Reconstitution of the oocyte nucleolus in mice through a single nucleolar protein, NPM2

Ogushi, Sugako; Yamagata, Kazuya; Obuse, Chikashi; Furuta, Keiko; Wakayama, Teruhiko; Matzuk, Martin M.; Saitou, Mitinori

doi:10.1242/jcs.195875

Cited by 25 publications

(33 citation statements)

References 51 publications

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“…Essentially, our observations confirmed the results obtained by Ogushi et al (2017) who injected Npm2 mRNA into previously enucleolated mouse oocytes. The embryos where pronuclei contained tiny NPBs did not develop after fertilization.…”

supporting

confidence: 91%

“…Finally, Ogushi et al, (2017) demonstrated that development of zygotes originating from oocytes without NLBs can be rescued by injecting them with Npm2 mRNA. Interestingly, when 1.2mg/ml of mRNA was injected, the pronuclei contained very small NPBs and the zygotes reached the blastocyst stage only sporadically.…”

Section: Towards Clarifying the Role Of Npbs In Zygotesmentioning

confidence: 99%

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Function of atypical mammalian oocyte/zygote nucleoli and its implications for reproductive biology and medicine

Fulka

Benc²,

Loi³

et al. 2019

Int. J. Dev. Biol.

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Mammalian oocytes/zygotes contain atypical nucleoli that are composed exclusively of a dense fibrillar material. It has been commonly accepted that these nucleoli serve as a repository of components that are used later on, as the embryo develops, for the construction of typical tripartite nucleoli. Indeed, when nucleoli were removed from immature oocytes (enucleolation) and these oocytes were then matured, fertilized or parthenogenetically activated, development of the produced embryos ceased after one or two cleavages with no detectable nucleoli in nuclei. This indicated that zygotic nucleoli originate exclusively from oocytes, i.e. are maternally inherited. Recently published results, however, do not support this developmental biology dogma and demonstrate that maternal nucleoli in one-cell stage embryos are necessary only during a very short time period after fertilization when they serve as a major heterochromatin organizing structures. Nevertheless, it still remains to be determined, which other functions/roles the atypical oocyte/zygote nucleoli eventually have.

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supporting

confidence: 91%

Section: Towards Clarifying the Role Of Npbs In Zygotesmentioning

confidence: 99%

Function of atypical mammalian oocyte/zygote nucleoli and its implications for reproductive biology and medicine

Fulka

Benc²,

Loi³

et al. 2019

Int. J. Dev. Biol.

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“…In the absence of NPM2, oocytes and embryos lack NLB and NPB and show defects in heterochromatin structures. Consistent with a role of NPM2 in nucleolus and heterochromatin, a recent study showed that the expression of NPM2 in Npm2-null oocytes sufficed to reconstitute nucleolar structures in enucleolated embryos, and rescued their first mitotic division and full-term development [68].…”

Section: Box 1 Preimplantation Developmental Stagesmentioning

confidence: 59%

“…The removal of NPBs 10 h after sperm injection did not affect embryo development and new nucleoli could form after several cell divisions, suggesting that the nucleoli can originate from de novo synthesized materials [67]. Data also suggest that the developmental defects observed in embryos fertilized with enucleolated oocytes are due to problems with chromosome segregation, mislocalization of centromeric proteins, abnormal first embryonic S-phase progression, and replication stress [44,68]. Consistent with defects linked to genome stability, during the first embryonic cell cycle, embryos lacking NPBs showed a significant reduction in major and minor satellite DNA and a decrease in satellite transcripts by more than half [44].…”

Section: Box 1 Preimplantation Developmental Stagesmentioning

confidence: 93%

Nucleolus and rRNA Gene Chromatin in Early Embryo Development

Kresoja‐Rakic

Santoro

2019

Trends in Genetics

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The nucleolus is the largest substructure in the nucleus and forms around the nucleolar organizer regions (NORs), which comprise hundreds of rRNA genes. Recent evidence highlights further functions of the nucleolus that go beyond ribosome biogenesis. Data indicate that the nucleolus acts as a compartment for the location and regulation of repressive genomic domains and, together with the nuclear lamina, represents the hub for the organization of the inactive heterochromatin. In this review, we discuss recent findings that have revealed how nucleolar structure and rRNA gene chromatin states are regulated during early mammalian development and their contribution to the higher-order spatial organization of the genome. The Multifunctional Nucleolus: From Ribosome Producer to Organizer of Genome Architecture The nucleolus (see Glossary) is the largest subnuclear compartment of the cell and forms around regions of chromosomes containing stretches of tandem repetitive rRNA genes, known as nucleolar organizer regions (NORs). The nucleolus is responsible for the production of ribosomes, a highly regulated process that is essential for growth and development. Ribosome biogenesis is initiated in the nucleolus by RNA polymerase I (Pol I), which, together with a dedicated set of basal transcription factors, such as TIF1A, the TBP-TAFI complex SL1, and the DNA architectural upstream binding factor (UBF) [1,2], transcribes hundreds of rRNA genes to generate 45S/47S pre-rRNA in mammalian cells (Figure 1A). This rRNA precursor is chemically modified and processed to form 28S, 18S, and 5.8S rRNAs, which are then assembled with ribosomal proteins and 5S rRNA and exported from the nucleus to give rise to active ribosomes in the cytoplasm [3]. Increasing evidence suggests that the function of the nucleolus and rRNA genes goes beyond ribosome biogenesis. One aspect that has received significant interest over the past decade is the link between the nucleolus and rRNA genes with the organization of genome architecture. Clustering of heterochromatin at nucleoli is a phenomenon that occurs in all cells. Furthermore, regions located close to the nucleolus (nucleolar-associated domains, NADs) have low gene densities, low transcriptional levels, and repressive histone modifications [4-8]. Since similar heterochromatic and repressive regions are also located to the nuclear lamina, the nucleolus, together with the nuclear lamina, can be considered the hub for the organization of the inactive chromatin in the cell [8-10]. In this review, we address the role of the nucleolus as a subnuclear compartment for the organization of heterochromatin. We discuss recent findings that have revealed how nucleolar structure and rRNA gene chromatin states are regulated during gametogenesis and early mammalian development, and their contribution in the higher-order spatial organization of the genome. Nucleolus and rRNA Genes in Somatic Cells In somatic cells, the nucleolus is a membraneless compartment with a peculiar tripartite architecture: the fibrillar cen...

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“…Further, a few candidate proteins (i.e. NPM2, NCL, SSRP1 and NOLC1) have been found in mouse oocyte NPB (25), together with other key nucleolar proteins (26). Likewise, the somatic nucleolus is rich in small RNAs including microRNAs (miRNAs) (27).…”

Section: The Composition Of the Npb And Potential Mechanisms For Its mentioning

confidence: 99%

The Oocyte’s Nucleolus Precursor Body: The Globe for Life

Benc

Pendovski

Murín

et al. 2018

Macedonian Veterinary Review

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The nucleolus is the cell organelle responsible for ribosome synthesis and, hence, for protein synthesis. In the mammalian oocyte, the nucleolus compacts into a dense sphere with no ribosome synthesis well in advance of ovulation. It seems, that this body is of utmost importance for the development of the embryo. It is unknown, however, how it exerts this essential function. During the last two decades, great attention has been paid to the study of nucleogenesis in oocytes and early embryos, with transcription of ribosomal DNA being evaluated as one of the criteria of normal development. In this review, we summarize some aspects of nucleolus transformation during oocyte growth, as well as during early embryonic development with possible impact on the quality of the embryos used in biomedical research. This knowledge in connection with further observations will substantially contribute to the development of new criteria suitable for evaluation of oocytes and embryos used in biomedical application.

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Reconstitution of the oocyte nucleolus in mice through a single nucleolar protein, NPM2

Cited by 25 publications

References 51 publications

Function of atypical mammalian oocyte/zygote nucleoli and its implications for reproductive biology and medicine

Function of atypical mammalian oocyte/zygote nucleoli and its implications for reproductive biology and medicine

Nucleolus and rRNA Gene Chromatin in Early Embryo Development

The Oocyte’s Nucleolus Precursor Body: The Globe for Life

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