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Structure of chromatin remodeler Swi2/Snf2 in the resting state.

Xia X, Liu X, Li T, Fang X, Chen Z
Nat Struct Mol Biol 23 722-9 (2016)
Cited: 34 times
EuropePMC logo PMID: 27399259

Abstract

SWI2/SNF2 family proteins regulate a myriad of nucleic acid transactions by sliding, removing and reconstructing nucleosomes in eukaryotic cells. They contain two RecA-like core domains, which couple ATP hydrolysis and DNA translocation to chromatin remodeling. Here we report the crystal structure of Snf2 from the yeast Myceliophthora thermophila. The data show the two RecA-like core domains of Snf2 stacking together and twisting their ATP-binding motifs away from each other, thus explaining the inactivity of the protein in the ground state. We identified several DNA-binding elements, which are fully exposed to solvent, thus suggesting that the protein is poised for its incoming substrate. The catalytic core of Snf2 showed a high chromatin-remodeling activity, which was suppressed by the N-terminal HSA domain. Our findings reveal that the catalytic core of Snf2 is a competent remodeling machine, which rests in an inactive conformation and requires a large conformational change upon activation.

Articles - 5hzr mentioned but not cited (9)

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  2. Cancer-Associated Gain-of-Function Mutations Activate a SWI/SNF-Family Regulatory Hub. Clapier CR, Verma N, Parnell TJ, Cairns BR. Mol Cell 80 712-725.e5 (2020)
  3. Structural insights into assembly and function of the RSC chromatin remodeling complex. Baker RW, Reimer JM, Carman PJ, Turegun B, Arakawa T, Dominguez R, Leschziner AE. Nat Struct Mol Biol 28 71-80 (2021)
  4. Structure and functional interactions of INO80 actin/Arp module. Zhang X, Wang X, Zhang Z, Cai G. J Mol Cell Biol 11 345-355 (2019)
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  6. Mechanism of Rad26-assisted rescue of stalled RNA polymerase II in transcription-coupled repair. Yan C, Dodd T, Yu J, Leung B, Xu J, Oh J, Wang D, Ivanov I. Nat Commun 12 7001 (2021)
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  8. Crystal structure of the full Swi2/Snf2 remodeler Mot1 in the resting state. Butryn A, Woike S, Shetty SJ, Auble DT, Hopfner KP. Elife 7 e37774 (2018)
  9. Crystal structure of the ATPase-C domain of the chromatin remodeller Fun30 from Saccharomyces cerevisiae. Liu L, Jiang T. Acta Crystallogr F Struct Biol Commun 73 9-15 (2017)


Reviews citing this publication (7)

  1. Mechanisms of action and regulation of ATP-dependent chromatin-remodelling complexes. Clapier CR, Iwasa J, Cairns BR, Peterson CL. Nat Rev Mol Cell Biol 18 407-422 (2017)
  2. Exploiting vulnerabilities of SWI/SNF chromatin remodelling complexes for cancer therapy. Wanior M, Krämer A, Knapp S, Joerger AC. Oncogene 40 3637-3654 (2021)
  3. INO80 and SWR1 complexes: the non-identical twins of chromatin remodelling. Willhoft O, Wigley DB. Curr Opin Struct Biol 61 50-58 (2020)
  4. Sophisticated Conversations between Chromatin and Chromatin Remodelers, and Dissonances in Cancer. Clapier CR. Int J Mol Sci 22 5578 (2021)
  5. Collaboration through chromatin: motors of transcription and chromatin structure. Gamarra N, Narlikar GJ. J Mol Biol 433 166876 (2021)
  6. Molecular basis for chromatin assembly and modification by multiprotein complexes. Ricketts MD, Han J, Szurgot MR, Marmorstein R. Protein Sci 28 329-343 (2019)
  7. Energy-driven genome regulation by ATP-dependent chromatin remodellers. Eustermann S, Patel AB, Hopfner KP, He Y, Korber P. Nat Rev Mol Cell Biol (2023)

Articles citing this publication (18)

  1. Modular Organization and Assembly of SWI/SNF Family Chromatin Remodeling Complexes. Mashtalir N, D'Avino AR, Michel BC, Luo J, Pan J, Otto JE, Zullow HJ, McKenzie ZM, Kubiak RL, St Pierre R, Valencia AM, Poynter SJ, Cassel SH, Ranish JA, Kadoch C. Cell 175 1272-1288.e20 (2018)
  2. Mechanism of chromatin remodelling revealed by the Snf2-nucleosome structure. Liu X, Li M, Xia X, Li X, Chen Z. Nature 544 440-445 (2017)
  3. Structure of the RSC complex bound to the nucleosome. Ye Y, Wu H, Chen K, Clapier CR, Verma N, Zhang W, Deng H, Cairns BR, Gao N, Chen Z. Science 366 838-843 (2019)
  4. Structure and regulation of the chromatin remodeller ISWI. Yan L, Wang L, Tian Y, Xia X, Chen Z. Nature 540 466-469 (2016)
  5. Cryo-EM structures of remodeler-nucleosome intermediates suggest allosteric control through the nucleosome. Armache JP, Gamarra N, Johnson SL, Leonard JD, Wu S, Narlikar GJ, Cheng Y. Elife 8 e46057 (2019)
  6. Architecture of the chromatin remodeler RSC and insights into its nucleosome engagement. Patel AB, Moore CM, Greber BJ, Luo J, Zukin SA, Ranish J, Nogales E. Elife 8 e54449 (2019)
  7. The nucleosomal acidic patch relieves auto-inhibition by the ISWI remodeler SNF2h. Gamarra N, Johnson SL, Trnka MJ, Burlingame AL, Narlikar GJ. Elife 7 e35322 (2018)
  8. Mechanistic Insights into Autoinhibition of the Oncogenic Chromatin Remodeler ALC1. Lehmann LC, Hewitt G, Aibara S, Leitner A, Marklund E, Maslen SL, Maturi V, Chen Y, van der Spoel D, Skehel JM, Moustakas A, Boulton SJ, Deindl S. Mol Cell 68 847-859.e7 (2017)
  9. Structural reorganization of the chromatin remodeling enzyme Chd1 upon engagement with nucleosomes. Sundaramoorthy R, Hughes AL, Singh V, Wiechens N, Ryan DP, El-Mkami H, Petoukhov M, Svergun DI, Treutlein B, Quack S, Fischer M, Michaelis J, Böttcher B, Norman DG, Owen-Hughes T. Elife 6 e22510 (2017)
  10. Actin-related proteins regulate the RSC chromatin remodeler by weakening intramolecular interactions of the Sth1 ATPase. Turegun B, Baker RW, Leschziner AE, Dominguez R. Commun Biol 1 1 (2018)
  11. Structure of the primed state of the ATPase domain of chromatin remodeling factor ISWI bound to the nucleosome. Chittori S, Hong J, Bai Y, Subramaniam S. Nucleic Acids Res 47 9400-9409 (2019)
  12. In vivo analysis reveals that ATP-hydrolysis couples remodeling to SWI/SNF release from chromatin. Tilly BC, Chalkley GE, van der Knaap JA, Moshkin YM, Kan TW, Dekkers DH, Demmers JA, Verrijzer CP. Elife 10 e69424 (2021)
  13. Structural basis of ALC1/CHD1L autoinhibition and the mechanism of activation by the nucleosome. Wang L, Chen K, Chen Z. Nat Commun 12 4057 (2021)
  14. Structural basis for the multi-activity factor Rad5 in replication stress tolerance. Shen M, Dhingra N, Wang Q, Cheng C, Zhu S, Tian X, Yu J, Gong X, Li X, Zhang H, Xu X, Zhai L, Xie M, Gao Y, Deng H, He Y, Niu H, Zhao X, Xiang S. Nat Commun 12 321 (2021)
  15. Mechanism of action of the SWI/SNF family complexes. Chen K, Yuan J, Sia Y, Chen Z. Nucleus 14 2165604 (2023)
  16. Structural basis for activation of Swi2/Snf2 ATPase RapA by RNA polymerase. Shi W, Zhou W, Chen M, Yang Y, Hu Y, Liu B. Nucleic Acids Res 49 10707-10716 (2021)
  17. The ATPase BRG1/SMARCA4 is a protein interaction platform that recruits BAF subunits and the transcriptional repressor REST/NRSF in neural progenitor cells. Jayaprakash S, Drakulic S, Zhao Z, Sander B, Golas MM. Mol Cell Biochem 461 171-182 (2019)
  18. A SAM-key domain required for enzymatic activity of the Fun30 nucleosome remodeler. Karl LA, Galanti L, Bantele SC, Metzner F, Šafarić B, Rajappa L, Foster B, Pires VB, Bansal P, Chacin E, Basquin J, Duderstadt KE, Kurat CF, Bartke T, Hopfner KP, Pfander B. Life Sci Alliance 6 e202201790 (2023)


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