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Physiology of Gametes and Fertilization

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

Deadline for manuscript submissions: closed (30 June 2021) | Viewed by 29379

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Dr. Katerina Komrskova

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BIOCEV Group, Department of Zoology, Charles University in Prague, Vinicna 7, 2 128 44 Prague, Czech Republic
Interests: fertilization; sperm; capacitation; acrosome reaction; gamete fusion; gamete protein interactions; tetraspanins; infertility
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Dr. Pavla Postlerova

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Laboratory of Reproductive Biology, Institute of Biotechnology of the Czech Academy of Sciences, BIOCEV, Prumyslova 595, 252 50 Vestec, Czech Republic
Department of Veterinary Sciences, Faculty of Agrobiology, Food and Natural Resources, University of Life Sciences Prague, Kamycka 129, 165 00 Prague 6, Czech Republic

Dr. Michaela Frolikova

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Laboratory of Reproductive Biology, Institute of Biotechnology of the Czech Academy of Sciences, BIOCEV, Prumyslova 595, 252 50 Vestec, Czech Republic

Special Issue Information

Dear Colleagues,

In spite of all knowledge we have gained from research into mammalian fertilization and the physiological changes that the male gamete must undergo to be able to fertilize the egg, the actual sperm interaction with the egg, including binding and fusion, is still covered in a veil of mystery.

Sperm-egg membrane interaction and fusion is mediated by many molecular components. There are numerous molecules located on sperm and oocyte membranes that are part of key protein networks that differ in their protein composition.

This special issue is dedicated to the physiology of gametes and fertilization and aims to introduce the reader to new and original research targeting the molecular mechanisms involved in reproduction.

In order to understand the entirety of the fusion process involving the binding and fusion of mammalian gametes, new mechanisms that sperm and egg undergo during maturation as well as interactions between sperm and egg membrane proteins need further research.

It is hoped that outcome of the studies published here-in can be used as the catalyst for developing additional applicational research to be utilized in both animal breading programs and human assisted reproduction.

Dr. Katerina Komrskova
Dr. Pavla Postlerova
Dr. Michaela Frolikova
Guest Editors

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Published Papers (10 papers)

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Research

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23 pages, 8531 KiB

Open AccessArticle

In Vitro versus Cryo-Induced Capacitation of Bovine Spermatozoa, Part 2: Changes in the Expression Patterns of Selected Transmembrane Channels and Protein Kinase A

by Filip Benko, Veronika Fialková, Jana Žiarovská, Michal Ďuračka, Norbert Lukáč and Eva Tvrdá

Int. J. Mol. Sci. 2022, 23(23), 14646; https://doi.org/10.3390/ijms232314646 - 24 Nov 2022

Cited by 7 | Viewed by 3340

Abstract

Since the molecular similarities and differences among physiological capacitation and cryocapacitation have not been studied in detail, this study was designed to assess the gene and protein expression levels of the Cation channel of sperm (CatSper) 1 and 2, sodium bicarbonate (Na⁺/HCO₃⁻) cotransporter (NBC) and protein kinase A (PKA) in un-capacitated (control), in vitro capacitated (CAP) and cryopreserved (CRYO) bovine spermatozoa. All samples were subjected to motility evaluation using the computer assisted sperm analysis and chlortetracycline (CTC) assay for the assessment of the capacitation patterns. Furthermore, quantitative reverse transcription PCR (qRT-PCR) and Western blots were used to monitor the expression patterns of the selected capacitation markers. The results showed a significant reduction in the gene and protein expression levels of CatSper1 and 2 in the CRYO group when compared to the CAP group (p < 0.0001). In the case of NBC, the results were not significantly different or were inconclusive. While a non-significant down-regulation of PKA was found in the CRYO group, a significant reduction in the expression of the PKA protein was found in frozen-thawed spermatozoa in comparison to the CAP group (p < 0.05). In conclusion, we may hypothesize that while in vitro capacitated and cryopreserved spermatozoa exhibit CTC-patterns consistent with capacitation events, the molecular machinery underlying CTC-positivity may be different. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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15 pages, 4030 KiB

Open AccessArticle

Granulosa Cell Specific Loss of Adar in Mice Delays Ovulation, Oocyte Maturation and Leads to Infertility

by Rikki N. Nelson, V. Praveen Chakravarthi, Anamika Ratri, Xiaoman Hong, Jan A. Gossen and Lane K. Christenson

Int. J. Mol. Sci. 2022, 23(22), 14001; https://doi.org/10.3390/ijms232214001 - 13 Nov 2022

Cited by 1 | Viewed by 2682

Abstract

Adenosine deaminases acting on RNA-(ADAR) comprise one family of RNA editing enzymes that specifically catalyze adenosine to inosine (A-to-I) editing. A granulosa cell (GC) specific Adar depleted mouse model [Adar ^flox/flox:Cyp19a1-Cre/+ (gcAdarKO)] was used to evaluate the role of ADAR1 during the periovulatory period. Loss of Adar in GCs led to failure to ovulate at 16 h post-hCG, delayed oocyte germinal vesicle breakdown and severe infertility. RNAseq analysis of GC collected from gcAdarKO and littermate control mice at 0 and 4 h post-hCG following a super-ovulatory dose of eCG (48 h), revealed minimal differences after eCG treatment alone (0 h), consistent with normal folliculogenesis observed histologically and uterine estrogenic responses. In contrast, 300 differential expressed genes (DEGs; >1.5-fold change and FDRP < 0.1) were altered at 4 h post-hCG. Ingenuity pathway analysis identified many downstream targets of estrogen and progesterone pathways, while multiple genes involved in inflammatory responses were upregulated in the gcAdarKO GCs. Temporal expression analysis of GCs at 0, 4, 8, and 12 h post-hCG of Ifi44, Ifit1, Ifit3b, and Oas1g and Ovgp1 confirmed upregulation of these inflammatory and interferon genes and downregulation of Ovgp1 a glycoprotein involved in oocyte zona pellucida stability. Thus, loss of ADAR1 in GCs leads to increased expression of inflammatory and interferon response genes which are temporally linked to ovulation failure, alterations in oocyte developmental progression and infertility. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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14 pages, 1938 KiB

Open AccessArticle

Oxidative Stress-Related Signaling Pathways Predict Oocytes’ Fertilization In Vitro and Embryo Quality

by Paolo Giovanni Artini, Giorgia Scarfò, Ilaria Marzi, Jonathan Fusi, Maria Elena Obino, Ferdinando Franzoni, Elisa Zappelli, Elisa Chelucci, Claudia Martini, Vito Cela and Simona Daniele

Int. J. Mol. Sci. 2022, 23(21), 13442; https://doi.org/10.3390/ijms232113442 - 3 Nov 2022

Cited by 10 | Viewed by 1906

Abstract

Oocyte development and fertilization are largely influenced by the microenvironment of the follicular fluid (FF), and the exploration of its molecular/metabolic composition may help in improving in vitro fertilization (IVF) outcomes. Here, the concentrations of molecules related to oxidative stress/inflammation were measured in FF from follicles at oocyte retrieval during IVF. Here, the FF antioxidant potential was correlated with the number of retrieved/mature oocytes and the number of fertilized ones. FF collected from the follicles of normal fertilized oocytes presented an elevated antioxidant capability, lower levels of pro-inflammatory molecules (i.e., IL-6, IL-8, IL-12, TGF-β, and HIF-1α), and a higher IL-10 concentration. FF samples from follicles at oocyte retrieval that resulted in top-quality embryos displayed a peculiar antioxidant capability and a further decrease in proinflammatory molecules when compared with FF, giving rise to poor-quality embryos. Finally, pro-inflammatory molecules were lower and accompanied by a high antioxidant capability in samples giving rise to successful embryo implantation. The antioxidant capability and IL-10 displayed a good predictive ability for fertilization and embryo quality. Overall, our data showed the great influence of oxidative stress on the oocytes’ fertilization, and shed light on the importance of controlling the inflammatory and oxidative status of FF to obtain good-quality embryos with significant implantation potential. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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20 pages, 2797 KiB

Open AccessArticle

Cyclic FEE Peptide Improves Human Sperm Movement Parameters without Modification of Their Energy Metabolism

by Nathalie Le Foll, Jean-Christophe Pont, Audrey L’Hostis, Thomas Guilbert, Frédéric Bouillaud, Jean-Philippe Wolf and Ahmed Ziyyat

Int. J. Mol. Sci. 2021, 22(20), 11263; https://doi.org/10.3390/ijms222011263 - 19 Oct 2021

Cited by 3 | Viewed by 1952

Abstract

Cyclic fertilin peptide (cFEE: phenylalanine, glutamic acid; glutamic acid) improves gamete interaction in humans. We investigate whether it could be via improvement of sperm movement parameters and their mitochondrial ATP production. Sperm movement parameters were studied using computer-assisted sperm analysis (CASA) in sperm samples from 38 patients with normal sperm in medium supplemented with cyclic fertilin against a control group. Sperm mitochondrial functions were studied using donor’s sperm, incubated or not with cFEE. It was evaluated by the measurement of their ATP production using bioluminescence, their respiration by high resolution oxygraphy, and of mitochondrial membrane potential (MMP) using potentiometric dyes and flow cytometry. cFEE significantly improved sperm movement parameters and percentage of hyperactivated sperm. Impact of inhibitors showed OXPHOS as the predominant energy source for sperm movement. However, cFEE had no significant impact on any of the analyzed mitochondrial bioenergetic parameters, suggesting that it could act via a more efficient use of its energy resources. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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13 pages, 2157 KiB

Open AccessArticle

αV Integrin Expression and Localization in Male Germ Cells

by Veronika Palenikova, Michaela Frolikova, Eliska Valaskova, Pavla Postlerova and Katerina Komrskova

Int. J. Mol. Sci. 2021, 22(17), 9525; https://doi.org/10.3390/ijms22179525 - 2 Sep 2021

Cited by 3 | Viewed by 2635

Abstract

Integrins are transmembrane receptors that facilitate cell adhesion and cell–extracellular matrix communication. They are involved in the sperm maturation including capacitation and gamete interaction, resulting in successful fertilization. αV integrin belongs to the integrin glycoprotein superfamily, and it is indispensable for physiological spermiogenesis and testosterone production. We targeted the gene and protein expression of the αV integrin subunit and described its membrane localization in sperm. Firstly, in mouse, we traced αV integrin gene expression during spermatogenesis in testicular fraction separated by elutriation, and we detected gene activity in spermatogonia, spermatocytes, and round spermatids. Secondly, we specified αV integrin membrane localization in acrosome-intact and acrosome-reacted sperm and compared its pattern between mouse, pig, and human. Using immunodetection and structured illumination microscopy (SIM), the αV integrin localization was confined to the plasma membrane covering the acrosomal cap area and also to the inner acrosomal membrane of acrosome-intact sperm of all selected species. During the acrosome reaction, which was induced on capacitated sperm, the αV integrin relocated and was detected over the whole sperm head. Knowledge of the integrin pattern in mature sperm prepares the ground for further investigation into the pathologies and related fertility issues in human medicine and veterinary science. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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26 pages, 7382 KiB

Open AccessArticle

Core Histones Are Constituents of the Perinuclear Theca of Murid Spermatozoa: An Assessment of Their Synthesis and Assembly during Spermiogenesis and Function after Gametic Fusion

by Lauren E. Hamilton, Morgan Lion, Luis Aguila, João Suzuki, Genevieve Acteau, Nicole Protopapas, Wei Xu, Peter Sutovsky, Mark Baker and Richard Oko

Int. J. Mol. Sci. 2021, 22(15), 8119; https://doi.org/10.3390/ijms22158119 - 29 Jul 2021

Cited by 8 | Viewed by 3432

Abstract

The perinuclear theca (PT) of the eutherian sperm head is a cytoskeletal-like structure that houses proteins involved in important cellular processes during spermiogenesis and fertilization. Building upon our novel discovery of non-nuclear histones in the bovine PT, we sought to investigate whether this PT localization was a conserved feature of eutherian sperm. Employing cell fractionation, immunodetection, mass spectrometry, qPCR, and intracytoplasmic sperm injections (ICSI), we examined the localization, developmental origin, and functional potential of histones from the murid PT. Immunodetection localized histones to the post-acrosomal sheath (PAS) and the perforatorium (PERF) of the PT but showed an absence in the sperm nucleus. MS/MS analysis of selectively extracted PT histones indicated that predominately core histones (i.e., H3, H3.3, H2B, H2A, H2AX, and H4) populate the murid PT. These core histones appear to be de novo-synthesized in round spermatids and assembled via the manchette during spermatid elongation. Mouse ICSI results suggest that early embryonic development is delayed in the absence of PT-derived core histones. Here, we provide evidence that core histones are de novo-synthesized prior to PT assembly and deposited in PT sub-compartments for subsequent involvement in chromatin remodeling of the male pronucleus post-fertilization. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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21 pages, 2517 KiB

Open AccessArticle

Bull Sperm Capacitation Is Accompanied by Redox Modifications of Proteins

by Agnieszka Mostek, Anna Janta, Anna Majewska and Andrzej Ciereszko

Int. J. Mol. Sci. 2021, 22(15), 7903; https://doi.org/10.3390/ijms22157903 - 23 Jul 2021

Cited by 13 | Viewed by 4350

Abstract

The ability to fertilise an egg is acquired by the mammalian sperm during the complex biochemical process called capacitation. Capacitation is accompanied by the production of reactive oxygen species (ROS), but the mechanism of redox regulation during capacitation has not been elucidated. This study aimed to verify whether capacitation coincides with reversible oxidative post-translational modifications of proteins (oxPTMs). Flow cytometry, fluorescence microscopy and Western blot analyses were used to verify the sperm capacitation process. A fluorescent gel-based redox proteomic approach allowed us to observe changes in the level of reversible oxPTMs manifested by the reduction or oxidation of susceptible cysteines in sperm proteins. Sperm capacitation was accompanied with redox modifications of 48 protein spots corresponding to 22 proteins involved in the production of ROS (SOD, DLD), playing a role in downstream redox signal transfer (GAPDHS and GST) related to the cAMP/PKA pathway (ROPN1L, SPA17), acrosome exocytosis (ACRB, sperm acrosome associated protein 9, IZUMO4), actin polymerisation (CAPZB) and hyperactivation (TUBB4B, TUB1A). The results demonstrated that sperm capacitation is accompanied by altered levels of oxPTMs of a group of redox responsive proteins, filling gaps in our knowledge concerning sperm capacitation. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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12 pages, 5984 KiB

Open AccessArticle

Ribonucleic Acid Export 1 Is a Kinetochore-Associated Protein That Participates in Chromosome Alignment in Mouse Oocytes

by Fan Chen, Xiao-Fei Jiao, Fei Meng, Yong-Sheng Wang, Zhi-Ming Ding, Yi-Liang Miao, Jia-Jun Xiong and Li-Jun Huo

Int. J. Mol. Sci. 2021, 22(9), 4841; https://doi.org/10.3390/ijms22094841 - 3 May 2021

Cited by 2 | Viewed by 2455

Abstract

Ribonucleic acid export 1 (Rae1) is an important nucleoporin that participates in mRNA export during the interphase of higher eukaryotes and regulates the mitotic cell cycle. In this study, small RNA interference technology was used to knockdown Rae1, and immunofluorescence, immunoblotting, and chromosome spreading were used to study the role of Rae1 in mouse oocyte meiotic maturation. We found that Rae1 is a crucial regulator of meiotic maturation of mouse oocytes. After the resumption of meiosis (GVBD), Rae1 was concentrated on the kinetochore structure. The knockdown of Rae1 by a specific siRNA inhibited GVBD progression at 2 h, finally leading to a decreased 14 h polar body extrusion (PBE) rate. However, a comparable 14 h PBE rate was found in the control, and the Rae1 knockdown groups that had already undergone GVBD. Furthermore, we found elevated PBE after 9.5 h in the Rae1 knockdown oocytes. Further analysis revealed that Rae1 depletion significantly decreased the protein level of securin. In addition, we detected weakened kinetochore–microtubule (K-MT) attachments, misaligned chromosomes, and an increased incidence of aneuploidy in the Rae1 knockdown oocytes. Collectively, we propose that Rae1 modulates securin protein levels, which contribute to chromosome alignment, K-MT attachments, and aneuploidy in meiosis. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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Review

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30 pages, 565 KiB

Open AccessReview

Advanced Sperm Selection Strategies as a Treatment for Infertile Couples: A Systematic Review

by Jordi Ribas-Maynou, Isabel Barranco, Maria Sorolla-Segura, Marc Llavanera, Ariadna Delgado-Bermúdez and Marc Yeste

Int. J. Mol. Sci. 2022, 23(22), 13859; https://doi.org/10.3390/ijms232213859 - 10 Nov 2022

Cited by 4 | Viewed by 2608

Abstract

Assisted reproductive technology (ART) is an essential tool to overcome infertility, and is a worldwide disease that affects millions of couples at reproductive age. Sperm selection is a crucial step in ART treatment, as it ensures the use of the highest quality sperm for fertilization, thus increasing the chances of a positive outcome. In recent years, advanced sperm selection strategies for ART have been developed with the aim of mimicking the physiological sperm selection that occurs in the female genital tract. This systematic review sought to evaluate whether advanced sperm selection techniques could improve ART outcomes and sperm quality/functionality parameters compared to traditional sperm selection methods (swim-up or density gradients) in infertile couples. According to preferred reporting items for systematic reviews and meta-analyses (PRISMA guidelines), the inclusion and exclusion criteria were defined in a PICOS (population, intervention, comparator, outcome, study) table. A systematic search of the available literature published in MEDLINE-PubMed until December 2021 was subsequently conducted. Although 4237 articles were recorded after an initial search, only 47 studies were finally included. Most reports (30/47; 63.8%) revealed an improvement in ART outcomes after conducting advanced vs. traditional sperm selection methods. Among those that also assessed sperm quality/functionality parameters (12/47), there was a consensus (10/12; 83.3%) about the beneficial effect of advanced sperm selection methods on these variables. In conclusion, the application of advanced sperm selection methods improves ART outcomes. In spite of this, as no differences in the reproductive efficiency between advanced methods has been reported, none can be pointed out as a gold standard to be conducted routinely. Further research addressing whether the efficiency of each method relies on the etiology of infertility is warranted. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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12 pages, 2694 KiB

Open AccessReview

Impact of Global Transcriptional Silencing on Cell Cycle Regulation and Chromosome Segregation in Early Mammalian Embryos

by Martin Anger, Lenka Radonova, Adela Horakova, Diana Sekach and Marketa Charousova

Int. J. Mol. Sci. 2021, 22(16), 9073; https://doi.org/10.3390/ijms22169073 - 23 Aug 2021

Cited by 4 | Viewed by 2495

Abstract

The onset of an early development is, in mammals, characterized by profound changes of multiple aspects of cellular morphology and behavior. These are including, but not limited to, fertilization and the merging of parental genomes with a subsequent transition from the meiotic into the mitotic cycle, followed by global changes of chromatin epigenetic modifications, a gradual decrease in cell size and the initiation of gene expression from the newly formed embryonic genome. Some of these important, and sometimes also dramatic, changes are executed within the period during which the gene transcription is globally silenced or not progressed, and the regulation of most cellular activities, including those mentioned above, relies on controlled translation. It is known that the blastomeres within an early embryo are prone to chromosome segregation errors, which might, when affecting a significant proportion of a cell within the embryo, compromise its further development. In this review, we discuss how the absence of transcription affects the transition from the oocyte to the embryo and what impact global transcriptional silencing might have on the basic cell cycle and chromosome segregation controlling mechanisms. Full article

(This article belongs to the Special Issue Physiology of Gametes and Fertilization)

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