Brownian dynamics simulation of directional sliding of histone octamers caused by DNA bending

Chromatin-remodeling complexes such as SWI/SNF and RSC of yeast can perturb the structure of nucleosomes in an ATP-dependent manner. Experimental results prove that this chromatin remodeling process involves DNA bending. We simulate the effect of DNA bending, caused by chromatin-remodeling complexes, on directional sliding of histone octamers by Brownian dynamics simulation. The simulation results show that, after a DNA loop being generated at the side of a nucleosome, the histone octamer slides towards this DNA loop until the loop disappears. The DNA loop size is an important factor affecting the process of directional sliding of the histone octamer.

Figure 1

(Color online) After getting a stable nucleosome structure (a), a DNA bending with contour length of $9{\sigma }_m$ is introduced at the left side of the nucleosome (b). The histone octamer slides towards this DNA loop. The length unit for all the axes is ${\sigma }_m$ (i.e., $2.3\mathrm{nm}$). (The same length unit is used in all the following similar figures.) The time corresponding to each snapshot is: (a) 0; (b) 0.009; (c) 0.046; (d) 0.114; (e) 0.2; and (f) $0.858\mathrm{s}$. The yellow spheres represent the DNA part that initially wrap around the histone octamer. The pink DNA sphere represents the location where the bending starts.

Figure 2

The distance between the histone octamer and every DNA sphere. These curves correspond to the snapshots in Fig. 1. The time is: (a) 0; (b) 0.009; (c) 0.046; (d) 0.114; (e) 0.2; and (f) $0.858\mathrm{s}$. The horizontal axes correspond to the serial numbers of the DNA spheres. The vertical axes correspond to the center distances between the histone octamer and the DNA spheres.

Figure 3

(a) The sliding distance and (b) the sliding speed of the histone octamer as a function of time. The solid curve in (b) is a polynomial fit of the dots for guiding the eyes.

Figure 4

(Color online) When three DNA loops are introduced successively, the histone octamer slides continually. The time corresponding to every snapshot is: (a) 0.0681; (b) 2.4701; (c) 2.6074; (d) 5.1462; (e) 5.2148; and (f) $7.7193\mathrm{s}$. The contour length of each DNA loop is $14{\sigma }_m$.

Figure 5

The sliding distance of the histone octamer as a function of time.

Figure 6

The energy of the system in the process of histone octamer’s sliding.

Figure 7

(Color online) When the contour length of the DNA loop is increased to $20{\sigma }_m$, the histone octamer does not slide. The snapshot is taken at $0.586\mathrm{s}$ after the bending is introduced.

Figure 8

(a) The histone octamer’s average sliding speed as a function of DNA loop size. (b) The time for the histone octamer to slide 90% of the DNA loop size. Dots are the results of simulation. Solid curves are the fits (see text).

Figure 9

(Color online) The histone octamer stops directional sliding when the DNA loop is released. The DNA loop size is $9{\sigma }_m$. (a) The histone octamer slides a distance of $4.8{\sigma }_m$ towards the DNA loop in $0.245\mathrm{s}$. (b) Snapshot taken at $0.858\mathrm{s}$ after the DNA loop is released at the time of $0.245\mathrm{s}$.

Figure 10

Relation between the bending time and the percent of sliding distance relative to the contour length of the DNA loop. The DNA loop size is $14{\sigma }_m$.

Figure 11

(Color online) Model for the interaction between a nucleosome and a chromatin-remodeling complex. In the model, the histone octamer (the large green sphere) slides after a DNA bending is produced by the chromatin-remodeling complex (gray balls connected with blue bars) at one side of the nucleosome. In the process of the histone octamer’s sliding, the DNA loop is shrinking. At last, the DNA loop disappears and the histone octamer stops sliding.