Genetic and Genomic Regulation of Ovarian and Testicular Functions in Animals

A special issue of Genes (ISSN 2073-4425). This special issue belongs to the section "Animal Genetics and Genomics".

Deadline for manuscript submissions: closed (20 June 2021) | Viewed by 33153

Special Issue Editors


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Guest Editor
GenPhySE, Université de Toulouse, INRAE, ENVT, 31326, Castanet Tolosan, France
Interests: testis; molecular endocrinology; circular RNAs; gene expression; genome annotation; structural mutants (duplication, deletion)

E-Mail Website
Guest Editor
Division of Animal Sciences, University of Missouri, Columbia, MO 65211, USA
Interests: oocyte meiosis; in vitro fertilization; early embryo development; cell cycle; ovarian function

Special Issue Information

Dear Colleagues,

This Special Issue will publish research articles and reviews on gene/genome function, gene/genome regulation, and coordination of gene expression in gonads. We would like manuscripts where the genes and their transcripts constitute the core of the work.

  • Manuscripts concerning the description of genes involved at different periods of testicular activity are welcome. How the testis manages these different periods? (which, depending on the species, are more or less overlapping). The timing of puberty is still an interesting question (is late-onset puberty faster?).
  • We also encourage the submission of manuscripts concerning the understanding of the molecular function of non-coding transcripts in (regulation of) the testicular metabolism, since lnc and circRNAs are particularly numerous in this tissue.
  • Manuscripts concerning the analysis of the consequences of genetic alteration (structural modification, mutation) on testicular function or development are also welcome.
  • We invite authors to submit manuscripts aimed to understand the role(s) of genes involved in the wide range of biological events in ovaries including oogenesis, folliculogenesis, steroidogenesis, oocyte biology, and communication and interaction between the oocyte and surrounding somatic cells.
  • We also encourage the submission of manuscripts identifying genetic markers that can predict ovarian reserve, gamete quality, and ovarian diseases.
  • Authors are especially encouraged to submit manuscripts aiming to improve ovarian functions by regulating (inhibition/activation) identified genes.

Dr. Annie Robic
Dr. Ahmed Balboula
Guest Editors

Manuscript Submission Information

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Keywords

  • genes, genome
  • sheep, cattle, pig, horse, avian, rabbit, (yak, alpaca)
  • gene expression: coding and non-coding transcripts (small RNA, lnc, circRNAs…)
  • regulation, interactions, coordination, inhibition, activation
  • methylation of DNA
  • testis development: fetal/postnatal/pubertal testis development
  • spermatogenesis
  • steroidogenesis
  • oogenesis
  • folliculogenesis
  • ovarian development
  • gamete biology
  • animals

Published Papers (9 papers)

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Research

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10 pages, 1687 KiB  
Article
Effect of E-64 Supplementation during In Vitro Maturation on the Developmental Competence of Bovine OPU-Derived Oocytes
by Ahmed Z. Balboula, Mansour Aboelenain, Miki Sakatani, Ken-Ichi Yamanaka, Hanako Bai, Takahiro Shirozu, Manabu Kawahara, Abd Elraouf O. Hegab, Samy M. Zaabel and Masashi Takahashi
Genes 2022, 13(2), 324; https://doi.org/10.3390/genes13020324 - 10 Feb 2022
Cited by 4 | Viewed by 2651
Abstract
Recovery of bovine oocytes using the ovum pick-up (OPU) technique offers the advantage of rapid genetic improvement through propagation of desired genes from animals with high genetic qualities. However, the developmental competence of OPU-derived immature oocytes remains relatively poor. We previously found that [...] Read more.
Recovery of bovine oocytes using the ovum pick-up (OPU) technique offers the advantage of rapid genetic improvement through propagation of desired genes from animals with high genetic qualities. However, the developmental competence of OPU-derived immature oocytes remains relatively poor. We previously found that cathepsin B gene expression and activity are increased in poor quality oocytes and embryos compared to good quality ones. In this study, we investigated the effect of E-64 (cathepsin B inhibitor) supplementation during in vitro maturation (IVM) on the developmental competence of OPU-derived immature oocytes and the quality of the produced blastocysts. Our results showed that supplementation of IVM medium with E-64 significantly improved the developmental competence of OPU-derived immature oocytes as evidenced by the significant increase of the blastocyst rate. Importantly, the presence of E-64 during IVM also significantly improved blastocyst quality by increasing the total cell number and decreasing the percentage of TUNEL positive cells. These results indicate that E-64 supplementation during IVM is a promising tool to improve the efficiency of OPU-IVF program by improving the developmental competence of OPU-derived immature oocytes. Full article
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23 pages, 7338 KiB  
Article
Hyaluronan and Collagen Are Prominent Extracellular Matrix Components in Bovine and Porcine Ovaries
by Wendena S. Parkes, Farners Amargant, Luhan T. Zhou, Cecilia E. Villanueva, Francesca E. Duncan and Michele T. Pritchard
Genes 2021, 12(8), 1186; https://doi.org/10.3390/genes12081186 - 30 Jul 2021
Cited by 16 | Viewed by 3654
Abstract
The extracellular matrix (ECM) is a major component of the ovarian stroma. Collagen and hyaluronan (HA) are critical ovarian stromal ECM molecules that undergo age-dependent changes in the mouse and human. How these matrix components are regulated and organized in other mammalian species [...] Read more.
The extracellular matrix (ECM) is a major component of the ovarian stroma. Collagen and hyaluronan (HA) are critical ovarian stromal ECM molecules that undergo age-dependent changes in the mouse and human. How these matrix components are regulated and organized in other mammalian species with reproductive characteristics similar to women such as cows and pigs, has not been systematically investigated. Therefore, we performed histological, molecular, and biochemical analyses to characterize collagen and HA in these animals. Bovine ovaries had more collagen than porcine ovaries when assessed biochemically, and this was associated with species-specific differences in collagen gene transcripts: Col3a1 was predominant in cow ovaries while Col1a1 was predominant in pig ovaries. We also observed more HA in the porcine vs. bovine ovary. HA was distributed across three molecular weight ranges (<100 kDa, 100–300 kDa, and >300 kDa) in ovarian tissue and follicular fluid, with tissue having more >300 kDa HA than the other two ranges. Transcripts for HA synthesis and degradation enzymes, Has3 and Hyal2, respectively, were predominant in cow ovaries, whereas Has2, Kiaa1199, and Tmem2 tended to be predominant in pig ovaries. Together, our findings have implications for the composition, organization, and regulation of the ovarian ECM in large mammalian species, including humans. Full article
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13 pages, 1859 KiB  
Article
Meiotic Silencing in Pigs: A Case Study in a Translocated Azoospermic Boar
by Nicolas Mary, Anne Calgaro, Harmonie Barasc, Nathalie Bonnet, Stéphane Ferchaud, Isabelle Raymond-Letron, Alain Ducos and Alain Pinton
Genes 2021, 12(8), 1137; https://doi.org/10.3390/genes12081137 - 27 Jul 2021
Cited by 1 | Viewed by 1841
Abstract
Carriers of balanced constitutional reciprocal translocations usually present a normal phenotype, but often show reproductive disorders. For the first time in pigs, we analyzed the meiotic process of an autosome–autosome translocation associated with azoospermia. Meiotic process analysis revealed the presence of unpaired autosomal [...] Read more.
Carriers of balanced constitutional reciprocal translocations usually present a normal phenotype, but often show reproductive disorders. For the first time in pigs, we analyzed the meiotic process of an autosome–autosome translocation associated with azoospermia. Meiotic process analysis revealed the presence of unpaired autosomal segments with histone γH2AX accumulation sometimes associated with the XY body. Additionally, γH2AX signals were observed on apparently synapsed autosomes other than the SSC1 or SSC15, as previously observed in Ataxia with oculomotor apraxia type 2 patients or knock-out mice for the Senataxin gene. Gene expression showed a downregulation of genes selected on chromosomes 1 and 15, but no upregulation of SSCX genes. We hypothesized that the total meiotic arrest observed in this boar might be due to the silencing of crucial autosomal genes by the mechanism referred to as meiotic silencing of unsynapsed chromatin (MSUC). Full article
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17 pages, 1546 KiB  
Article
Differential Transcript Profiles in Cumulus-Oocyte Complexes Originating from Pre-Ovulatory Follicles of Varied Physiological Maturity in Beef Cows
by Sarah E. Moorey, Jenna M. Monnig, Michael F. Smith, M. Sofia Ortega, Jonathan A. Green, Ky G. Pohler, G. Alan Bridges, Susanta K. Behura and Thomas W. Geary
Genes 2021, 12(6), 893; https://doi.org/10.3390/genes12060893 - 10 Jun 2021
Cited by 13 | Viewed by 2927
Abstract
Small dominant follicle diameter at induced ovulation, but not at spontaneous ovulation, decreased pregnancy rate, fertilization rate, and day seven embryo quality in beef cows. We hypothesized that the physiological status of the follicle at GnRH-induced ovulation has a direct effect on the [...] Read more.
Small dominant follicle diameter at induced ovulation, but not at spontaneous ovulation, decreased pregnancy rate, fertilization rate, and day seven embryo quality in beef cows. We hypothesized that the physiological status of the follicle at GnRH-induced ovulation has a direct effect on the transcriptome of the Cumulus-Oocyte complex, thereby affecting oocyte competence and subsequent embryo development. The objective of this study was to determine if the transcriptome of oocytes and associated cumulus cells (CC) differed among small (≤11.7 mm) and large follicles (≥12.7 mm) exposed to a GnRH-induced gonadotropin surge and follicles (11.7–14.0 mm) exposed to an endogenous gonadotropin surge (spontaneous follicles). RNA sequencing data, from pools of four oocytes or their corresponding CC, revealed 69, 94, and 83 differentially expressed gene transcripts (DEG) among oocyte pools from small versus large, small versus spontaneous, and large versus spontaneous follicle classifications, respectively. An additional 128, 98, and 80 DEG were identified among small versus large, small versus spontaneous, and large versus spontaneous follicle CC pools, respectively. The biological pathway “oxidative phosphorylation” was significantly enriched with DEG from small versus spontaneous follicle oocyte pools (FDR < 0.01); whereas the glycolytic pathway was significantly enriched with DEG from CC pools obtained from large versus small follicles (FDR < 0.01). These findings collectively suggest that altered carbohydrate metabolism within the Cumulus-Oocyte complex likely contributes to the decreased competency of oocytes from small pre-ovulatory follicles exposed to an exogenous GnRH-induced gonadotropin surge. Full article
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19 pages, 4635 KiB  
Article
Correlation Networks Provide New Insights into the Architecture of Testicular Steroid Pathways in Pigs
by Annie Robic, Thomas Faraut, Katia Feve, Sarah Djebali, Armelle Prunier, Catherine Larzul and Laurence Liaubet
Genes 2021, 12(4), 551; https://doi.org/10.3390/genes12040551 - 9 Apr 2021
Cited by 4 | Viewed by 2457
Abstract
Steroid metabolism is a fundamental process in the porcine testis to provide testosterone but also estrogens and androstenone, which are essential for the physiology of the boar. This study concerns boars at an early stage of puberty. Using a RT-qPCR approach, we showed [...] Read more.
Steroid metabolism is a fundamental process in the porcine testis to provide testosterone but also estrogens and androstenone, which are essential for the physiology of the boar. This study concerns boars at an early stage of puberty. Using a RT-qPCR approach, we showed that the transcriptional activities of several genes providing key enzymes involved in this metabolism (such as CYP11A1) are correlated. Surprisingly, HSD17B3, a key gene for testosterone production, was absent from this group. An additional weighted gene co-expression network analysis was performed on two large sets of mRNA-seq to identify co-expression modules. Of these modules, two containing either CYP11A1 or HSD17B3 were further analyzed. This comprehensive correlation meta-analysis identified a group of 85 genes with CYP11A1 as hub gene, but did not allow the characterization of a robust correlation network around HSD17B3. As the CYP11A1-group includes most of the genes involved in steroid synthesis pathways (including LHCGR encoding for the LH receptor), it may control the synthesis of most of the testicular steroids. The independent expression of HSD17B3 probably allows part of the production of testosterone to escape this control. This CYP11A1-group contained also INSL3 and AGT genes encoding a peptide hormone and an angiotensin peptide precursor, respectively. Full article
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13 pages, 2953 KiB  
Article
Metabonomic Insights into the Sperm Activation Mechanisms in Ricefield Eel (Monopterus albus)
by Huiying Zhang, Yang Liu, Lingling Zhou, Shaohua Xu, Cheng Ye, Haifeng Tian, Zhong Li and Guangfu Hu
Genes 2020, 11(11), 1259; https://doi.org/10.3390/genes11111259 - 26 Oct 2020
Cited by 9 | Viewed by 2534
Abstract
In fish, sperm motility activation is one of the most essential procedures for fertilization. Previous studies have mainly focused on the external environmental effects and intracellular signals in sperm activation; however, little is known about the metabolic process of sperm motility activation in [...] Read more.
In fish, sperm motility activation is one of the most essential procedures for fertilization. Previous studies have mainly focused on the external environmental effects and intracellular signals in sperm activation; however, little is known about the metabolic process of sperm motility activation in fish. In the present study, using ricefield eel (Monopterus albus) sperm as a model, metabonomics was used to analyze the metabolic mechanism of the sperm motility activation in fish. Firstly, 529 metabolites were identified in the sperm of ricefield eel, which were clustered into the organic acids, amino acids, nucleotides, benzene, and carbohydrates, respectively. Among them, the most abundant metabolites in sperm were L-phenylalanine, DL-leucine, L-leucine, lysolecithin choline 18:0, L-tryptophan, adenine, hypoxanthine, 7-Methylguanine, shikimic acid, and L-tyrosine. Secondly, compared to pre-activated sperm, the level of S-sulfo-L-cysteine and L-asparagine were both increased in the post-activated sperm. Ninety-two metabolites were decreased in the post-activated sperm, including quinic acid, acetylsalicylic acid, 7,8-dihydro L-biopterin, citric acid, glycylphenylalanine, and dihydrotachysterol (DHT). Finally, basing on the pathway analysis, we found that the changed metabolites in sperm motility activation were mainly clustered into energy metabolism and anti-oxidative stress. Fish sperm motility activation would be accompanied by the release of a large amount of energy, which might damage the genetic material of sperm. Thus, the anti-oxidative stress function is a critical process to maintain the normal physiological function of sperm. Full article
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17 pages, 3233 KiB  
Article
A Preliminary Study on the Characteristics of microRNAs in Ovarian Stroma and Follicles of Chuanzhong Black Goat during Estrus
by Tingting Lu, Xian Zou, Guangbin Liu, Ming Deng, Baoli Sun, Yongqing Guo, Dewu Liu and Yaokun Li
Genes 2020, 11(9), 970; https://doi.org/10.3390/genes11090970 - 21 Aug 2020
Cited by 11 | Viewed by 2643
Abstract
microRNAs (miRNAs) play a significant role in ovarian follicular maturity, but miRNA expression patterns in ovarian stroma (OS), large follicles (LF), and small follicles (SF) have been rarely explored. We herein aimed to identify miRNAs, their target genes and signaling pathways, as well [...] Read more.
microRNAs (miRNAs) play a significant role in ovarian follicular maturity, but miRNA expression patterns in ovarian stroma (OS), large follicles (LF), and small follicles (SF) have been rarely explored. We herein aimed to identify miRNAs, their target genes and signaling pathways, as well as their interaction networks in OS, LF, and SF of Chuanzhong black goats at the estrus phase using small RNA-sequencing. We found that the miRNA expression profiles of LF and SF were more similar than those of OS—32, 16, and 29 differentially expressed miRNAs were identified in OS vs. LF, OS vs. SF, and LF vs. SF, respectively. Analyses of functional enrichment and the miRNA-targeted gene interaction network suggested that miR-182 (SMC3), miR-122 (SGO1), and miR-206 (AURKA) were involved in ovarian organogenesis and hormone secretion by oocyte meiosis. Furthermore, miR-202-5p (EREG) and miR-485-3p (FLT3) were involved in follicular maturation through the MAPK signaling pathway, and miR-2404 (BMP7 and CDKN1C) played a key role in follicular development through the TGF-β signaling pathway and cell cycle; nevertheless, further research is warranted. To our knowledge, this is the first study to investigate miRNA expression patterns in OS, LF, and SF of Chuanzhong black goats during estrus. Our findings provide a theoretical basis to elucidate the role of miRNAs in follicular maturation. These key miRNAs might provide candidate biomarkers for the diagnosis of follicular maturation and will assist in developing new therapeutic targets for female goat infertility. Full article
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Review

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21 pages, 28704 KiB  
Review
Zona Pellucida Genes and Proteins: Essential Players in Mammalian Oogenesis and Fertility
by Paul M. Wassarman and Eveline S. Litscher
Genes 2021, 12(8), 1266; https://doi.org/10.3390/genes12081266 - 19 Aug 2021
Cited by 23 | Viewed by 8841
Abstract
All mammalian oocytes and eggs are surrounded by a relatively thick extracellular matrix (ECM), the zona pellucida (ZP), that plays vital roles during oogenesis, fertilization, and preimplantation development. Unlike ECM surrounding somatic cells, the ZP is composed of only a few glycosylated proteins, [...] Read more.
All mammalian oocytes and eggs are surrounded by a relatively thick extracellular matrix (ECM), the zona pellucida (ZP), that plays vital roles during oogenesis, fertilization, and preimplantation development. Unlike ECM surrounding somatic cells, the ZP is composed of only a few glycosylated proteins, ZP1–4, that are unique to oocytes and eggs. ZP1–4 have a large region of polypeptide, the ZP domain (ZPD), consisting of two subdomains, ZP-N and ZP-C, separated by a short linker region, that plays an essential role in polymerization of nascent ZP proteins into crosslinked fibrils. Both subdomains adopt immunoglobulin (Ig)-like folds for their 3-dimensional structure. Mouse and human ZP genes are encoded by single-copy genes located on different chromosomes and are highly expressed in the ovary by growing oocytes during late stages of oogenesis. Genes encoding ZP proteins are conserved among mammals, and their expression is regulated by cis-acting sequences located close to the transcription start-site and by the same/similar trans-acting factors. Nascent ZP proteins are synthesized, packaged into vesicles, secreted into the extracellular space, and assembled into long, crosslinked fibrils that have a structural repeat, a ZP2-ZP3 dimer, and constitute the ZP matrix. Fibrils are oriented differently with respect to the oolemma in the inner and outer layers of the ZP. Sequence elements in the ZPD and the carboxy-terminal propeptide of ZP1–4 regulate secretion and assembly of nascent ZP proteins. The presence of both ZP2 and ZP3 is required to assemble ZP fibrils and ZP1 and ZP4 are used to crosslink the fibrils. Inactivation of mouse ZP genes by gene targeting has a detrimental effect on ZP formation around growing oocytes and female fertility. Gene sequence variations in human ZP genes due to point, missense, or frameshift mutations also have a detrimental effect on ZP formation and female fertility. The latter mutations provide additional support for the role of ZPD subdomains and other regions of ZP polypeptide in polymerization of human ZP proteins into fibrils and matrix. Full article
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13 pages, 2522 KiB  
Review
The Crazy Ovary
by Philippe Monget, Ken McNatty and Danielle Monniaux
Genes 2021, 12(6), 928; https://doi.org/10.3390/genes12060928 - 18 Jun 2021
Cited by 12 | Viewed by 4361
Abstract
From fetal life until senescence, the ovary is an extremely active tissue undergoing continuous structural and functional changes. These ever-changing events are best summarized by a quotation attributed to Plato when describing motion in space and time—‘nothing ever is but is always becoming…’. [...] Read more.
From fetal life until senescence, the ovary is an extremely active tissue undergoing continuous structural and functional changes. These ever-changing events are best summarized by a quotation attributed to Plato when describing motion in space and time—‘nothing ever is but is always becoming…’. With respect to the ovary, these changes include, at the beginning, the processes of follicular formation and thereafter those of follicular growth and atresia, steroidogenesis, oocyte maturation, and decisions relating to the number of mature oocytes that are ovulated for fertilization and the role of the corpus luteum. The aims of this review are to offer some examples of these complex and hitherto unknown processes. The ones herein have been elucidated from studies undertaken in vitro or from normal in vivo events, natural genetic mutations or after experimental inactivation of gene function. Specifically, this review offers insights concerning the initiation of follicular growth, pathologies relating to poly-ovular follicles, the consequences of premature loss of germ cells or oocytes loss, the roles of AMH (anti-Müllerian hormone) and BMP (bone morphogenetic protein) genes in regulating follicular growth and ovulation rate together with species differences in maintaining luteal function during pregnancy. Collectively, the evidence suggests that the oocyte is a key organizer of normal ovarian function. It has been shown to influence the phenotype of the adjacent somatic cells, the growth and maturation of the follicle, and to determine the ovulation rate. When germ cells or oocytes are lost prematurely, the ovary becomes disorganized and a wide range of pathologies may arise. Full article
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