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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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Selected significant modification-remodeling pairs. (A-D) Distributions of expression levels (log2 transformed) accompanying the perturbation of the remodeler are presented for the modification cohort and the control group (rest of the genes). Modification levels at promoters are also shown for the remodeling cohort and the control group. Ac represents acetylation, while me indicates methylation (e.g. me3 indicates trimethylation). Error bars were calculated by bootstrapping.
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Figure 2: Selected significant modification-remodeling pairs. (A-D) Distributions of expression levels (log2 transformed) accompanying the perturbation of the remodeler are presented for the modification cohort and the control group (rest of the genes). Modification levels at promoters are also shown for the remodeling cohort and the control group. Ac represents acetylation, while me indicates methylation (e.g. me3 indicates trimethylation). Error bars were calculated by bootstrapping.

Mentions: Rsc3, Rsc8 and Rsc30 are components of the RSC chromatin remodeling complex which contains almost half of the known bromodomains in the yeast genome for binding acetylated lysines [15]. A recent study has demonstrated that the ATP-dependent remodelling complex RSC shows a striking preference for H3 but not H4 acetylated chromatin [5]. It has also been reported that H3K14 (i.e. histone H3 lysine 14) acetylation acts to increase recruitment of the RSC to nucleosomes [16]. Our results are consistent with these observations: the three components interact with H3 acetylation, but not H4 acetylation. Rsc3 interacts with H3K9, H3K14, and H3Nterm acetylation, Rsc30 is associated with H3K9, H3K14, H3K18, and H3Nterm acetylation, and Rsc8 is connected with H3K14, H3K18, and H3Nterm acetylation. In addition to these known interactions, our results show that Rsc3 interacts with H2A.ZK14 acetylation, Rsc30 is associated with H2A.ZK14 acetylation, H3K4 and H3K36 trimethylation, and Rsc8 is connected with H2A.ZK14 acetylation and H3K4 trimethylation. Interestingly, our results demonstrate that Rsc3 and Rsc30 regulate the associated modification cohort in distinct ways (positive and negative regulation, respectively, Figure 2A, B), consistent with experimental evidence that they have different roles in regulation, although they interact physically [17].


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)

Selected significant modification-remodeling pairs. (A-D) Distributions of expression levels (log2 transformed) accompanying the perturbation of the remodeler are presented for the modification cohort and the control group (rest of the genes). Modification levels at promoters are also shown for the remodeling cohort and the control group. Ac represents acetylation, while me indicates methylation (e.g. me3 indicates trimethylation). 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 2: Selected significant modification-remodeling pairs. (A-D) Distributions of expression levels (log2 transformed) accompanying the perturbation of the remodeler are presented for the modification cohort and the control group (rest of the genes). Modification levels at promoters are also shown for the remodeling cohort and the control group. Ac represents acetylation, while me indicates methylation (e.g. me3 indicates trimethylation). Error bars were calculated by bootstrapping.
Mentions: Rsc3, Rsc8 and Rsc30 are components of the RSC chromatin remodeling complex which contains almost half of the known bromodomains in the yeast genome for binding acetylated lysines [15]. A recent study has demonstrated that the ATP-dependent remodelling complex RSC shows a striking preference for H3 but not H4 acetylated chromatin [5]. It has also been reported that H3K14 (i.e. histone H3 lysine 14) acetylation acts to increase recruitment of the RSC to nucleosomes [16]. Our results are consistent with these observations: the three components interact with H3 acetylation, but not H4 acetylation. Rsc3 interacts with H3K9, H3K14, and H3Nterm acetylation, Rsc30 is associated with H3K9, H3K14, H3K18, and H3Nterm acetylation, and Rsc8 is connected with H3K14, H3K18, and H3Nterm acetylation. In addition to these known interactions, our results show that Rsc3 interacts with H2A.ZK14 acetylation, Rsc30 is associated with H2A.ZK14 acetylation, H3K4 and H3K36 trimethylation, and Rsc8 is connected with H2A.ZK14 acetylation and H3K4 trimethylation. Interestingly, our results demonstrate that Rsc3 and Rsc30 regulate the associated modification cohort in distinct ways (positive and negative regulation, respectively, Figure 2A, B), consistent with experimental evidence that they have different roles in regulation, although they interact physically [17].

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
Related in: MedlinePlus