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SWI/SNF- and RSC-catalyzed nucleosome mobilization requires internal DNA loop translocation within nucleosomes.

ABSTRACT: The multisubunit SWI/SNF and RSC complexes utilize energy derived from ATP hydrolysis to mobilize nucleosomes and render the DNA accessible for various nuclear processes. Here we test the idea that remodeling involves intermediates with mobile DNA bulges or loops within the nucleosome by cross-linking the H2A N- or C-terminal tails together to generate protein "loops" that constrict separation of the DNA from the histone surface. Analyses indicate that this intranucleosomal cross-linking causes little or no change in remodeling-dependent exposure of DNA sequences within the nucleosome to restriction enzymes. However, cross-linking inhibits nucleosome mobilization and blocks complete movement of nucleosomes to extreme end positions on the DNA fragments. These results are consistent with evidence that nucleosome remodeling involves intermediates with DNA loops on the nucleosome surface but indicate that such loops do not freely diffuse about the surface of the histone octamer. We propose a threading model for movement of DNA loops around the perimeter of the nucleosome core.

SUBMITTER: Liu N

PROVIDER: S-EPMC3187282 | biostudies-literature | 2011 Oct

REPOSITORIES: biostudies-literature

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SWI/SNF- and RSC-catalyzed nucleosome mobilization requires internal DNA loop translocation within nucleosomes.

Liu Ning N Peterson Craig L CL Hayes Jeffrey J JJ

Molecular and cellular biology 20110822 20

The multisubunit SWI/SNF and RSC complexes utilize energy derived from ATP hydrolysis to mobilize nucleosomes and render the DNA accessible for various nuclear processes. Here we test the idea that remodeling involves intermediates with mobile DNA bulges or loops within the nucleosome by cross-linking the H2A N- or C-terminal tails together to generate protein "loops" that constrict separation of the DNA from the histone surface. Analyses indicate that this intranucleosomal cross-linking causes ...[more]

PMID: 21859889

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Project description:SWI/SNF-family chromatin remodelling complexes conduct nucleosome sliding and ejection to provide DNA-binding proteins access to their sites in chromatin. RSC is an essential and abundant SWI/SNF-family chromatin remodeller from S. cerevisiae that both slides and ejects nucleosomes. However, how ejection versus sliding is chosen, regulated and implemented by any remodeller remains largely unknown. The RSC catalytic subunit Sth1 conducts ATP-dependent DNA translocation, pumping DNA around the nucleosome, providing a property that might underlie both sliding and ejection. Sth1 shares with other SWI/SNF-family ATPases direct binding to two nuclear actin-related proteins (ARPs), but how ARPs impact DNA translocation, sliding and ejection is unknown. Here, we reveal that nucleosome ejection by RSC requires ARPs, and that ARPs improve ‘coupling’ – the efficiency of DNA translocation by Sth1 relative to ATP hydrolysis – thus, enhancing DNA translocation. We further characterize two domains within Sth1 (termed PTH and P1), showing they separately regulate ATP hydrolysis or ‘coupling’, respectively. Interestingly, gain-of-function PTH or P1 mutations suppress arpΔ lethality, and improve ATPase or coupling activities, enabling Sth1 to efficiently slide and eject nucleosomes without ARPs. Moreover, PTH mutations greatly improved DNA translocation velocity. Overall, our results provide a logic for regulating nucleosome sliding versus ejection: both modes involve DNA translocation, but ejection requires a higher magnitude. Here, low-to-moderate ATPase and coupling activity integrate to confer low-to-moderate sliding, whereas high ATPase and/or coupling combine to provide efficient and rapid DNA translocation, consistent with the simultaneous rupture of multiple histone-DNA contacts, causing histone loss/ejection. Our discovery of an ARP module and regulatory domains that regulate sliding and ejection suggests a mechanistic platform through which activators and histone epitopes may guide the remodelling outcome of SWI/SNF-family chromatin remodellers.

Dataset Information

SWI/SNF- and RSC-catalyzed nucleosome mobilization requires internal DNA loop translocation within nucleosomes.

Publications

SWI/SNF- and RSC-catalyzed nucleosome mobilization requires internal DNA loop translocation within nucleosomes.

Similar Datasets

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