Localisation of RNAs and proteins in nucleolar precursor bodies of early mouse embryos

Lavrentyeva, Elena A.; Shishova, K. V.; Kagarlitsky, German; Зацепина, О. В.

doi:10.1071/rd15200

Cited by 10 publications

(12 citation statements)

References 53 publications

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“…Upon fertilization, the NLBs that disappeared during oocyte meiotic maturation reappear in both maternal and paternal pronuclei of zygotes in the form of nucleolus precursor bodies (NPBs), which persist throughout the first four cell cycles [52] (Figure 2 for RNA and detectable amounts of RNA appear on the NPB surface only after resumption of rRNA gene transcription [53]. Accordingly, during the late two-cell and four-cell stages, UBF and Nopp140, two nucleolar proteins that are associated with FC and DFC of the nucleolus, localize around the periphery of the NPBs [51].…”

Section: Box 1 Preimplantation Developmental Stagesmentioning

confidence: 99%

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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Section: Box 1 Preimplantation Developmental Stagesmentioning

confidence: 99%

Nucleolus and rRNA Gene Chromatin in Early Embryo Development

Kresoja‐Rakic

Santoro

2019

Trends in Genetics

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“…Firstly, at the 1-cell stage, several teams have suggested that NPBs ensure the correct remodeling of heterochromatin regions composed of “major satellite” sequences (Ogushi and Saitou 2010 ; Jachowicz et al 2013 ; Fulka and Langerova 2014 ; Kyogoku et al 2014 ). Secondly, these NPBs serve as a platform for the development of functional nucleoli from the end of the 2-cell stage through the morula stage (Zatsepina et al 2003 ; Lavrentyeva et al 2015 ; Koné et al 2016 ). In the mouse, the removal of nucleolus-like structures from the growing oocyte, or the removal of NPBs at the start of the 1-cell stage, can lead to an arrest of development at the 2-cell stage.…”

Section: Introductionmentioning

confidence: 99%

Three-dimensional analysis of nuclear heterochromatin distribution during early development in the rabbit

et al. 2018

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Changes to the spatial organization of specific chromatin domains such as constitutive heterochromatin have been studied extensively in somatic cells. During early embryonic development, drastic epigenetic reprogramming of both the maternal and paternal genomes, followed by chromatin remodeling at the time of embryonic genome activation (EGA), have been observed in the mouse. Very few studies have been performed in other mammalian species (human, bovine, or rabbit) and the data are far from complete. During this work, we studied the three-dimensional organization of pericentromeric regions during the preimplantation period in the rabbit using specific techniques (3D-FISH) and tools (semi-automated image analysis). We observed that the pericentromeric regions (identified with specific probes for Rsat I and Rsat II genomic sequences) changed their shapes (from pearl necklaces to clusters), their nuclear localizations (from central to peripheral), as from the 4-cell stage. This reorganization goes along with histone modification changes and reduced amount of interactions with nucleolar precursor body surface. Altogether, our results suggest that the 4-cell stage may be a crucial window for events necessary before major EGA, which occurs during the 8-cell stage in the rabbit.Electronic supplementary materialThe online version of this article (10.1007/s00412-018-0671-z) contains supplementary material, which is available to authorized users.

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“…transformation of dense nucleolar precursor bodies (NPBs) into functional reticulated nucleoli. Active nucleoli consist of fibrillar centres (FCs), a dense fibrillar component (DFC) and a granular component (GC) (Lavrentyeva et al , 2015).…”

Section: Introductionmentioning

confidence: 99%

Maternally inherited rRNA triggers de novo nucleolus formation in porcine embryos

Morovic

Strejcek

Benc

et al. 2018

Zygote

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SummaryThe present study examines the role of RNA polymerase I (RPI)-mediated transcription, maternally inherited rRNA and nucleolar proteins in the resumption of fibrillogranular nucleoli during embryonic genome activation (EGA) in porcine embryos. Late 4-cell embryos were incubated in the absence (control) or presence of actinomycin D (AD) (0.2 μg/ml for inhibition of RPI; 2.0 μg/ml for inhibition of total transcription) and late 2-cell embryos were cultured to the late 4-cell stage with 0.2 μg/ml AD to block EGA. Embryos were then processed for reverse-transcriptase polymerase chain reaction (RT-PCR), and for autoradiography (ARG), transmission electron microscopy (TEM), fluorescence in situ hybridization (FISH), silver staining and immunofluorescence (for RPI). Embryos in the control group displayed extranucleolar and intranucleolar ARG labelling, and exhibited de novo synthesis of rRNA and reticulated functional nucleoli. Nucleolar proteins were located in large foci. After RPI inhibition, nucleolar precursors transformed into segregated fibrillogranular structures, however no fibrillar centres were observed. The localization of rDNA and clusters of rRNA were detected in 57.1% immunoprecipitated (IP) analyzed nucleoli and dispersed RPI; 30.5% of nuclei showed large deposits of nucleolar proteins. Embryos from the AD-2.0 group did not display any transcriptional activity. Nucleolar formation was completely blocked, however 39.4% of nuclei showed rRNA clusters; 85.7% of nuclei were co-localized with nucleolar proteins. Long-term transcriptional inhibition resulted in the lack of ARG and RPI labelling; 40% of analyzed nuclei displayed the accumulation of rRNA molecules into large foci. In conclusion, maternally inherited rRNA co-localized with rDNA and nucleolar proteins can initiate a partial nucleolar assembly, resulting in the formation of fibrilogranular structures independently on activation of RPI-mediated transcription.

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Localisation of RNAs and proteins in nucleolar precursor bodies of early mouse embryos

Cited by 10 publications

References 53 publications

Nucleolus and rRNA Gene Chromatin in Early Embryo Development

Nucleolus and rRNA Gene Chromatin in Early Embryo Development

Three-dimensional analysis of nuclear heterochromatin distribution during early development in the rabbit

Maternally inherited rRNA triggers de novo nucleolus formation in porcine embryos

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