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Cells
Special Issues
The Cell Biology of Fertilization
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The Cell Biology of Fertilization

A special issue of Cells (ISSN 2073-4409). This special issue belongs to the section "Cell Proliferation and Division".

Deadline for manuscript submissions: 31 December 2024 | Viewed by 7160

Special Issue Editors

Dr. Luigia Santella

E-Mail Website
Guest Editor
Research Director, Stazione Zoologica Anton Dohrn, Napoli, Italy
Interests: maturation; fertilization, actin cytoskeleton, calcium signalling; cell biology; developmental biology
Dr. Nunzia Limatola

E-Mail Website
Guest Editor
Research Infrastructures for Marine Biological Resources, Napoli, Italy
Interests: maturation; fertilization, actin cytoskeleton, calcium signalling; cell biology; developmental biology

Special Issue Information

Dear Colleagues,

Fertilization that is required for activating oocytes stimulated at different maturation stages is a critical process in embryo development. Since the beginning, the study of oogenesis and spermatogenesis and the many events that precede and follow the interaction of male and female gametes have highlighted the complexity of the fertilization process. During the past few years, significant advances have been made in deciphering the crucial role played by the structural reorganization of the cortex of oocytes during the maturation of several species that are necessary to ensure optimal fertilization conditions. Studies on the sequential spatial/temporal series of fast events regulating the fertilization process have provided live cell imaging methodologies and insights for clarifying the changes induced by the egg's extracellular coats on the sperm physiology and the interaction of species–species complementary receptors on the sperm and egg plasma membranes. Following gamete fusion, the changes in the egg plasma membrane potential, intracellular calcium and pH, and the subsequent actin remodeling to ensure monospermic fertilization and regulate cleavage demonstrate the complex program of cell signaling in sustaining the control of vital cellular activities. Thus, in addition to shedding light on the cell signaling between male and female gametes, studies on maturation and fertilization processes using large cells will help us understand the basic structural and biochemical mechanisms regulating critical cellular functions in response to a myriad of stimuli.

This Special Issue aims to assemble various lines of research to provide an in-depth description of the "state-of-the-art" regarding the fertilizability of gametes, their species-specific interaction, the signal transduction of egg activation, and cleavage.

Dr. Luigia Santella
Dr. Nunzia Limatola
Guest Editors

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Keywords

  • oocyte maturation
  • acrosome reaction
  • gamete interaction
  • actin remodelling
  • calcium
  • monospermy

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Published Papers (6 papers)

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Research

Jump to: Review

16 pages, 2834 KiB  
Article
A Novel Method to Profile Transcripts Encoding SH2 Domains in the Patiria miniata Mature Egg Transcriptome
by Lauren Bates, Emily Wiseman, Alexis Whetzel and David J. Carroll
Cells 2024, 13(22), 1898; https://doi.org/10.3390/cells13221898 - 18 Nov 2024
Viewed by 399
Abstract
The critical mechanism to restart zygote metabolism and prevent polyspermy during fertilization is the intracellular Ca2+ increase. All of the signaling molecules leading to the Ca2+ rise are not fully known in any species. In the sea star Patiria miniata, [...] Read more.
The critical mechanism to restart zygote metabolism and prevent polyspermy during fertilization is the intracellular Ca2+ increase. All of the signaling molecules leading to the Ca2+ rise are not fully known in any species. In the sea star Patiria miniata, SFK1, SFK3, and PLCγ participate in this fertilization Ca2+ increase. These proteins share common regulatory features, including signaling via tyrosine phosphorylation and their SH2 domains. In this study, we explore two different bioinformatic strategies to identify transcripts in the Patiria miniata mature egg transcriptome (Accession PRJNA398668) that code for proteins possessing an SH2 domain. The first identified the longest open reading frame for each transcript and then utilized similarity searching tools to provide identities for each transcript. The second, novel, method involved a six-frame translation of the entire transcriptome to identify SH2 domain-containing proteins. The identified transcripts were aligned against the NCBI non-redundant database and the SwissProt database. Eighty-two transcripts that encoded SH2 domains were identified. Of these, 33 were only found using the novel method. This work furthers research into egg activation by providing possible target proteins for future experiments and a novel method for identifying specific proteins of interest within a de novo transcriptome. Full article
(This article belongs to the Special Issue The Cell Biology of Fertilization)
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14 pages, 11443 KiB  
Article
Immunohistochemical Characterization of Spermatogenesis in the Ascidian Ciona robusta
by Haruka Sakurai, Kogiku Shiba, Katsumi Takamura and Kazuo Inaba
Cells 2024, 13(22), 1863; https://doi.org/10.3390/cells13221863 - 11 Nov 2024
Viewed by 472
Abstract
Animals show diverse processes of gametogenesis in the evolutionary pathway. Here, we characterized the spermatogenic cells in the testis of the marine invertebrate Ciona robusta. Ciona sperm differentiate in a non-cystic type of testis, comprising many follicles with various sizes and stages of [...] Read more.
Animals show diverse processes of gametogenesis in the evolutionary pathway. Here, we characterized the spermatogenic cells in the testis of the marine invertebrate Ciona robusta. Ciona sperm differentiate in a non-cystic type of testis, comprising many follicles with various sizes and stages of spermatogenic cells. In the space among follicles, we observed free cells that were recognized by antibody against Müllerian inhibiting substance, a marker for vertebrate Sertoli cells. We further categorized the spermatogenic cells into four round stages (RI to RIV) and three elongated stages (EI to EIII) by morphological and immunohistochemical criteria. An antibody against a vertebrate Vasa homolog recognized a few large spermatogonium-like cells (RI) near the basal wall of a follicle. Consistent with the period of meiosis, a synaptonemal complex protein SYCP3 was recognized from early spermatocytes (RII) to early spermatids (E1). Acetylated tubulins were detected in spermatids before flagellar elongation at the RIV stage and became distributed along the flagella. Electron microscopy showed that the free cells outside the testicular follicle possessed a characteristic of vertebrate Sertoli cells. These results would provide a basis for basic and comparative studies on the mechanism of spermatogenesis. Full article
(This article belongs to the Special Issue The Cell Biology of Fertilization)
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27 pages, 11038 KiB  
Article
The Effect of Synthetic Polyamine BPA-C8 on the Fertilization Process of Intact and Denuded Sea Urchin Eggs
by Nunzia Limatola, Jong Tai Chun, Jean-Louis Schmitt, Jean-Marie Lehn and Luigia Santella
Cells 2024, 13(17), 1477; https://doi.org/10.3390/cells13171477 - 2 Sep 2024
Viewed by 856
Abstract
Sea urchin eggs are covered with layers of extracellular matrix, namely, the vitelline layer (VL) and jelly coat (JC). It has been shown that sea urchin eggs’ JC components serve as chemoattractants or ligands for the receptor on the fertilizing sperm to promote [...] Read more.
Sea urchin eggs are covered with layers of extracellular matrix, namely, the vitelline layer (VL) and jelly coat (JC). It has been shown that sea urchin eggs’ JC components serve as chemoattractants or ligands for the receptor on the fertilizing sperm to promote the acrosome reaction. Moreover, the egg’s VL provides receptors for conspecific sperm to bind, and, to date, at least two sperm receptors have been identified on the surface of sea urchin eggs. Interestingly, however, according to our previous work, denuded sea urchin eggs devoid of the JC and VL do not fail to become fertilized by sperm. Instead, they are bound and penetratedby multiple sperm, raising the possibility that an alternative pathway independent of the VL-residing sperm receptor may be at work. In this research, we studied the roles of the JC and VL using intact and denuded eggs and the synthetic polyamine BPA-C8. BPA-C8 is known to bind to the negatively charged macromolecular complexes in the cells, such as the JC, VL, and the plasma membrane of echinoderm eggs, as well as to the actin filaments in fibroblasts. Our results showed that, when added to seawater, BPA-C8 significantly repressed the Ca2+ wave in the intact P. lividus eggs at fertilization. In eggs deprived of the VL and JC, BPA-C8 binds to the plasma membrane and increases fibrous structures connecting microvilli, thereby allowing the denuded eggs to revert towards monospermy at fertilization. However, the reduced Ca2+ signal in denuded eggs was nullified compared to the intact eggs because removing the JC and VL already decreased the Ca2+ wave. BPA-C8 does not cross the VL and the cell membrane of unfertilized sea urchin eggs to diffuse into the cytoplasm at variance with the fibroblasts. Indeed, the jasplakinolide-induced polymerization of subplasmalemmal actin filaments was inhibited in the eggs microinjected with BPA-C8, but not in the ones bath-incubated with the same dose of BPA-C8. Full article
(This article belongs to the Special Issue The Cell Biology of Fertilization)
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14 pages, 3354 KiB  
Article
Thirteen Ovary-Enriched Genes Are Individually Not Essential for Female Fertility in Mice
by Anh Hoang Pham, Chihiro Emori, Yu Ishikawa-Yamauchi, Keizo Tokuhiro, Maki Kamoshita, Yoshitaka Fujihara and Masahito Ikawa
Cells 2024, 13(10), 802; https://doi.org/10.3390/cells13100802 - 8 May 2024
Cited by 1 | Viewed by 1375
Abstract
Infertility is considered a global health issue as it currently affects one in every six couples, with female factors reckoned to contribute to partly or solely 50% of all infertility cases. Over a thousand genes are predicted to be highly expressed in the [...] Read more.
Infertility is considered a global health issue as it currently affects one in every six couples, with female factors reckoned to contribute to partly or solely 50% of all infertility cases. Over a thousand genes are predicted to be highly expressed in the female reproductive system and around 150 genes in the ovary. However, some of their functions in fertility remain to be elucidated. In this study, 13 ovary and/or oocyte-enriched genes (Ccdc58, D930020B18Rik, Elobl, Fbxw15, Oas1h, Nlrp2, Pramel34, Pramel47, Pkd1l2, Sting1, Tspan4, Tubal3, Zar1l) were individually knocked out by the CRISPR/Cas9 system. Mating tests showed that these 13 mutant mouse lines were capable of producing offspring. In addition, we observed the histology section of ovaries and performed in vitro fertilization in five mutant mouse lines. We found no significant anomalies in terms of ovarian development and fertilization ability. In this study, 13 different mutant mouse lines generated by CRISPR/Cas9 genome editing technology revealed that these 13 genes are individually not essential for female fertility in mice. Full article
(This article belongs to the Special Issue The Cell Biology of Fertilization)
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Review

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25 pages, 2945 KiB  
Review
Cytosolic and Acrosomal pH Regulation in Mammalian Sperm
by Julio C. Chávez, Gabriela Carrasquel-Martínez, Sandra Hernández-Garduño, Arturo Matamoros Volante, Claudia L. Treviño, Takuya Nishigaki and Alberto Darszon
Cells 2024, 13(10), 865; https://doi.org/10.3390/cells13100865 - 17 May 2024
Cited by 1 | Viewed by 1457
Abstract
As in most cells, intracellular pH regulation is fundamental for sperm physiology. Key sperm functions like swimming, maturation, and a unique exocytotic process, the acrosome reaction, necessary for gamete fusion, are deeply influenced by pH. Sperm pH regulation, both intracellularly and within organelles [...] Read more.
As in most cells, intracellular pH regulation is fundamental for sperm physiology. Key sperm functions like swimming, maturation, and a unique exocytotic process, the acrosome reaction, necessary for gamete fusion, are deeply influenced by pH. Sperm pH regulation, both intracellularly and within organelles such as the acrosome, requires a coordinated interplay of various transporters and channels, ensuring that this cell is primed for fertilization. Consistent with the pivotal importance of pH regulation in mammalian sperm physiology, several of its unique transporters are dependent on cytosolic pH. Examples include the Ca2+ channel CatSper and the K+ channel Slo3. The absence of these channels leads to male infertility. This review outlines the main transport elements involved in pH regulation, including cytosolic and acrosomal pH, that participate in these complex functions. We present a glimpse of how these transporters are regulated and how distinct sets of them are orchestrated to allow sperm to fertilize the egg. Much research is needed to begin to envision the complete set of players and the choreography of how cytosolic and organellar pH are regulated in each sperm function. Full article
(This article belongs to the Special Issue The Cell Biology of Fertilization)
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12 pages, 1276 KiB  
Review
Sperm-Induced Ca2+ Release in Mammalian Eggs: The Roles of PLCζ, InsP3, and ATP
by Karl Swann
Cells 2023, 12(24), 2809; https://doi.org/10.3390/cells12242809 - 10 Dec 2023
Cited by 2 | Viewed by 1657
Abstract
Mammalian egg activation at fertilization is triggered by a long-lasting series of increases in cytosolic Ca2+ concentration. These Ca2+ oscillations are due to the production of InsP3 within the egg and the subsequent release of Ca2+ from the endoplasmic [...] Read more.
Mammalian egg activation at fertilization is triggered by a long-lasting series of increases in cytosolic Ca2+ concentration. These Ca2+ oscillations are due to the production of InsP3 within the egg and the subsequent release of Ca2+ from the endoplasmic reticulum into the cytosol. The generation of InsP3 is initiated by the diffusion of sperm-specific phospholipase Czeta1 (PLCζ) into the egg after gamete fusion. PLCζ enables a positive feedback loop of InsP3 production and Ca2+ release which then stimulates further InsP3 production. Most cytosolic Ca2+ increases in eggs at fertilization involve a fast Ca2+ wave; however, due to the limited diffusion of InsP3, this means that InsP3 must be generated from an intracellular source rather than at the plasma membrane. All mammalian eggs studied generated Ca2+ oscillations in response to PLCζ, but the sensitivity of eggs to PLCζ and to some other stimuli varies between species. This is illustrated by the finding that incubation in Sr2+ medium stimulates Ca2+ oscillations in mouse and rat eggs but not eggs from other mammalian species. This difference appears to be due to the sensitivity of the type 1 InsP3 receptor (IP3R1). I suggest that ATP production from mitochondria modulates the sensitivity of the IP3R1 in a manner that could account for the differential sensitivity of eggs to stimuli that generate Ca2+ oscillations. Full article
(This article belongs to the Special Issue The Cell Biology of Fertilization)
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Planned Papers

The below list represents only planned manuscripts. Some of these manuscripts have not been received by the Editorial Office yet. Papers submitted to MDPI journals are subject to peer-review.

Title: Differential transport of dynein subunits during spermatogenesis in ascidian spermatozoa
Authors: Haruka Sakurai, Alu Konno, Kogiku Shiba, Katsumi Takamura, Kazuo Inaba
Affiliation: Shimoda Marine Research Center, University of Tsukuba, 5-10-1, Shimoda, Shizuoka, 415-0025, Japan

Title: Fertilization envelope elevation is blocked by hormonal stimulation of 1-methyladenine until germinal vesicle breakdown due to Rac1 activation.
Authors: Sakurako Aida 1, Yuna Yamazaki 1, Nunzia Limatola 2, Luigia Santella 2, Kazuyoshi Chiba 1
Affiliation: 1. Department of Biological Sciences,Ochanomizu University,2-1-1 Ohtsuka, Bunkyo-ku, Tokyo 112-8610, Japan; 2. Stazione Zoologica Anton Dohrn,Villa Comunale 80121, Napoli, Italy.

Title: Identification of SH2 domain-containing transcripts in the Patiria miniata mature egg transcriptome
Authors: Lauren Bates 1, Emily Wiseman 2, Alexis Whetzel 3 and David J. Carroll 3
Affiliation: 1 – West Virginia Laboratories, South Charleston, WV, USA; 2 – BioScryb Genomics, Durham, NC, USA; 3 – Department of Biochemistry and Molecular Genetics, Midwestern University, Glendale, AZ, USA.

Title: Extracellular Ubiquitin-Proteasome System: Its Importance in Deuterostome Fertilization
Authors: Hitoshi Sawada and Takako Saito
Affiliation: 1. Department of Applied Life Sciences, Faculty of Agriculture, Shizuoka University, Shizuoka 422-8529, Japan 2. Shizuoka Institute for the Study of Marine Biology and Chemistry, Shizuoka University, Shizuoka 422-8529, Japan

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