Lampbrush chromosome studies in the post‐genomic era

Krasikova, Alla; Fishman, Veniamin; Kulikova, Tatiana

doi:10.1002/bies.202200250

Cited by 6 publications

(6 citation statements)

References 47 publications

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“…FISH probes were prepared from the chicken BAC-clone library CHORI-261 (https://bacpacresources.org/chicken261.htm) to the selected genomic regions (Table S2). BAC-clone based probes were labelled either with biotin-11-dUTP (Lumiprobe), digoxigenin-11-dUTP (Jena Bioscience) or aminoallyl-dUTP-ATTO-647N (Jena Bioscience) by nick-translation as described in (Krasikova et al . 2023a).…”

Section: Methodsmentioning

confidence: 99%

“…Lampbrush chromosome chromatin is distinctly structured, with a predetermined chromomere-loop configuration. Active transcription of various genomic sequences takes place on the lateral loops, also called transcription loops (Morgan 2018;Mirny and Solovei 2021;Krasikova et al 2023a). The extraordinary length of the lateral loops and the density of newly synthesised RNA make it possible to visualise and map individual transcription units with exceptional resolution (Kaufmann et al 2012;.…”

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The first chicken oocyte nucleus whole transcriptomic profile defines the spectrum of maternal mRNA and non-coding RNA genes transcribed by the lampbrush chromosomes

Krasikova,

Kulikova,

Schelkunov

et al. 2024

Preprint

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Lampbrush chromosomes, with their unusually high rate of nascent RNA synthesis, provide a valuable model for studying the mechanisms of global transcriptome up-regulation. Here, we aimed to establish a full set of sequences transcribed on the lateral loops of chicken lampbrush chromosomes. For the first time, a whole-genomic profile of transcription along the entire length of all lampbrush chromosomes in the chicken karyotype including sex chromosomes and dot chromosomes was obtained. For that, we performed RNA-seq of oocyte nuclear and cytoplasmic total RNA, poly(A) RNA and small RNA libraries and aligned expressed RNA sequences against the chicken genome. This led to the identification of a full spectrum of maternal RNAs that accumulate in the nucleus and cytoplasm of chicken oocytes at the lampbrush chromosome stage, are then transferred to the zygote and can be used during the early stages of embryogenesis, including transcripts of protein-coding genes, long non-coding RNAs and small housekeeping non-coding RNAs. We also present the first high-throughput transcriptome characterisation of miRNAs and piRNAs in chicken oocytes at the lampbrush chromosome stage. Major targets of predicted piRNAs include CR1 and LTR containing retrotransposable elements. Transcription of tandem repeat arrays including 41bp higher-order repeats as well as unique centromere sequences was demonstrated by alignment against the whole telomere-to-telomere chromosome assemblies. We show that transcription of telomere-derived RNAs, including telomeric repeat-containing RNA (TERRA) and subtelomeric repeat-containing RNA, is initiated at adjacent LTR elements. With nuclear RNA-seq, we obtained information about a wider set of transcripts, including long non-coding RNAs retained in the nucleus and stable intronic sequence RNAs (sisRNAs). We identified 5’ UTR sisRNAs that may potentially support host gene transcription both during oogenesis and after activation of the embryonic genome. For a number of protein-coding genes, we visualised nascent transcripts and demonstrated their co-transcriptional splicing on the lateral loops of lampbrush chromosomes by RNA-FISH. The nuclear RNA-seq profile predicted the chromomere-loop organisation of the genomic regions. During oocyte maturation, transcriptional unit boundaries were maintained, while transcriptional output tended to decrease. We conclude that cytoplasmic and nuclear transcripts emerge from nascent transcripts on the lateral loops of lampbrush chromosomes. Most of gene transcripts are initiated at promoters, normally spliced, terminated and polyadenylated. The set of genes transcribed on the lampbrush chromosomes is required for basic cellular processes, is characterised by a broad expression pattern and is similar to sets of genes expressed in other hypertranscriptional systems. We conclude that hypertranscription on the lateral loops of giant lampbrush chromosomes is the main mechanism for synthesising large amounts of transferred to the embryo maternal RNA for thousands of genes.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The first chicken oocyte nucleus whole transcriptomic profile defines the spectrum of maternal mRNA and non-coding RNA genes transcribed by the lampbrush chromosomes

Krasikova,

Kulikova,

Schelkunov

et al. 2024

Preprint

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“…In this type of oogenesis, high transcriptional output leads to appearance of extremely elongated lampbrush chromosomes with a typical chromomere-loop structure. Lampbrush chromosomes are found in diplotene stage oocytes of all vertebrates with the exception of mammals [24][25][26][27][28]. At this stage of oogenesis chromosomes nearly lack any transchromosomal interactions except for the formation of bivalents between homologous chromosomes.…”

Section: Introductionmentioning

confidence: 99%

Assignment of the somatic A/B compartments to chromatin domains in giant transcriptionally active lampbrush chromosomes

Krasikova

Kulikova

Ramos

et al. 2023

Preprint

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The three-dimensional configuration of the eukaryotic genome is an emerging area of research. Chromosome conformation capture outlined genome segregation into large scale A and B compartments corresponding mainly to transcriptionally active and repressive chromatin. It remains unknown how the compartmentalization of the genome changes in growing oocytes of animals with hypertranscriptional type of oogenesis. In this type of oogenesis, highly elongated chromosomes, called lampbrush chromosomes, acquire a characteristic chromomere-loop appearance, representing one of the classical model systems for studying the structural and functional organization of chromatin domains. Here, we compared the distribution of A/B compartments in chicken somatic cells with chromatin domains in lampbrush chromosomes. We found that in lampbrush chromosomes, the extended chromatin domains, restricted by compartment boundaries in somatic cells, disintegrate into individual chromomeres. Next, we performed FISH-mapping of the genomic loci, which belong to A or B chromatin compartments as well as to A/B compartment transition regions in embryonic fibroblasts on isolated lampbrush chromosomes. We established, that in chicken lampbrush chromosomes, clusters of dense compact chromomeres bearing short lateral loops and enriched with repressive epigenetic modifications generally correspond to constitutive B compartments in somatic cells. These results suggest that gene-poor regions tend to be packed into chromomeres. Clusters of small loose chromomeres with relatively long lateral loops show no obvious correspondence with either A or B compartment identity. Some genes belonging to facultative B (sub-) compartments can be tissue-specifically transcribed during oogenesis, forming distinct lateral loops.

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“…In this type of oogenesis, high transcriptional output leads to appearance of extremely elongated lampbrush chromosomes with a typical chromomere-loop structure. Lampbrush chromosomes are found in diplotene stage oocytes of all vertebrates with the exception of mammals [ 24 – 28 ]. At this stage of oogenesis chromosomes nearly lack any trans -chromosomal interactions except for the formation of bivalents between homologous chromosomes.…”

Section: Introductionmentioning

confidence: 99%

Assignment of the somatic A/B compartments to chromatin domains in giant transcriptionally active lampbrush chromosomes

Krasikova

Kulikova

Ramos

et al. 2023

Epigenetics & Chromatin

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Background The three-dimensional configuration of the eukaryotic genome is an emerging area of research. Chromosome conformation capture outlined genome segregation into large scale A and B compartments corresponding mainly to transcriptionally active and repressive chromatin. It remains unknown how the compartmentalization of the genome changes in growing oocytes of animals with hypertranscriptional type of oogenesis. Such oocytes are characterized by highly elongated chromosomes, called lampbrush chromosomes, which acquire a typical chromomere-loop appearance, representing one of the classical model systems for exploring the structural and functional organization of chromatin domains. Results Here, we compared the distribution of A/B compartments in chicken somatic cells with chromatin domains in lampbrush chromosomes. We found that in lampbrush chromosomes, the extended chromatin domains, restricted by compartment boundaries in somatic cells, disintegrate into individual chromomeres. Next, we performed FISH-mapping of the genomic loci, which belong to A or B chromatin compartments as well as to A/B compartment transition regions in embryonic fibroblasts on isolated lampbrush chromosomes. We found, that in chicken lampbrush chromosomes, clusters of dense compact chromomeres bearing short lateral loops and enriched with repressive epigenetic modifications generally correspond to constitutive B compartments in somatic cells. A compartments align with lampbrush chromosome segments with smaller, less compact chromomeres, longer lateral loops, and a higher transcriptional status. Clusters of small loose chromomeres with relatively long lateral loops show no obvious correspondence with either A or B compartment identity. Some genes belonging to facultative B (sub-) compartments can be tissue-specifically transcribed during oogenesis, forming distinct lateral loops. Conclusions Here, we established a correspondence between the A/B compartments in somatic interphase nucleus and chromatin segments in giant lampbrush chromosomes from diplotene stage oocytes. The chromomere-loop structure of the genomic regions corresponding to interphase A and B compartments reveals the difference in how they are organized at the level of chromatin domains. The results obtained also suggest that gene-poor regions tend to be packed into chromomeres.

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Lampbrush chromosome studies in the post‐genomic era

Cited by 6 publications

References 47 publications

The first chicken oocyte nucleus whole transcriptomic profile defines the spectrum of maternal mRNA and non-coding RNA genes transcribed by the lampbrush chromosomes

The first chicken oocyte nucleus whole transcriptomic profile defines the spectrum of maternal mRNA and non-coding RNA genes transcribed by the lampbrush chromosomes

Assignment of the somatic A/B compartments to chromatin domains in giant transcriptionally active lampbrush chromosomes

Assignment of the somatic A/B compartments to chromatin domains in giant transcriptionally active lampbrush chromosomes

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