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The Development, Differentiation, and Toxicity of Gametes
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The Development, Differentiation, and Toxicity of Gametes

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 2021) | Viewed by 64287

Special Issue Editor

Prof. Dr. Youngsok Choi

E-Mail Website
Guest Editor
Department of Stem Cell and Regenerative Biotechnology and Humanized Pig Center (SRC), Konkuk Institute of Technology, Konkuk University, Seoul 05029, Republic of Korea
Interests: apoptosis regulatory proteins; von Hippel Lindau protein; apoptosis; fertility preservation; ovulation induction; vitrification; synaptonemal complex; meiosis; chromosome pairing
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Germ cell development and differentiation is very important for maintaining and preserving fertility in both males and females. In recent years, infertility has been increasing due to various factors that cause the abnormal development and differentiation of germ cells. These include both genetic and environmental factors that result in toxicity. Identifying the exact factors leading to abnormal development and toxicity of germ cells over the lifespan is of great importance. This requires continued efforts, which will give us the better understanding necessary to overcome infertility related to germ cell development and differentiation. In this issue, we would like to invite potential researchers who are working toward revealing the causes of infertility, and solving the problem from various aspects such as the development, differentiation, and toxicity of germ cells.

Prof. Youngsok Choi
Guest Editor

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Keywords

  • germ cell development
  • germ cell differentiation
  • gonadotoxicity
  • environmental factor
  • cancer drug

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Published Papers (22 papers)

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Editorial

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4 pages, 183 KiB  
Editorial
The Development, Differentiation, and Toxicity in Reproduction
by Byeongseok Kim and Youngsok Choi
Int. J. Mol. Sci. 2022, 23(13), 7183; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23137183 - 28 Jun 2022
Viewed by 1070
Abstract
This Special Issue is intended to provide up-to-date information on reproduction, including the reproduction of germ cells and reproductive organs (ovary, testis, and uterus) [...] Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)

Research

Jump to: Editorial, Review

17 pages, 10226 KiB  
Article
Regulation and Function of Laminin A5 during Mouse and Human Decidualization
by Zhen-Shan Yang, Hai-Yang Pan, Wen-Wen Shi, Si-Ting Chen, Ying Wang, Meng-Yuan Li, Hai-Yi Zhang, Chen Yang, Ai-Xia Liu and Zeng-Ming Yang
Int. J. Mol. Sci. 2022, 23(1), 199; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23010199 - 24 Dec 2021
Cited by 6 | Viewed by 2799
Abstract
Decidualization is essential to the establishment of pregnancy in rodents and primates. Laminin A5 (encoding by Laminin α5) is a member of the laminin family, which is mainly expressed in the basement membranes. Although laminins regulate cellular phenotype maintenance, adhesion, migration, growth, [...] Read more.
Decidualization is essential to the establishment of pregnancy in rodents and primates. Laminin A5 (encoding by Laminin α5) is a member of the laminin family, which is mainly expressed in the basement membranes. Although laminins regulate cellular phenotype maintenance, adhesion, migration, growth, and differentiation, the expression, function, and regulation of laminin A5 during early pregnancy are still unknown. Therefore, we investigated the expression and role of laminin A5 during mouse and human decidualization. Laminin A5 is highly expressed in mouse decidua and artificially induced deciduoma. Laminin A5 is significantly increased under in vitro decidualization. Laminin A5 knockdown significantly inhibits the expression of Prl8a2, a marker for mouse decidualization. Progesterone stimulates the expression of laminin A5 in ovariectomized mouse uterus and cultured mouse stromal cells. We also show that progesterone regulates laminin A5 through the PKA-CREB-C/EBPβ pathway. Laminin A5 is also highly expressed in human pregnant decidua and cultured human endometrial stromal cells during in vitro decidualization. Laminin A5 knockdown by siRNA inhibits human in vitro decidualization. Collectively, our study reveals that laminin A5 may play a pivotal role during mouse and human decidualization via the PKA-CREB-C/EBPβ pathway. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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12 pages, 2885 KiB  
Article
Expression and Regulation of CD73 during the Estrous Cycle in Mouse Uterus
by Jihyun Lee, Haeun Park, Sohyeon Moon, Jeong-Tae Do, Kwonho Hong and Youngsok Choi
Int. J. Mol. Sci. 2021, 22(17), 9403; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22179403 - 30 Aug 2021
Cited by 6 | Viewed by 4063
Abstract
Cluster of differentiation 73 (CD73, also known as ecto-5′-nucleotidase) is an enzyme that converts AMP into adenosine. CD73 is a surface enzyme bound to the outside of the plasma membrane expressed in several cells and regulates immunity and inflammation. In particular, it is [...] Read more.
Cluster of differentiation 73 (CD73, also known as ecto-5′-nucleotidase) is an enzyme that converts AMP into adenosine. CD73 is a surface enzyme bound to the outside of the plasma membrane expressed in several cells and regulates immunity and inflammation. In particular, it is known to inhibit T cell-mediated immune responses. However, the regulation of CD73 expression by hormones in the uterus is not yet clearly known. In this study, we investigated the expression of CD73 in ovariectomized mice treated with estrogen or progesterone and its regulation in the mouse uterus during the estrous cycle. The level of CD73 expression was dynamically regulated in the uterus during the estrous cycle. CD73 protein expression was high in proestrus, estrus, and diestrus, whereas it was relatively low in the metestrus stage. Immunofluorescence revealed that CD73 was predominantly expressed in the cytoplasm of the luminal and glandular epithelium and the stroma of the endometrium. The expression of CD73 in ovariectomized mice was gradually increased by progesterone treatment. However, estrogen injection did not affect its expression. Moreover, CD73 expression was increased when estrogen and progesterone were co-administered and was inhibited by the pretreatment of the progesterone receptor antagonist RU486. These findings suggest that the expression of CD73 is dynamically regulated by estrogen and progesterone in the uterine environment, and that there may be a synergistic effect of estrogen and progesterone. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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14 pages, 4310 KiB  
Article
ZDHHC19 Is Dispensable for Spermatogenesis, but Is Essential for Sperm Functions in Mice
by Shuai Wang, Hongjie Qiao, Pengxiang Wang, Yuan Wang and Danian Qin
Int. J. Mol. Sci. 2021, 22(16), 8894; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22168894 - 18 Aug 2021
Cited by 9 | Viewed by 2326
Abstract
Spermatogenesis is a complicated process involving mitotically proliferating spermatogonial cells, meiotically dividing spermatocytes, and spermatid going through maturation into spermatozoa. The post-translational modifications of proteins play important roles in this biological process. S-palmitoylation is one type of protein modifications catalyzed by zinc [...] Read more.
Spermatogenesis is a complicated process involving mitotically proliferating spermatogonial cells, meiotically dividing spermatocytes, and spermatid going through maturation into spermatozoa. The post-translational modifications of proteins play important roles in this biological process. S-palmitoylation is one type of protein modifications catalyzed by zinc finger Asp-His-His-Cys (ZDHHC)-family palmitoyl S-acyltransferases. There are 23 mammalian ZDHHCs that have been identified in mouse. Among them, Zdhhc19 is highly expressed in adult testis. However, the in vivo function of Zdhhc19 in mouse spermatogenesis and fertility remains unknown. In this study, we knocked out the Zdhhc19 gene by generating a 2609 bp deletion from exon 3 to exon 6 in mice. No differences were found in testis morphology and testis/body weight ratios upon Zdhhc19 deletion. Spermatogenesis was not disrupted in Zdhhc19 knockout mice, in which properly developed TRA98+ germ cells, SYCP3+ spermatocytes, and TNP1+ spermatids/spermatozoa were detected in seminiferous tubules. Nevertheless, Zdhhc19 knockout mice were male infertile. Zdhhc19 deficient spermatozoa exhibited multiple defects including abnormal morphology of sperm tails and heads, decreased motility, and disturbed acrosome reaction. All of these led to the inability of Zdhhc19 mutant sperm to fertilize oocytes in IVF assays. Taken together, our results support the fact that Zdhhc19 is a testis enriched gene dispensable for spermatogenesis, but is essential for sperm functions in mice. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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14 pages, 2775 KiB  
Article
Identification and Characterization of the Most Common Genetic Variant Responsible for Acephalic Spermatozoa Syndrome in Men Originating from North Africa
by Caroline Cazin, Yasmine Boumerdassi, Guillaume Martinez, Selima Fourati Ben Mustapha, Marjorie Whitfield, Charles Coutton, Nicolas Thierry-Mieg, Pierre Di Pizio, Nathalie Rives, Christophe Arnoult, Aminata Touré, Pierre F. Ray, Raoudha Zouari, Christophe Sifer and Zine-Eddine Kherraf
Int. J. Mol. Sci. 2021, 22(4), 2187; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22042187 - 22 Feb 2021
Cited by 5 | Viewed by 2678
Abstract
Acephalic spermatozoa syndrome (ASS) is a rare but extremely severe type of teratozoospermia, defined by the presence of a majority of headless flagella and a minority of tail-less sperm heads in the ejaculate. Like the other severe monomorphic teratozoospermias, ASS has a strong [...] Read more.
Acephalic spermatozoa syndrome (ASS) is a rare but extremely severe type of teratozoospermia, defined by the presence of a majority of headless flagella and a minority of tail-less sperm heads in the ejaculate. Like the other severe monomorphic teratozoospermias, ASS has a strong genetic basis and is most often caused by bi-allelic variants in SUN5 (Sad1 and UNC84 domain-containing 5). Using whole exome sequencing (WES), we investigated a cohort of nine infertile subjects displaying ASS. These subjects were recruited in three centers located in France and Tunisia, but all originated from North Africa. Sperm from subjects carrying candidate genetic variants were subjected to immunofluorescence analysis and transmission electron microscopy. Moreover, fluorescent in situ hybridization (FISH) was performed on sperm nuclei to assess their chromosomal content. Variant filtering permitted us to identify the same SUN5 homozygous frameshift variant (c.211+1_211+2dup) in 7/9 individuals (78%). SUN5 encodes a protein localized on the posterior part of the nuclear envelope that is necessary for the attachment of the tail to the sperm head. Immunofluorescence assays performed on sperm cells from three mutated subjects revealed a total absence of SUN5, thus demonstrating the deleterious impact of the identified variant on protein expression. Transmission electron microscopy showed a conserved flagellar structure and a slightly decondensed chromatin. FISH did not highlight a higher rate of chromosome aneuploidy in spermatozoa from SUN5 patients compared to controls, indicating that intra-cytoplasmic sperm injection (ICSI) can be proposed for patients carrying the c.211+1_211+2dup variant. These results suggest that the identified SUN5 variant is the main cause of ASS in the North African population. Consequently, a simple and inexpensive genotyping of the 211+1_211+2dup variant could be beneficial for affected men of North African origin before resorting to more exhaustive genetic analyses. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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15 pages, 2928 KiB  
Article
Paternal Inheritance of Bisphenol A Cardiotoxic Effects: The Implications of Sperm Epigenome
by Marta Lombó and María Paz Herráez
Int. J. Mol. Sci. 2021, 22(4), 2125; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22042125 - 20 Feb 2021
Cited by 11 | Viewed by 2458
Abstract
Parental exposure to bisphenol A (BPA) has been linked to a greater incidence of congenital diseases. We have demonstrated that BPA induces in zebrafish males an increase in the acetylation of sperm histones that is transmitted to the blastomeres of the unexposed progeny. [...] Read more.
Parental exposure to bisphenol A (BPA) has been linked to a greater incidence of congenital diseases. We have demonstrated that BPA induces in zebrafish males an increase in the acetylation of sperm histones that is transmitted to the blastomeres of the unexposed progeny. This work is aimed to determine whether histone hyperacetylation promoted by paternal exposure to BPA is the molecular mechanism underlying the cardiogenesis impairment in the descendants. Zebrafish males were exposed to 100 and 2000 µg/L BPA during early spermatogenesis and mated with non-exposed females. We analyzed in the progeny the expression of genes involved in cardiogenesis and the epigenetic profile. Once the histone hyperacetylation was confirmed, treatment with epigallocatechin gallate (EGCG), an inhibitor of histone acetyltransferases, was assayed on F1 embryos. Embryos from males exposed to 2000 µg/L BPA overexpressed the transcription factor hand2 and the receptor esr2b, showing their own promoters—as well as that of kat6a—an enrichment in H3K9ac. In embryos treated with EGCG, both gene expression and histone acetylation (global and specific) returned to basal levels, and the phenotype was recovered. As shown by the results, the histone hyperacetylated landscape promoted by BPA in the sperm alters the chromatin structure of the progeny, leading to the overexpression of the histone acetyltransferase and genes involved in cardiogenesis. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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21 pages, 7223 KiB  
Article
New Gene Markers Expressed in Porcine Oviductal Epithelial Cells Cultured Primary In Vitro Are Involved in Ontological Groups Representing Physiological Processes of Porcine Oocytes
by Magdalena Kulus, Wiesława Kranc, Katarzyna Wojtanowicz-Markiewicz, Piotr Celichowski, Agata Światły-Błaszkiewicz, Eliza Matuszewska, Patrycja Sujka-Kordowska, Aneta Konwerska, Maciej Zdun, Rut Bryl, Maria Wieczorkiewicz, Jakub Kulus, Bogusława Stelmach, Katarzyna Stefańska, Joanna Budna-Tukan, James N. Petitte, Paul Mozdziak, Kornel Ratajczak, Jan Matysiak, Jędrzej M. Jaśkowski, Michał Nowicki and Bartosz Kempistyadd Show full author list remove Hide full author list
Int. J. Mol. Sci. 2021, 22(4), 2082; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22042082 - 19 Feb 2021
Cited by 1 | Viewed by 3034
Abstract
Changes that occur within oviducts after fertilization are dependent on post-ovulation events, including oocyte-oviduct interactions. Although general processes are well-defined, the molecular basis are poorly understood. Recently, new marker genes involved in ‘cell development’, ‘cell growth’, ‘cell differentiation’ and ‘cell maturation’ processes have [...] Read more.
Changes that occur within oviducts after fertilization are dependent on post-ovulation events, including oocyte-oviduct interactions. Although general processes are well-defined, the molecular basis are poorly understood. Recently, new marker genes involved in ‘cell development’, ‘cell growth’, ‘cell differentiation’ and ‘cell maturation’ processes have been identified in porcine oocytes. The aim of the study was to assess the expression profile of genes in primary in vitro cultured oviductal epithelial cells (OECs), clustered in Gene Ontology groups which enveloped markers also identified in porcine oocytes. OECs (from 45 gilts) were surgically removed and cultured in vitro for ≤ 30 days, and then subjected to molecular analyses. The transcriptomic and proteomic profiles of cells cultured during 7, 15 and 30 days were investigated. Additionally, morphological/histochemical analyzes were performed. The results of genes expression profiles were validated after using RT-qPCR. The results showed a significant upregulation of UNC45B, NOX4, VLDLR, ITGB3, FMOD, SGCE, COL1A2, LOX, LIPG, THY1 and downregulation of SERPINB2, CD274, TXNIP, CELA1, DDX60, CRABP2, SLC5A1, IDO1, ANPEP, FST. Detailed knowledge of the molecular pathways occurring in the OECs and the gametes that contact them may contribute both to developments of basic science of physiology, and new possibilities in advanced biotechnology of assisted reproduction. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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13 pages, 7331 KiB  
Article
The Expression Levels and Cellular Localization of Pigment Epithelium Derived Factor (PEDF) in Mouse Testis: Its Possible Involvement in the Differentiation of Spermatogonial Cells
by Noy Bagdadi, Alaa Sawaied, Ali AbuMadighem, Eitan Lunenfeld and Mahmoud Huleihel
Int. J. Mol. Sci. 2021, 22(3), 1147; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22031147 - 24 Jan 2021
Cited by 4 | Viewed by 2425
Abstract
Pigment epithelium derived factor (PEDF) is a multifunctional secretory soluble glycoprotein that belongs to the serine protease inhibitor (serpin) family. It was reported to have neurotrophic, anti-angiogenic and anti-tumorigenic activity. Recently, PEDF was found in testicular peritubular cells and it was assumed to [...] Read more.
Pigment epithelium derived factor (PEDF) is a multifunctional secretory soluble glycoprotein that belongs to the serine protease inhibitor (serpin) family. It was reported to have neurotrophic, anti-angiogenic and anti-tumorigenic activity. Recently, PEDF was found in testicular peritubular cells and it was assumed to be involved in the avascular nature of seminiferous tubules. The aim of this study was to determine the cellular origin, expression levels and target cells of PEDF in testicular tissue of immature and adult mice under physiological conditions, and to explore its possible role in the process of spermatogenesis in vitro. Using immunofluorescence staining, we showed that PEDF was localized in spermatogenic cells at different stages of development as well as in the somatic cells of the testis. Its protein levels in testicular homogenates and Sertoli cells supernatant showed a significant decrease with age. PEDF receptor (PEDF-R) was localized within the seminiferous tubule cells and in the interstitial cells compartment. Its RNA expression levels showed an increase with age until 8 weeks followed by a decrease. RNA levels of PEDF-R showed the opposite trend of the protein. Addition of PEDF to cultures of isolated cells from the seminiferous tubules did not changed their proliferation rate, however, a significant increase was observed in number of meiotic/post meiotic cells at 1000 ng/mL of PEDF; indicating an in vitro differentiation effect. This study may suggest a role for PEDF in the process of spermatogenesis. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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14 pages, 3519 KiB  
Article
Nonylphenol Induces Apoptosis through ROS/JNK Signaling in a Spermatogonia Cell Line
by Hyun-Jung Park, Ran Lee, Hyunjin Yoo, Kwonho Hong and Hyuk Song
Int. J. Mol. Sci. 2021, 22(1), 307; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22010307 - 30 Dec 2020
Cited by 18 | Viewed by 3571
Abstract
Nonylphenol (NP) is an endocrine-disruptor chemical that negatively affects reproductive health. Testes exposure to NP results in testicular structure disruption and a reduction in testicular size and testosterone levels. However, the effects of NP on spermatogonia in testes have not been fully elucidated. [...] Read more.
Nonylphenol (NP) is an endocrine-disruptor chemical that negatively affects reproductive health. Testes exposure to NP results in testicular structure disruption and a reduction in testicular size and testosterone levels. However, the effects of NP on spermatogonia in testes have not been fully elucidated. In this study, the molecular mechanisms of NP in GC-1 spermatogonia (spg) cells were investigated. We found that cell viability significantly decreased and apoptosis increased in a dose-dependent manner when GC-1 spg cells were exposed to NP. Furthermore, the expression levels of the pro-apoptotic proteins increased, whereas anti-apoptosis markers decreased in NP-exposed GC-1 spg cells. We also found that NP increased reactive oxygen species (ROS) generation, suggesting that ROS-induced activation of the MAPK signaling pathway is the molecular mechanism of NP-induced apoptosis in GC-1 spg cells. Thus, NP could induce c-Jun phosphorylation; dose-dependent expression of JNK, MKK4, p53, and p38; and the subsequent inhibition of ERK1/2 and MEK1/2 phosphorylation. The genes involved in apoptosis and JNK signaling were also upregulated in GC-1 spg cells treated with NP compared to those in the controls. Our findings suggest that NP induces apoptosis through ROS/JNK signaling in GC-1 spg cells. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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14 pages, 3005 KiB  
Article
Induction of Oxidative Stress and Mitochondrial Dysfunction by Juglone Affects the Development of Bovine Oocytes
by Ahmed Atef Mesalam, Marwa El-Sheikh, Myeong-Don Joo, Atif Ali Khan Khalil, Ayman Mesalam, Mi-Jeong Ahn and Il-Keun Kong
Int. J. Mol. Sci. 2021, 22(1), 168; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22010168 - 26 Dec 2020
Cited by 12 | Viewed by 2809
Abstract
Juglone, a major naphthalenedione component of walnut trees, has long been used in traditional medicine as an antimicrobial and antitumor agent. Nonetheless, its impact on oocyte and preimplantation embryo development has not been entirely clarified. Using the bovine model, we sought to elucidate [...] Read more.
Juglone, a major naphthalenedione component of walnut trees, has long been used in traditional medicine as an antimicrobial and antitumor agent. Nonetheless, its impact on oocyte and preimplantation embryo development has not been entirely clarified. Using the bovine model, we sought to elucidate the impact of juglone treatment during the in vitro maturation (IVM) of oocytes on their maturation and development of embryos. Results showed a severe reduction in oocyte nuclear maturation and cumulus expansion and a significant increase in mitochondrial dysfunction and reactive oxygen species (ROS) levels in cumulus–oocyte complexes (COCs) treated with juglone (12.5, 25.0, and 50.0 µM). In addition, RT–qPCR showed downregulation of the expansion-related (HAS2, TNFAIP6, PTX3, and PTGS2) and mitochondrial (ATPase6 and ATP5F1E) genes in juglone-treated COCs. Moreover, the development rates of day 4 total cleavage and 8–16 cell stage embryos, as well as day 8 blastocysts, were significantly reduced following exposure to juglone. Using immunofluorescence, the apoptotic marker caspase-9 was overexpressed in oocytes exposed to juglone (25.0 µM) compared to the untreated control. In conclusion, our study reports that exposing bovine oocytes to 12.5–50.0 µM of juglone can reduce their development through the direct induction of ROS accumulation, apoptosis, and mitochondrial dysfunction. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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18 pages, 3222 KiB  
Article
Gestational Exposure to Bisphenol A Affects Testicular Morphology, Germ Cell Associations, and Functions of Spermatogonial Stem Cells in Male Offspring
by Polash Chandra Karmakar, Jin Seop Ahn, Yong-Hee Kim, Sang-Eun Jung, Bang-Jin Kim, Hee-Seok Lee and Buom-Yong Ryu
Int. J. Mol. Sci. 2020, 21(22), 8644; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21228644 - 17 Nov 2020
Cited by 6 | Viewed by 1989
Abstract
Exposure to bisphenol A (BPA) in the gestational period damages the reproductive health of offspring; detailed evidence regarding BPA-induced damage in testicular germ cells of offspring is still limited. In this study, pregnant mice (F0) were gavaged with three BPA doses (50 μg, [...] Read more.
Exposure to bisphenol A (BPA) in the gestational period damages the reproductive health of offspring; detailed evidence regarding BPA-induced damage in testicular germ cells of offspring is still limited. In this study, pregnant mice (F0) were gavaged with three BPA doses (50 μg, 5 mg, and 50 mg/kg body weight (bw)/day; tolerable daily intake (TDI), no-observed-adverse-effect-level (NOAEL), and lowest-observed-adverse-effect level (LOAEL), respectively) on embryonic days 7 to 14, followed by investigation of the transgenerational effects of such exposure in male offspring. We observed that the NOAEL- and LOAEL-exposed F1 offspring had abnormalities in anogenital distance, nipple retention, and pubertal onset (days), together with differences in seminiferous epithelial stages and testis morphology. These effects were eradicated in the next F2 and F3 generations. Moreover, there was an alteration in the ratio of germ cell population and the apoptosis rate in germ cells increased in F1 offspring at the LOAEL dose. However, the total number of spermatogonia remained unchanged. Finally, a reduction in the stemness properties of spermatogonial stem cells in F1 offspring was observed upon LOAEL exposure. Therefore, we provide evidence of BPA-induced disruption of physiology and functions in male germ cells during the gestational period. This may lead to several reproductive health issues and infertility in offspring. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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13 pages, 1745 KiB  
Article
Identification of the Lineage Markers and Inhibition of DAB2 in In Vitro Fertilized Porcine Embryos
by Jong-Nam Oh, Mingyun Lee, Gyung Cheol Choe, Dong-Kyung Lee, Kwang-Hwan Choi, Seung-Hun Kim, Jinsol Jeong and Chang-Kyu Lee
Int. J. Mol. Sci. 2020, 21(19), 7275; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21197275 - 01 Oct 2020
Cited by 7 | Viewed by 2060
Abstract
Specification of embryonic lineages is an important question in the field of early development. Numerous studies analyzed the expression patterns of the candidate transcripts and proteins in humans and mice and clearly determined the markers of each lineage. To overcome the limitations of [...] Read more.
Specification of embryonic lineages is an important question in the field of early development. Numerous studies analyzed the expression patterns of the candidate transcripts and proteins in humans and mice and clearly determined the markers of each lineage. To overcome the limitations of human and mouse embryos, the expression of the marker transcripts in each cell has been investigated using in vivo embryos in pigs. In vitro produced embryos are more accessible, can be rapidly processed with low cost. Therefore, we analyzed the characteristics of lineage markers and the effects of the DAB2 gene (trophectoderm marker) in in vitro fertilized porcine embryos. We investigated the expression levels of the marker genes during embryonic stages and distribution of the marker proteins was assayed in day 7 blastocysts. Then, the shRNA vectors were injected into the fertilized embryos and the differences in the marker transcripts were analyzed. Marker transcripts showed diverse patterns of expression, and each embryonic lineage could be identified with localization of marker proteins. In DAB2-shRNA vectors injected embryos, HNF4A and PDGFRA were upregulated. DAB2 protein level was lower in shRNA-injected embryos without significant differences. Our results will contribute to understanding of the mechanisms of embryonic lineage specification in pigs. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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14 pages, 2555 KiB  
Article
Effect of Triclosan Exposure on Developmental Competence in Parthenogenetic Porcine Embryo during Preimplantation
by Min Ju Kim, Hyo-Jin Park, Sanghoon Lee, Hyo-Gu Kang, Pil-Soo Jeong, Soo Hyun Park, Young-Ho Park, Jong-Hee Lee, Kyung Seob Lim, Seung Hwan Lee, Bo-Woong Sim, Sun-Uk Kim, Seong-Keun Cho, Deog-Bon Koo and Bong-Seok Song
Int. J. Mol. Sci. 2020, 21(16), 5790; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21165790 - 12 Aug 2020
Cited by 13 | Viewed by 3100
Abstract
Triclosan (TCS) is included in various healthcare products because of its antimicrobial activity; therefore, many humans are exposed to TCS daily. While detrimental effects of TCS exposure have been reported in various species and cell types, the effects of TCS exposure on early [...] Read more.
Triclosan (TCS) is included in various healthcare products because of its antimicrobial activity; therefore, many humans are exposed to TCS daily. While detrimental effects of TCS exposure have been reported in various species and cell types, the effects of TCS exposure on early embryonic development are largely unknown. The aim of this study was to determine if TCS exerts toxic effects during early embryonic development using porcine parthenogenetic embryos in vitro. Porcine parthenogenetic embryos were cultured in in vitro culture medium with 50 or 100 µM TCS for 6 days. Developmental parameters including cleavage and blastocyst formation rates, developmental kinetics, and the number of blastomeres were assessed. To determine the toxic effects of TCS, apoptosis, oxidative stress, and mitochondrial dysfunction were assessed. TCS exposure resulted in a significant decrease in 2-cell rate and blastocyst formation rate, as well as number of blastomeres, but not in the cleavage rate. TCS also increased the number of apoptotic blastomeres and the production of reactive oxygen species. Finally, TCS treatment resulted in a diffuse distribution of mitochondria and decreased the mitochondrial membrane potential. Our results showed that TCS exposure impaired porcine early embryonic development by inducing DNA damage, oxidative stress, and mitochondrial dysfunction. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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16 pages, 5443 KiB  
Article
Paternal Exposure to Bisphenol-A Transgenerationally Impairs Testis Morphology, Germ Cell Associations, and Stemness Properties of Mouse Spermatogonial Stem Cells
by Polash Chandra Karmakar, Jin Seop Ahn, Yong-Hee Kim, Sang-Eun Jung, Bang-Jin Kim, Hee-Seok Lee, Sun-Uk Kim, Md Saidur Rahman, Myung-Geol Pang and Buom-Yong Ryu
Int. J. Mol. Sci. 2020, 21(15), 5408; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21155408 - 29 Jul 2020
Cited by 10 | Viewed by 2801
Abstract
Bisphenol-A (BPA) exposure in an adult male can affect the reproductive system, which may also adversely affect the next generation. However, there is a lack of comprehensive data on the BPA-induced disruption of the association and functional characteristics of the testicular germ cells, [...] Read more.
Bisphenol-A (BPA) exposure in an adult male can affect the reproductive system, which may also adversely affect the next generation. However, there is a lack of comprehensive data on the BPA-induced disruption of the association and functional characteristics of the testicular germ cells, which the present study sought to investigate. Adult male mice were administered BPA doses by gavage for six consecutive weeks and allowed to breed, producing generations F1–F4. Testis samples from each generation were evaluated for several parameters, including abnormal structure, alterations in germ cell proportions, apoptosis, and loss of functional properties of spermatogonial stem cells (SSCs). We observed that at the lowest-observed-adverse-effect level (LOAEL) dose, the testicular abnormalities and alterations in seminiferous epithelium staging persisted in F0–F2 generations, although a reduced total spermatogonia count was found only in F0. However, abnormalities in the proportions of germ cells were observed until F2. Exposure of the male mice (F0) to BPA alters the morphology of the testis along with the association of germ cells and stemness properties of SSCs, with the effects persisting up to F2. Therefore, we conclude that BPA induces physiological and functional disruption in male germ cells, which may lead to reproductive health issues in the next generation. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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16 pages, 3967 KiB  
Article
BRG1 Is Dispensable for Sertoli Cell Development and Functions in Mice
by Shuai Wang, Pengxiang Wang, Dongli Liang and Yuan Wang
Int. J. Mol. Sci. 2020, 21(12), 4358; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21124358 - 19 Jun 2020
Cited by 5 | Viewed by 2676
Abstract
Sertoli cells are somatic supporting cells in spermatogenic niche and play critical roles in germ cell development, but it is yet to be understood how epigenetic modifiers regulate Sertoli cell development and contribution to spermatogenesis. BRG1 (Brahma related gene 1) is a catalytic [...] Read more.
Sertoli cells are somatic supporting cells in spermatogenic niche and play critical roles in germ cell development, but it is yet to be understood how epigenetic modifiers regulate Sertoli cell development and contribution to spermatogenesis. BRG1 (Brahma related gene 1) is a catalytic subunit of the mammalian SWI/SNF chromatin remodeling complex and participates in transcriptional regulation. The present study aimed to define the functions of BRG1 in mouse Sertoli cells during mouse spermatogenesis. We found that BRG1 protein was localized in the nuclei of both Sertoli cells and germ cells in seminiferous tubules. We further examined the requirement of BRG1 in Sertoli cell development using a Brg1 conditional knockout mouse model and two Amh-Cre mouse strains to specifically delete Brg1 gene from Sertoli cells. We found that the Amh-Cre mice from Jackson Laboratory had inefficient recombinase activities in Sertoli cells, while the other Amh-Cre strain from the European Mouse Mutant Archive achieved complete Brg1 deletion in Sertoli cells. Nevertheless, the conditional knockout of Brg1 from Sertoli cells by neither of Amh-Cre strains led to any detectable abnormalities in the development of either Sertoli cells or germ cells, suggesting that BRG1-SWI/SNF complex is dispensable to the functions of Sertoli cells in spermatogenesis. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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13 pages, 2284 KiB  
Article
Butylparaben Is Toxic to Porcine Oocyte Maturation and Subsequent Embryonic Development Following In Vitro Fertilization
by Pil-Soo Jeong, Sanghoon Lee, Soo-Hyun Park, Min Ju Kim, Hyo-Gu Kang, Tsevelmaa Nanjidsuren, Hee-Chang Son, Bong-Seok Song, Deog-Bon Koo, Bo-Woong Sim and Sun-Uk Kim
Int. J. Mol. Sci. 2020, 21(10), 3692; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21103692 - 24 May 2020
Cited by 23 | Viewed by 3941
Abstract
Parabens are widely used in personal care products due to their antimicrobial effects. Although the toxicity of parabens has been reported, little information is available on the toxicity of butylparaben (BP) on oocyte maturation. Therefore, we investigated the effects of various concentrations of [...] Read more.
Parabens are widely used in personal care products due to their antimicrobial effects. Although the toxicity of parabens has been reported, little information is available on the toxicity of butylparaben (BP) on oocyte maturation. Therefore, we investigated the effects of various concentrations of BP (0 μM, 100 μM, 200 μM, 300 μM, 400 μM, and 500 μM) on the in vitro maturation of porcine oocytes. BP supplementation at a concentration greater than 300 μM significantly reduced the proportion of complete cumulus cell expansion and metaphase II oocytes compared to the control. The 300 μM BP significantly decreased fertilization, cleavage, and blastocyst formation rates with lower total cell numbers and a higher rate of apoptosis in blastocysts compared to the control. The BP-treated oocytes showed significantly higher reactive oxygen species (ROS) levels, and lower glutathione (GSH) levels than the control. BP significantly increased the aberrant mitochondrial distribution and decreased mitochondrial function compared to the control. BP-treated oocytes exhibited significantly higher percentage of γ-H2AX, annexin V-positive oocytes and expression of LC3 than the control. In conclusion, we demonstrated that BP impaired oocyte maturation and subsequent embryonic development, by inducing ROS generation and reducing GSH levels. Furthermore, BP disrupted mitochondrial function and triggered DNA damage, early apoptosis, and autophagy in oocytes. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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15 pages, 1815 KiB  
Article
Toxic Effects of Nonylphenol on Neonatal Testicular Development in Mouse Organ Culture
by Hyun-Jung Park, Mingtian Zhang, Won-Young Lee, Kwon-Ho Hong, Jeong Tae Do, Chankyu Park and Hyuk Song
Int. J. Mol. Sci. 2020, 21(10), 3491; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21103491 - 15 May 2020
Cited by 19 | Viewed by 3196
Abstract
Nonylphenol (NP) is an alkylphenol that is widely used in chemical manufacturing. Exposure to this toxic environmental contaminant has been shown to negatively affect the reproductive system. Herein, we evaluated the toxicity of NP in mouse testes, while using in vitro organ culture. [...] Read more.
Nonylphenol (NP) is an alkylphenol that is widely used in chemical manufacturing. Exposure to this toxic environmental contaminant has been shown to negatively affect the reproductive system. Herein, we evaluated the toxicity of NP in mouse testes, while using in vitro organ culture. Mouse testicular fragments (MTFs), derived from five-day postpartum neonatal mouse testes, were exposed to different concentrations of NP (1–50 μM) for 30 days. The results showed that NP impaired germ cell development and maintenance. Furthermore, NP significantly downregulated the transcript levels of both undifferentiated and differentiated germ cell marker genes relative to those in controls. In particular, a high dose of NP (50 µM) led to complete germ cell depletion and resulted in spermatogenic failure, despite the presence of Sertoli and Leydig cells. In addition, the mRNA expression of steroidogenic enzymes, such as steroidogenic acute regulatory protein (STAR), Cytochrome P450 Family 11 Subfamily A Member 1 (Cyp11α1), Cytochrome P450 17A1 (Cyp17α1), and androgen receptor (AR), increased with increasing concentration of NP. Conversely, the expression of estrogen receptor alpha (ESR1) and Cytochrome P450 family 19 subfamily A member 1 (Cyp19α1) in NP-exposed MTFs decreased when compared to that of the control. Taken together, this study demonstrates that NP has a negative effect on prepubertal spermatogenesis and germ cell maintenance and it disrupts steroidogenesis and induces hormonal imbalance in MTFs. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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13 pages, 4551 KiB  
Article
Peroxisome Proliferator-Activated Receptor Gamma Modulator Promotes Neonatal Mouse Primordial Follicle Activation In Vitro
by Sook Young Yoon, Ran Kim, Hyunmee Jang, Dong Hyuk Shin, Jin Il Lee, Dongwon Seol, Dong Ryul Lee, Eun Mi Chang and Woo Sik Lee
Int. J. Mol. Sci. 2020, 21(9), 3120; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21093120 - 28 Apr 2020
Cited by 13 | Viewed by 3110
Abstract
Peroxisome proliferator-activated receptor gamma (PPARγ) is known as a regulator of cellular functions, including adipogenesis and immune cell activation. The objectives of this study were to investigate the expression of PPARγ and identify the mechanism of primordial follicle activation via PPARγ modulators in [...] Read more.
Peroxisome proliferator-activated receptor gamma (PPARγ) is known as a regulator of cellular functions, including adipogenesis and immune cell activation. The objectives of this study were to investigate the expression of PPARγ and identify the mechanism of primordial follicle activation via PPARγ modulators in mouse ovaries. We first measured the gene expression of PPARγ and determined its relationship with phosphatase and tensin homolog (PTEN), protein kinase B (AKT1), and forkhead box O3a (FOXO3a) expression in neonatal mouse ovaries. We then incubated neonatal mouse ovaries with PPARγ modulators, including rosiglitazone (a synthetic agonist of PPARγ), GW9662 (a synthetic antagonist of PPARγ), and cyclic phosphatidic acid (cPA, a physiological inhibitor of PPARγ), followed by transplantation into adult ovariectomized mice. After the maturation of the transplanted ovaries, primordial follicle growth activation, follicle growth, and embryonic development were evaluated. Finally, the delivery of live pups after embryo transfer into recipient mice was assessed. While PPARγ was expressed in ovaries from mice of all ages, its levels were significantly increased in ovaries from 20-day-old mice. In GW9662-treated ovaries in vitro, PTEN levels were decreased, AKT was activated, and FOXO3a was excluded from the nuclei of primordial follicles. After 1 month, cPA-pretreated, transplanted ovaries produced the highest numbers of oocytes and polar bodies, exhibited the most advanced embryonic development, and had the greatest blastocyst formation rate compared to the rosiglitazone- and GW9662-pretreated groups. Additionally, the successful delivery of live pups after embryo transfer into the recipient mice transplanted with cPA-pretreated ovaries was confirmed. Our study demonstrates that PPARγ participates in primordial follicle activation and development, possibly mediated in part by the PI3K/AKT signaling pathway. Although more studies are required, adapting these findings for the activation of human primordial follicles may lead to treatments for infertility that originates from poor ovarian reserves. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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17 pages, 3794 KiB  
Article
Exposure of Triclosan in Porcine Oocyte Leads to Superoxide Production and Mitochondrial-Mediated Apoptosis during In Vitro Maturation
by Hyo-Jin Park, Bong-Seok Song, Jin-Woo Kim, Seul-Gi Yang, Sun-Uk Kim and Deog-Bon Koo
Int. J. Mol. Sci. 2020, 21(9), 3050; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms21093050 - 26 Apr 2020
Cited by 9 | Viewed by 3151
Abstract
While triclosan (TCS) exerts detrimental effects on female reproduction, the effect of TCS-derived toxins on porcine oocytes during in vitro maturation (IVM) is unclear. This study investigated the effects of TCS on mitochondrion-derived reactive oxygen species (ROS) production and apoptosis pathways during porcine [...] Read more.
While triclosan (TCS) exerts detrimental effects on female reproduction, the effect of TCS-derived toxins on porcine oocytes during in vitro maturation (IVM) is unclear. This study investigated the effects of TCS on mitochondrion-derived reactive oxygen species (ROS) production and apoptosis pathways during porcine oocyte maturation. Porcine oocytes were treated with TCS (1, 10, and 100 μM) and triphenylphosphonium chloride (Mito-TEMPO; 0.1 μM), and matured cumulus oocyte complexes (COCs) were stained with orcein, dichlorofluorescein diacetate (DCF-DA), and Mito-SOX. Proteins and mRNA levels of factors related to cumulus expansion and mitochondrion-mediated apoptosis and antioxidant enzymes were analyzed by western blotting and reverse-transcription polymerase chain reaction (RT-PCR), respectively. Meiotic maturation and cumulus cell expansion significantly decreased for COCs after TCS treatment along with an increase in mitochondrial superoxide levels at 44 h of IVM. Further, mitochondrion-related antioxidant enzymes and apoptosis markers were significantly elevated in porcine COCs following TCS-mediated oxidative damage. The protective effect of Mito-TEMPO as a specific superoxide scavenger from TCS toxin improved the maturation capacity of porcine COCs. Mito-TEMPO downregulated the mitochondrial apoptosis of TCS-exposed porcine COCs by reducing superoxide level. In conclusion, our data demonstrate that TCS mediates toxicity during porcine oocyte maturation through superoxide production and mitochondrion-mediated apoptosis. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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Review

Jump to: Editorial, Research

16 pages, 2160 KiB  
Review
Hippo Signaling in the Endometrium
by Sohyeon Moon, Semi Hwang, Byeongseok Kim, Siyoung Lee, Hyoukjung Kim, Giwan Lee, Kwonho Hong, Hyuk Song and Youngsok Choi
Int. J. Mol. Sci. 2022, 23(7), 3852; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms23073852 - 31 Mar 2022
Cited by 7 | Viewed by 3017
Abstract
The uterus is essential for embryo implantation and fetal development. During the estrous cycle, the uterine endometrium undergoes dramatic remodeling to prepare for pregnancy. Angiogenesis is an essential biological process in endometrial remodeling. Steroid hormones regulate the series of events that occur during [...] Read more.
The uterus is essential for embryo implantation and fetal development. During the estrous cycle, the uterine endometrium undergoes dramatic remodeling to prepare for pregnancy. Angiogenesis is an essential biological process in endometrial remodeling. Steroid hormones regulate the series of events that occur during such remodeling. Researchers have investigated the potential factors, including angiofactors, involved in endometrial remodeling. The Hippo signaling pathway discovered in the 21st century, plays important roles in various cellular functions, including cell proliferation and cell death. However, its role in the endometrium remains unclear. In this review, we describe the female reproductive system and its association with the Hippo signaling pathway, as well as novel Hippo pathway genes and potential target genes. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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12 pages, 3046 KiB  
Review
DAXX Is a Crucial Factor for Proper Development of Mammalian Oocytes and Early Embryos
by Irina Bogolyubova and Dmitry Bogolyubov
Int. J. Mol. Sci. 2021, 22(3), 1313; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22031313 - 28 Jan 2021
Cited by 7 | Viewed by 2855
Abstract
The Death-domain associated protein 6 (DAXX) is an evolutionarily conserved and ubiquitously expressed multifunctional protein that is implicated in many cellular processes, including transcription, cellular proliferation, cell cycle regulation, Fas-induced apoptosis, and many other events. In the nucleus, DAXX interacts with transcription factors, [...] Read more.
The Death-domain associated protein 6 (DAXX) is an evolutionarily conserved and ubiquitously expressed multifunctional protein that is implicated in many cellular processes, including transcription, cellular proliferation, cell cycle regulation, Fas-induced apoptosis, and many other events. In the nucleus, DAXX interacts with transcription factors, epigenetic modifiers, and chromatin-remodeling proteins such as the transcription regulator ATRX—the α-thalassemia/mental retardation syndrome X-linked ATP-dependent helicase II. Accordingly, DAXX is considered one of the main players involved in chromatin silencing and one of the most important factors that maintain integrity of the genome. In this brief review, we summarize available data regarding the general and specific functions of DAXX in mammalian early development, with special emphasis on the function of DAXX as a chaperone of the histone variant H3.3. Since H3.3 plays a key role in the developmental processes, especially in the pronounced rearrangements of heterochromatin compartment during oogenesis and embryogenesis, DAXX can be considered as an important factor supporting proper development. Specifically, loss of DAXX affects the recruitment of ATRX, transcription of tandem repeats and telomere functions, which results in a decrease in the viability of early embryos. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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16 pages, 1609 KiB  
Review
Insights from the Applications of Single-Cell Transcriptomic Analysis in Germ Cell Development and Reproductive Medicine
by Hyeonwoo La, Hyunjin Yoo, Eun Joo Lee, Nguyen Xuan Thang, Hee Jin Choi, Jeongheon Oh, Ji Hyun Park and Kwonho Hong
Int. J. Mol. Sci. 2021, 22(2), 823; https://0-doi-org.brum.beds.ac.uk/10.3390/ijms22020823 - 15 Jan 2021
Cited by 14 | Viewed by 3803
Abstract
Mechanistic understanding of germ cell formation at a genome-scale level can aid in developing novel therapeutic strategies for infertility. Germ cell formation is a complex process that is regulated by various mechanisms, including epigenetic regulation, germ cell-specific gene transcription, and meiosis. Gonads contain [...] Read more.
Mechanistic understanding of germ cell formation at a genome-scale level can aid in developing novel therapeutic strategies for infertility. Germ cell formation is a complex process that is regulated by various mechanisms, including epigenetic regulation, germ cell-specific gene transcription, and meiosis. Gonads contain a limited number of germ cells at various stages of differentiation. Hence, genome-scale analysis of germ cells at the single-cell level is challenging. Conventional genome-scale approaches cannot delineate the landscape of genomic, transcriptomic, and epigenomic diversity or heterogeneity in the differentiating germ cells of gonads. Recent advances in single-cell genomic techniques along with single-cell isolation methods, such as microfluidics and fluorescence-activated cell sorting, have helped elucidate the mechanisms underlying germ cell development and reproductive disorders in humans. In this review, the history of single-cell transcriptomic analysis and their technical advantages over the conventional methods have been discussed. Additionally, recent applications of single-cell transcriptomic analysis for analyzing germ cells have been summarized. Full article
(This article belongs to the Special Issue The Development, Differentiation, and Toxicity of Gametes)
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