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The radial nuclear positioning of genes correlates with features of megabase-sized chromatin domains

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Abstract

A nonrandom radial nuclear organization of genes has been well documented. This study provides further evidence that radial positioning depends on features of corresponding ∼1 Mbp chromatin domains (CDs), which represent the basic units of higher-order chromatin organization. We performed a quantitative three-dimensional analysis of the radial nuclear organization of three genes located on chromosome 1 in a DG75 Burkitt lymphoma-derived cell line. Quantitative real-time polymerase chain reaction revealed similar transcription levels for the three selected genes, whereas the total expression strength (TES) calculated as the sum of transcription of all genes annotated within a surrounding window of about 1 Mbp DNA differed for each region. Radial nuclear position of the studied CDs correlated with TES, i.e., the domain with the highest TES occupied the most interior position. Positions of CDs with stable TES values were stably maintained even under experimental conditions, resulting in genome-wide changes of the expression levels of many other genes. Our results strongly support the hypothesis that knowledge of the local chromatin environment is essential to predict the radial nuclear position of a gene.

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Abbreviations

CD:

chromatin domain

CT:

chromosome territory

Ct:

cycle threshold

ΔCt:

delta (difference) in Ct value compared to the control

FISH:

fluorescence in situ hybridization

IC:

interchromatin compartment

ICD:

interchromosomal domain

Mbp:

Mega base pairs

qPCR:

quantitative real-time polymerase chain reaction

RT-PCR:

reverse transcription polymerase chain reaction

SCD:

spherical 1 Mbp chromatin domain (model)

TES:

total expression strength

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Acknowledgment

This work was financially supported by the Deutsche Forschungsgemeinschaft, Collaborative Research Center 684 (SFB684) projects A2 to SD and TC and A6 to SKB. We thank Jens Nagel for the practical help with the data evaluation.

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Authors and Affiliations

  1. Department Biologie II, Ludwig-Maximilians-Universität München, 82152, Planegg, Martinsried, Germany

    Alexandra C. Kölbl, Daniela Weigl, Tobias Thormeyer, Thomas Cremer & Steffen Dietzel

  2. Medizinische Klinik und Poliklinik III, Ludwig-Maximilians-Universität München, Munich, Germany

    Medhanie Mulaw & Stefan K. Bohlander

  3. Clinical Cooperative Group Leukemia, Helmholtz Zentrum München, Munich, Germany

    Medhanie Mulaw & Stefan K. Bohlander

  4. Walter-Brendel-Zentrum für Experimentelle Medizin, Ludwig-Maximilians-Universität München, Marchioninistr. 27, 81377, Munich, Germany

    Steffen Dietzel

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  1. Alexandra C. Kölbl
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ESM 1

Microarray data of differentially regulated probe sets after 24 h of CALM-AF10 induction. Induced cell populations were compared to non-induced CALM/AF10+ cells, as well as induced and non-induced empty vector control cells (24 h after induction).Only differentially regulated probe sets that are associated with annotated genes are shown, as indicated in the table header. The fold differential regulation is indicated in the last column. Probe.Set.ID = affymetrix probe set identifier; Representative.Public.ID = Representative Public domain ID; UniGene.ID = Unigene id of the gene being interrogated; Gene.Symbol = Symbol of the gene; Chromosomal.Location = chromosomal location of the gene in the human genome; Ensembl = Ensembl id; Entrez.Gene = Entrez gene id; SwissProt = SwissProt id of the protein product of the gene; RefSeq.Protein.ID = RefSeq id of the protein; RefSeq.Transcript.ID = RefSeq id of the transcript; fold change = change between induced and control samples, described as a ratio of expression of a given probe set (XLS 400 kb)

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Kölbl, A.C., Weigl, D., Mulaw, M. et al. The radial nuclear positioning of genes correlates with features of megabase-sized chromatin domains. Chromosome Res 20, 735–752 (2012). https://doi.org/10.1007/s10577-012-9309-9

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  • DOI: https://doi.org/10.1007/s10577-012-9309-9

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