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Genome-wide analysis of interactions between ATP-dependent chromatin remodeling and histone modifications.

Dai Z, Dai X, Xiang Q, Feng J, Wang J, Deng Y, He C - BMC Genomics (2009)

Bottom Line: Our results also demonstrate that most chromatin remodeling-modification interactions act via interactions of remodelers with both histone-modifying enzymes and histone residues.We also found that the co-occurrence of both modification and remodeling has significantly different influences on multiple gene features (e.g. nucleosome occupancy) compared with the presence of either one.Our results suggest that distinct strategies for regulating chromatin activity are selectively employed by genes with different properties.

View Article: PubMed Central - HTML - PubMed

Affiliation: Electronic Department, Sun Yat-Sen University, Guangzhou, PR China. zhimdai@gmail.com

ABSTRACT

Background: ATP-dependent chromatin remodeling and the covalent modification of histones play central roles in determining chromatin structure and function. Although several specific interactions between these two activities have been elaborated, the global landscape remains to be elucidated.

Results: In this paper, we have developed a computational method to generate the first genome-wide landscape of interactions between ATP-dependent chromatin remodeling and the covalent modification of histones in Saccharomyces cerevisiae. Our method succeeds in identifying known interactions and uncovers many previously unknown interactions between these two activities. Analysis of the genome-wide picture revealed that transcription-related modifications tend to interact with more chromatin remodelers. Our results also demonstrate that most chromatin remodeling-modification interactions act via interactions of remodelers with both histone-modifying enzymes and histone residues. We also found that the co-occurrence of both modification and remodeling has significantly different influences on multiple gene features (e.g. nucleosome occupancy) compared with the presence of either one.

Conclusion: We gave the first genome-wide picture of ATP-dependent chromatin remodeling-histone modification interactions. We also revealed how these two activities work together to regulate chromatin structure and function. Our results suggest that distinct strategies for regulating chromatin activity are selectively employed by genes with different properties.

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Gene features that distinguish the three cohorts. (A) Average values that correspond to nucleosome occupancy [34], transcription rate [26], gene expression level [26], openING rate, the turnover rate of H3 histone [27] and PNAP II occupancy [44] are shown for modification-independent cohort (green), remodeling-independent cohort (red) and modification and remodeling cohort (blue). Values in each property were normalized (nucleosome occupancy and turnover rates were normalized among all promoters, RNAP II occupancy were normalized among all 200 bp upstream regions), such that their means are zero and standard deviations are one. (B) Ratio of transcription factor binding sites [37] localized in nucleosome [34], as well as ratio of promoters with multiple binding sites [37], TATA box [41], and H2A.Z [42] is shown for modification-independent cohort (green), remodeling-independent cohort (red), modification and remodeling cohort (blue) and all genes (purple). Error bars were calculated by bootstrapping.
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Figure 3: Gene features that distinguish the three cohorts. (A) Average values that correspond to nucleosome occupancy [34], transcription rate [26], gene expression level [26], openING rate, the turnover rate of H3 histone [27] and PNAP II occupancy [44] are shown for modification-independent cohort (green), remodeling-independent cohort (red) and modification and remodeling cohort (blue). Values in each property were normalized (nucleosome occupancy and turnover rates were normalized among all promoters, RNAP II occupancy were normalized among all 200 bp upstream regions), such that their means are zero and standard deviations are one. (B) Ratio of transcription factor binding sites [37] localized in nucleosome [34], as well as ratio of promoters with multiple binding sites [37], TATA box [41], and H2A.Z [42] is shown for modification-independent cohort (green), remodeling-independent cohort (red), modification and remodeling cohort (blue) and all genes (purple). Error bars were calculated by bootstrapping.

Mentions: We first analyzed the three gene cohorts in terms of nucleosome occupancy. Recent studies have measured high-resolution nucleosome occupancy across the yeast genome [34,35]. These valuable data allow for a direct examination of the effect of different activities on nucleosome occupancy. Modification and remodeling cohort promoters have significantly lower nucleosome occupancy [34] than the other two cohorts (Figure 3A). It is known that genomic DNA sequence is an important determinant of nucleosome positioning [36]. However, there is no significant difference in sequence preferences for nucleosomes [34,36] among the three cohorts (data not shown), indicating that the differences in nucleosome occupancy among the three cohorts are not due to the differences in sequence preferences for nucleosomes. These results imply that a combination of ATP-dependent chromatin remodeling and histone modifications causes lower nucleosome occupancy.


Genome-wide analysis of interactions between ATP-dependent chromatin remodeling and histone modifications.

Dai Z, Dai X, Xiang Q, Feng J, Wang J, Deng Y, He C - BMC Genomics (2009)

Gene features that distinguish the three cohorts. (A) Average values that correspond to nucleosome occupancy [34], transcription rate [26], gene expression level [26], openING rate, the turnover rate of H3 histone [27] and PNAP II occupancy [44] are shown for modification-independent cohort (green), remodeling-independent cohort (red) and modification and remodeling cohort (blue). Values in each property were normalized (nucleosome occupancy and turnover rates were normalized among all promoters, RNAP II occupancy were normalized among all 200 bp upstream regions), such that their means are zero and standard deviations are one. (B) Ratio of transcription factor binding sites [37] localized in nucleosome [34], as well as ratio of promoters with multiple binding sites [37], TATA box [41], and H2A.Z [42] is shown for modification-independent cohort (green), remodeling-independent cohort (red), modification and remodeling cohort (blue) and all genes (purple). Error bars were calculated by bootstrapping.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2713269&req=5

Figure 3: Gene features that distinguish the three cohorts. (A) Average values that correspond to nucleosome occupancy [34], transcription rate [26], gene expression level [26], openING rate, the turnover rate of H3 histone [27] and PNAP II occupancy [44] are shown for modification-independent cohort (green), remodeling-independent cohort (red) and modification and remodeling cohort (blue). Values in each property were normalized (nucleosome occupancy and turnover rates were normalized among all promoters, RNAP II occupancy were normalized among all 200 bp upstream regions), such that their means are zero and standard deviations are one. (B) Ratio of transcription factor binding sites [37] localized in nucleosome [34], as well as ratio of promoters with multiple binding sites [37], TATA box [41], and H2A.Z [42] is shown for modification-independent cohort (green), remodeling-independent cohort (red), modification and remodeling cohort (blue) and all genes (purple). Error bars were calculated by bootstrapping.
Mentions: We first analyzed the three gene cohorts in terms of nucleosome occupancy. Recent studies have measured high-resolution nucleosome occupancy across the yeast genome [34,35]. These valuable data allow for a direct examination of the effect of different activities on nucleosome occupancy. Modification and remodeling cohort promoters have significantly lower nucleosome occupancy [34] than the other two cohorts (Figure 3A). It is known that genomic DNA sequence is an important determinant of nucleosome positioning [36]. However, there is no significant difference in sequence preferences for nucleosomes [34,36] among the three cohorts (data not shown), indicating that the differences in nucleosome occupancy among the three cohorts are not due to the differences in sequence preferences for nucleosomes. These results imply that a combination of ATP-dependent chromatin remodeling and histone modifications causes lower nucleosome occupancy.

Bottom Line: Our results also demonstrate that most chromatin remodeling-modification interactions act via interactions of remodelers with both histone-modifying enzymes and histone residues.We also found that the co-occurrence of both modification and remodeling has significantly different influences on multiple gene features (e.g. nucleosome occupancy) compared with the presence of either one.Our results suggest that distinct strategies for regulating chromatin activity are selectively employed by genes with different properties.

View Article: PubMed Central - HTML - PubMed

Affiliation: Electronic Department, Sun Yat-Sen University, Guangzhou, PR China. zhimdai@gmail.com

ABSTRACT

Background: ATP-dependent chromatin remodeling and the covalent modification of histones play central roles in determining chromatin structure and function. Although several specific interactions between these two activities have been elaborated, the global landscape remains to be elucidated.

Results: In this paper, we have developed a computational method to generate the first genome-wide landscape of interactions between ATP-dependent chromatin remodeling and the covalent modification of histones in Saccharomyces cerevisiae. Our method succeeds in identifying known interactions and uncovers many previously unknown interactions between these two activities. Analysis of the genome-wide picture revealed that transcription-related modifications tend to interact with more chromatin remodelers. Our results also demonstrate that most chromatin remodeling-modification interactions act via interactions of remodelers with both histone-modifying enzymes and histone residues. We also found that the co-occurrence of both modification and remodeling has significantly different influences on multiple gene features (e.g. nucleosome occupancy) compared with the presence of either one.

Conclusion: We gave the first genome-wide picture of ATP-dependent chromatin remodeling-histone modification interactions. We also revealed how these two activities work together to regulate chromatin structure and function. Our results suggest that distinct strategies for regulating chromatin activity are selectively employed by genes with different properties.

Show MeSH