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Nature Communications Aug 2023The piRNA pathway is essential for female fertility in golden hamsters and likely humans, but not in mice. However, the role of individual PIWIs in mammalian...
The piRNA pathway is essential for female fertility in golden hamsters and likely humans, but not in mice. However, the role of individual PIWIs in mammalian reproduction remains poorly understood outside of mice. Here, we describe the expression profiles, subcellular localization, and knockout-associated reproductive defects for all four PIWIs in golden hamsters. In female golden hamsters, PIWIL1 and PIWIL3 are highly expressed throughout oogenesis and early embryogenesis, while knockout of PIWIL1 leads to sterility, and PIWIL3 deficiency results in subfertility with lagging zygotic development. PIWIL1 can partially compensate for TE silencing in PIWIL3 knockout females, but not vice versa. PIWIL1 and PIWIL4 are the predominant PIWIs expressed in adult and postnatal testes, respectively, while PIWIL2 is present at both stages. Loss of any PIWI expressed in testes leads to sterility and severe but distinct spermatogenesis disorders. These findings illustrate the non-redundant regulatory functions of PIWI-piRNAs in gametogenesis and early embryogenesis in golden hamsters, facilitating study of their role in human fertility.
Topics: Adult; Cricetinae; Humans; Male; Female; Animals; Mice; Mesocricetus; Gametogenesis; Oogenesis; Spermatogenesis; Craniocerebral Trauma; Infertility; Piwi-Interacting RNA; Argonaute Proteins
PubMed: 37644029
DOI: 10.1038/s41467-023-40650-x -
Sexual Development : Genetics,... 2023The nematode, Caenorhabditis elegans has proven itself as a valuable model for investigating metazoan biology. C. elegans have a transparent body, an invariant cell... (Review)
Review
BACKGROUND
The nematode, Caenorhabditis elegans has proven itself as a valuable model for investigating metazoan biology. C. elegans have a transparent body, an invariant cell lineage, and a high level of genetic conservation which makes it a desirable model organism. Although used to elucidate many aspects of somatic biology, a distinct advantage of C. elegans is its well annotated germline which allows all aspects of oogenesis to be observed in real time within a single animal. C. elegans hermaphrodites have two U-shaped gonad arms which produce their own sperm that is later stored to fertilise their own oocytes. These two germlines take up much of the internal space of each animal and germ cells are therefore the most abundant cell present within each animal. This feature and the genetic phenotypes observed for mutant worm gonads have allowed many novel findings that established our early understanding of germ cell dynamics. The mutant phenotypes also allowed key features of meiosis and germ cell maturation to be unveiled.
SUMMARY
This review will focus on the key aspects that make C. elegans an outstanding model for exploring each feature of oogenesis. This will include the fundamental steps associated with germline function and germ cell maturation and will be of use for those interested in exploring reproductive metazoan biology.
KEY MESSAGES
Since germ cell biology is highly conserved in animals, much can be gained from study of a simple metazoan like C. elegans. Past findings have enhanced understanding on topics that would be more laborious or challenging in more complex animal models.
Topics: Animals; Male; Caenorhabditis elegans; Caenorhabditis elegans Proteins; Semen; Oogenesis; Oocytes; Germ Cells
PubMed: 37232019
DOI: 10.1159/000531019 -
Seminars in Cell & Developmental Biology Dec 2018The transition from oocyte to embryo marks the onset of development. This process requires complex regulation to link developmental signals with profound changes in mRNA... (Review)
Review
The transition from oocyte to embryo marks the onset of development. This process requires complex regulation to link developmental signals with profound changes in mRNA translation, cell cycle control, and metabolism. This control is beginning to be understood for most organisms, and research in the fruit fly Drosophila melanogaster has generated new insights. Recent findings have increased our understanding of the roles played by hormone and Ca signaling events as well as metabolic remodeling crucial for this transition. Specialized features of the structure and assembly of the meiotic spindle have been identified. The changes in protein levels, mRNA translation, and polyadenylation that occur as the oocyte becomes an embryo have been identified together with key aspects of their regulation. Here we highlight these important developments and the insights they provide on the intricate regulation of this dramatic transition.
Topics: Animals; Drosophila; Embryo, Mammalian; Embryonic Development; Humans; Meiosis; Oocytes; Oogenesis; Protein Biosynthesis
PubMed: 29448071
DOI: 10.1016/j.semcdb.2018.02.019 -
Biology of Reproduction Feb 2022In vitro follicle development (IVFD) is an adequate model to obtain basic knowledge of folliculogenesis and provides a tool for ovarian toxicity screening. IVFD yielding... (Review)
Review
In vitro follicle development (IVFD) is an adequate model to obtain basic knowledge of folliculogenesis and provides a tool for ovarian toxicity screening. IVFD yielding competent oocytes may also offer an option for fertility and species preservation. To promote follicle growth and oocyte maturation in vitro, various culture systems are utilized for IVFD in rodents, domestic animals, wild animals, nonhuman primates, and humans. Follicle culture conditions have been improved by optimizing gonadotropin levels, regulatory factors, nutrient supplements, oxygen concentration, and culture matrices. This review summarizes quality assessment of oocytes generated from in vitro-developed antral follicles from the preantral stage, including oocyte epigenetic and genetic profile, cytoplasmic and nuclear maturation, preimplantation embryonic development following in vitro fertilization, as well as pregnancy and live offspring after embryo transfer. The limitations of oocyte quality evaluation following IVFD and the gaps in our knowledge of IVFD to support proper oocyte development are also discussed. The information may advance our understanding of the requirements for IVFD, with a goal of producing competent oocytes with genetic integrity to sustain embryonic development resulting in healthy offspring.
Topics: Animals; Embryonic Development; Female; Fertilization in Vitro; Oocytes; Oogenesis; Ovarian Follicle; Pregnancy
PubMed: 34962509
DOI: 10.1093/biolre/ioab242 -
Biology of Reproduction Nov 2022Oogenesis and folliculogenesis are considered as complex and species-specific cellular differentiation processes, which depend on the in vivo ovarian follicular... (Review)
Review
Oogenesis and folliculogenesis are considered as complex and species-specific cellular differentiation processes, which depend on the in vivo ovarian follicular environment and endocrine cues. Considerable efforts have been devoted to driving the differentiation of female primordial germ cells toward mature oocytes outside of the body. The recent experimental attempts have laid stress on offering a suitable microenvironment to assist the in vitro folliculogenesis and oogenesis. Despite developing a variety of bioengineering techniques and generating functional mature gametes through in vitro oogenesis in earlier studies, we still lack knowledge of appropriate microenvironment conditions for building biomimetic culture systems for female fertility preservation. Therefore, this review paper can provide a source for a large body of scientists developing cutting-edge in vitro culture systems for female germ cells or setting up the next generation of reproductive medicine as feasible options for female infertility treatment. The focal point of this review outlines advanced bioengineering technologies such as 3D biofabricated hydrogels/scaffolds and microfluidic systems utilized with female germlines for fertility preservation through in vitro folliculogenesis and oogenesis.
Topics: Female; Animals; Ovarian Follicle; Oogenesis; Fertility; Germ Cells; Bioengineering; Oocytes
PubMed: 35947985
DOI: 10.1093/biolre/ioac160 -
Cellular and Molecular Life Sciences :... Aug 2023Controlled mRNA storage and stability is essential for oocyte meiosis and early embryonic development. However, how to regulate mRNA storage and stability in mammalian...
Controlled mRNA storage and stability is essential for oocyte meiosis and early embryonic development. However, how to regulate mRNA storage and stability in mammalian oogenesis remains elusive. Here we showed that LSM14B, a component of membraneless compartments including P-body-like granules and mitochondria-associated ribonucleoprotein domain (MARDO) in germ cell, is indispensable for female fertility. To reveal loss of LSM14B disrupted primordial follicle assembly and caused mRNA reduction in non-growing oocytes, which was concomitant with the impaired assembly of P-body-like granules. 10× Genomics single-cell RNA-sequencing and immunostaining were performed. Meanwhile, we conducted RNA-seq analysis of GV-stage oocytes and found that Lsm14b deficiency not only impaired the maternal mRNA accumulation but also disrupted the translation in fully grown oocytes, which was closely associated with dissolution of MARDO components. Moreover, Lsm14b-deficient oocytes reassembled a pronucleus containing decondensed chromatin after extrusion of the first polar body, through compromising the activation of maturation promoting factor, while the defects were restored via WEE1/2 inhibitor. Together, our findings reveal that Lsm14b plays a pivotal role in mammalian oogenesis by specifically controlling of oocyte mRNA storage and stability.
Topics: Animals; Female; RNA, Messenger; Oocytes; Oogenesis; Ovarian Follicle; Meiosis; Fertility; Mammals
PubMed: 37578641
DOI: 10.1007/s00018-023-04898-2 -
Biology of Reproduction Apr 2021Oocyte mitochondria are unique organelles that establish a founder population in primordial germ cells (PGCs). As the oocyte matures in the postnatal mammalian ovary... (Review)
Review
Oocyte mitochondria are unique organelles that establish a founder population in primordial germ cells (PGCs). As the oocyte matures in the postnatal mammalian ovary during folliculogenesis it increases exponentially in volume, and the oocyte mitochondria population proliferates to about 100 000 mitochondria per healthy, mature murine oocyte. The health of the mature oocyte and subsequent embryo is highly dependent on the oocyte mitochondria. Mitochondria are especially sensitive to toxic insults, as they are a major source of reactive oxygen species (ROS), they contain their own DNA (mtDNA) that is unprotected by histone proteins, they contain the electron transport chain that uses electron donors, including oxygen, to generate ATP, and they are important sensors for overall cellular stress. Here we review the effects that toxic insults including chemotherapeutics, toxic metals, plasticizers, pesticides, polycyclic aromatic hydrocarbons (PAHs), and ionizing radiation can have on oocyte mitochondria. This is very clearly a burgeoning field, as our understanding of oocyte mitochondria and metabolism is still relatively new, and we contend much more research is needed to understand the detrimental impacts of exposure to toxicants on oocyte mitochondria. Developing this field further can benefit our understanding of assisted reproductive technologies and the developmental origins of health and disease (DOHaD).
Topics: Animals; Antineoplastic Agents; DNA, Mitochondrial; Drug-Related Side Effects and Adverse Reactions; Environmental Pollutants; Female; Humans; Mammals; Mitochondria; Oocytes; Oogenesis; Oxidative Stress; Pharmaceutical Preparations
PubMed: 33412584
DOI: 10.1093/biolre/ioab002 -
ELife Nov 2022Recent studies show that pre-follicular mouse oogenesis takes place in germline cysts, highly conserved groups of oogonial cells connected by intercellular bridges that...
Recent studies show that pre-follicular mouse oogenesis takes place in germline cysts, highly conserved groups of oogonial cells connected by intercellular bridges that develop as nurse cells as well as an oocyte. Long studied in and insect gametogenesis, female germline cysts acquire cytoskeletal polarity and traffic centrosomes and organelles between nurse cells and the oocyte to form the Balbiani body, a conserved marker of polarity. Mouse oocyte development and nurse cell dumping are supported by dynamic, cell-specific programs of germline gene expression. High levels of perinatal germ cell death in this species primarily result from programmed nurse cell turnover after transfer rather than defective oocyte production. The striking evolutionary conservation of early oogenesis mechanisms between distant animal groups strongly suggests that gametogenesis and early embryonic development in vertebrates and invertebrates share even more in common than currently believed.
Topics: Female; Pregnancy; Mice; Animals; Drosophila; Oogenesis; Germ Cells; Oocytes; Gametogenesis
PubMed: 36445738
DOI: 10.7554/eLife.83230 -
Cells Jan 2022SCF-dependent proteolysis was first discovered via genetic screening of budding yeast almost 25 years ago. In recent years, more and more functions of SCF (Skp1-Cullin... (Review)
Review
SCF-dependent proteolysis was first discovered via genetic screening of budding yeast almost 25 years ago. In recent years, more and more functions of SCF (Skp1-Cullin 1-F-box) ligases have been described, and we can expect the number of studies on this topic to increase. SCF ligases, which are E3 ubiquitin multi-protein enzymes, catalyse protein ubiquitination and thus allow protein degradation mediated by the 26S proteasome. They play a crucial role in the degradation of cell cycle regulators, regulation of the DNA repair and centrosome cycle and play an important role in several diseases. SCF ligases seem to be needed during all phases of development, from oocyte formation through fertilization, activation of the embryonic genome to embryo implantation. In this review, we summarize known data on SCF ligase-mediated degradation during oogenesis and embryogenesis. In particular, SCF and SCF are among the most important and best researched ligases during early development. SCF is crucial for the oogenesis of and mouse and also in and embryogenesis. SCF participates in the degradation of several RNA-binding proteins and thereby affects the regulation of gene expression during the meiosis of . Nevertheless, a large number of SCF ligases that are primarily involved in embryogenesis remain to be elucidated.
Topics: Animals; Embryonic Development; Models, Biological; Oocytes; Oogenesis; SKP Cullin F-Box Protein Ligases; Substrate Specificity
PubMed: 35053348
DOI: 10.3390/cells11020234 -
Asian Journal of Andrology 2015Germ cells are the precursors of the sperm and oocytes and hence are critical for survival of the species. In mammals, they are specified during fetal life, migrate to... (Comparative Study)
Comparative Study Review
Germ cells are the precursors of the sperm and oocytes and hence are critical for survival of the species. In mammals, they are specified during fetal life, migrate to the developing gonads and then undergo a critical period during which they are instructed, by the soma, to adopt the appropriate sexual fate. In a fetal ovary, germ cells enter meiosis and commit to oogenesis, whereas in a fetal testis, they avoid entry into meiosis and instead undergo mitotic arrest and mature toward spermatogenesis. Here, we discuss what we know so far about the regulation of sex-specific differentiation of germ cells, considering extrinsic molecular cues produced by somatic cells, as well as critical intrinsic changes within the germ cells. This review focuses almost exclusively on our understanding of these events in the mouse model.
Topics: Animals; Cell Differentiation; Female; Germ Cells; Male; Meiosis; Mice; Mice, Inbred C57BL; Mitosis; Oogenesis; Sex Determination Processes; Spermatogenesis; Tretinoin
PubMed: 25791730
DOI: 10.4103/1008-682X.150037