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Central and Local Modulators of Reproduction and Fertility: An Update 2.0

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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 January 2023) | Viewed by 29263

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Prof. Dr. Rosaria Meccariello

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Department of Movement and Wellness Sciences, Parthenope University of Naples, Via Medina 40, I-80133 Naples, Italy
Interests: endocannabinoid system; endocannabinoids–GnRH–steroids crosstalk; kisspeptins; reproduction; HPG axis; spermatogenesis; spermatozoa; endocrine disruptors; epigenetics
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Dear Colleagues,

Reproduction and fertility depend on the hypothalamus–pituitary–gonad (HPG) axis. The key actor in HPG axis activity is the hypothalamic gonadotropin-releasing hormone (GnRH), a decapeptide able to induce the discharge of pituitary gonadotropins (follicle-stimulating hormone (FSH) and luteinizing hormone (LH)), which in turn sustain the production of sex steroids by gonads, with successful gametogenesis as a result. In addition to intricate endocrine communication routes, paracrine and autocrine communications along the HPG axis also ensure successful gametogenesis. In this respect the list of centrally and peripherally produced modulators of reproduction is growing and deserves attention in order to preserve both reproduction and fertility through the formation of high-quality gametes. In fact, reproduction is highly sensitive to environmental factors such as diet, stress, or endocrine disruptors, among others, and the possibility of the epigenetic modulation of reproduction with transgenerational outcomes has recently been raised. To date, several modulators exert their activity within the hypothalamus, modulating the activity of GnRH-secreting neurons in response to exogenous and endogenous environmental “cues”; similarly, peripherally produced modulators directly affect gametogenesis with effects on reproduction and fertility. Despite experimental evidence, molecular and epigenetic regulatory mechanisms of HPG activity remain to be fully elucidated, hence the need to fill this gap in order to devise clinically effective treatment strategies.

This Special Issue aims at expanding the current knowledge on central and local modulators of reproduction and fertility in both physiological and pathological conditions, as well as on their possible therapeutic exploitation. Experimental studies in in vitro and in vivo models, review articles, and clinical studies are all welcome for consideration.

Dr. Rosaria Meccariello
Guest Editor

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Keywords

reproduction
fertility
HPG axis
testis
ovary
spermatogenesis
ovogenesis
gametes
GnRH
gonadotropins
sex steroids
kisspeptins
GnIH
metabolic sensors
leptin
endocannabinoids
autocrine/paracrine regulators
protein/peptide hormones
lipid mediators
epigenetics

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Published Papers (12 papers)

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Editorial

Jump to: Research, Review

5 pages, 211 KiB

Open AccessEditorial

Central and Local Modulators of Reproduction and Fertility: An Update

by Rosaria Meccariello

Int. J. Mol. Sci. 2022, 23(9), 5285; https://doi.org/10.3390/ijms23095285 - 9 May 2022

Cited by 3 | Viewed by 1896

Abstract

Infertility is currently one of the most important health troubles in industrialised countries after cardio-vascular diseases and cancer [...] Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

Research

Jump to: Editorial, Review

15 pages, 4741 KiB

Open AccessArticle

Endocannabinoid System Components of the Female Mouse Reproductive Tract Are Modulated during Reproductive Aging

by Gianna Rossi, Valentina Di Nisio, Alessandro Chiominto, Sandra Cecconi and Mauro Maccarrone

Int. J. Mol. Sci. 2023, 24(8), 7542; https://doi.org/10.3390/ijms24087542 - 19 Apr 2023

Cited by 4 | Viewed by 1787

Abstract

The endocannabinoid (eCB) system has gained ground as a key modulator of several female fertility-related processes, under physiological/pathological conditions. Nevertheless, its modulation during reproductive aging remains unclear. This study aimed to investigate the expression levels of the main receptors (cannabinoid receptor 1,CB₁; cannabinoid receptor 2, CB₂; G-protein coupled receptor, GPR55; and transient receptor potential vanilloid type 1 channel, TRPV1) and metabolic enzymes (N-acylphosphatidylethanolamine phospholipase D, NAPE-PLD; fatty acid amide hydrolase, FAAH; monoacylglycerol lipase, MAGL; and diacylglycerol lipase, DAGL-α and -β) of this system in the ovaries, oviducts, and uteri of mice at prepubertal, adult, late reproductive, and post-reproductive stages through quantitative ELISA and immunohistochemistry. The ELISA showed that among the receptors, TRPV1 had the highest expression and significantly increased during aging. Among the enzymes, NAPE-PLD, FAAH, and DAGL-β were the most expressed in these organs at all ages, and increased age-dependently. Immunohistochemistry revealed that, regardless of age, NAPE-PLD and FAAH were mainly found in the epithelial cells facing the lumen of the oviduct and uteri. Moreover, in ovaries, NAPE-PLD was predominant in the granulosa cells, while FAAH was sparse in the stromal compartment. Of note, the age-dependent increase in TRPV1 and DAGL-β could be indicative of increased inflammation, while that of NAPE-PLD and FAAH could suggest the need to tightly control the levels of the eCB anandamide at late reproductive age. These findings offer new insights into the role of the eCB system in female reproduction, with potential for therapeutic exploitation. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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16 pages, 5939 KiB

Open AccessArticle

Early Pregnancy Regulates Expression of IkappaB Family in Ovine Spleen and Lymph Nodes

by Shengya Fang, Chunjiang Cai, Ying Bai, Leying Zhang and Ling Yang

Int. J. Mol. Sci. 2023, 24(6), 5156; https://doi.org/10.3390/ijms24065156 - 8 Mar 2023

Cited by 1 | Viewed by 1694

Abstract

Early pregnancy modulates the maternal immune system, including the spleen and lymph nodes, which participate in maternal innate and adaptive immune responses. Methods: Ovine spleens and lymph nodes were sampled at day 16 of the estrous cycle, and at days 13, 16 and 25 of gestation, and qRT-PCR, Western blot and immunohistochemistry analysis were used to analyze the expression of the IκB family, including BCL-3, IκBα, IκBβ, IκBε, IKKγ, IκBNS and IκBζ. Early pregnancy induced expression of BCL-3, IκBα, IκBε, IKKγ and IκBζ, and expression of BCL-3, IκBβ and IκBNS peaked at day 16 of pregnancy in the spleen. However, early pregnancy suppressed the expression of BCL-3 and IκBNS, but stimulated the expression of IκBβ and IκBζ, and expression levels of IκBα, IκBβ, IκBε and IKKγ peaked in lymph nodes at days 13 and/or 16 of pregnancy. Early pregnancy changed the expression of the IκB family in the maternal spleen and lymph node in a tissue-specific manner, suggesting that the modulation of the IκB family may be involved in regulation of maternal functions of the spleen and lymph nodes, which are necessary for the establishment of maternal immune tolerance during early pregnancy in sheep. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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18 pages, 3823 KiB

Open AccessArticle

Human Chorionic Gonadotropin-Stimulated Interleukin-4-Induced-1 (IL4I1) Promotes Human Decidualization via Aryl Hydrocarbon Receptor

by Jia-Mei Luo, Tong-Tong Zhang, Yu-Ying He, Hui-Na Luo, Yu-Qi Hong and Zeng-Ming Yang

Int. J. Mol. Sci. 2023, 24(4), 3163; https://doi.org/10.3390/ijms24043163 - 5 Feb 2023

Cited by 7 | Viewed by 2340

Abstract

Decidualization is necessary for the successful establishment of early pregnancy in rodents and humans. Disturbed decidualization results in recurrent implantation failure, recurrent spontaneous abortion, and preeclampsia. Tryptophan (Trp), one of the essential amino acids in humans, has a positive effect on mammalian pregnancy. Interleukin 4-induced gene 1 (IL4I1) is a recently identified enzyme that can metabolize L-Trp to activate aryl hydrocarbon receptor (AHR). Although IDO1-catalyzed kynurenine (Kyn) from Trp has been shown to enhance human in vitro decidualization via activating AHR, whether IL4I1-catalyzed metabolites of Trp are involved in human decidualization is still unknown. In our study, human chorionic gonadotropin stimulates IL4I1 expression and secretion from human endometrial epithelial cells through ornithine decarboxylase-induced putrescine production. Either IL4I1-catalyzed indole-3-pyruvic acid (I3P) or its metabolite indole-3-aldehyde (I3A) from Trp is able to induce human in vitro decidualization by activating AHR. As a target gene of AHR, Epiregulin induced by I3P and I3A promotes human in vitro decidualization. Our study indicates that IL4I1-catalyzed metabolites from Trp can enhance human in vitro decidualization through AHR-Epiregulin pathway. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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18 pages, 4062 KiB

Open AccessArticle

Low-Dose Sodium Salicylate Promotes Ovulation by Regulating Steroids via CYP17A1

by Tao Li, Xuehua Ren, Tianjiao Li, Lian Yu, Mingming Teng, Yi Zheng and Anmin Lei

Int. J. Mol. Sci. 2023, 24(3), 2579; https://doi.org/10.3390/ijms24032579 - 30 Jan 2023

Cited by 3 | Viewed by 2312

Abstract

To meet the current demand of assisted reproduction and animal breeding via superovulation and reduce the impact of hormone drugs, it is necessary to develop new superovulation drugs. This study examined the role of inflammation and steroids in ovulation. Sodium salicylate can regulate inflammation and steroids. However, the effect of sodium salicylate on ovulation has not been studied. In this study, mice were intraperitoneally injected with different concentrations of sodium salicylate for four consecutive days. The effects of sodium salicylate on oocyte quality and on the number of ovulations were examined, and these effects were compared with those of pregnant horse serum gonadotropin (PMSG)/follicle-stimulating hormone (FSH) treatment. We found that low-dose sodium salicylate increased the levels of ovulation hormones and inflammation by promoting the expression of CYP17A1. Sodium salicylate had the same effect as the commonly used superovulation drug PMSG/FSH and reduced the histone methylation level. Sodium salicylate can promote ovulation in mice and Awang sheep. It can greatly decrease the use of hormone drugs, reduce breeding costs and physical impacts, and can thus be used for livestock breeding. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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18 pages, 4269 KiB

Open AccessArticle

Effect of Disulfiram on the Reproductive Capacity of Female Mice

by Mingming Teng, Yuan Luo, Chan Wang and Anmin Lei

Int. J. Mol. Sci. 2023, 24(3), 2371; https://doi.org/10.3390/ijms24032371 - 25 Jan 2023

Cited by 2 | Viewed by 4738

Abstract

In the process of assisted reproduction, the high-oxygen in vitro environment can easily cause oxidative damage to oocytes. Disulfiram (DSF) can play an anti-oxidant or pro-oxidant role in different cells, and the effect of DSF on oocytes remains unclear. Moreover, it remains unclear whether the use of DSF in the early stages of pregnancy has a negative impact on the fetus. In this study, we found that DSF increased serum FSH levels and increased the ovulation rate in mice. Moreover, DSF enhanced the antioxidant capacity of oocytes and contributed to the success rate of in vitro fertilization. Moreover, the use of DSF in early pregnancy in mice increased the uterine horn volume and the degree of vascularization, which contributed to a successful pregnancy. In addition, it was found that DSF regulated the mRNA expression of angiogenesis-related genes (VEGF), follicular development-related genes (C1QTNF3, mTOR and PI3K), ovulation-related genes (MAPK1, MAPK3 and p38 MAPK) and antioxidant-related genes (GPX4 and CAT). These results indicate that DSF is helpful for increasing the antioxidant capacity of oocytes and the ovulation rate. In early pregnancy in mice, DSF promotes pregnancy by increasing the degree and volume of uterine vascularization. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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21 pages, 5110 KiB

Open AccessArticle

Primary Cilia Restrain PI3K-AKT Signaling to Orchestrate Human Decidualization

by Bo Li, Ya-Ping Yan, Chen Liang, Yu-Ying He, Ying Wang, Meng-Yuan Li, Si-Ting Chen, Yue Li, Ai-Xia Liu, Gui-Jun Yan and Zeng-Ming Yang

Int. J. Mol. Sci. 2022, 23(24), 15573; https://doi.org/10.3390/ijms232415573 - 8 Dec 2022

Cited by 10 | Viewed by 2496

Abstract

Endometrial decidualization plays a pivotal role during early pregnancy. Compromised decidualization has been tightly associated with recurrent implantation failure (RIF). Primary cilium is an antenna-like sensory organelle and acts as a signaling nexus to mediate Hh, Wnt, TGFβ, BMP, FGF, and Notch signaling. However, whether primary cilium is involved in human decidualization is still unknown. In this study, we found that primary cilia are present in human endometrial stromal cells. The ciliogenesis and cilia length are increased by progesterone during in vitro and in vivo decidualization. Primary cilia are abnormal in the endometrium of RIF patients. Based on data from both assembly and disassembly of primary cilia, it has been determined that primary cilium is essential to human decidualization. Trichoplein (TCHP)-Aurora A signaling mediates cilia disassembly during human in vitro decidualization. Mechanistically, primary cilium modulates human decidualization through PTEN-PI3K-AKT-FOXO1 signaling. Our study highlights primary cilium as a novel decidualization-related signaling pathway. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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15 pages, 1520 KiB

Open AccessArticle

Short-Chain Fatty Acids Modulate Sperm Migration through Olfactory Receptor 51E2 Activity

by Emanuela Teveroni, Fiorella Di Nicuolo, Edoardo Vergani, Carmine Bruno, Giuseppe Maulucci, Giada Bianchetti, Anna Laura Astorri, Giuseppe Grande, Jacopo Gervasoni, Lavinia Santucci, Marco De Spirito, Andrea Urbani, Alfredo Pontecorvi, Francesca Mancini and Domenico Milardi

Int. J. Mol. Sci. 2022, 23(21), 12726; https://doi.org/10.3390/ijms232112726 - 22 Oct 2022

Cited by 6 | Viewed by 1854

Abstract

The non-orthotopic expression of olfactory receptors (ORs) includes the male reproductive system, and in particular spermatozoa; their active ligands could be essential to sperm chemotaxis and chemical sperm–oocyte communication. OR51E2 expression has been previously reported on sperm cells’ surface. It has been demonstrated in different cellular models that olfactory receptor 51E2 (OR51E2) binds volatile short-chain fatty acids (SCFAs) as specific ligands. In the present research, we make use of Western blot, confocal microscopy colocalization analysis, and the calcium-release assay to demonstrate the activation of sperm cells through OR51E2 upon SCFAs stimulus. Moreover, we perform a novel modified swim-up assay to study the involvement of OR51E2/SCFAs in sperm migration. Taking advantage of computer-assisted sperm analysis (CASA system), we determine the kinematics parameters of sperm cells migrating towards SCFAs-enriched medium, revealing that these ligands are able to promote a more linear sperm-cell orientation. Finally, we obtain SCFAs by mass spectrometry in cervico-vaginal mucus and show for the first time that a direct incubation between cervical mucus and sperm cells could promote their activation. This study can shed light on the possible function of chemosensory receptors in successful reproduction activity, laying the foundation for the development of new strategies for the treatment of infertile individuals. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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16 pages, 1594 KiB

Open AccessArticle

Multigenerational Exposure to Uranium Changes Sperm Metabolome in Rats

by Stéphane Grison, Audrey Legendre, Ljubica Svilar, Christelle Elie, Dimitri Kereselidze, Céline Gloaguen, Philippe Lestaevel, Jean-Charles Martin and Maâmar Souidi

Int. J. Mol. Sci. 2022, 23(15), 8349; https://doi.org/10.3390/ijms23158349 - 28 Jul 2022

Cited by 3 | Viewed by 1763

Abstract

Male infertility is a major public health issue that can be induced by a host of lifestyle risk factors such as environment, nutrition, smoking, stress, and endocrine disruptors. Regarding the human population exposed to uranium, it is necessary to explore these effects on male reproduction in multigenerational studies. The sensitivity of mass spectrometry (MS)-based methods has already proved to be extremely useful in metabolite identification in rats exposed to low doses of uranium, but also in human sperm. We applied this method to rat sperm over three generations (F0, F1 and F2) with multigenerational uranium exposure. Our results show a significant content of uranium in generation F0, and a reduction in the pregnancy rate only in generation F1. Based on principal component analysis (PCA), we observed discriminant profiles between generations. The partial least squares discriminant analysis (PLS-DA) of the 48 annotated variables confirmed that parental exposure of generation F0 (during both the preconceptional and prenatal periods) can have metabolic effects on spermatozoa for the next two generations. Metabolomics applied to epididymal spermatozoa is a novel approach to detecting the multigenerational effects of uranium in an experimental model, but could be also recommended to identify potential biomarkers evaluating the impact of uranium on sperm in exposed infertile men. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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21 pages, 5809 KiB

Open AccessArticle

Central Kisspeptin Does Not Affect ERK1/2 or p38 Phosphorylation in Oxytocin Neurons of Late-Pregnant Rats

by Mehwish Abbasi, Rachael A. Augustine, Karl J. Iremonger and Colin H. Brown

Int. J. Mol. Sci. 2022, 23(14), 7729; https://doi.org/10.3390/ijms23147729 - 13 Jul 2022

Cited by 2 | Viewed by 1890

Abstract

Oxytocin is secreted by hypothalamic supraoptic nucleus (SON) and paraventricular nucleus (PVN) oxytocin neurons to induce uterine contractions during parturition. Increased activation of oxytocin neurons at parturition involves a network of afferent inputs that increase oxytocin neuron excitability. Kisspeptin fibre density increases around oxytocin neurons during pregnancy, and central kisspeptin administration excites oxytocin neurons only in late pregnancy. Kisspeptin signals via extracellular regulated kinase 1/2 (ERK1/2) and p38. Therefore, to determine whether kisspeptin excites oxytocin neurons via ERK1/2-p38 signalling in late-pregnant rats, we performed immunohistochemistry for phosphorylated ERK1/2 (pERK1/2) and phosphorylated p38 (p-p38) in oxytocin neurons of non-pregnant and late-pregnant rats. Intracerebroventricular (ICV) kisspeptin administration (2 µg) did not affect pERK1/2 or p-p38 expression in SON and PVN oxytocin neurons of non-pregnant or late-pregnant rats. Furthermore, ICV kisspeptin did not affect pERK1/2 or p-p38 expression in brain areas with major projections to the SON and PVN: the nucleus tractus solitarius, rostral ventrolateral medulla, locus coeruleus, dorsal raphe nucleus, organum vasculosum of the lamina terminalis, median preoptic nucleus, subfornical organ, anteroventral periventricular nucleus, periventricular nucleus and arcuate nucleus. Hence, kisspeptin-induced excitation of oxytocin neurons in late pregnancy does not appear to involve ERK1/2 or p38 activation in oxytocin neurons or their afferent inputs. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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Review

Jump to: Editorial, Research

12 pages, 1135 KiB

Open AccessReview

Neurotensin and Its Involvement in Reproductive Functions: An Exhaustive Review of the Literature

by Pauline Arbogast, Guillaume Gauchotte, Romane Mougel, Olivier Morel, Ahmed Ziyyat and Mikaël Agopiantz

Int. J. Mol. Sci. 2023, 24(5), 4594; https://doi.org/10.3390/ijms24054594 - 27 Feb 2023

Cited by 6 | Viewed by 2531

Abstract

Neurotensin (NTS) is a peptide discovered in 1973, which has been studied in many fields and mainly in oncology for its action in tumor growth and proliferation. In this review of the literature, we wanted to focus on its involvement in reproductive functions. NTS participates in an autocrine manner in the mechanisms of ovulation via NTS receptor 3 (NTSR3), present in granulosa cells. Spermatozoa express only its receptors, whereas in the female reproductive system (endometrial and tube epithelia and granulosa cells), we find both NTS secretion and the expression of its receptors. It consistently enhances the acrosome reaction of spermatozoa in mammals in a paracrine manner via its interaction with NTSR1 and NTSR2. Furthermore, previous results on embryonic quality and development are discordant. NTS appears to be involved in the key stages of fertilization and could improve the results of in vitro fertilization, especially through its effect on the acrosomal reaction. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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22 pages, 814 KiB

Open AccessReview

The Clinical Application of Growth Hormone and Its Biological and Molecular Mechanisms in Assisted Reproduction

by Peipei Pan and Xuefeng Huang

Int. J. Mol. Sci. 2022, 23(18), 10768; https://doi.org/10.3390/ijms231810768 - 15 Sep 2022

Cited by 7 | Viewed by 2867

Abstract

Growth hormone (GH) has been used as a co-gonadotrophin in assisted reproduction, particularly in poor ovarian responders. The application of GH has been alleged to activate primordial follicles and improve oocyte quality, embryo quality, and steroidogenesis. However, the effects of GH on the live birth rate among women is controversial. Additionally, although the basic biological mechanisms that lead to the above clinical differences have been investigated, they are not yet well understood. The actions of GH are mediated by GH receptors (GHRs) or insulin-like growth factors (IGFs). GH regulates the vital signal transduction pathways that are involved in primordial follicular activation, steroidogenesis, and oocyte maturation. However, the therapeutic windows and duration of GH administration during assisted reproductive technology require further investigation. The review aimed to clarify the role of GH in human fertility from a molecular and biological point of view to provide evidence for proper GH administration. Full article

(This article belongs to the Special Issue Central and Local Modulators of Reproduction and Fertility: An Update 2.0)

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