caused by reactive oxygen species (ROS) is one of the causes of aging. Oxidative damage affects replication and transcription of mtDNA and results in a decline in mitochondrial function which in turn leads to enhanced ROS production and further damage to mtDNA. In this paper, we will present the current understanding of the interplay between ROS and mitochondria and will discuss their potential impact on aging and age-related diseases.
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            Stem cells and the impact of ROS signaling.

            An appropriate balance between self-renewal and differentiation is crucial for stem cell function during both early development and tissue homeostasis throughout life. Recent evidence from both pluripotent embryonic and adult stem cell studies suggests that this balance is partly regulated by reactive oxygen species (ROS), which, in synchrony with metabolism, mediate the cellular redox state. In this Primer, we summarize what ROS are and how they are generated in the cell, as well as their downstream molecular targets. We then review recent findings that provide molecular insights into how ROS signaling can influence stem cell homeostasis and lineage commitment, and discuss the implications of this for reprogramming and stem cell ageing. We conclude that ROS signaling is an emerging key regulator of multiple stem cell populations.
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              Oxygen consumption and usage during physical exercise: the balance between oxidative stress and ROS-dependent adaptive signaling.

              The complexity of human DNA has been affected by aerobic metabolism, including endurance exercise and oxygen toxicity. Aerobic endurance exercise could play an important role in the evolution of Homo sapiens, and oxygen was not important just for survival, but it was crucial to redox-mediated adaptation. The metabolic challenge during physical exercise results in an elevated generation of reactive oxygen species (ROS) that are important modulators of muscle contraction, antioxidant protection, and oxidative damage repair, which at moderate levels generate physiological responses. Several factors of mitochondrial biogenesis, such as peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α), mitogen-activated protein kinase, and SIRT1, are modulated by exercise-associated changes in the redox milieu. PGC-1α activation could result in decreased oxidative challenge, either by upregulation of antioxidant enzymes and/or by an increased number of mitochondria that allows lower levels of respiratory activity for the same degree of ATP generation. Endogenous thiol antioxidants glutathione and thioredoxin are modulated with high oxygen consumption and ROS generation during physical exercise, controlling cellular function through redox-sensitive signaling and protein-protein interactions. Endurance exercise-related angiogenesis, up to a significant degree, is regulated by ROS-mediated activation of hypoxia-inducible factor 1α. Moreover, the exercise-associated ROS production could be important to DNA methylation and post-translation modifications of histone residues, which create heritable adaptive conditions based on epigenetic features of chromosomes. Accumulating data indicate that exercise with moderate intensity has systemic and complex health-promoting effects, which undoubtedly involve regulation of redox homeostasis and signaling.
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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, CA USA )
                1932-6203
                13 April 2017
                2017
                : 12
                : 4
                : e0175427
                Affiliations
                [1 ]National Primate Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea
                [2 ]Futuristic Animal Resource & Research Center, Korea Research Institute of Bioscience and Biotechnology, Chungcheongbuk-do, Republic of Korea
                [3 ]Department of Biological Science, College of Natural Sciences, Wonkwang University, Jeollabuk-do, Republic of Korea
                [4 ]Department of Functional Genomics, University of Science and Technology, Daejeon, Republic of Korea
                Peking University Third Hospital, CHINA
                Author notes

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

                • Conceptualization: SEM BWS SBY SUK KTC.

                • Formal analysis: SEM SAC YHK YL YBJ JSK JWH.

                • Funding acquisition: KTC.

                • Methodology: BWS PSJ.

                • Project administration: SUK KTC.

                • Resources: BSS PK KJJ SRL.

                • Software: SBY SEM HJY.

                • Supervision: SUK KTC.

                • Validation: SBY YHP BSS JSK.

                • Writing – original draft: SEM BWS SBY SUK KTC.

                • Writing – review & editing: YKC.

                Article
                PONE-D-16-35962
                10.1371/journal.pone.0175427
                5391019
                28406938
                3705418f-800f-4dbd-abca-08af83d27362
                © 2017 Mun et al

                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.

                History
                : 12 September 2016
                : 24 March 2017
                Page count
                Figures: 8, Tables: 0, Pages: 23
                Funding
                This study was supported by grants from the KRIBB Research Initiative Programs (KGM4251723), the Bio & Medical Technology Development Program of the NRF funded by the Korean government, MSIP (NRF-2012M3A9B6055362), and the Next-Generation BioGreen 21 Program (PJ0099592016), Rural Development Administration, Republic of Korea.
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Embryology
                Blastocysts
                Biology and Life Sciences
                Developmental Biology
                Embryology
                Embryos
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Cell Death
                Apoptosis
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Germ Cells
                OVA
                Oocytes
                Physical Sciences
                Chemistry
                Chemical Compounds
                Oxides
                Peroxides
                Hydrogen Peroxide
                Biology and Life Sciences
                Developmental Biology
                Embryogenesis
                Biology and Life Sciences
                Biochemistry
                Antioxidants
                Research and Analysis Methods
                Microscopy
                Light Microscopy
                Fluorescence Microscopy
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Uncategorized
                Uncategorized

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