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Three-dimensional architecture of tandem repeats in chicken interphase nucleus

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Abstract

Tandem repeats belong to a class of genomic repetitive elements that form arrays of head-to-tail monomers. Due to technical difficulties in sequencing and assembly of large tandem repeat arrays, it remains largely unknown by which mechanisms tandem-repeat-containing regions aid in maintenance of ordered radial genome organization during interphase. Here we analyzed spatial distribution of several types of tandem repeats in interphase nuclei of chicken MDCC-MSB1 cells and somatic tissues relative to heterochromatin compartments and nuclear center. We showed that telomere and subtelomere repeats generally localize at the nuclear or chromocenters periphery. A tandem repeat known as CNM, typical for centromere regions of gene-dense microchromosomes, forms interchromosome clusters and occupies DAPI-positive chromocenters that appear predominantly within the nuclear interior. In contrast, centromere-specific tandem repeats of the majority of gene-poor macrochromosomes are embedded into the peripheral layer of heterochromatin. Chicken chromocenters rarely comprise centromere sequences of both macro- and microchromosomes, whose territories localize in different radial nuclear zones. Possible mechanisms of observed tandem repeats positioning and its implication in highly ordered arrangement of chromosome territories in chicken interphase nucleus are discussed.

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Abbreviations

3C:

Chromosome conformation capture

3D:

Three-dimensional

BAC:

Bacterial artificial chromosome

Cen:

Centromere-specific sequence

CENP:

Centromere protein

CEF:

Chicken embryonic fibroblasts

CNM:

Chicken nuclear-membrane-associated repeat

CR1:

Chicken repetitive 1 element

DAPI:

4′,6-Diamidino-2-phenylindole

FISH:

Fluorescent in situ hybridization

GGA:

Chicken (Gallus gallus) chromosome

LAD:

Lamina-associated domain

MDCC:

Marek’s disease chicken cell line

PO41:

Pattern of 41 bp repeat

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Acknowledgments

The research of NK (performed GGA4 arms microdissection) was supported by the Jena/St Petersburg University Partnership Program funded by DAAD. The research of AM, AZ, MS, and AK (performed all other experiments and drafted the manuscript) was supported by Russian Science Foundation (grant #14-14-00131). The work was partially performed using experimental equipment of the Research Resource Centers “Chromas” and “Molecular and Cell Technologies” of St Petersburg State University.

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Authors and Affiliations

  1. Saint Petersburg State University, Saint Petersburg, 198504, Russia

    Antonina Maslova, Anna Zlotina, Marina Sidorova & Alla Krasikova

  2. Institute of Human Genetics, Jena University Hospital, Friedrich Schiller University, Jena, Germany

    Nadezhda Kosyakova

Authors
  1. Antonina Maslova
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  2. Anna Zlotina
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  3. Nadezhda Kosyakova
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  4. Marina Sidorova
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  5. Alla Krasikova
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Correspondence to Alla Krasikova.

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Responsible Editors: Maria Assunta Biscotti, Pat Heslop-Harrison and Ettore Olmo

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Fig. S1

Chromocenters in chicken interphase nuclei. a, b, c Single confocal sections of three representative DAPI-stained MDCC-MSB1 lymphoblast nuclei. Arrows point on chromocenters located within nuclear interior (2 on the panel a’) and at the inner border of peripheral heterochromatin (1 and 3 on the panel a’) or within peripheral heterochromatin near the nuclear envelope (1 and 2 on the panel b’). Blocks of perinucleolar heterochromatin (arrowheads) surround nucleoli (c’). a”, b”, c” Prominent peaks in fluorescence intensity profiles through the line regions of interest (ROI). Scale bars 5 μm (PDF 517 kb)

Fig. S2

Patterns of active and inactive chromatin marks in chicken MDCC-MSB1 lymphoblasts. Single confocal sections of nuclei after immunofluorescent staining with specific antibodies against dimethylated H3K9 (а’), trimethylated H3K9 (b’), trimethylated H3K27 (c’), trimethylated H3K4 (d’), hyperacetylated H4 (e’), and Sm proteins of snRNPs (f’). Nuclei are counterstained with DAPI (a–g). Arrows indicate chromocenters, arrowheads point to nucleoli. Scale bars 5 μm (PDF 724 kb)

Fig. S3

CNM clusters in chicken somatic cells. Single confocal sections of chicken MDCC-MSB1 lymphoblast (а–а”), chicken embryonic fibroblasts (b–b”), erythrocytes (c–c”), ovarian somatic cells (d–d”), smooth muscle cells (e–e”), lamina propria cells (f–f”), and enterocytes (g–g”) of small intestine villi after FISH detection of CNM repeats (a’–g’). Nuclei are counterstained with DAPI (a–g). In all cell types, CNM-rich foci (arrowheads) co-localize with DAPI-positive chromocenters (arrows) (a”–g”). Boxplots below show the number of CNM foci in different cell types (h). Boxes represent median and quartiles, while whiskers show maximal and minimal values. Scale bars 10 μm (PDF 1380 kb)

Fig. S4

Localization of W-specific tandem repeats within the chromocenter that is largely devoid of CNM repeats. a’, b’ Single confocal sections of nuclei after dual-color FISH detection of EcoRI, SspI, and XhoI repeats. a, b Nuclei counterstained with DAPI. a”, b” 3D surface reconstructions of corresponding nuclei with segmented chromocenters and EcoRI-, SspI-, and XhoI-repeat foci. Scale bars 5 μm (PDF 277 kb)

Fig. S5

Localization of CNM foci relative to nucleoli in chicken MDCC-MSB1 lymphoblasts. a’–d’ Single confocal sections of nuclei after immunofluorescent staining with antibody against fibrillarin and FISH detection of CNM repeats. a–d Nuclei counterstained with DAPI. Arrowheads point on CNM foci associated with nucleoli. Arrows mark CNM arrays which do not localize to nucleolus. Scale bars 5 μm (PDF 469 kb)

Fig. S6

Distribution of centromere regions of chicken macrochromosomes and microchromosome 27 relative to peripheral heterochromatin in chicken interphase nucleus. a, b, c, d Schematic drawings of centromere position (green circle) variants relative to peripheral heterochromatin (blue), chromocenters (dark blue), and inner nuclear region (light blue). a’, b’, c’, d’ Representative single confocal images of MDCC-MSB1 and CEF cell nuclei after FISH detection of Cen. Nuclei are counterstained with DAPI. a”, b”, c”, d” Bar graphs, demonstrating relative frequencies of Cen1–4, 7, 8, 11, Z and 27 locations in depicted nuclear regions of MDCC-MSB1 cells. Scale bars 5 μm (PDF 739 kb)

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Maslova, A., Zlotina, A., Kosyakova, N. et al. Three-dimensional architecture of tandem repeats in chicken interphase nucleus. Chromosome Res 23, 625–639 (2015). https://doi.org/10.1007/s10577-015-9485-5

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