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Mammalian Gametes: Molecular Traits Shaping Their Form and Fate 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 (28 February 2023) | Viewed by 28613

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Dr. Pilar Coy

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Departamento de Fisiología, Facultad de Veterinaria, Universidad de Murcia, 30071 Murcia, Spain
Interests: mammalian gametes; reproduction; fertilization; embryo development; epigenetics; oviduct; reproductive fluids
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Special Issue Information

Dear Colleagues,

From their ultrastructure to their epigenetic reprogramming, from their molecular composition to their response to stress or to environmental conditions, gametes are the most amazing cells in an organism. Despite their variety of forms and sizes, they are designed to reach a common fate—fertilization (or maybe not?). The molecular mechanisms behind this role seem to be similar, but occasionally, interspecific differences appear, surprising the scientific community. Today, many secrets remain undiscovered, while, in parallel, the human species is inexorably heading towards a steady decline in fertility rates. Thus, it is more necessary than ever continue researching about the physiology and pathology of gametes; the causes of their genetic and epigenetic alterations; and the methods for diagnosing, preventing, and treating all of the disorders affecting these cells.

Tentative topics:

Is the fertilising sperm different from its partners? Can ultrastructural studies distinguish one each other? Are there molecular traits that can be used as biomarkers?
Are all oocytes designed to be fertilised or are some of them designed to sacrifice themselves for their partners? Can we distinguish one from the other?
How different are sperm DNA methylation patterns between mammalian species? What is the biological meaning of such differences?
How different are oocyte DNA methylation patterns between mammalian species? Which is the biological meaning of such differences?
Oocyte secreted factors, oocyte proteomes, and oocytes mRNA from GV to Met II. How similar are they between species?
Sperm and oocyte response to stress.
Sperm response to in vivo vs. in vitro conditions? Do we really know something about physiological capacitation?
Oocyte adaptation to follicular and oviductal environments.
Sperm and oocyte morphometrical traits: what can we learn from the studies in the different mammals?

Dr. Pilar Coy
Guest Editor

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Keywords

mammalian gametes
reproduction
fertilization
embryo development
epigenetics
oviduct
reproductive fluids

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Published Papers (7 papers)

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Research

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17 pages, 3331 KiB

Open AccessArticle

Transcriptomics Reveal Molecular Differences in Equine Oocytes Vitrified before and after In Vitro Maturation

by Daniel Angel-Velez, Tim Meese, Mohamed Hedia, Andrea Fernandez-Montoro, Tine De Coster, Osvaldo Bogado Pascottini, Filip Van Nieuwerburgh, Jan Govaere, Ann Van Soom, Krishna Pavani and Katrien Smits

Int. J. Mol. Sci. 2023, 24(8), 6915; https://doi.org/10.3390/ijms24086915 - 7 Apr 2023

Cited by 4 | Viewed by 2685

Abstract

In the last decade, in vitro embryo production in horses has become an established clinical practice, but blastocyst rates from vitrified equine oocytes remain low. Cryopreservation impairs the oocyte developmental potential, which may be reflected in the messenger RNA (mRNA) profile. Therefore, this study aimed to compare the transcriptome profiles of metaphase II equine oocytes vitrified before and after in vitro maturation. To do so, three groups were analyzed with RNA sequencing: (1) fresh in vitro matured oocytes as a control (FR), (2) oocytes vitrified after in vitro maturation (VMAT), and (3) oocytes vitrified immature, warmed, and in vitro matured (VIM). In comparison with fresh oocytes, VIM resulted in 46 differentially expressed (DE) genes (14 upregulated and 32 downregulated), while VMAT showed 36 DE genes (18 in each category). A comparison of VIM vs. VMAT resulted in 44 DE genes (20 upregulated and 24 downregulated). Pathway analyses highlighted cytoskeleton, spindle formation, and calcium and cation ion transport and homeostasis as the main affected pathways in vitrified oocytes. The vitrification of in vitro matured oocytes presented subtle advantages in terms of the mRNA profile over the vitrification of immature oocytes. Therefore, this study provides a new perspective for understanding the impact of vitrification on equine oocytes and can be the basis for further improvements in the efficiency of equine oocyte vitrification. Full article

(This article belongs to the Special Issue Mammalian Gametes: Molecular Traits Shaping Their Form and Fate 2.0)

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17 pages, 2915 KiB

Open AccessArticle

Effects of Follicle-Stimulating Hormone on Human Sperm Motility In Vitro

by Rossella Cannarella, Francesca Mancuso, Nunziata Barone, Iva Arato, Cinzia Lilli, Catia Bellucci, Marco Musmeci, Giovanni Luca, Sandro La Vignera, Rosita A. Condorelli and Aldo E. Calogero

Int. J. Mol. Sci. 2023, 24(7), 6536; https://doi.org/10.3390/ijms24076536 - 31 Mar 2023

Cited by 1 | Viewed by 1774

Abstract

To evaluate whether the follicle-stimulating hormone (FSH) receptor (FSHR) is expressed in human spermatozoa and the effects of FSH incubation on sperm function. Twenty-four Caucasian men were recruited. Thirteen patients had asthenozoospermia, and the remaining 11 had normal sperm parameters (controls). After confirming FSHR expression, spermatozoa from patients and controls were incubated with increasing concentrations of human purified FSH (hpFSH) to reassess FSHR expression and localization and to evaluate progressive and total sperm motility, the mitochondrial membrane potential, and protein kinase B (AKT) 473 and 308 phosphorylation. FSHR is expressed in the post-acrosomal segment, neck, midpiece, and tail of human spermatozoa. Its localization does not differ between patients and controls. Incubation with hpFSH at a concentration of 30 mIU/mL appeared to increase FSHR expression mainly in patients. Incubation of human spermatozoa with hpFSH overall resulted in an overall deterioration of both progressive and total motility in patients and controls and worse mitochondrial function only in controls. Finally, incubation with FSH increased AKT⁴⁷³/tubulin phosphorylation to a greater extent than AKT³⁰⁸. FSHR is expressed in the post-acrosomal region, neck, midpiece, and tail of human spermatozoa. Contrary to a previous study, we report a negative effect of FSH on sperm motility and mitochondrial function. FSH also activates the AKT⁴⁷³ signaling pathway. Full article

(This article belongs to the Special Issue Mammalian Gametes: Molecular Traits Shaping Their Form and Fate 2.0)

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19 pages, 5821 KiB

Open AccessArticle

Effect of Superovulation Treatment on Oocyte’s DNA Methylation

by Jordana S. Lopes, Elena Ivanova, Salvador Ruiz, Simon Andrews, Gavin Kelsey and Pilar Coy

Int. J. Mol. Sci. 2022, 23(24), 16158; https://doi.org/10.3390/ijms232416158 - 18 Dec 2022

Cited by 5 | Viewed by 2652

Abstract

Controlled ovarian stimulation is a necessary step in some assisted reproductive procedures allowing a higher collection of female gametes. However, consequences of this stimulation for the gamete or the offspring have been shown in several mammals. Most studies used comparisons between oocytes from different donors, which may contribute to different responses. In this work, we use the bovine model in which each animal serves as its own control. DNA methylation profiles were obtained by single-cell whole-genome bisulfite sequencing of oocytes from pre-ovulatory unstimulated follicles compared to oocytes from stimulated follicles. Results show that the global percentage of methylation was similar between groups, but the percentage of methylation was lower for non-stimulated oocytes in the imprinted genes APEG3, MEG3, and MEG9 and higher in TSSC4 when compared to stimulated oocytes. Differences were also found in CGI of imprinted genes: higher methylation was found among non-stimulated oocytes in MEST (PEG1), IGF2R, GNAS (SCG6), KvDMR1 ICR UMD, and IGF2. In another region around IGF2, the methylation percentage was lower for non-stimulated oocytes when compared to stimulated oocytes. Data drawn from this study might help to understand the molecular reasons for the appearance of certain syndromes in assisted reproductive technologies-derived offspring. Full article

(This article belongs to the Special Issue Mammalian Gametes: Molecular Traits Shaping Their Form and Fate 2.0)

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15 pages, 1824 KiB

Open AccessArticle

Fatty Acids and Metabolomic Composition of Follicular Fluid Collected from Environments Associated with Good and Poor Oocyte Competence in Goats

by Dolors Izquierdo, Montserrat Roura, Míriam Pérez-Trujillo, Sandra Soto-Heras and María-Teresa Paramio

Int. J. Mol. Sci. 2022, 23(8), 4141; https://doi.org/10.3390/ijms23084141 - 8 Apr 2022

Cited by 7 | Viewed by 2195

Abstract

In goats, embryo oocyte competence is affected by follicle size regardless the age of the females. In previous studies we have found differences in blastocyst development between oocytes coming of small (<3 mm) and large follicles (>3 mm) in prepubertal (1–2 months-old) goats. Oocyte competence and Follicular Fluid (FF) composition changes throughout follicle growth. The aim of this study was to analyze Fatty Acids (FAs) composition and metabolomic profiles of FF recovered from small and large follicles of prepubertal goats and follicles of adult goats. FAs were analyzed by chromatography and metabolites by 1H-Nuclear Magnetic Resonance (1H-NMR) Spectrometry. The results showed important differences between adult and prepubertal follicles: (a) the presence of α,β-glucose in adult and no detection in prepubertal; (b) lactate, -N-(CH3)3 groups and inositol were higher in prepubertal (c) the percentage of Linolenic Acid, Total Saturated Fatty Acids and n-3 PUFAs were higher in adults; and (d) the percentage of Linoleic Acid, total MUFAs, PUFAs, n-6 PUFAs and n-6 PUFAs: n-3 PUFAs ratio were higher in prepubertal goats. Not significant differences were found in follicle size of prepubertal goats, despite the differences in oocyte competence for in vitro embryo production. Full article

(This article belongs to the Special Issue Mammalian Gametes: Molecular Traits Shaping Their Form and Fate 2.0)

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17 pages, 12397 KiB

Open AccessArticle

Evaluation of Controlled Ovarian Stimulation Protocols in Patients with Normal and Low Ovarian Reserve: Analyses of miRNAs and Selected Target Genes Involved in the Proliferation of Human Cumulus Cells and Oocyte Quality

by Giulia Russo, Valentina Notarstefano, Nina Montik, Giorgia Gioacchini, Elisabetta Giorgini, Anna Rita Polidori, Fulvia Antonia Candela, Andrea Ciavattini, Maurizio Cignitti and Oliana Carnevali

Int. J. Mol. Sci. 2022, 23(3), 1713; https://doi.org/10.3390/ijms23031713 - 2 Feb 2022

Cited by 2 | Viewed by 3964

Abstract

The oocyte and the surrounding cumulus cells (CCs) are deeply linked by a complex bidirectional cross-talk. In this light, the molecular analysis of the CCs is nowadays considered to be precious in providing information on oocyte quality. It is now clear that miRNAs play a key role in several ovarian functions, such as folliculogenesis, steroidogenesis, and ovulation. Thus, in this study, specific miRNAs, together with their target genes, were selected and investigated in CCs to assess the response of patients with normal (NR) and low (LR) ovarian reserve to two different controlled ovarian stimulation (COS) protocols, based on rFSH and hMG. Moreover, a Fourier transform infrared microspectroscopy (FTIRM) analysis was performed to evaluate DNA conformational changes in CCs and to relate them with the two COS protocols. The results evidenced a modulation of the expression of miRNAs and related target genes involved in CCs’ proliferation, in vasculogenesis, angiogenesis, genomic integrity, and oocyte quality, with different effects according to the ovarian reserve of patients. Moreover, the COS protocols determined differences in DNA conformation and the methylation state. In particular, the results clearly showed that treatment with rFSH is the most appropriate in NR patients with normal ovarian reserve, while treatment with hMG appears to be the most suitable in LR patients with low ovarian reserve. Full article

(This article belongs to the Special Issue Mammalian Gametes: Molecular Traits Shaping Their Form and Fate 2.0)

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11 pages, 958 KiB

Open AccessArticle

Next Generation Sequencing Detects Premeiotic Errors in Human Oocytes

by Harita Ghevaria, Sioban SenGupta, Roy Naja, Rabi Odia, Holly Exeter, Paul Serhal, Xavier Viñals Gonzalez, Xuhui Sun and Joy Delhanty

Int. J. Mol. Sci. 2022, 23(2), 665; https://doi.org/10.3390/ijms23020665 - 8 Jan 2022

Cited by 6 | Viewed by 4793

Abstract

Autosomal aneuploidy is the leading cause of embryonic and foetal death in humans. This arises mainly from errors in meiosis I or II of oogenesis. A largely ignored source of error stems from germinal mosaicism, which leads to premeiotic aneuploidy. Molecular cytogenetic studies employing metaphase fluorescence in situ hybridization and comparative genomic hybridisation suggest that premeiotic aneuploidy may affect 10–20% of oocytes overall. Such studies have been criticised on technical grounds. We report here an independent study carried out on unmanipulated oocytes that have been analysed using next generation sequencing (NGS). This study confirms that the incidence of premeiotic aneuploidy in an unselected series of oocytes exceeds 10%. A total of 140 oocytes donated by 42 women gave conclusive results; of these, 124 (88.5%) were euploid. Sixteen out of 140 (11.4%) provided evidence of premeiotic aneuploidy. Of the 140, 112 oocytes were immature (germinal vesicle or metaphase I), of which 10 were aneuploid (8.93%); the remaining 28 were intact metaphase II - first polar body complexes, and six of these were aneuploid (21.4%). Of the 16 aneuploid cells, half contained simple errors (one or two abnormal chromosomes) and half contained complex errors. We conclude that germinal mosaicism leading to premeiotic aneuploidy is a consistent finding affecting at least 10% of unselected oocytes from women undergoing egg collection for a variety of reasons. The importance of premeiotic aneuploidy lies in the fact that, for individual oocytes, it greatly increases the risk of an aneuploid mature oocyte irrespective of maternal age. As such, this may account for some cases of aneuploid conceptions in very young women. Full article

(This article belongs to the Special Issue Mammalian Gametes: Molecular Traits Shaping Their Form and Fate 2.0)

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Review

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15 pages, 1562 KiB

Open AccessReview

Chromosome Segregation in the Oocyte: What Goes Wrong during Aging

by Marta Wasielak-Politowska and Paweł Kordowitzki

Int. J. Mol. Sci. 2022, 23(5), 2880; https://doi.org/10.3390/ijms23052880 - 7 Mar 2022

Cited by 31 | Viewed by 9840

Abstract

Human female fertility and reproductive lifespan decrease significantly with age, resulting in an extended post-reproductive period. The central dogma in human female reproduction contains two important aspects. One is the pool of oocytes in the human ovary (the ovarian reserve; approximately 10⁶ at birth), which diminishes throughout life until menopause around the age of 50 (approximately 10³ oocytes) in women. The second is the quality of oocytes, including the correctness of meiotic divisions, among other factors. Notably, the increased rate of sub- and infertility, aneuploidy, miscarriages, and birth defects are associated with advanced maternal age, especially in women above 35 years of age. This postponement is also relevant for human evolution; decades ago, the female aging-related fertility drop was not as important as it is today because women were having their children at a younger age. Spindle assembly is crucial for chromosome segregation during each cell division and oocyte maturation, making it an important event for euploidy. Consequently, aberrations in this segregation process, especially during the first meiotic division in human eggs, can lead to implantation failure or spontaneous abortion. Today, human reproductive medicine is also facing a high prevalence of aneuploidy, even in young females. However, the shift in the reproductive phase of humans and the strong increase in errors make the problem much more dramatic at later stages of the female reproductive phase. Aneuploidy in human eggs could be the result of the non-disjunction of entire chromosomes or sister chromatids during oocyte meiosis, but partial or segmental aneuploidies are also relevant. In this review, we intend to describe the relevance of the spindle apparatus during oocyte maturation for proper chromosome segregation in the context of maternal aging and the female reproductive lifespan. Full article

(This article belongs to the Special Issue Mammalian Gametes: Molecular Traits Shaping Their Form and Fate 2.0)

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