The genome and the nucleus: a marriage made by evolution

Abstract

Genomes are housed within cell nuclei as individual chromosome territories. Nuclei contain several architectural structures that interact and influence the genome. In this review, we discuss how the genome may be organised within its nuclear environment with the position of chromosomes inside nuclei being either influenced by gene density or by chromosomes size. We compare interphase genome organisation in diverse species and reveal similarities and differences between evolutionary divergent organisms. Genome organisation is also discussed with relevance to regulation of gene expression, development and differentiation and asks whether large movements of whole chromosomes are really observed during differentiation. Literature and data describing alterations to genome organisation in disease are also discussed. Further, the nuclear structures that are involved in genome function are described, with reference to what happens to the genome when these structures contain protein from mutant genes as in the laminopathies.

Radial chromatin positioning is shaped by local gene density, not by gene expression

“…Such patterns have been found evolutionarily conserved over several hundred millions of years (Alexandrova et al 2003;Federico et al 2006;Habermann et al 2001;Neusser et al 2007;Postberg et al 2005;Tanabe et al 2002) and illustrate that the radial arrangement of chromatin in the interphase nucleus represents a basic principle of nuclear architecture (for review, see Foster and Bridger 2005;Kosak and Groudine 2004;Misteli 2004;Pederson 2004;Zink 2006).…”

The radial arrangement of the human chromosome 7 in the lymphocyte cell nucleus is associated with chromosomal band gene density

“…In fact, the chromosomal DNA showing the highest GC level is endowed with the highest gene densities, early replication during the S phase of the cell cycle, and a more open chromatin structure, in contrast to the GC-poorest DNA that has the opposite features (Ferreira et al 1997;Sadoni et al 1999;Saccone et al, 2002;Tanabe et al 2002a;Boutanaev et al 2005;Foster and Bridger 2005;Petrova et al 2006). The compartmentalization of the cell nucleus is also associated with gene expression activity, with transcripts and splicing snRNPs preferentially located at the nuclear interior, whereas the nuclear periphery, largely occupied by heterochromatin, is generally transcriptionally inactive (Strouboulis and Wolffe 1996; Brown et al 1997;Andrulis et al 1998;Cockell and Gasser 1999;Lukasova et al 2002;Foster and Bridger 2005). A striking example, in this regard, concerns the inactive X chromosome in mammalian female cells, which is typically located towards the nuclear envelope forming the very compact structure of the Barr body, but with a large number of genes located away from the bulk of the chromosome territory (Clemson et al 2006).…”

Parental genomes mix in mule and human cell nuclei

“…Gene-rich as well as small chromosomes are preferentially at internal positions and gene-poor or large chromosomes at peripheral positions (for reviews, see Foster and Bridger 2005;Cremer et al 2006;Lanctôt et al 2007). Homologous association as observed in Drosophila can be excluded as a general theme in mammals, since numerous FISH studies found two distinct chromosome territories in interphase nuclei.…”