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Condensin and cohesin complexity: the expanding repertoire of functions

Nature Reviews Genetics volume 11, pages 391–404 (2010)Cite this article

Subjects

Key Points

  • Cohesin contributes to intrachromosomal loops that regulate metazoan gene expression by constraining interactions between promoter and enhancer elements. These structures can be subject to regulation during development.

  • Condensin binds yeast tRNA genes to promote their aggregation at the nucleolus and can inhibit interactions between homologous chromosomes during interphase.

  • The Caenorhabditis elegans dosage compensation complex serves as a paradigm for the regulation of gene expression by condensin. The complex regulates transcription across an entire sex chromosome but does not always bind in proximity to regulatory targets.

  • Cohesin is required for the acquisition of cell-lineage-specific traits in the Drosophila melanogaster nervous system, and this role does not require passage through the cell cycle.

  • Meiosis-specific functions of condensin and cohesin abound. Condensin regulates the number and distribution of double-strand breaks and crossovers, whereas cohesin is essential for the assembly of a structure called the axial element, which forms on meiotic chromosomes and is important for proper association of homologous chromosomes and for crossover recombination.

  • Specialization of condensin and cohesin function is achieved through swapping of homologous subunits to create molecular machines with similar architecture but distinct biological roles.

Abstract

Condensin and cohesin complexes act in diverse nuclear processes in addition to their widely known roles in chromosome compaction and sister chromatid cohesion. Recent work has elucidated the contribution of condensin and cohesin to interphase genome organization, control of gene expression, metazoan development and meiosis. Despite these wide-ranging functions, several themes have come to light: both complexes establish higher-order chromosome structure by inhibiting or promoting interactions between distant genomic regions, both complexes influence the chromosomal association of other proteins, and both complexes achieve functional specialization by swapping homologous subunits. Emerging data are expanding the range of processes in which condensin and cohesin are known to participate and are enhancing our knowledge of how chromosome architecture is regulated to influence numerous cellular functions.

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Figure 1: Dosage compensation in Caenorhabditis elegans.
Figure 2: Cohesin function in gene expression.

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Acknowledgements

We apologize to researchers whose work we were unable to cite owing to space constraints. We thank R. Holmes, F. Tan and L. Wahba for comments on the manuscript, A. Michel and B. Pferdehirt for images in figure 1, and J. Gunther for illustrations. A.J.W. has been funded by a Sir Henry Welcome Post-Doctoral Research Fellowship and B.J.M. by the US National Institutes of Health. B.J.M. is an Investigator of the Howard Hughes Medical Institute.

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Author notes

  1. Andrew J. Wood and Aaron F. Severson: These authors contributed equally to this work.

Authors and Affiliations

  1. Howard Hughes Medical Institute and Department of Molecular and Cell Biology, University of California-Berkeley, 16 Barker Hall, MC 3204, Berkeley, 94720-3204, California, USA

    Andrew J. Wood, Aaron F. Severson & Barbara J. Meyer

  2. Department of Medical and Molecular Genetics, King's College London, Guy's Hospital, London, SE1 9RT, UK

    Andrew J. Wood

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  1. Andrew J. Wood
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WormBase

Glossary

Catenations

Topological linkages between duplex DNA. Catenations between sister chromatids arise during replication.

CCCTC-binding factor

A zinc-finger protein associated with diverse context-dependent effects on transcription.

Insulator

A genetic boundary element that limits the distance over which regulatory signals can act.

Chromosome conformation capture

A method for identifying physical interactions between distant DNA sequences.

Nucleolus

A subnuclear region in which components of the translational machinery are synthesized. It is a site of abundant transcription by RNA polymerase I and III.

Transvection

The ability of a gene on one chromosome to influence the activity of an allele on the opposite chromosome when the chromosomes are paired.

Polytene chromosomes

DNA structures containing many paired sister chromatids, which are produced by multiple rounds of DNA replication without cell division.

Supercoils

Twists applied to DNA that can occur in the same (positive) or opposite (negative) orientation to the double helix.

Position effect variegation

Variegated expression patterns that arise owing to intercellular differences in epigenetic gene silencing, typically observed when reporter genes are brought into proximity with heterochromatin.

Genomic imprinting

Epigenetic marks that are differentially established during male and female gametogenesis and lead to allele-specific gene expression after fertilization.

Axon pruning

The selective loss of neuronal outgrowths to refine synaptic connectivity during development.

Genetic mosaics

Animals in which homozygous mutations are carried by only a small clone of cells.

Axial elements

Linear structures that assemble along the length of meiotic chromosomes. Axial elements become the lateral elements of the mature synaptonemal complex.

Co-orient

Attach to microtubules from the same spindle pole.

Bi-orient

Attach to microtubules from opposite spindle poles.

Synaptonemal complex

A proteinaceous structure that forms between pairs of homologous chromosomes during synapsis and facilitates crossover recombination.

Separase

A cysteine protease that cleaves the α-kleisin subunit of cohesin at the onset of anaphase to allow sister chromatid disjunction.

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Wood, A., Severson, A. & Meyer, B. Condensin and cohesin complexity: the expanding repertoire of functions. Nat Rev Genet 11, 391–404 (2010). https://doi.org/10.1038/nrg2794

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