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Mathilde Daudon CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France
Centre de recherche en reproduction et fertilité, Faculté de médecine vétérinaire, Université de Montréal, St-Hyacinthe QC Canada

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Christelle Ramé CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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Christopher Price Centre de recherche en reproduction et fertilité, Faculté de médecine vétérinaire, Université de Montréal, St-Hyacinthe QC Canada

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Joëlle Dupont CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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In brief

Fertility in the dairy cow is low during the post-partum period of negative energy balance and high plasma irisin concentrations. This study shows irisin modulates granulosa cell glucose metabolism and impairs steroidogenesis.

Abstract

Fibronectin type III domain-containing 5 (FNDC5) is a transmembrane protein discovered in 2012 that is cleaved to release the adipokine-myokine, irisin. Originally described as an exercise hormone that browns white adipose tissue and increases glucose metabolism, irisin secretion also increases during periods of rapid adipose mobilization, such as the post-partum period in dairy cattle when ovarian activity is suppressed. The effect of irisin on follicle function is unclear and may be species-dependent. In this study, we hypothesized that irisin may compromise granulosa cell function in cattle using a well-established in vitro cell culture model. We detected FNDC5 mRNA and both FNDC5 and cleaved irisin proteins in follicle tissue and in follicular fluid. The abundance of FNDC5 mRNA was increased by the treatment of cells with the adipokine visfatin but not by other adipokines tested. The addition of recombinant irisin to granulosa cells decreased basal and insulin-like growth factor 1- and follicle-stimulating hormone-dependent estradiol and progesterone secretion and increased cell proliferation but had no effect on viability. Irisin decreased GLUT1, GLUT3, and GLUT4 mRNA levels in granulosa cells and increased lactate release in the culture medium. The mechanism of action is in part through MAPK3/1 but not Akt, MAPK14, or PRKAA. We conclude that irisin may regulate bovine folliculogenesis by modulating granulosa cell steroidogenesis and glucose metabolism.

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Lucie Tosca
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Christelle Ramé
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Christine Chabrolle
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Sophie Tesseraud Unité de Physiologie de la Reproduction et des Comportements, Unité de Recherches Avicoles, Institut National de la Recherche Agronomique (INRA), UMR85, F-37 380 Nouzilly, France

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Joëlle Dupont
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Although its mechanism of action is still unclear, metformin is an anti-diabetic drug effective to restore cyclicity and spontaneous ovulation in women with polycystic ovary syndrome. It may also reduce the risk of cancer. We have recently shown that metformin treatment decreases steroidogenesis through AMP-activated kinase (AMPK) in granulosa cells of various species. Here, we investigated the effects and the molecular mechanisms of metformin in IGF1-induced proliferation and protein synthesis in cultured bovine granulosa cells. Treatment with metformin (10 mM) for 24 h reduced cell proliferation and the levels of cyclin D2 and E, and increased the associations cyclin D2/p21 and cyclin D2/p27 without affecting cell viability in response to IGF1 (10−8 M). It also decreased IGF1-induced protein synthesis and phosphorylation of P70S6 kinase and ribosomal S6 protein. Interestingly, metformin treatment for 1 h decreased MAPK3/1 (ERK1/2) and P90RSK phosphorylation without affecting AKT phosphorylation in response to IGF1. Adenovirus-mediated expression of dominant-negative AMPK totally abolished the effects of metformin on cell proliferation and phosphorylation of P70S6K in response to IGF1. It also eliminated the inhibitory effects of metformin on MAPK3/1 and P90RSK phosphorylation. Taken together, our results strongly suggest that metformin reduces cell growth, protein synthesis, MAPK3/1, and P90RSK phosphorylation in response to IGF1 through an AMPK-dependent mechanism in cultured bovine granulosa cells.

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Mélodie Diot INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France

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Maxime Reverchon INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France

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Christelle Ramé INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France

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Yannick Baumard INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France

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Joëlle Dupont INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France
INRA, CNRS, Université François Rabelais de Tours, IFCE, INRA, UMR85 Physiologie de la Reproduction et des Comportements, F‐37380 Nouzilly, France

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In mammals, nicotinamide phosphoribosyltransferase (NAMPT) is an adipokine produced by adipose tissue that is found in intracellular and extracellular compartments. The intracellular form of NAMPT is a nicotinamide phosphoribosyltransferase, whereas the extracellular form is considered an adipokine. In humans, NAMPT regulates energy metabolism and reproductive functions, such as ovarian steroidogenesis. To date, no study has investigated the role of NAMPT in hen ovaries. We investigated whether NAMPT is present in hen ovarian follicles and its role in granulosa cells. Using RT-PCR, western blotting and immunocytochemistry, we detected mRNA transcripts and proteins related to NAMPT in theca and granulosa cells from pre-ovulatory follicles. Using RT-PCR, we demonstrated that mRNA NAMPT levels were higher in granulosa cells than they were in theca cells and that during follicle development, theca cell levels decreased, whereas levels remained unchanged in granulosa cells. NAMPT protein quantities were significantly higher in theca cells than they were in granulosa cells, but they were unchanged during follicular development. Plasma NAMPT levels, as determined by ELISA and immunoblotting, were significantly lower in adult hens than they were in juveniles. In vitro, treatment with human recombinant NAMPT (100 ng/ml, 48 h) halved basal and IGF1-induced progesterone secretion, and this was associated with a reduction in STAR and HSD3B protein levels and MAPK3/1 phosphorylation levels in granulosa cells. These effects were abolished by the addition of FK866, a specific inhibitor of NAMPT enzymatic activity. Moreover, NAMPT had no effect on granulosa cell proliferation. In conclusion, NAMPT is present in hen ovarian cells and inhibits progesterone production in granulosa cells.

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Mathilde Daudon CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France
Centre de recherche en reproduction et fertilité, Faculté de médecine vétérinaire, Université de Montréal, Saint Hyacinthe, Quebec, Canada

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Christelle Ramé CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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Christopher A Price Centre de recherche en reproduction et fertilité, Faculté de médecine vétérinaire, Université de Montréal, Saint Hyacinthe, Quebec, Canada

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Joëlle Dupont CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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In brief

Dairy cattle experience a period of infertility postpartum that is caused in part by the development of IGF1/insulin resistance. This study suggests that an adipokine, FNDC3A, reduces IGF1-dependent glycolysis and may contribute to postpartum infertility.

Abstract

Dairy cows go through a period of subfertility after parturition, triggered in part by a disruption of energy homeostasis. The mobilization of body fat alters the secretion of adipokines, which have been shown to impact ovarian function. Fibronectin type III domain-containing 3A (FNDC3A) is a recently discovered adipokine-myokine, and FNDC3A mRNA abundance in subcutaneous adipose tissue is increased postpartum in cattle. In this study, we hypothesized that FNDC3A may compromise granulosa cell function in cattle and investigated this using a well-established in vitro cell culture model. Here, we demonstrate the presence of FNDC3A protein associated with extracellular vesicles in follicular fluid and in plasma, suggesting an endocrine role for this adipokine. FNDC3A protein and mRNA was also detected in the bovine ovary (cortex, granulosa and theca cells, cumulus, oocyte and corpus luteum). Abundance of FNDC3A mRNA in granulosa cells from small follicles was increased by in vitro treatment with the adipokines leptin and TNF but not by visfatin, resistin, adiponectin, chemerin or IGF1. Addition of recombinant FNDC3A at physiological doses (10 ng/mL) to granulosa cells decreased IGF1-dependent progesterone but not estradiol secretion and IGF1-dependent lactate secretion and abundance of GLUT3 and GLUT4 mRNA. This concentration of FNDC3A increased cell viability, abundance of mRNA encoding a putative receptor FOLR1, and increased phosphorylation of Akt. Collectively, these data suggest that FNDC3A may regulate folliculogenesis in cattle by modulating IGF1-dependent granulosa cell steroidogenesis and glucose metabolism.

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Alix Barbe INRAE, UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France

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Patrycja Kurowska Laboratory of Physiology and Toxicology of Reproduction, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Krakow, Poland

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Christelle Rame INRAE, UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France

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Pascal Froment INRAE, UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France

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Agnieszka Rak Laboratory of Physiology and Toxicology of Reproduction, Institute of Zoology and Biomedical Research, Jagiellonian University in Krakow, Krakow, Poland

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Joëlle Dupont INRAE, UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France

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Adipolin (C1QTNF12) has been described as a regulator of metabolism and is linked with the pathophysiology of PCOS. In this study, for the first time, we show the expression of C1QTNF12 in granulosa cells and its positive effect on porcine granulosa cell proliferation and steroid synthesis.

Abstract

Adipolin (C1QTNF12) is a recently discovered adipokine that plays an important role in glucose and insulin level regulation. Previous studies showed its reduced level in serum of women suffering from polycystic ovarian syndrome; however, whether C1QTNF12 regulates ovary function is still unknown. The aim of the study was first to determine the level of C1QTNF12 in the porcine ovarian follicles granulosa cells (Gc) and then its in vitro effect on proliferation and steroidogenesis as well as phosphorylation of several signalling pathways. Our results showed that the expression of C1QTNF12 was dependent on follicle size and was higher at the mRNA and protein level in Gc of small than large follicles from both prepubertal and mature animals. Similar pattern was observed for C1QTNF12 concentration in porcine follicular fluid. Additionally, we observed immunolocalisation of C1QTNF12 in Gc, theca cells and oocytes. We found that C1QTNF12 stimulated porcine Gc proliferation via the activation of protein kinase B (AKT). Moreover, C1QTNF12 enhanced progesterone, testosterone and oestradiol secretion by elevating STAR, CYP11A1, HSD3B and CYP19A1 mRNA expression and by activation of MAP3/1 pathway. Additionally, C1QTNF12 increased pMAP3/1-to-MAP3/1 protein expression ratio and enhanced IGF1-induced pTyr-IGF1Rβ-to-IGFR1β and pMAP3/1-to-MAP3/1 protein ratios. Taken together, C1QTNF12 could act directly on proliferation and steroid synthesis and serve as an important factor in in vivo ovarian follicle function, possibly regulating the course of folliculogenesis.

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Virginie Maillard Unité de Physiologie de la Reproduction et des Comportements, UMR85, Equipe Métabolisme et Reproduction, Institut National de la Recherche Agronomique, F-37 380 Nouzilly, France

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Pascal Froment Unité de Physiologie de la Reproduction et des Comportements, UMR85, Equipe Métabolisme et Reproduction, Institut National de la Recherche Agronomique, F-37 380 Nouzilly, France

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Christelle Ramé Unité de Physiologie de la Reproduction et des Comportements, UMR85, Equipe Métabolisme et Reproduction, Institut National de la Recherche Agronomique, F-37 380 Nouzilly, France

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Svetlana Uzbekova Unité de Physiologie de la Reproduction et des Comportements, UMR85, Equipe Métabolisme et Reproduction, Institut National de la Recherche Agronomique, F-37 380 Nouzilly, France

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Sébastien Elis Unité de Physiologie de la Reproduction et des Comportements, UMR85, Equipe Métabolisme et Reproduction, Institut National de la Recherche Agronomique, F-37 380 Nouzilly, France

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Joëlle Dupont Unité de Physiologie de la Reproduction et des Comportements, UMR85, Equipe Métabolisme et Reproduction, Institut National de la Recherche Agronomique, F-37 380 Nouzilly, France

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Resistin, initially identified in adipose tissue and macrophages, was implicated in insulin resistance. Recently, its mRNA was found in hypothalamo–pituitary axis and rat testis, leading us to hypothesize that resistin may be expressed in ovary. In this study, we determined in rats and cows 1) the characterization of resistin in ovary by RT-PCR, immunoblotting, and immunohistochemistry and 2) the effects of recombinant resistin (10, 100, 333, and 667 ng/ml)±IGF1 (76 ng/ml) on steroidogenesis, proliferation, and signaling pathways of granulosa cells (GC) measured by enzyme immunoassay, [3H]thymidine incorporation, and immunoblotting respectively. We observed that resistin mRNA and protein were present in several bovine and rat ovarian cells. Nevertheless, only bovine GC abundantly expressed resistin mRNA and protein. Resistin treatment decreased basal but not IGF1-induced progesterone (P<0.05; whatever the dose) and estradiol (P<0.005; for 10 and 333 ng/ml) production by bovine GC. In rats, resistin (10 ng/ml) increased basal and IGF1-induced progesterone secretion (P<0.0001), without effect on estradiol release. We found no effect of resistin on rat GC proliferation. Conversely, in cows, resistin increased basal proliferation (P<0.0001; for 100–667 ng/ml) and decreased IGF1-induced proliferation of GC (P<0.0001; for 10–333 ng/ml) associated with a decrease in cyclin D2 protein level (P<0.0001). Finally, resistin stimulated AKT and p38-MAPK phosphorylation in both species, ERK1/2-MAPK phosphorylation in rats and had the opposite effect on the AMPK pathway (P<0.05). In conclusion, our results show that resistin is expressed in rat and bovine ovaries. Furthermore, it can modulate GC functions in basal state or in response to IGF1 in vitro.

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Anthony Estienne CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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Namya Mellouk CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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Alice Bongrani CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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Ingrid Plotton Molecular Endocrinology and Rare Diseases, University Hospital, Claude Bernard Lyon 1 University, Bron, France

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Ingrid Langer Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire, Université Libre de Bruxelles, Brussels, Belgium

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Christelle Ramé CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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Claire Petit Department of Reproductive Medicine and Biology, University Hospital of Tours, Tours, France

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Fabrice Guérif CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France
Department of Reproductive Medicine and Biology, University Hospital of Tours, Tours, France

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Pascal Froment CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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Joëlle Dupont CNRS, IFCE, INRAE, Université de Tours, PRC, Nouzilly, France

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Polycystic ovarian syndrome (PCOS) is the main cause of infertility in women. It is frequently associated with reduced progesterone production by human luteinised granulosa cells (hlGCs). However, the molecular mechanisms involved in these steroidogenesis alterations in PCOS patients are unclear. In a dihydrotestosterone-induced PCOS mouse model, steroid production is maintained in the setting of chemokine-like receptor 1 (Cmklr1) knockout. Thus, chemerin and chemerin receptors in terms of expression and progesterone regulation could be different in control and PCOS hlGCs. We first confirmed that progesterone levels in both plasma (P  < 0.0001) and follicular fluid (FF) (P  < 0.0001) were significantly reduced in PCOS normal weight women compared to control women. These data were associated with a lower STAR mRNA expression in both in vivo (P  < 0.0001) and in vitro (P  < 0.0001) hlGCs from PCOS women. Secondly, chemerin FF levels (P  < 0.0001) and RARRES2 (P  < 0.05) and CMKLR1 (P  < 0.0001) mRNA levels in GCs were higher in PCOS normal weight patients. Thirdly, treatment of hlGCs with a specific nanobody (the VHH CA4910) targeting the human receptor for CMKLR1 leading to its inactivation abolished chemerin-induced progesterone inhibition, suggesting the involvement of CMKLR1 in this process. Furthermore, the inhibition of progesterone secretion induced by chemerin was two-fold higher in PCOS hlGCs (P  < 0.05). Moreover, the VHH CA4910 reinstated a normal progesterone secretion with lower concentrations in PCOS hlGCs, suggesting a different chemerin sensitivity between PCOS and control hlGCs. Thus, chemerin, through CMKLR1, could be involved in the steroidogenesis alterations in PCOS hlGCs.

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Claude Fabre-Nys UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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Audrey Chanvallon UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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Nathalie Debus UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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Dominique François UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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Frédéric Bouvier UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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Joelle Dupont UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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Lionel Lardic UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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Didier Lomet UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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Christelle Ramé UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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Rex J Scaramuzzi UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France
UMR 7247 Physiologie de la Reproduction et des Comportements, UMR 868 ‘Elevage des Ruminants en Régions Chaudes’, INRA SAGA, INRA Bourges, Department of Comparative Biological Sciences, CNRS, Institut Français du Cheval et de l'Équitation, Université de Tours, PRC Centre INRA Val de Loire, 37380 Nouzilly, France

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The proportion of anoestrous ewes ovulating after exposure to a sexually active ram is variable mainly due to whether an LH surge is induced. The aim of this study was to determine the role of oestradiol (E2) in the ram-induced LH surge. In one study, we measured the plasma concentrations of E2 in ewes of different breeds before and after the ‘ram effect’ and related these patterns to the presence and latency of the LH surge, while another compared ovarian responses with the ‘ram effect’ following exposure to rams for 2 or 12 h. In all ewes, the concentration of E2 increased 2–4 h after rams were introduced and remained elevated for 14.5±0.86 h. The quantity of E2 secreted before the LH surge varied among breeds as did the mean concentration of E2. The granulosa cells of IF ewes collected after 12 h exposure to rams secreted more E2 and progesterone and had higher levels of StAR than the 2 h group but in MV ewes there was no differences between these groups for any of these parameters. These results demonstrate that the LH surge induced by the rams is a result of increased E2 secretion associated with increased levels of STAR in granulosa cells and that these responses varied among breeds. The results suggest that the variable occurrence of a LH surge and ovulation may be the result of variable ovarian responses to the ‘ram effect’ and insensitivity of the hypothalamus to the E2-positive feedback signal.

Free French abstract: A French translation of this abstract is freely available at http://www.reproduction-online.org/content/149/5/511/suppl/DC1.

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Namya Mellouk INRA UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France
CNRS UMR7247 Physiologie de la Reproduction et des Comportements, Nouzilly, France
Université François Rabelais de Tours, Tours, France
IFCE, Nouzilly, France

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Christelle Ramé INRA UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France
CNRS UMR7247 Physiologie de la Reproduction et des Comportements, Nouzilly, France
Université François Rabelais de Tours, Tours, France
IFCE, Nouzilly, France

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Joël Delaveau INRA – Unité Expérimentale du Pôle d’Expérimentation Avicole de Tours UEPEAT, Nouzilly, France

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Christophe Rat INRA – Unité Expérimentale du Pôle d’Expérimentation Avicole de Tours UEPEAT, Nouzilly, France

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Maxime Marchand INRA – Unité Expérimentale du Pôle d’Expérimentation Avicole de Tours UEPEAT, Nouzilly, France

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Frédéric Mercerand INRA – Unité Expérimentale du Pôle d’Expérimentation Avicole de Tours UEPEAT, Nouzilly, France

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Angélique Travel ITAVI – Centre INRA Centre Val de Loire, Nouzilly, France

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Aurélien Brionne INRA – Unité de Recherches Avicoles, Nouzilly, France

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Pascal Chartrin INRA – Unité de Recherches Avicoles, Nouzilly, France

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Linlin Ma INRA UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France
CNRS UMR7247 Physiologie de la Reproduction et des Comportements, Nouzilly, France
Université François Rabelais de Tours, Tours, France
IFCE, Nouzilly, France

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Pascal Froment INRA UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France
CNRS UMR7247 Physiologie de la Reproduction et des Comportements, Nouzilly, France
Université François Rabelais de Tours, Tours, France
IFCE, Nouzilly, France

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Joëlle Dupont INRA UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France
CNRS UMR7247 Physiologie de la Reproduction et des Comportements, Nouzilly, France
Université François Rabelais de Tours, Tours, France
IFCE, Nouzilly, France

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Overfed hens selected for their rapid growth become fatter and develop reproductive disorders. Herein, we aimed to demonstrate that food restriction leading to a weight reduction and/or a supplementation with fish oil may be effective in preventing reproductive disorders through the regulation of adipokine expression in broiler hens. This study included four groups of food restricted (Rt) or ad libitum hens (Ad, feeding at a rate 1.7 times greater than Rt hens) supplemented or unsupplemented with fish oil (1%). The Rt diet significantly increased plasma chemerin (RARRES2) levels during the laying period, delayed sexual maturity by one week and improved egg quality and fertility. These effects were associated with higher progesterone production in response to IGF1 (or LH) in cultured granulosa cells and in vivo egg yolk, as compared with Ad hens. Fish oil supplementation had similar effects to the Rt diet on progesterone (P < 0.05), but without any effect on fertility. Using RT-PCR, we found that RARRES2 levels were lower in theca cells of Rt hens and NAMPT levels were increased by the fish oil supplementation. A significant positive correlation between RARRES2 expression in granulosa cells and the weight of F1 preovulatory follicle was observed, as well as a negative correlation of plasma RARRES2 levels with hatchability. Thus, food restriction but not fish oil supplementation improved fertility, and this was associated with variations in RARRES2 plasma and ovarian expression in hens.

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Gonçalo Pereira CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Lisboa, Portugal

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Ricardo Bexiga CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Lisboa, Portugal

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João Chagas e Silva CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Lisboa, Portugal

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Elisabete Silva CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Lisboa, Portugal

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Christelle Ramé INRAE, UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France

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Joëlle Dupont INRAE, UMR85 Physiologie de la Reproduction et des Comportements, Nouzilly, France

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Yongzhi Guo Division of Reproduction, Department of Clinical Sciences, SLU, Uppsala, Sweden

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Patrice Humblot Division of Reproduction, Department of Clinical Sciences, SLU, Uppsala, Sweden

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Luís Lopes-da-Costa CIISA – Centro de Investigação Interdisciplinar em Sanidade Animal, Faculdade de Medicina Veterinária, Universidade de Lisboa, Lisboa, Portugal

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Adipokines emerged as regulators of metabolism and inflammation in several scenarios. This study evaluated the relationship between adipokines (adiponectin, chemerin and visfatin) and cytological (subclinical) endometritis, by comparing healthy (without), transient (recovered by 45 days postpartum (DPP)) and persistent (until 45 DPP) endometritis cows (n = 49). Cows with persistent endometritis had higher adiponectin concentrations in plasma (at 21 DPP, P < 0.05 and at 45 DPP, P < 0.01) and in uterine fluid (at 45 DPP, P < 0.001), and higher chemerin concentrations in plasma (P < 0.05) and uterine fluid (P < 0.01) at 45 DPP than healthy cows. Cows with persistent endometritis had higher gene transcription in the cellular pellet of uterine fluid and protein expression in the endometrium of these adipokines and their receptors than healthy cows. Adiponectin plasma concentrations allowed to discriminate healthy from persistent endometritis cows, in 87% (21 DPP) and 98% (45 DPP) of cases, and adiponectin and chemerin uterine fluid concentrations at 45 DPP allowed for this discrimination in 100% of cases. Cows with concentrations above the cutoff were a minimum of 3.5 (plasma 21 DPP), 20.4 (plasma 45 DPP), and 33.3 (uterine fluid 45 DPP) times more at risk of evidencing persistent endometritis at 45 DPP than cows with concentrations below the cutoff. Overall, results indicate a relationship between adipokine signalling and the inflammatory status of the postpartum uterus of dairy cows, evidencing that adipokines represent suitable biomarkers of subclinical endometritis, able to predict the risk of persistence of inflammation.

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