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Interactions between Energy Metabolism and Fertility in Human and Animal Models

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A special issue of International Journal of Molecular Sciences (ISSN 1422-0067). This special issue belongs to the section "Molecular Endocrinology and Metabolism".

Deadline for manuscript submissions: closed (31 December 2021) | Viewed by 24187

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Prof. Dr. Joëlle Dupont

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INRA UMR 85 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France
Interests: interaction metabolism and reproduction; fertility; ovary; adipose tissue; cellular signalling; human and animal models

Dr. Pascal Froment

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INRA UMR 85 Physiologie de la Reproduction et des Comportements, F-37380 Nouzilly, France

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Dear Colleagues,

The link between metabolism and reproduction has been well documented for several decades. Some evidence shows that variation of energy metabolism may improve or alter both male and female fertility in many species, including humans. Fertility is the result of many physiological processes, including gametogenesis, fecundation, embryo development and implantation, placentation, pregnancy, and parturition. All these steps involve numerous organs or tissues, such as the hypothalamo-pituitary–gonadal axis, uterus, and placenta that are energy-sensitive. Metabolic signals or energy sensors can be hormones (adipokines, insulin, etc.), nutrients (glucose, lipid, amino acids, essential minerals or vitamins), or neuropeptides that are now known to act directly or indirectly on the cells at different levels of the reproductive axis. They can transduce their signals through specific receptors and signaling pathways. In this Special Issue, we propose to discuss the role of these metabolic signals on the male and female fertility regulation in normal and pathological conditions in different species, including humans.

Prof. Joëlle Dupont
Dr. Pascal Froment
Guest Editors

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Keywords

Hypothalamo–pituitary–gonadal axis
Embryo development and pregnancy
Metabolites and neuropeptides
Hormones and signaling

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Research

18 pages, 3311 KiB

Open AccessArticle

Expression and Impact of Vaspin on In Vitro Oocyte Maturation through MAP3/1 and PRKAA1 Signalling Pathways

by Patrycja Kurowska, Ewa Mlyczyńska, Anthony Estienne, Alix Barbe, Iwona Rajska, Katarzyna Soból, Katarzyna Poniedziałek-Kempny, Joelle Dupont and Agnieszka Rak

Int. J. Mol. Sci. 2020, 21(24), 9342; https://doi.org/10.3390/ijms21249342 - 8 Dec 2020

Cited by 13 | Viewed by 2634

Abstract

Oocyte maturation is a critical stage in embryo production and female reproduction. The aims of this study were to determine: (i) the mRNA and protein expression of vaspin and its receptor 78-kDa glucose-regulated (GRP78) in porcine cumulus–oocyte complexes (COCs) by real-time PCR and Western blot analysis, respectively, and their localisation by immunofluorescence; and (ii) the effects of vaspin on in vitro oocyte maturation (IVM) and the involvement of mitogen ERK1/2 (MAP3/1)- and AMPKα (PRKAA1)-activated kinases in the studied processes. Porcine COCs were matured in vitro for 22 h or 44 h with vaspin at a dose of 1 ng/mL and nuclear maturation assessed by Hoechst 33342 or DAPI staining and the measurement of progesterone (P4) level in the maturation medium. We showed that vaspin and GRP78 protein expression increased in oocytes and cumulus cells after IVM. Moreover, vaspin enhanced significantly porcine oocyte IVM and P4 concentration, as well as MAP3/1 phosphorylation, while decreasing PRKAA1. Using pharmacological inhibitors of MAP3/1 (PD98059) and PRKAA1 (Compound C), we observed that the effect of vaspin was reversed to the control level by all studied parameters. In conclusion, vaspin, by improving in vitro oocyte maturation via MAP3/1 and PRKAA1 kinase pathways, can be a new factor to improve in vitro fertilisation protocols. Full article

(This article belongs to the Special Issue Interactions between Energy Metabolism and Fertility in Human and Animal Models)

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20 pages, 2865 KiB

Open AccessArticle

Profiling of Tryptophan Metabolic Pathways in the Rat Fetoplacental Unit during Gestation

by Cilia Abad, Rona Karahoda, Petr Kastner, Ramon Portillo, Hana Horackova, Radim Kucera, Petr Nachtigal and Frantisek Staud

Int. J. Mol. Sci. 2020, 21(20), 7578; https://doi.org/10.3390/ijms21207578 - 14 Oct 2020

Cited by 18 | Viewed by 4680

Abstract

Placental homeostasis of tryptophan is essential for fetal development and programming. The two main metabolic pathways (serotonin and kynurenine) produce bioactive metabolites with immunosuppressive, neurotoxic, or neuroprotective properties and their concentrations in the fetoplacental unit must be tightly regulated throughout gestation. Here, we investigated the expression/function of key enzymes/transporters involved in tryptophan pathways during mid-to-late gestation in rat placenta and fetal organs. Quantitative PCR and heatmap analysis revealed the differential expression of several genes involved in serotonin and kynurenine pathways. To identify the flux of substrates through these pathways, Droplet Digital PCR, western blot, and functional analyses were carried out for the rate-limiting enzymes and transporters. Our findings show that placental tryptophan metabolism to serotonin is crucial in mid-gestation, with a subsequent switch to fetal serotonin synthesis. Concurrently, at term, the close interplay between transporters and metabolizing enzymes of both placenta and fetal organs orchestrates serotonin homeostasis and prevents hyper/hypo-serotonemia. On the other hand, the placental production of kynurenine increases during pregnancy, with a low contribution of fetal organs throughout gestation. Any external insult to this tightly regulated harmony of transporters and enzymes within the fetoplacental unit may affect optimal in utero conditions and have a negative impact on fetal programming. Full article

(This article belongs to the Special Issue Interactions between Energy Metabolism and Fertility in Human and Animal Models)

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18 pages, 2532 KiB

Open AccessArticle

Flutamide Alters the Expression of Chemerin, Apelin, and Vaspin and Their Respective Receptors in the Testes of Adult Rats

by Malgorzata Brzoskwinia, Laura Pardyak, Agnieszka Rak, Alicja Kaminska, Anna Hejmej, Sylwia Marek, Malgorzata Kotula-Balak and Barbara Bilinska

Int. J. Mol. Sci. 2020, 21(12), 4439; https://doi.org/10.3390/ijms21124439 - 22 Jun 2020

Cited by 20 | Viewed by 4700

Abstract

Adipokines influence energy metabolism and have effects on male reproduction, including spermatogenesis and/or Sertoli cell maturation; however, the relationship between these active proteins and androgens in testicular cells is limited. Here, we studied the impact of short-term exposure to flutamide (an anti-androgen that blocks androgen receptors) on the expression of chemerin, apelin, vaspin and their receptors (CCRL2, CMKLR1, GPR1, APLNR, GRP78, respectively) in adult rat testes. Moreover, the levels of expression of lipid metabolism-modulating proteins (PLIN1, perilipin1; TSPO, translocator protein) and intercellular adherens junction proteins (nectin-2 and afadin) were determined in testicular cells. Plasma levels of adipokines, testosterone and cholesterol were also evaluated. Gene expression techniques used included the quantitative real-time polymerase chain reaction (qRT-PCR), Western blot (WB) and immunohistochemistry (IHC). The androgen-mediated effects observed post-flutamide treatment were found at the gonadal level as chemerin, apelin, and vaspin gene expression alterations at mRNA and protein levels were detected, whereas the cellular targets for these adipokines were recognised by localisation of respective receptors in testicular cells. Plasma concentrations of all adipokines were unchanged, whereas plasma cholesterol content and testosterone level increased after flutamide exposure. Differential distribution of adipokine receptors indicates potential para- or autocrine action of the adipokines within the rat testes. Additionally, changes in the expression of PLIN1 and TSPO, involved in the initial step of testosterone synthesis in Leydig cells, suggest that testicular cells represent a target of flutamide action. Increase in the gene expression of PLIN1 and TSPO and higher total plasma cholesterol content indicates enhanced availability of cholesterol in Leydig cells as a result of androgen-mediated effects of flutamide. Alterations in adherens junction protein expression in the testis confirm the flutamide efficacy in disruption of androgen signalling and presumably lead to impaired para- and autocrine communication, important for proper functioning of adipokines. Full article

(This article belongs to the Special Issue Interactions between Energy Metabolism and Fertility in Human and Animal Models)

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20 pages, 6984 KiB

Open AccessArticle

Mitochondrial Function in Modulating Human Granulosa Cell Steroidogenesis and Female Fertility

by Dilip Bhargava Sreerangaraja Urs, Wen-Han Wu, Katerina Komrskova, Pavla Postlerova, Yung-Feng Lin, Chii-Ruey Tzeng and Shu-Huei Kao

Int. J. Mol. Sci. 2020, 21(10), 3592; https://doi.org/10.3390/ijms21103592 - 19 May 2020

Cited by 105 | Viewed by 11511

Abstract

Ovarian follicle steroidogenesis associated with embryo quality results in a successful pregnancy. Each follicle consists of an oocyte surrounded by granulosa cells, which secrete several steroid and peptide hormones. Follicles harvested from women who conceived after assisted reproductive therapy (ART) had significantly higher estradiol levels in follicular fluids than the follicles from women who failed to conceive after ART. The higher follicular estradiol levels correlate well with successful fertilization following ART. Mitochondria are the central sites for steroid hormone biosynthesis. The first and rate-limiting step in the biosynthesis of steroid hormones occurs in the mitochondria of granulosa cells. In the present study, we hypothesized that the mitochondria in granulosa cells are critical for maintaining oocyte quality and fertility capacity. This study aims to clarify the relationship between mitochondrial function and granulosa cell steroidogenesis, and the relationship between hormone levels and fertility capacity. Sera, follicular fluids and granulosa cells were obtained from individuals undergoing IVF-ET treatment. The oocyte numbers, oocyte quality, fertilization rate, and pregnancy rate were also recorded. The patients who provided the granulosa cells were further classified into four groups: endometriosis, ovarian endometrioma, endometriosis without ovarian endometrioma, and polycystic ovary syndrome (PCOS); patients with other female factor infertility and male factor infertility were used as controls. We measured the levels of estradiol (E2) by radioimmunoassay. Concurrently, we analyzed the mitochondrial mass and membrane potential, and apoptosis by flow cytometry using nonyl acridine orange, TMRE, Annexin V-FITC and PI. Mitochondrial morphology was visualized by transfection with pLV-mitoDsRed. In addition, we assessed the protein levels of steroidogenic enzymes, steroidogenic acute regulatory protein (StAR) and 3β-hydroxysteroid dehydrogenase (3β-HSD) by Western blot. The results showed significantly decreased serum E2 and follicular E2 levels, and decreased IVF outcomes, in the patients with endometriosis. Reduced mitochondrial mass and decreased mitochondrial membrane potential were correlated with lower E2. Furthermore, a significant decrease in StAR and 3β-HSD was found in patients with ovarian endometrioma. The enzyme levels of StAR and 3β-HSD were highly correlated with E2 levels. Finally, elevated cumulus cell apoptosis was found in the patient group with ovarian endometrioma and PCOS. In conclusion, mitochondrial dysfunction of human granulosa cells may contribute to the decline of steroidogenesis, decreased fertilization rate, oocyte maturation rate, and oocyte quality, and it can ultimately jeopardize fertility. Full article

(This article belongs to the Special Issue Interactions between Energy Metabolism and Fertility in Human and Animal Models)

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