Abstract
The expression of genes is regulated at many levels. Perhaps the area in which least is known is how nuclear organization influences gene expression. Studies of higher-order chromatin arrangements and their dynamic interactions with other nuclear components have been boosted by recent technical advances. The emerging view is that chromosomes are compartmentalized into discrete territories. The location of a gene within a chromosome territory seems to influence its access to the machinery responsible for specific nuclear functions, such as transcription and splicing. This view is consistent with a topological model for gene regulation.
Key Points
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Chromosomes occupy discrete territories in the cell nucleus and contain distinct chromosome-arm and chromosome-band domains.
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Chromosome territories (CTs) with different gene densities occupy distinct nuclear positions.
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Gene-poor, mid-to-late-replicating chromatin is enriched in nuclear compartments that are located at the nuclear periphery and at the perinucleolar region.
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A compartment for gene-dense, early-replicating chromatin is separated from the compartments for mid-to-late-replicating chromatin.
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Chromatin domains with a DNA content of ∼1 Mb can be detected in nuclei during interphase and in non-cycling cells.
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The interchromatin compartment (IC) contains various types of non-chromatin domains with factors for transcription, splicing, DNA replication and repair.
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The CT–IC model predicts that a specific topological relationship between the IC and chromatin domains is essential for gene regulation.
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The transcriptional status of genes correlates with gene positioning in CTs.
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A dynamic repositioning of genes with respect to centromeric heterochromatin has a role in gene silencing and activation.
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Various computer models of CTs and nuclear architecture make different predictions that can be validated by experimental tests.
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Comprehensive understanding of gene regulation requires much more detailed knowledge of gene expression in the context of nuclear architecture and organization.
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Acknowledgements
This work was supported by the Deutsche Forschungsgemein-schaft, the BMBF (German Human Genome Project) and the German–Israeli Foundation. A first version of the CT–IC model was developed with P. Lichter and others in 1993. We are indebted to our present and past co-workers for helping us to shape the views presented here. We thank S. Fakan, T. Misteli, T. Pederson, R. Driel, L. Zech and several unnamed referees for their helpful comments.
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Glossary
- EPIGENETICS
-
Any heritable influence (in the progeny of cells or of individuals) on gene activity, unaccompanied by a change in DNA sequence.
- CHROMOSOME PAINTING
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Visualization of individual, whole chromosomes by fluorescence in situ hybridization (FISH).
- CENTROMERIC HETEROCHROMATIN
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Comprises the genetically inert, constitutive heterochromatin of the centromere and is built up from tandem repetitive DNA sequences.
- EPIFLUORESCENCE MICROSCOPY
-
The entire cell is illuminated and fluorescence is recorded through the same objective from an entire focal plane.
- ABBE LIMIT
-
Theoretical limit of light-microscopic resolution defined in 1873 by Ernst Abbe. This limit holds for conventional light microscopy but can be overcome by new laser microscopic approaches (Box 1).
- SPECKLES
-
Irregularly shaped regions that contain splicing factors. At the electron-microscopic level they correspond to interchromatin granule clusters (IGCs), which function in the storage and supply of components of the pre-mRNA splicing machinery, and perichromatin fibrils located in the vicinity of IGCs.
- CAJAL BODIES
-
(also known as coiled bodies). Nuclear organelles of unknown function named in honour of Ramón y Cajal. Cajal bodies are possibly sites of assembly or modification of the transcription machinery of the nucleus.
- PML BODIES
-
Contain wild-type promyelocytic leukaemia (PML) protein and other proteins. Their function remains elusive, but might be related to transcription control.
- CHROMATIN FIBRES
-
These 30-nm fibres are produced by the compaction of 10-nm nucleosome fibres. Nucleosome fibres are visible under the electron microscope after treatments that unfold higher-order chromatin packaging into a 'beads-on-a-string' 10-nm diameter form.
- MICRODISSECTION PROBES
-
DNA probes established from microdissected chromosomal subregions. The probes are useful for the labelling of chromosome arms and bands.
- CONFOCAL LASER SCANNING MICROSCOPES
-
(CLSM). A three-dimensional cell is illuminated and the fluorescence is recorded point by point.
- SC-35 DOMAINS
-
The essential non-snRNP (small nuclear ribonucleoprotein particles) splicing factor SC-35 shows a speckled distribution in the nucleus that co-localizes with snRNPs in speckles.
- LOOP BASE SPRINGS
-
In the multiloop subcompartment model of chromosome territory architecture, stiff springs were assumed to exist at the loop bases for a simulation of chromosome territory anchor proteins.
- CHROMOSOME TERRITORY ANCHOR PROTEINS
-
Proteins that are essential for the maintenance of chromosome territories.
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Cremer, T., Cremer, C. Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Nat Rev Genet 2, 292–301 (2001). https://doi.org/10.1038/35066075
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DOI: https://doi.org/10.1038/35066075
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