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      Impact of preovulatory follicle maturity on oocyte metabolism and embryo development

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          Abstract

          Improved oocyte competence for embryo development and pregnancy was observed following ovulation of preovulatory follicles with greater physiological maturity, as indicated by estradiol production, prior to the gonadotropin-releasing hormone (GnRH)-induced luteinizing hormone (LH) surge. It was hypothesized that follicular fluid from preovulatory follicles of greater maturity better supports the maturing oocyte's metabolic requirements and improves embryo development. The objective was to determine if differences in preovulatory follicular fluid due to follicle maturity influence oocyte metabolism during in vitro maturation (IVM) and affect embryo development. Bovine preovulatory follicular fluid was collected 18 h after a GnRH-induced LH surge. Serum estradiol concentration at GnRH administration categorized follicles as greater or lesser maturity. Immature bovine oocytes were submitted to 24 h IVM in medium supplemented with 20% follicular fluid from preovulatory follicles of greater or lesser maturity. Embryo development was recorded. Oocyte maturation media and media conditioned by developing embryos were submitted for metabolomics. A randomized block design was utilized to determine differences in embryo development and media metabolites ( P ≤ 0.05). Blastocysts from oocytes matured in greater vs. lesser maturity follicular fluid had a more moderate rate of development ( P = 0.01). At the conclusion of 24 h IVM, abundance of 66 metabolites differed between greater and lesser follicle maturity treatments. Nine metabolites differed in media conditioned by developing embryos. Metabolome results suggest improved amino acid, purine, and glucose metabolism, followed by a more efficient rate of embryo development, in oocytes matured in greater vs lesser maturity follicular fluid.

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          Most cited references64

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          Amino acids: metabolism, functions, and nutrition.

          Guoyao Wu (2009)
          Recent years have witnessed the discovery that amino acids (AA) are not only cell signaling molecules but are also regulators of gene expression and the protein phosphorylation cascade. Additionally, AA are key precursors for syntheses of hormones and low-molecular weight nitrogenous substances with each having enormous biological importance. Physiological concentrations of AA and their metabolites (e.g., nitric oxide, polyamines, glutathione, taurine, thyroid hormones, and serotonin) are required for the functions. However, elevated levels of AA and their products (e.g., ammonia, homocysteine, and asymmetric dimethylarginine) are pathogenic factors for neurological disorders, oxidative stress, and cardiovascular disease. Thus, an optimal balance among AA in the diet and circulation is crucial for whole body homeostasis. There is growing recognition that besides their role as building blocks of proteins and polypeptides, some AA regulate key metabolic pathways that are necessary for maintenance, growth, reproduction, and immunity. They are called functional AA, which include arginine, cysteine, glutamine, leucine, proline, and tryptophan. Dietary supplementation with one or a mixture of these AA may be beneficial for (1) ameliorating health problems at various stages of the life cycle (e.g., fetal growth restriction, neonatal morbidity and mortality, weaning-associated intestinal dysfunction and wasting syndrome, obesity, diabetes, cardiovascular disease, the metabolic syndrome, and infertility); (2) optimizing efficiency of metabolic transformations to enhance muscle growth, milk production, egg and meat quality and athletic performance, while preventing excess fat deposition and reducing adiposity. Thus, AA have important functions in both nutrition and health.
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            A New View into the Regulation of Purine Metabolism: The Purinosome.

            Other than serving as building blocks for DNA and RNA, purine metabolites provide a cell with the necessary energy and cofactors to promote cell survival and proliferation. A renewed interest in how purine metabolism may fuel cancer progression has uncovered a new perspective into how a cell regulates purine need. Under cellular conditions of high purine demand, the de novo purine biosynthetic enzymes cluster near mitochondria and microtubules to form dynamic multienzyme complexes referred to as 'purinosomes'. In this review, we highlight the purinosome as a novel level of metabolic organization of enzymes in cells, its consequences for regulation of purine metabolism, and the extent that purine metabolism is being targeted for the treatment of cancers.
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              Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality.

              The aim of this study is to examine the effect of bovine oocyte maturation, fertilization or culture in vivo or in vitro on the proportion of oocytes reaching the blastocyst stage, and on blastocyst quality as measured by survival following vitrification. In Experiment 1, 4 groups of oocytes were used: (1) immature oocytes from 2-6 mm follicles; (2) immature oocytes from > 6 mm follicles; (3) immature oocytes recovered in vivo just before the LH surge; and (4) in vivo matured oocytes. Significantly more blastocysts developed from oocytes matured in vivo than those recovered just before the LH surge or than oocytes from 2-6 mm follicles. Results from > 6 mm follicles were intermediate. All blastocysts had low survival following vitrification. In Experiment 2, in vivo matured oocytes were either (1) fertilized in vitro or (2) fertilized in vivo by artificial insemination and the resulting presumptive zygotes recovered on day 1. Both groups were then cultured in vitro. In vivo fertilized oocytes had a significantly higher blastocyst yield than those fertilized in vitro. Blastocyst quality was similar between the groups. Both groups had low survival following vitrification. In Experiment 3a, presumptive zygotes produced by in vitro maturation (IVM)/fertilization (IVF) were cultured either in vitro in synthetic oviduct fluid, or in vivo in the ewe oviduct. In Experiment 3b, in vivo matured/in vivo fertilized zygotes were either surgically recovered on day 1 and cultured in vitro in synthetic oviduct fluid, or were nonsurgically recovered on day 7. There was no difference in blastocyst yields between groups of zygotes originating from the same source (in vivo or in vitro fertilization) irrespective of whether culture took place in vivo or in vitro. However, there was a dramatic effect on blastocyst quality with those blastocysts produced following in vivo culture surviving vitrification at significantly higher rates than their in vitro cultured counterparts. Collectively, these results indicate that the intrinsic quality of the oocyte is the main factor affecting blastocyst yields, while the conditions of embryo culture have a crucial role in determining blastocyst quality. Copyright 2002 Wiley-Liss, Inc.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PNAS Nexus
                PNAS Nexus
                pnasnexus
                PNAS Nexus
                Oxford University Press (US )
                2752-6542
                May 2024
                30 April 2024
                30 April 2024
                : 3
                : 5
                : pgae181
                Affiliations
                Department of Animal Science, University of Tennessee Institute of Agriculture and AgResearch , 2506 River Drive, Knoxville, TN 37996, USA
                Department of Animal Science, University of Tennessee Institute of Agriculture and AgResearch , 2506 River Drive, Knoxville, TN 37996, USA
                Department of Animal Science, University of Tennessee Institute of Agriculture and AgResearch , 2506 River Drive, Knoxville, TN 37996, USA
                Department of Animal Science, University of Tennessee Institute of Agriculture and AgResearch , 2506 River Drive, Knoxville, TN 37996, USA
                Department of Animal Science, University of Tennessee Institute of Agriculture and AgResearch , 2506 River Drive, Knoxville, TN 37996, USA
                Department of Chemistry, University of Tennessee , 1420 Circle Dr., Knoxville, TN 37996, USA
                Department of Chemistry, University of Tennessee , 1420 Circle Dr., Knoxville, TN 37996, USA
                Department of Animal Science, University of Tennessee Institute of Agriculture and AgResearch , 2506 River Drive, Knoxville, TN 37996, USA
                Department of Animal Science, University of Tennessee Institute of Agriculture and AgResearch , 2506 River Drive, Knoxville, TN 37996, USA
                Department of Animal Science, University of Tennessee Institute of Agriculture and AgResearch , 2506 River Drive, Knoxville, TN 37996, USA
                Department of Animal Science, University of Tennessee Institute of Agriculture and AgResearch , 2506 River Drive, Knoxville, TN 37996, USA
                Author notes
                To whom correspondence should be addressed: Email: smoorey5@ 123456utk.edu

                Competing Interest: The authors declare no competing interest.

                Author information
                https://orcid.org/0009-0007-2562-0678
                https://orcid.org/0000-0003-3013-9233
                https://orcid.org/0000-0003-0270-4127
                https://orcid.org/0000-0001-6809-3862
                https://orcid.org/0000-0001-9243-3863
                Article
                pgae181
                10.1093/pnasnexus/pgae181
                11095542
                38752021
                defbc6f4-51c0-4571-a963-e06a830d765d
                © The Author(s) 2024. Published by Oxford University Press on behalf of National Academy of Sciences.

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 04 January 2024
                : 17 April 2024
                : 13 May 2024
                Page count
                Pages: 12
                Funding
                Funded by: Agriculture and Food Research Initiative Competitive;
                Award ID: 2023-67015-39454
                Funded by: USDA National Institute of Food and Agriculture, USDA Multistate project NE 2227, and The University of Tennessee AgResearch and Department of Animal Science;
                Categories
                Biological, Health, and Medical Sciences
                AcademicSubjects/MED00010
                AcademicSubjects/SCI00010
                AcademicSubjects/SOC00010
                PNAS_Nexus/ag-sci

                bovine,cumulus-oocyte complex metabolism,embryo development,follicular fluid,preovulatory follicle

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