The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte to embryo transition

Fulka, Helena; Langerova, Alena

doi:10.1242/dev.105940

Cited by 71 publications

(97 citation statements)

References 50 publications

(64 reference statements)

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“…After fertilization, extensive chromatin reprogramming occurs in both pronuclei. Pericentric heterochromatin reorganizes and forms a ring(s) around NPB(s) (Probst and Almouzni, 2011;Fulka and Langerova, 2014). Pericentric satellites are methylated but there are distinct differences between both pronuclei (maternal versus paternal).…”

Section: Zygotes Without Npbs Develop To Live-born Pupsmentioning

confidence: 99%

De novo formation of nucleoli in developing mouse embryos originating from enucleolated zygotes

et al. 2014

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The large, compact oocyte nucleoli, sometimes referred to as nucleolus precursor bodies (NPBs), are essential for embryonic development in mammals; in their absence, the oocytes complete maturation and can be fertilized, but no nucleoli are formed in the zygote or embryo, leading to developmental failure. It has been convincingly documented that zygotes inherit the oocyte nucleolar material and form NPBs again in pronuclei. It is commonly accepted that during early embryonic development, the original compact zygote NPBs gradually transform into reticulated nucleoli of somatic cells. Here, we show that zygote NPBs are not required for embryonic and full-term development in the mouse. When NPBs were removed from late-stage zygotes by micromanipulation, the enucleolated zygotes developed to the blastocyst stage and, after transfer to recipients, live pups were obtained. We also describe de novo formation of nucleoli in developing embryos. After removal of NPBs from zygotes, they formed new nucleoli after several divisions. These results indicate that the zygote NPBs are not used in embryonic development and that the nucleoli in developing embryos originate from de novo synthesized materials.

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Section: Zygotes Without Npbs Develop To Live-born Pupsmentioning

confidence: 99%

De novo formation of nucleoli in developing mouse embryos originating from enucleolated zygotes

et al. 2014

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“…Moreover, the critical time point, when the nucleolus is required for early embryonic development, appears to be at the early step of pronucleus formation (Kyogoku et al, 2014;Ogushi and Saitou, 2010). Zygotes from enucleolated mouse oocytes have been shown to exhibit mis-localization of centromeric proteins (Ogushi and Saitou, 2010), delay in enlargement of the paternal pronucleus (Inoue et al, 2011), alteration of DNA replication timing and abnormal deposition of fas death-domain-associated protein (DAXX), a histone H3.3 chaperone protein for repetitive regions of the genome (Fulka and Langerova, 2014;Voon and Wong, 2016). In mouse Npm2-null zygotes, hypo-acetylated histone H3 on the heterochromatin surrounding nucleoli is lost (Burns et al, 2003).…”

Section: Introductionmentioning

confidence: 99%

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

Ogushi

Yamagata²,

Obuse

et al. 2017

Journal of Cell Science

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The mammalian oocyte nucleolus, the most prominent subcellular organelle in the oocyte, is vital in early development, yet its key functions and constituents remain unclear. We show here that the parthenotes/zygotes derived from enucleolated oocytes exhibited abnormal heterochromatin formation around parental pericentromeric DNAs, which led to a significant mitotic delay and frequent chromosome mis-segregation upon the first mitotic division. A proteomic analysis identified nucleoplasmin 2 (NPM2) as a dominant component of the oocyte nucleolus. Consistently, Npm2-deficient oocytes, which lack a normal nucleolar structure, showed chromosome segregation defects similar to those in enucleolated oocytes, suggesting that nucleolar loss, rather than micromanipulation-related damage to the genome, leads to a disorganization of higher-order chromatin structure in pronuclei and frequent chromosome mis-segregation during the first mitosis. Strikingly, expression of NPM2 alone sufficed to reconstitute the nucleolar structure in enucleolated embryos, and rescued their first mitotic division and full-term development. The nucleolus rescue through NPM2 required the pentamer formation and both the N-and C-terminal domains. Our findings demonstrate that the NPM2-based oocyte nucleolus is an essential platform for parental chromatin organization in early embryonic development.

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“…Loss of maternal ATRX results in chromosome instability in mouse oocytes and early embryos [58]. In mouse embryogenesis, the dynamics of ATRX reflect the processes of nuclear reorganization related to the gradual activation of chromosomal transcription [59,60]. Genome inactivation in the final steps of R. temporaria karyosphere development can result in the accumulation of ATRX in extrachromosomal elements such as the KC.…”

Section: Discussionmentioning

confidence: 99%

The karyosphere capsule inRana temporariaoocytes contains structural and DNA-binding proteins

Ilicheva

Podgornaya

Bogolyubov

2018

Nucleus

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During the last stages of oogenesis, oocyte chromosomes condense and come close together, forming the so-called karyosphere. Karyosphere formation is accompanied by an essential decrease in transcriptional activity. In the grass frog Rana temporaria, the karyosphere is surrounded by an extrachromosomal capsule that separates the chromosomes from the rest of the nucleoplasm. The karyosphere capsule (KC) of R. temporaria has been investigated in detail at the ultrastructural level, but its protein composition remained largely unknown. We demonstrate here that nuclear actin, especially F-actin, as well as lamins A/C and B are the most abundant proteins of the KC. Key proteins of nuclear pore complexes, such as Nup93 and Nup35, are also detectable in the KC. New antibodies recognizing the telomere-binding protein TRF2 allowed us to localize TRF2 in nuclear speckles. We also found that the R. temporaria KC contains some proteins involved in chromatin remodeling, including topoisomerase II and ATRX. Thus, we believe that KC isolates the chromosomes from the rest of the nucleoplasm during the final period of oocyte growth (late diplotene) and represents a specialized oocyte nuclear compartment to store a variety of factors involved in nuclear metabolism that can be used in future early development.Abbreviations: BrUTP: 5-bromouridine 5’-triphosphate; CytD: cytochalasin D; IGCs: interchromatin granule clasters; IgG: immunoglobulin G; KC: karyosphere capsule; Mw: molecular weight; NE: nuclear envelope; PBS: phosphate buffered saline; SDS-PAGE: sodium dodecyl sulfate polyacrylamide gel electrophoresis; Topo II: topoisomerase II

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The maternal nucleolus plays a key role in centromere satellite maintenance during the oocyte to embryo transition

Cited by 71 publications

References 50 publications

De novo formation of nucleoli in developing mouse embryos originating from enucleolated zygotes

De novo formation of nucleoli in developing mouse embryos originating from enucleolated zygotes

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

The karyosphere capsule inRana temporariaoocytes contains structural and DNA-binding proteins

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