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Nucleosome–Chd1 structure and implications for chromatin remodelling - Nature

  • ️Cramer, Patrick
  • ️Wed Oct 11 2017

References

  1. Narlikar, G. J., Sundaramoorthy, R. & Owen-Hughes, T. Mechanisms and functions of ATP-dependent chromatin-remodeling enzymes. Cell 154, 490–503 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Delmas, V., Stokes, D. G. & Perry, R. P. A mammalian DNA-binding protein that contains a chromodomain and an SNF2/SWI2-like helicase domain. Proc. Natl Acad. Sci. USA 90, 2414–2418 (1993)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  3. Lieleg, C. et al. Nucleosome spacing generated by ISWI and CHD1 remodelers is constant regardless of nucleosome density. Mol. Cell. Biol. 35, 1588–1605 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Hughes, A. L. & Rando, O. J. Comparative genomics reveals Chd1 as a determinant of nucleosome spacing in vivo. G3 (Bethesda) 5, 1889–1897 (2015)

    CAS  Google Scholar 

  5. Lusser, A., Urwin, D. L. & Kadonaga, J. T. Distinct activities of CHD1 and ACF in ATP-dependent chromatin assembly. Nat. Struct. Mol. Biol. 12, 160–166 (2005)

    CAS  PubMed  Google Scholar 

  6. Skene, P. J., Hernandez, A. E., Groudine, M. & Henikoff, S. The nucleosomal barrier to promoter escape by RNA polymerase II is overcome by the chromatin remodeler Chd1. eLife 3, e02042 (2014)

    PubMed  PubMed Central  Google Scholar 

  7. Gaspar-Maia, A. et al. Chd1 regulates open chromatin and pluripotency of embryonic stem cells. Nature 460, 863–868 (2009)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  8. Liu, X., Li, M., Xia, X., Li, X. & Chen, Z. Mechanism of chromatin remodelling revealed by the Snf2-nucleosome structure. Nature 544, 440–445 (2017)

    ADS  CAS  PubMed  Google Scholar 

  9. Nodelman, I. M. et al. Interdomain communication of the Chd1 chromatin remodeler across the DNA gyres of the nucleosome. Mol. Cell 65, 447–459.e6 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Lowary, P. T. & Widom, J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19–42 (1998)

    CAS  PubMed  Google Scholar 

  11. Vasudevan, D., Chua, E. Y. D. & Davey, C. A. Crystal structures of nucleosome core particles containing the ‘601’ strong positioning sequence. J. Mol. Biol. 403, 1–10 (2010)

    CAS  PubMed  Google Scholar 

  12. Hauk, G., McKnight, J. N., Nodelman, I. M. & Bowman, G. D. The chromodomains of the Chd1 chromatin remodeler regulate DNA access to the ATPase motor. Mol. Cell 39, 711–723 (2010)

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Sharma, A., Jenkins, K. R., Héroux, A. & Bowman, G. D. Crystal structure of the chromodomain helicase DNA-binding protein 1 (Chd1) DNA-binding domain in complex with DNA. J. Biol. Chem. 286, 42099–42104 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Mohanty, B., Helder, S., Silva, A. P. G., Mackay, J. P. & Ryan, D. P. The chromatin remodelling protein CHD1 contains a previously unrecognised C-terminal helical domain. J. Mol. Biol. 428, 4298–4314 (2016)

    CAS  PubMed  Google Scholar 

  15. Sundaramoorthy, R. et al. Structural reorganization of the chromatin remodeling enzyme Chd1 upon engagement with nucleosomes. eLife 6, e22510–e22528 (2017)

    PubMed  PubMed Central  Google Scholar 

  16. Sinha, K. K., Gross, J. D. & Narlikar, G. J. Distortion of histone octamer core promotes nucleosome mobilization by a chromatin remodeler. Science 355, eaaa3761 (2017)

    PubMed  PubMed Central  Google Scholar 

  17. McKnight, J. N., Jenkins, K. R., Nodelman, I. M., Escobar, T. & Bowman, G. D. Extranucleosomal DNA binding directs nucleosome sliding by Chd1. Mol. Cell. Biol. 31, 4746–4759 (2011)

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Bednar, J. et al. Structure and dynamics of a 197 bp nucleosome in complex with linker histone H1. Mol. Cell 66, 384–397.e8 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Gu, M. & Rice, C. M. Three conformational snapshots of the hepatitis C virus NS3 helicase reveal a ratchet translocation mechanism. Proc. Natl Acad. Sci. USA 107, 521–528 (2010)

    ADS  CAS  PubMed  Google Scholar 

  20. Sengoku, T., Nureki, O., Nakamura, A., Kobayashi, S. & Yokoyama, S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 125, 287–300 (2006)

    CAS  PubMed  Google Scholar 

  21. Huang, S. et al. Recurrent deletion of CHD1 in prostate cancer with relevance to cell invasiveness. Oncogene 31, 4164–4170 (2012)

    CAS  PubMed  Google Scholar 

  22. Singleton, M. R., Dillingham, M. S. & Wigley, D. B. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76, 23–50 (2007)

    CAS  PubMed  Google Scholar 

  23. Dürr, H., Körner, C., Müller, M., Hickmann, V. & Hopfner, K.-P. X-ray structures of the Sulfolobus solfataricus SWI2/SNF2 ATPase core and its complex with DNA. Cell 121, 363–373 (2005)

    PubMed  Google Scholar 

  24. Saha, A., Wittmeyer, J. & Cairns, B. R. Chromatin remodeling through directional DNA translocation from an internal nucleosomal site. Nat. Struct. Mol. Biol. 12, 747–755 (2005)

    CAS  PubMed  Google Scholar 

  25. Saikrishnan, K., Powell, B., Cook, N. J., Webb, M. R. & Wigley, D. B. Mechanistic basis of 5′-3′ translocation in SF1B helicases. Cell 137, 849–859 (2009)

    CAS  PubMed  Google Scholar 

  26. Hopfner, K.-P. & Michaelis, J. Mechanisms of nucleic acid translocases: lessons from structural biology and single-molecule biophysics. Curr. Opin. Struct. Biol. 17, 87–95 (2007)

    CAS  PubMed  Google Scholar 

  27. Wigley, D. B. & Bowman, G. D. A glimpse into chromatin remodeling. Nat. Struct. Mol. Biol. 24, 498–500 (2017)

    CAS  PubMed  Google Scholar 

  28. Le Gallo, M. et al. Exome sequencing of serous endometrial tumors identifies recurrent somatic mutations in chromatin-remodeling and ubiquitin ligase complex genes. Nat. Genet. 44, 1310–1315 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Clapier, C. R., Längst, G., Corona, D. F., Becker, P. B. & Nightingale, K. P. Critical role for the histone H4 N terminus in nucleosome remodeling by ISWI. Mol. Cell. Biol. 21, 875–883 (2001)

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Nodelman, I. M. et al. The Chd1 chromatin remodeler can sense both entry and exit sides of the nucleosome. Nucleic Acids Res. 44, 7580–7591 (2016)

    PubMed  PubMed Central  Google Scholar 

  31. Clapier, C. R. & Cairns, B. R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273–304 (2009)

    CAS  PubMed  Google Scholar 

  32. Leonard, J. D. & Narlikar, G. J. A nucleotide-driven switch regulates flanking DNA length sensing by a dimeric chromatin remodeler. Mol. Cell 57, 850–859 (2015)

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Yan, L., Wang, L., Tian, Y., Xia, X. & Chen, Z. Structure and regulation of the chromatin remodeller ISWI. Nature 540, 466–469 (2016)

    ADS  CAS  PubMed  Google Scholar 

  34. Xu, Y. et al. Architecture of the RNA polymerase II-Paf1C-TFIIS transcription elongation complex. Nat. Commun. 8, 15741 (2017)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  35. Vos, S. M. et al. Architecture and RNA binding of the human negative elongation factor. eLife 5, e14981 (2016)

    PubMed  PubMed Central  Google Scholar 

  36. Luger, K., Rechsteiner, T. J. & Richmond, T. J. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119, 1–16 (1999)

    CAS  PubMed  Google Scholar 

  37. Dyer, P. N. et al. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23–44 (2003)

    Google Scholar 

  38. Maskell, D. P. et al. Structural basis for retroviral integration into nucleosomes. Nature 523, 366–369 (2015)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  39. Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017)

    CAS  PubMed  PubMed Central  Google Scholar 

  40. Zhang, K. Gctf: Real-time CTF determination and correction. J. Struct. Biol. 193, 1–12 (2016)

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  41. Scheres, S. H. W. A Bayesian view on cryo-EM structure determination. J. Mol. Biol. 415, 406–418 (2012)

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Kimanius, D., Forsberg, B. O., Scheres, S. H. & Lindahl, E. Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2. eLife 5, e18722 (2016)

    PubMed  PubMed Central  Google Scholar 

  43. Plaschka, C. et al. Transcription initiation complex structures elucidate DNA opening. Nature 533, 353–358 (2016)

    ADS  CAS  PubMed  Google Scholar 

  44. Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004)

    CAS  PubMed  Google Scholar 

  45. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D 66, 486–501 (2010)

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33–38 (1996)

    CAS  PubMed  Google Scholar 

  47. Trabuco, L. G., Villa, E., Mitra, K., Frank, J. & Schulten, K. Flexible fitting of atomic structures into electron microscopy maps using molecular dynamics. Structure 16, 673–683 (2008)

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Adams, P. D . et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213–221 (2010)

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Thomsen, N. D. & Berger, J. M. Running in reverse: the structural basis for translocation polarity in hexameric helicases. Cell 139, 523–534 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Schrödinger, LLC. The PyMOL Molecular Graphics System, v.1.8 (Schrödinger, 2015)

  51. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013)

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M. & Barton, G. J. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189–1191 (2009)

    CAS  PubMed  PubMed Central  Google Scholar 

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