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      Preovulatory Aging In Vivo and In Vitro Affects Maturation Rates, Abundance of Selected Proteins, Histone Methylation Pattern and Spindle Integrity in Murine Oocytes

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          Abstract

          Delayed ovulation and delayed fertilization can lead to reduced developmental competence of the oocyte. In contrast to the consequences of postovulatory aging of the oocyte, hardly anything is known about the molecular processes occurring during oocyte maturation if ovulation is delayed (preovulatory aging). We investigated several aspects of oocyte maturation in two models of preovulatory aging: an in vitro follicle culture and an in vivo mouse model in which ovulation was postponed using the GnRH antagonist cetrorelix. Both models showed significantly reduced oocyte maturation rates after aging. Furthermore, in vitro preovulatory aging deregulated the protein abundance of the maternal effect genes Smarca4 and Nlrp5, decreased the levels of histone H3K9 trimethylation and caused major deterioration of chromosome alignment and spindle conformation. Protein abundance of YBX2, an important regulator of mRNA stability, storage and recruitment in the oocyte, was not affected by in vitro aging. In contrast, in vivo preovulatory aging led to reduction in Ybx2 transcript and YBX2 protein abundance. Taken together, preovulatory aging seems to affect various processes in the oocyte, which could explain the low maturation rates and the previously described failures in fertilization and embryonic development.

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          Most cited references39

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          Maternal control of early mouse development.

          The hiatus between oocyte and embryonic gene transcription dictates a role for stored maternal factors in early mammalian development. Encoded by maternal-effect genes, these factors accumulate during oogenesis and enable the activation of the embryonic genome, the subsequent cleavage stages of embryogenesis and the initial establishment of embryonic cell lineages. Recent studies in mice have yielded new findings on the role of maternally provided proteins and multi-component complexes in preimplantation development. Nevertheless, significant gaps remain in our mechanistic understanding of the networks that regulate early mammalian embryogenesis, which provide an impetus and opportunities for future investigations.
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            Mater, a maternal effect gene required for early embryonic development in mice.

            Maternal effect genes produce mRNA or proteins that accumulate in the egg during oogenesis. We show here that Mater, a mouse oocyte protein dependent on the maternal genome, is essential for embryonic development beyond the two-cell stage. Females lacking the maternal effect gene Mater are sterile. Null males are fertile.
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              A subcortical maternal complex essential for preimplantation mouse embryogenesis.

              We have identified a subcortical maternal complex (SCMC) that assembles during oocyte growth and is essential for zygotes to progress beyond the first embryonic cell divisions. At least four maternally encoded proteins contribute to this MDa complex: FLOPED, MATER, and TLE6 interact with each other while Filia binds independently to MATER. Although the transcripts encoding these proteins are degraded during meiotic maturation and ovulation, the SCMC proteins persist in the early embryo. The SCMC, located in the subcortex of eggs, is excluded from regions of cell-cell contact in the cleavage-stage embryo and segregates to the outer cells of the morulae and blastocyst. Floped(tm/tm) and/or Mater(tm/tm) eggs lack the SCMC but can be fertilized. However, these embryos do not progress beyond cleavage stage development and female mice are sterile. The proteins are conserved in humans, and similar maternal effect mutations may result in recurrent embryonic loss.
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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
                9 September 2016
                2016
                : 11
                : 9
                : e0162722
                Affiliations
                [1 ]Institute of Human Genetics, University Hospital Essen, University Duisburg-Essen, Essen, Germany
                [2 ]Institute of Gene Technology/Microbiology, University of Bielefeld, Bielefeld, Germany
                [3 ]Institute of Anatomy, University Hospital Essen, University Duisburg-Essen, Essen, Germany
                China Agricultural University, CHINA
                Author notes

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

                • Conceptualization: RG BH UE.

                • Formal analysis: HD TT DD MH.

                • Funding acquisition: RG BH UE.

                • Investigation: HD TT DD MH.

                • Methodology: HD TT DD MH.

                • Project administration: RG BH UE.

                • Resources: RG UE BH.

                • Supervision: RG BH UE.

                • Validation: HD TT DD MH.

                • Visualization: HD TT DD MH.

                • Writing – original draft: HD UE.

                • Writing – review & editing: HD TT DD MH RG BH UE.

                Article
                PONE-D-16-12208
                10.1371/journal.pone.0162722
                5017692
                27611906
                93c70fe1-14e1-409c-b5f8-9d3da4377fe3
                © 2016 Demond 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
                : 24 March 2016
                : 26 August 2016
                Page count
                Figures: 5, Tables: 0, Pages: 18
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: HO 949/21-1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: EI 199/7-1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: FOR 1041
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: GR 1138/12-1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: FOR 1041
                Award Recipient :
                The study has been supported by the German Research Foundation (DFG, www.dfg.de, EI 199/7-1 | GR 1138/12-1 | HO 949/21-1 and FOR 1041). 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
                Cell Biology
                Cellular Types
                Animal Cells
                Germ Cells
                OVA
                Oocytes
                Biology and Life Sciences
                Developmental Biology
                Organism Development
                Aging
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Aging
                Medicine and Health Sciences
                Physiology
                Physiological Processes
                Aging
                Biology and Life Sciences
                Biochemistry
                Proteomics
                Protein Abundance
                Medicine and Health Sciences
                Endocrinology
                Endocrine Physiology
                Menstrual Cycle
                Ovulation
                Biology and Life Sciences
                Physiology
                Endocrine Physiology
                Menstrual Cycle
                Ovulation
                Medicine and Health Sciences
                Physiology
                Endocrine Physiology
                Menstrual Cycle
                Ovulation
                Biology and Life Sciences
                Physiology
                Reproductive Physiology
                Menstrual Cycle
                Ovulation
                Medicine and Health Sciences
                Physiology
                Reproductive Physiology
                Menstrual Cycle
                Ovulation
                Biology and life sciences
                Biochemistry
                Nucleic acids
                RNA
                Messenger RNA
                Research and Analysis Methods
                Specimen Preparation and Treatment
                Staining
                Chromosome Staining
                Research and Analysis Methods
                Microscopy
                Light Microscopy
                Fluorescence Microscopy
                Biology and life sciences
                Biochemistry
                Proteins
                DNA-binding proteins
                Histones
                Custom metadata
                All relevant data are within the paper.

                Uncategorized
                Uncategorized

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