Non-specific interactions are sufficient to explain the position of heterochromatic chromocenters and nucleoli in interphase nuclei - PubMed (original) (raw)
Non-specific interactions are sufficient to explain the position of heterochromatic chromocenters and nucleoli in interphase nuclei
S de Nooijer et al. Nucleic Acids Res. 2009 Jun.
Abstract
The organization of the eukaryote nucleus into functional compartments arises by self-organization both through specific protein-protein and protein-DNA interactions and non-specific interactions that lead to entropic effects, such as e.g. depletion attraction. While many specific interactions have so far been demonstrated, the contributions of non-specific interactions are still unclear. We used coarse-grained molecular dynamics simulations of previously published models for Arabidopsis thaliana chromatin organization to show that non-specific interactions can explain the in vivo localization of nucleoli and chromocenters. Also, we quantitatively demonstrate that chromatin looping contributes to the formation of chromosome territories. Our results are consistent with the previously published Rosette model for Arabidopsis chromatin organization and suggest that chromocenter-associated loops play a role in suppressing chromocenter clustering.
Figures
Figure 1.
Graphical depiction of the various models. The most simple model is the linear chain (LC) model, in which chromosomes are modelled as consisting of identical monomers (red) arranged in linear chains with harmonic spring potentials (yellow) connecting the monomers. The linear chains with chromocenters (LCC) model is almost identical to the LC model, but models the centromeric area of the chromocome as a large chromocenter (blue). An expansion of the LCC model is the looped arms with chromocenters model (LAC), in which the chains contain loops. In the Rosette model (after Fransz et al. 2002) the chromosome arms loop out from a chromocenter in several loops. Chromocenters, monomers and bonds are not drawn according to scale.
Figure 2.
Overview showing orthographically rendered snapshots of single configurations from LCC (top row), LAC (middle row) and Rosette (bottom row) model simulations containing 10 chromosomes, with chromocenters, in different colors. Of each configuration, three images are provided: left column shows all monomers in the simulation, middle column shows one chromosome, and the right column shows the localization of chromocenters and nucleoli (brown) only.
Figure 3.
Chromocenter localization and clustering. (a) Histogram showing the fraction of chromocenters in each radial position bin in a LCC model simulation. (b) Distribution of chromocenter radial positions in the Rosette model. (c) Clustering analysis on the simulations of (a and b) showing the average amount of chromocenter clusters in each simulation. (d) Distribution of chromocenter radial positions in the rosette model including a 1.5 μm nucleolus.
Figure 4.
Nucleolus positions in Arabidopsis. On the horizontal axis nucleolus position bins are shown each representing a shell of 0.1 times the nuclear volume available to the nucleolus. On the vertical axis, the fraction of nucleoli in each bin is shown. The solid line shows measured positions in A. thaliana mesophyl nuclei, the dashed line shows the prediction derived from the Rosette model, the line with alternating dashes and dots shows predictions from the LAC model, and the dotted line shows random localization (assuming the nucleolus to have an equal chance to localize to every available position in the nucleus).
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References
- Cremer T, Cremer C, Schneider T, Baumann H, Hens L, Kirsch-Volders M. Analysis of chromosome positions in the interphase nucleus of Chinese hamster cells by laser-UV-microirradiation experiments. Hum. Genet. 1982;62:201–209. - PubMed
- Handwerger K, Gall J. Subnuclear organelles: new insights into form and function. Trends Cell Biol. 2006;16:19–26. - PubMed
- Ye Q, Callebaut I, Pezhman A, Courvalin J, Worman H. Domain-specific interactions of human HP1-type chromodomain proteins and inner nuclear membrane protein LBR. J. Biol. Chem. 1997;272:14983–14989. - PubMed