The SnAC Domain of SWI/SNF is a Histone Anchor Required for Remodeling

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2012 Nov 15

PMID 23149935

Citations 33

Authors

Payel Sen

Paula Vivas

Mekonnen Lemma Dechassa

Alex M Mooney

Michael G Poirier

Blaine Bartholomew

Affiliations

Soon will be listed here.

Abstract

The SWI/SNF chromatin remodeling complex changes the positions where nucleosomes are bound to DNA, exchanges out histone dimers, and disassembles nucleosomes. All of these activities depend on ATP hydrolysis by the catalytic subunit Snf2, containing a DNA-dependent ATPase domain. Here we examine the role of another domain in Snf2 called SnAC (Snf2 ATP coupling) that was shown previously to regulate the ATPase activity of SWI/SNF. We have found that SnAC has another function besides regulation of ATPase activity that is even more critical for nucleosome remodeling by SWI/SNF. We have found that deletion of the SnAC domain strongly uncouples ATP hydrolysis from nucleosome movement. Deletion of SnAC does not adversely affect the rate, processivity, or pulling force of SWI/SNF to translocate along free DNA in an ATP-dependent manner. The uncoupling of ATP hydrolysis from nucleosome movement is shown to be due to loss of SnAC binding to the histone surface of nucleosomes. While the SnAC domain targets both the ATPase domain and histones, the SnAC domain as a histone anchor plays a more critical role in remodeling because it is required to convert DNA translocation into nucleosome movement.

Citing Articles

Single-molecule imaging of SWI/SNF chromatin remodelers reveals bromodomain-mediated and cancer-mutants-specific landscape of multi-modal DNA-binding dynamics.

Engl W, Kunstar-Thomas A, Chen S, Ng W, Sielaff H, Zhao Z Nat Commun. 2024; 15(1):7646.

PMID: 39223123 PMC: 11369179. DOI: 10.1038/s41467-024-52040-y.

Chromatin remodellers as therapeutic targets.

Malone H, Roberts C Nat Rev Drug Discov. 2024; 23(9):661-681.

PMID: 39014081 PMC: 11534152. DOI: 10.1038/s41573-024-00978-5.

The AT-hook is an evolutionarily conserved auto-regulatory domain of SWI/SNF required for cell lineage priming.

Saha D, Hailu S, Hada A, Lee J, Luo J, Ranish J Nat Commun. 2023; 14(1):4682.

PMID: 37542049 PMC: 10403523. DOI: 10.1038/s41467-023-40386-8.

SWI/SNF Chromatin Remodelers: Structural, Functional and Mechanistic Implications.

Singh A, Modak S, Chaturvedi M, Purohit J Cell Biochem Biophys. 2023; 81(2):167-187.

PMID: 37119511 DOI: 10.1007/s12013-023-01140-5.

Mechanism of action of the SWI/SNF family complexes.

Chen K, Yuan J, Sia Y, Chen Z Nucleus. 2023; 14(1):2165604.

PMID: 36633435 PMC: 9839376. DOI: 10.1080/19491034.2023.2165604.

References

Brower-Toland B, Smith C, Yeh R, Lis J, Peterson C, Wang M . Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc Natl Acad Sci U S A. 2002; 99(4):1960-5. PMC: 122302. DOI: 10.1073/pnas.022638399. View

Traviglia S, Datwyler S, Yan D, Ishihama A, Meares C . Targeted protein footprinting: where different transcription factors bind to RNA polymerase. Biochemistry. 2000; 38(48):15774-8. DOI: 10.1021/bi9917232. View

Zofall M, Persinger J, Kassabov S, Bartholomew B . Chromatin remodeling by ISW2 and SWI/SNF requires DNA translocation inside the nucleosome. Nat Struct Mol Biol. 2006; 13(4):339-46. DOI: 10.1038/nsmb1071. View

Szerlong H, Hinata K, Viswanathan R, Erdjument-Bromage H, Tempst P, Cairns B . The HSA domain binds nuclear actin-related proteins to regulate chromatin-remodeling ATPases. Nat Struct Mol Biol. 2008; 15(5):469-76. PMC: 2810487. DOI: 10.1038/nsmb.1403. View

Velankar S, Soultanas P, Dillingham M, Subramanya H, Wigley D . Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell. 1999; 97(1):75-84. DOI: 10.1016/s0092-8674(00)80716-3. View

Clapier C, Cairns B . The biology of chromatin remodeling complexes. Annu Rev Biochem. 2009; 78:273-304. DOI: 10.1146/annurev.biochem.77.062706.153223. View

Dang W, Bartholomew B . Domain architecture of the catalytic subunit in the ISW2-nucleosome complex. Mol Cell Biol. 2007; 27(23):8306-17. PMC: 2169183. DOI: 10.1128/MCB.01351-07. View

Kassabov S, Henry N, Zofall M, Tsukiyama T, Bartholomew B . High-resolution mapping of changes in histone-DNA contacts of nucleosomes remodeled by ISW2. Mol Cell Biol. 2002; 22(21):7524-34. PMC: 135677. DOI: 10.1128/MCB.22.21.7524-7534.2002. View

Chen H, Hahn S . Binding of TFIIB to RNA polymerase II: Mapping the binding site for the TFIIB zinc ribbon domain within the preinitiation complex. Mol Cell. 2003; 12(2):437-47. DOI: 10.1016/s1097-2765(03)00306-x. View

10.

Hota S, Bartholomew B . Diversity of operation in ATP-dependent chromatin remodelers. Biochim Biophys Acta. 2011; 1809(9):476-87. PMC: 3171594. DOI: 10.1016/j.bbagrm.2011.05.007. View

11.

Datwyler S, Meares C . Artificial iron-dependent proteases. Met Ions Biol Syst. 2001; 38:213-54. View

12.

Sirinakis G, Clapier C, Gao Y, Viswanathan R, Cairns B, Zhang Y . The RSC chromatin remodelling ATPase translocates DNA with high force and small step size. EMBO J. 2011; 30(12):2364-72. PMC: 3116276. DOI: 10.1038/emboj.2011.141. View

13.

Dechassa M, Zhang B, Horowitz-Scherer R, Persinger J, Woodcock C, Peterson C . Architecture of the SWI/SNF-nucleosome complex. Mol Cell Biol. 2008; 28(19):6010-21. PMC: 2547009. DOI: 10.1128/MCB.00693-08. View

14.

Chatterjee N, Sinha D, Lemma-Dechassa M, Tan S, Shogren-Knaak M, Bartholomew B . Histone H3 tail acetylation modulates ATP-dependent remodeling through multiple mechanisms. Nucleic Acids Res. 2011; 39(19):8378-91. PMC: 3201869. DOI: 10.1093/nar/gkr535. View

15.

Kagalwala M, Glaus B, Dang W, Zofall M, Bartholomew B . Topography of the ISW2-nucleosome complex: insights into nucleosome spacing and chromatin remodeling. EMBO J. 2004; 23(10):2092-104. PMC: 424408. DOI: 10.1038/sj.emboj.7600220. View

16.

Fairman-Williams M, Guenther U, Jankowsky E . SF1 and SF2 helicases: family matters. Curr Opin Struct Biol. 2010; 20(3):313-24. PMC: 2916977. DOI: 10.1016/j.sbi.2010.03.011. View

17.

Cairns B, Erdjument-Bromage H, Tempst P, Winston F, Kornberg R . Two actin-related proteins are shared functional components of the chromatin-remodeling complexes RSC and SWI/SNF. Mol Cell. 1998; 2(5):639-51. DOI: 10.1016/s1097-2765(00)80162-8. View

18.

Durr H, Korner C, Muller M, Hickmann V, Hopfner K . X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell. 2005; 121(3):363-73. DOI: 10.1016/j.cell.2005.03.026. View

19.

Lavigne M, Eskeland R, Azebi S, Saint-Andre V, Jang S, Batsche E . Interaction of HP1 and Brg1/Brm with the globular domain of histone H3 is required for HP1-mediated repression. PLoS Genet. 2009; 5(12):e1000769. PMC: 2782133. DOI: 10.1371/journal.pgen.1000769. View

20.

Thastrom A, Lowary P, Widom J . Measurement of histone-DNA interaction free energy in nucleosomes. Methods. 2004; 33(1):33-44. DOI: 10.1016/j.ymeth.2003.10.018. View