High-resolution whole-genome sequencing reveals that specific Chromatin Domains from most human chromosomes associate with nucleoli

Silvana van Koningsbruggen, Marek Gierlinski, Pieta Schofield, David Martin, Geoffrey J. Barton, Yavuz Ariyurek, Johan T. den Dunnen, Angus I. Lamond

    Research output: Contribution to journalArticle

    137 Citations (Scopus)

    Abstract

    The nuclear space is mostly occupied by chromosome territories and nuclear bodies. Although this organization of chromosomes affects gene function, relatively little is known about the role of nuclear bodies in the organization of chromosomal regions. The nucleolus is the best-studied subnuclear structure and forms around the rRNA repeat gene clusters on the acrocentric chromosomes. In addition to rDNA, other chromatin sequences also surround the nucleolar surface and may even loop into the nucleolus. These additional nucleolar-associated domains (NADs) have not been well characterized. We present here a whole-genome, high-resolution analysis of chromatin endogenously associated with nucleoli. We have used a combination of three complementary approaches, namely fluorescence comparative genome hybridization, high-throughput deep DNA sequencing and photoactivation combined with time-lapse fluorescence microscopy. The data show that specific sequences from most human chromosomes, in addition to the rDNA repeat units, associate with nucleoli in a reproducible and heritable manner. NADs have in common a high density of AT-rich sequence elements, low gene density and a statistically significant enrichment in transcriptionally repressed genes. Unexpectedly, both the direct DNA sequencing and fluorescence photoactivation data show that certain chromatin loci can specifically associate with either the nucleolus, or the nuclear envelope.

    Original languageEnglish
    Pages (from-to)3735-3748
    Number of pages14
    JournalMolecular Biology of the Cell
    Volume21
    Issue number21
    DOIs
    Publication statusPublished - 1 Nov 2010

    Keywords

    • TELOMERIC DNA-SEQUENCES
    • GENE-REGULATION
    • COILED BODIES
    • CELL-CYCLE
    • SPATIAL-ORGANIZATION
    • LIVING CELLS
    • RNA GENES
    • TERRITORIES
    • LOCALIZATION
    • ARCHITECTURE

    Cite this

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    title = "High-resolution whole-genome sequencing reveals that specific Chromatin Domains from most human chromosomes associate with nucleoli",
    abstract = "The nuclear space is mostly occupied by chromosome territories and nuclear bodies. Although this organization of chromosomes affects gene function, relatively little is known about the role of nuclear bodies in the organization of chromosomal regions. The nucleolus is the best-studied subnuclear structure and forms around the rRNA repeat gene clusters on the acrocentric chromosomes. In addition to rDNA, other chromatin sequences also surround the nucleolar surface and may even loop into the nucleolus. These additional nucleolar-associated domains (NADs) have not been well characterized. We present here a whole-genome, high-resolution analysis of chromatin endogenously associated with nucleoli. We have used a combination of three complementary approaches, namely fluorescence comparative genome hybridization, high-throughput deep DNA sequencing and photoactivation combined with time-lapse fluorescence microscopy. The data show that specific sequences from most human chromosomes, in addition to the rDNA repeat units, associate with nucleoli in a reproducible and heritable manner. NADs have in common a high density of AT-rich sequence elements, low gene density and a statistically significant enrichment in transcriptionally repressed genes. Unexpectedly, both the direct DNA sequencing and fluorescence photoactivation data show that certain chromatin loci can specifically associate with either the nucleolus, or the nuclear envelope.",
    keywords = "TELOMERIC DNA-SEQUENCES, GENE-REGULATION, COILED BODIES, CELL-CYCLE, SPATIAL-ORGANIZATION, LIVING CELLS, RNA GENES, TERRITORIES, LOCALIZATION, ARCHITECTURE",
    author = "{van Koningsbruggen}, Silvana and Marek Gierlinski and Pieta Schofield and David Martin and Barton, {Geoffrey J.} and Yavuz Ariyurek and {den Dunnen}, {Johan T.} and Lamond, {Angus I.}",
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    High-resolution whole-genome sequencing reveals that specific Chromatin Domains from most human chromosomes associate with nucleoli. / van Koningsbruggen, Silvana; Gierlinski, Marek; Schofield, Pieta; Martin, David; Barton, Geoffrey J.; Ariyurek, Yavuz; den Dunnen, Johan T.; Lamond, Angus I.

    In: Molecular Biology of the Cell, Vol. 21, No. 21, 01.11.2010, p. 3735-3748.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - High-resolution whole-genome sequencing reveals that specific Chromatin Domains from most human chromosomes associate with nucleoli

    AU - van Koningsbruggen, Silvana

    AU - Gierlinski, Marek

    AU - Schofield, Pieta

    AU - Martin, David

    AU - Barton, Geoffrey J.

    AU - Ariyurek, Yavuz

    AU - den Dunnen, Johan T.

    AU - Lamond, Angus I.

    PY - 2010/11/1

    Y1 - 2010/11/1

    N2 - The nuclear space is mostly occupied by chromosome territories and nuclear bodies. Although this organization of chromosomes affects gene function, relatively little is known about the role of nuclear bodies in the organization of chromosomal regions. The nucleolus is the best-studied subnuclear structure and forms around the rRNA repeat gene clusters on the acrocentric chromosomes. In addition to rDNA, other chromatin sequences also surround the nucleolar surface and may even loop into the nucleolus. These additional nucleolar-associated domains (NADs) have not been well characterized. We present here a whole-genome, high-resolution analysis of chromatin endogenously associated with nucleoli. We have used a combination of three complementary approaches, namely fluorescence comparative genome hybridization, high-throughput deep DNA sequencing and photoactivation combined with time-lapse fluorescence microscopy. The data show that specific sequences from most human chromosomes, in addition to the rDNA repeat units, associate with nucleoli in a reproducible and heritable manner. NADs have in common a high density of AT-rich sequence elements, low gene density and a statistically significant enrichment in transcriptionally repressed genes. Unexpectedly, both the direct DNA sequencing and fluorescence photoactivation data show that certain chromatin loci can specifically associate with either the nucleolus, or the nuclear envelope.

    AB - The nuclear space is mostly occupied by chromosome territories and nuclear bodies. Although this organization of chromosomes affects gene function, relatively little is known about the role of nuclear bodies in the organization of chromosomal regions. The nucleolus is the best-studied subnuclear structure and forms around the rRNA repeat gene clusters on the acrocentric chromosomes. In addition to rDNA, other chromatin sequences also surround the nucleolar surface and may even loop into the nucleolus. These additional nucleolar-associated domains (NADs) have not been well characterized. We present here a whole-genome, high-resolution analysis of chromatin endogenously associated with nucleoli. We have used a combination of three complementary approaches, namely fluorescence comparative genome hybridization, high-throughput deep DNA sequencing and photoactivation combined with time-lapse fluorescence microscopy. The data show that specific sequences from most human chromosomes, in addition to the rDNA repeat units, associate with nucleoli in a reproducible and heritable manner. NADs have in common a high density of AT-rich sequence elements, low gene density and a statistically significant enrichment in transcriptionally repressed genes. Unexpectedly, both the direct DNA sequencing and fluorescence photoactivation data show that certain chromatin loci can specifically associate with either the nucleolus, or the nuclear envelope.

    KW - TELOMERIC DNA-SEQUENCES

    KW - GENE-REGULATION

    KW - COILED BODIES

    KW - CELL-CYCLE

    KW - SPATIAL-ORGANIZATION

    KW - LIVING CELLS

    KW - RNA GENES

    KW - TERRITORIES

    KW - LOCALIZATION

    KW - ARCHITECTURE

    U2 - 10.1091/mbc.E10-06-0508

    DO - 10.1091/mbc.E10-06-0508

    M3 - Article

    C2 - 20826608

    VL - 21

    SP - 3735

    EP - 3748

    JO - Molecular Biology of the Cell

    JF - Molecular Biology of the Cell

    SN - 1059-1524

    IS - 21

    ER -