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      A grape seed extract maternal dietary supplementation improves egg quality and reduces ovarian steroidogenesis without affecting fertility parameters in reproductive hens

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          Abstract

          In broiler hens, the genetic selection increased susceptibility to metabolic disorders and reproductive dysfunctions. In human ovarian cells, grape seed extracts (GSE) improved steroid production. Here, we investigated the effects of a GSE dietary supplementation on egg production and quality, fertility parameters, Reactive Oxygen Species (ROS) and steroid content in yolk egg associated to plasma adipokines in broiler hens. For this, we designed two in vivo experiments, the first one included three groups of hens: A (control), B and C (supplemented with GSE at 0.5% and 1% of the total diet composition, respectively, since week 4), and the second one used two groups of hens: A (control) and D (supplemented with GSE at 1% of the total diet composition since hatching). We assessed the egg production from 23 th to 40 th weeks and quality at 33 th week. After artificial inseminations, the fertility parameters were calculated. In egg yolk, Reactive Oxygen Species (ROS) level and steroid production were evaluated by Ros-Glo H202 and ELISA assay, respectively. Expression of steroidogenic enzymes and adipokines and their receptors was determined by RT-qPCR in ovarian cells and plasma adipokines (RARRES2, ADIPOQ and NAMPT) were evaluated by specific ELISA assays. The fertility parameters and egg production were unaffected by GSE supplementation whatever the experiment (exp.). However, the rate of double-yolk eggs decreased for all GSE supplemented groups (exp. 1 P <0.01, exp.2, P<0.02). In exp.1, C group eggs were bigger and larger ( P<0.0001) and the shell elasticity was higher for both B and C ( P<0.0003) as compared to control. In the egg yolk, GSE supplementation in both exp. reduced ROS content and steroidogenesis consistent with a decrease in P450 aromatase and StAR mRNA expression and basal in vitro progesterone secretion in granulosa cells ( P<0.001). Interestingly, in both exp. RARRES2 plasma levels were positively correlated while ADIPOQ and NAMPT plasma levels were negatively correlated, with steroids and ROS in yolk ( P<0.0001). Taken together, maternal dietary GSE supplementation did not affect egg production and fertility parameters whereas it reduced ROS content and steroidogenesis in yolk egg. Furthermore, it ameliorated egg quality by decreasing the number of double-yolk eggs and by improving the size of normal eggs and the elasticity of the shell. Taken together, our data suggest the possibility of using dietary maternal GSE to improve egg quality.

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          Most cited references 51

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          Discovery and resupply of pharmacologically active plant-derived natural products: A review

          Medicinal plants have historically proven their value as a source of molecules with therapeutic potential, and nowadays still represent an important pool for the identification of novel drug leads. In the past decades, pharmaceutical industry focused mainly on libraries of synthetic compounds as drug discovery source. They are comparably easy to produce and resupply, and demonstrate good compatibility with established high throughput screening (HTS) platforms. However, at the same time there has been a declining trend in the number of new drugs reaching the market, raising renewed scientific interest in drug discovery from natural sources, despite of its known challenges. In this survey, a brief outline of historical development is provided together with a comprehensive overview of used approaches and recent developments relevant to plant-derived natural product drug discovery. Associated challenges and major strengths of natural product-based drug discovery are critically discussed. A snapshot of the advanced plant-derived natural products that are currently in actively recruiting clinical trials is also presented. Importantly, the transition of a natural compound from a “screening hit” through a “drug lead” to a “marketed drug” is associated with increasingly challenging demands for compound amount, which often cannot be met by re-isolation from the respective plant sources. In this regard, existing alternatives for resupply are also discussed, including different biotechnology approaches and total organic synthesis. While the intrinsic complexity of natural product-based drug discovery necessitates highly integrated interdisciplinary approaches, the reviewed scientific developments, recent technological advances, and research trends clearly indicate that natural products will be among the most important sources of new drugs also in the future.
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            Maternal hormones as a tool to adjust offspring phenotype in avian species.

            Avian eggs contain substantial amounts of maternal hormones and so provide an excellent model to study hormone-mediated maternal effects. We review this new and rapidly evolving field, taking an ecological and evolutionary approach and focusing on effects and function of maternal androgens in offspring development. Manipulation of yolk levels of androgens within the physiological range indicates that maternal androgens affect behaviour, growth, morphology, immune function and survival of the offspring, in some cases even long after fledging. Descriptive and experimental studies show systematic variation in maternal androgen deposition both within and among clutches, as well as in relation to the sex of the embryo. We discuss the potential adaptive value of maternal androgen transfer at all these three levels. We conclude that maternal androgen deposition in avian eggs provides a flexible mechanism of non-genetic inheritance, by which the mother can favour some offspring over others, and adjust their developmental trajectories to prevailing environmental conditions, producing different phenotypes. However, the literature is less consistent than often assumed and at all three levels, the functional explanations need further experimental testing. The field would greatly benefit from an analysis of the underlying physiological mechanisms.
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              Free radicals and grape seed proanthocyanidin extract: importance in human health and disease prevention.

              Free radicals have been implicated in over a hundred disease conditions in humans, including arthritis, hemorrhagic shock, atherosclerosis, advancing age, ischemia and reperfusion injury of many organs, Alzheimer and Parkinson's disease, gastrointestinal dysfunctions, tumor promotion and carcinogenesis, and AIDS. Antioxidants are potent scavengers of free radicals and serve as inhibitors of neoplastic processes. A large number of synthetic and natural antioxidants have been demonstrated to induce beneficial effects on human health and disease prevention. However, the structure-activity relationship, bioavailability and therapeutic efficacy of the antioxidants differ extensively. Oligomeric proanthocyanidins, naturally occurring antioxidants widely available in fruits, vegetables, nuts, seeds, flowers and bark, have been reported to possess a broad spectrum of biological, pharmacological and therapeutic activities against free radicals and oxidative stress. We have assessed the concentration- or dose-dependent free radical scavenging ability of a novel IH636 grape seed proanthocyanidin extract (GSPE) both in vitro and in vivo models, and compared the free radical scavenging ability of GSPE with vitamins C, E and beta-carotene. These experiments demonstrated that GSPE is highly bioavailable and provides significantly greater protection against free radicals and free radical-induced lipid peroxidation and DNA damage than vitamins C, E and beta-carotene. GSPE was also shown to demonstrate cytotoxicity towards human breast, lung and gastric adenocarcinoma cells, while enhancing the growth and viability of normal human gastric mucosal cells. The comparative protective effects of GSPE, vitamins C and E were examined on tobacco-induced oxidative stress and apoptotic cell death in human oral keratinocytes. Oxidative tissue damage was determined by lipid peroxidation and DNA fragmentation, while apoptotic cell death was assessed by flow cytometry. GSPE provided significantly better protection as compared to vitamins C and E, singly and in combination. GSPE also demonstrated excellent protection against acetaminophen overdose-induced liver and kidney damage by regulating bcl-X(L) gene, DNA damage and presumably by reducing oxidative stress. GSPE demonstrated excellent protection against myocardial ischemia-reperfusion injury and myocardial infarction in rats. GSPE was also shown to upregulate bcl(2) gene and downregulate the oncogene c-myc. Topical application of GSPE enhances sun protection factor in human volunteers, as well as supplementation of GSPE ameliorates chronic pancreatitis in humans. These results demonstrate that GSPE provides excellent protection against oxidative stress and free radical-mediated tissue injury.
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                Author and article information

                Contributors
                Role: Data curationRole: InvestigationRole: ValidationRole: Writing – original draft
                Role: Data curationRole: MethodologyRole: Validation
                Role: InvestigationRole: Validation
                Role: Investigation
                Role: ConceptualizationRole: Investigation
                Role: Investigation
                Role: ConceptualizationRole: Investigation
                Role: ConceptualizationRole: Investigation
                Role: ConceptualizationRole: Investigation
                Role: ConceptualizationRole: Investigation
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: MethodologyRole: SupervisionRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                14 May 2020
                2020
                : 15
                : 5
                Affiliations
                [1 ] INRAE UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France
                [2 ] CNRS UMR7247 Physiologie de la Reproduction et des Comportements, Nouzilly, France
                [3 ] Université François Rabelais de Tours, Tours, France
                [4 ] IFCE Nouzilly, Nouzilly, France
                [5 ] INRAE - Unité Expérimentale du Pôle d’Expérimentation Avicole de Tours UEPEAT, 1295, Nouzilly, Nouzilly, France
                [6 ] INRAE, UMR0083 Biologie des Oiseaux et Aviculture, Nouzilly, France
                [7 ] INDENA, Tours, France
                University of Illinois, UNITED STATES
                Author notes

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

                Article
                PONE-D-20-06306
                10.1371/journal.pone.0233169
                7224513
                32407420
                © 2020 Barbe 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.

                Page count
                Figures: 6, Tables: 5, Pages: 22
                Product
                Funding
                Funded by: Conseil Régional du Centre-Val de Loire (FR)
                Award ID: 32000820
                Award Recipient :
                The funder is Region Centre Val de Loire (project number 32000820). 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
                Nutrition
                Diet
                Medicine and Health Sciences
                Nutrition
                Diet
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Epithelial Cells
                Granulosa Cells
                Biology and Life Sciences
                Anatomy
                Biological Tissue
                Epithelium
                Epithelial Cells
                Granulosa Cells
                Medicine and Health Sciences
                Anatomy
                Biological Tissue
                Epithelium
                Epithelial Cells
                Granulosa Cells
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Lutein Cells
                Granulosa Cells
                Biology and Life Sciences
                Physiology
                Immune Physiology
                Cytokines
                Adipokines
                Medicine and Health Sciences
                Physiology
                Immune Physiology
                Cytokines
                Adipokines
                Biology and Life Sciences
                Immunology
                Immune System
                Innate Immune System
                Cytokines
                Adipokines
                Medicine and Health Sciences
                Immunology
                Immune System
                Innate Immune System
                Cytokines
                Adipokines
                Biology and Life Sciences
                Developmental Biology
                Molecular Development
                Cytokines
                Adipokines
                Biology and Life Sciences
                Biochemistry
                Hormones
                Lipid Hormones
                Progesterone
                Biology and Life Sciences
                Biochemistry
                Oxidative Damage
                Reactive Oxygen Species
                Physical Sciences
                Chemistry
                Chemical Compounds
                Organic Compounds
                Steroids
                Physical Sciences
                Chemistry
                Organic Chemistry
                Organic Compounds
                Steroids
                Biology and Life Sciences
                Biochemistry
                Hormones
                Androgens
                Testosterone
                Biology and Life Sciences
                Biochemistry
                Hormones
                Lipid Hormones
                Testosterone
                Biology and Life Sciences
                Cell Biology
                Oxidative Stress
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

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