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María Belén Poretti Instituto de Investigaciones en Ciencias de la Salud (INICSA, CONICET- UNC), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Argentina
Functional Pharmacology, Department of Neuroscience, Uppsala University, Uppsala, Sweden

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Santiago Bianconi Instituto de Investigaciones en Ciencias de la Salud (INICSA, CONICET- UNC), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Argentina
Functional Pharmacology, Department of Neuroscience, Uppsala University, Uppsala, Sweden

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Eugenia Luque Instituto de Investigaciones en Ciencias de la Salud (INICSA, CONICET- UNC), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Argentina

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Ana Carolina Martini Instituto de Investigaciones en Ciencias de la Salud (INICSA, CONICET- UNC), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Argentina

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Laura Vincenti Instituto de Investigaciones en Ciencias de la Salud (INICSA, CONICET- UNC), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Argentina

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Veronica Cantarelli Instituto de Investigaciones en Ciencias de la Salud (INICSA, CONICET- UNC), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Argentina

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Pedro Torres Instituto de Investigaciones en Ciencias de la Salud (INICSA, CONICET- UNC), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Argentina

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Marina Ponzio Instituto de Investigaciones en Ciencias de la Salud (INICSA, CONICET- UNC), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Argentina

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Helgi B Schiöth Functional Pharmacology, Department of Neuroscience, Uppsala University, Uppsala, Sweden

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Valeria Paola Carlini Instituto de Investigaciones en Ciencias de la Salud (INICSA, CONICET- UNC), CONICET and Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Argentina
Functional Pharmacology, Department of Neuroscience, Uppsala University, Uppsala, Sweden

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In brief

Ghrelin signals to the hypothalamus inhibit reproduction during times of food scarcity. In this study, we demonstrate that ghrelin impairs sperm quality in male mice.

Abstract

Ghrelin (GHRL) is an orexigenic peptide that has been investigated as one of the signals responsible for the reproductive performance of mammals under fluctuating metabolic conditions. Central GHRL administration impairs spermatogenesis in mice by regulating the hypothalamic–pituitary–gonadal axis function. In the present study, the hypothalamus role as a mediator of GHRL effects on sperm fertilizing capacity and male sexual behavior was evaluated. After 42 days of hypothalamic GHRL infusion or artificial cerebrospinal fluid, in vitro and in vivo sperm fertilizing capacity, testicular α-tubulin, speriolin gene expression and spermatic α-tubulin protein were evaluated. Hypothalamic expression of genes Kiss1, Gpr54 and Gnrh was also studied. The second group of animals was infused with one time only GHRL or artificial cerebrospinal fluid into the hypothalamus to evaluate the effects on sexual behavior. Results demonstrated that chronic GHRL administration to male mice significantly increased the percentages of pre-implantation embryo loss and the number of post-implantation embryo loss. In relation to the gene expression, our results show a relative decrease of Kiss1, Gpr54 and Spatc1. Although no significant differences were observed in the quantitative expression of α-tubulin protein, qualitative changes in its expression pattern were observed. In addition, a dual effect on sexual behavior was observed: 40% of the treated animals showed a significant reduction in the number of mounts and intromissions, while a 60% showed a significant decrease in ejaculation latency vs control animals. In conclusion, our results provide evidence that central GHRL administration possibly induces failure in embryo development and/or implantation in the females mated with treated males, possibly because of a negative effect in the α-tubulin pattern.

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María Belén Poretti INICSA, Facultad de Ciencias Médicas (CONICET-FCM), Instituto de Fisiología, Córdoba, Argentina
Department of Neuroscience, Functional Pharmacology, Uppsala University, Uppsala, Sweden

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Camila Frautschi Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Cátedra de Fisiología Humana, Córdoba, Argentina

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Eugenia Luque INICSA, Facultad de Ciencias Médicas (CONICET-FCM), Instituto de Fisiología, Córdoba, Argentina

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Santiago Bianconi Department of Neuroscience, Functional Pharmacology, Uppsala University, Uppsala, Sweden
Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Cátedra de Fisiología Humana, Córdoba, Argentina

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Ana Carolina Martini INICSA, Facultad de Ciencias Médicas (CONICET-FCM), Instituto de Fisiología, Córdoba, Argentina

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Graciela Stutz Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Cátedra de Fisiología Humana, Córdoba, Argentina

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Laura Vincenti Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Cátedra de Fisiología Humana, Córdoba, Argentina

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Maria Emilia Santillán Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Cátedra de Fisiología Humana, Córdoba, Argentina

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Marina Ponzio INICSA, Facultad de Ciencias Médicas (CONICET-FCM), Instituto de Fisiología, Córdoba, Argentina

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Helgi B Schiöth Department of Neuroscience, Functional Pharmacology, Uppsala University, Uppsala, Sweden

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Marta Fiol de Cuneo Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Cátedra de Fisiología Humana, Córdoba, Argentina

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Valeria Paola Carlini INICSA, Facultad de Ciencias Médicas (CONICET-FCM), Instituto de Fisiología, Córdoba, Argentina
Department of Neuroscience, Functional Pharmacology, Uppsala University, Uppsala, Sweden

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It has been demonstrated that food intake and reproductive physiology are both simultaneously modulated to optimize reproductive success under fluctuating metabolic conditions. Ghrelin (GHRL) is an orexigenic peptide identified as the endogenous ligand of the growth hormone secretagogue receptor that is being investigated for its potential role on reproduction. Considering that data available so far are still limited and characterization of GHRL action mechanism on the reproductive system has not been fully elucidated, we studied the participation of hypothalamus in GHRL effects on sperm functional activity, plasma levels of gonadotropins and histological morphology in mice testes after hypothalamic infusion of 0.3 or 3.0 nmol/day GHRL or artificial cerebrospinal fluid (ACSF) at different treatment periods. We found that GHRL 3.0 nmol/day administration for 42 days significantly reduced sperm concentration (GHRL 3.0 nmol/day = 14.05 ± 2.44 × 106/mL vs ACSF = 20.33 ± 1.35 × 106/mL, P < 0.05) and motility (GHRL 3.0 nmol/day = 59.40 ± 4.20% vs ACSF = 75.80 ± 1.40%, P < 0.05). In addition, histological studies showed a significant decrease percentage of spermatogonia (GHRL 3.0 nmol/day = 6.76 ± 0.68% vs ACSF = 9.56 ± 0.41%, P < 0.05) and sperm (GHRL 3.0 nmol/day = 24.24 ± 1.92% vs ACSF = 31.20 ± 3.06%, P < 0.05). These results were associated with a significant reduction in luteinizing hormone and testosterone plasma levels (P < 0.05). As GHRL is an orexigenic peptide, body weight and food intake were measured. Results showed that GHRL increases both parameters; however, the effect did not last beyond the first week of treatment. Results presented in this work confirm that central GHRL administration impairs spermatogenesis and suggest that this effect is mediated by inhibition of hypothalamic–pituitary–gonadal axis.

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Eugenia Mercedes Luque Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina

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Pedro Javier Torres Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina

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Nicolás de Loredo Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina

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Laura María Vincenti Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina

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Graciela Stutz Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina

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María Emilia Santillán Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina

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Rubén Daniel Ruiz Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina

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Marta Fiol de Cuneo Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina

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Ana Carolina Martini Facultad de Ciencias Médicas, Instituto de Fisiología, Universidad Nacional de Córdoba, Santa Rosa 1085, X5000ESU Córdoba, Argentina

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In order to clarify the physiological role of ghrelin in gestation, we evaluated the effects of administration of exogenous ghrelin (2 or 4 nmol/animal per day) or its antagonist (6 nmol/animal per day of (d-Lys3)GHRP6) on fertilization, early embryo development, and implantation periods in mice. Three experiments were performed, treating female mice with ghrelin or its antagonist: i) starting from 1 week before copulation to 12 h after copulation, mice were killed at day 18 of gestation; ii) since ovulation induction until 80 h later, when we retrieved the embryos from oviducts/uterus, and iii) starting from days 3 to 7 of gestation (peri-implantation), mice were killed at day 18. In experiments 1 and 3, the antagonist and/or the highest dose of ghrelin significantly increased the percentage of atrophied fetuses and that of females exhibiting this finding or a higher amount of corpora lutea compared with fetuses (nCL/nF) (experiment 3: higher nCL/nF-atrophied fetuses: ghrelin 4, 71.4–71.4% and antagonist, 75.0–62.5% vs ghrelin 2, 46.2−15.4% and control, 10–0.0%; n=7–13 females/group; P<0.01). In experiment 2, the antagonist diminished the fertilization rate, and both, ghrelin and the antagonist, delayed embryo development (blastocysts: ghrelin 2, 62.5%; ghrelin 4, 50.6%; and antagonist, 61.0% vs control 78.4%; n=82–102 embryos/treatment; P<0.0001). In experiment 3, additionally, ghrelin (4 nmol/day) and the antagonist significantly diminished the weight gain of fetuses and dams during pregnancy. Our results indicate that not only hyperghrelinemia but also the inhibition of the endogenous ghrelin effects exerts negative effects on the fertilization, implantation, and embryo/fetal development periods, supporting the hypothesis that ghrelin (in ‘adequate’ concentrations) has a physiological role in early gestational events.

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