Abstract
Chromatin assembly involves the combined action of ATP-dependent motor proteins and histone chaperones. Because motor proteins in chromatin assembly also function as chromatin remodeling factors, we investigated the relationship between ATP-driven chromatin assembly and chromatin remodeling in the generation of periodic nucleosome arrays. We found that chromatin remodeling-defective Chd1 motor proteins are able to catalyze ATP-dependent chromatin assembly. The resulting nucleosomes are not, however, spaced in periodic arrays. Wild-type Chd1, but not chromatin remodeling-defective Chd1, can catalyze the conversion of randomly-distributed nucleosomes into periodic arrays. These results reveal a functional distinction between ATP-dependent nucleosome assembly and chromatin remodeling, and suggest a model for chromatin assembly in which randomly-distributed nucleosomes are formed by the nucleosome assembly function of Chd1, and then regularly-spaced nucleosome arrays are generated by the chromatin remodeling activity of Chd1. These findings uncover an unforeseen level of specificity in the role of motor proteins in chromatin assembly. DOI:http://dx.doi.org/10.7554/eLife.00863.001.
Highlights
The assembly of nucleosomes is necessary for the regeneration of chromatin following DNA replication, transcription, and DNA repair, and is an active ATP-driven process, as originally discovered by Worcel et al (Glikin et al, 1984; Ruberti and Worcel, 1986)
ATP-dependent factors that participate in chromatin assembly include Chd1, ATRX, and several ISWI-containing complexes, such as ACF (ATP-utilizing chromatin assembly and remodeling factor), CHRAC, RSF, and ToRC (Toutatis-containing chromatin remodeling complex) (Ito et al, 1997; Varga-Weisz et al, 1997; Loyola et al, 2001; Lusser et al, 2005; Lewis et al, 2010; Emelyanov et al, 2012)
By using the restriction enzyme accessibility assay for chromatin remodeling, we found that remodeling activity of yChd1 was comparable to that of human Brg1 (hBrg1) over a range of concentrations (Figure 6A)
Summary
The assembly of nucleosomes is necessary for the regeneration of chromatin following DNA replication, transcription, and DNA repair, and is an active ATP-driven process, as originally discovered by Worcel et al (Glikin et al, 1984; Ruberti and Worcel, 1986). ATP-dependent factors that participate in chromatin assembly include Chd (chromo-ATPase/ helicase-DNA-binding protein 1), ATRX (alpha thalassemia/mental retardation syndrome X-linked), and several ISWI (imitation switch)-containing complexes, such as ACF (ATP-utilizing chromatin assembly and remodeling factor), CHRAC (chromatin accessibility complex), RSF (remodeling and spacing factor), and ToRC (Toutatis-containing chromatin remodeling complex) (Ito et al, 1997; Varga-Weisz et al, 1997; Loyola et al, 2001; Lusser et al, 2005; Lewis et al, 2010; Emelyanov et al, 2012) These motor proteins exhibit both chromatin assembly and remodeling activities, and are members of the SNF2 (sucrose non-fermenting 2) protein family, which comprises the ATPases that are known to be involved in chromatin remodeling
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