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Crystal structures of histone Sin mutant nucleosomes reveal altered protein-DNA interactions.

Muthurajan UM, Bao Y, Forsberg LJ, Edayathumangalam RS, Dyer PN, White CL, Luger K
EMBO J 23 260-71 (2004)
Related entries: 1p34, 1p3a, 1p3b, 1p3f, 1p3g, 1p3k, 1p3l, 1p3m, 1p3o, 1p3p

Cited: 101 times
EuropePMC logo PMID: 14739929

Abstract

Here we describe 11 crystal structures of nucleosome core particles containing individual point mutations in the structured regions of histones H3 and H4. The mutated residues are located at the two protein-DNA interfaces flanking the nucleosomal dyad. Five of the mutations partially restore the in vivo effects of SWI/SNF inactivation in yeast. We find that even nonconservative mutations of these residues (which exhibit a distinct phenotype in vivo) have only moderate effects on global nucleosome structure. Rather, local protein-DNA interactions are disrupted and weakened in a subtle and complex manner. The number of lost protein-DNA interactions correlates directly with an increased propensity of the histone octamer to reposition with respect to the DNA, and with an overall destabilization of the nucleosome. Thus, the disruption of only two to six of the approximately 120 direct histone-DNA interactions within the nucleosome has a pronounced effect on nucleosome mobility and stability. This has implications for our understanding of how these structures are made accessible to the transcription and replication machinery in vivo.

Articles - 1p3i mentioned but not cited (9)

  1. Crystal structures of histone Sin mutant nucleosomes reveal altered protein-DNA interactions. Muthurajan UM, Bao Y, Forsberg LJ, Edayathumangalam RS, Dyer PN, White CL, Luger K. EMBO J 23 260-271 (2004)
  2. DNA conformations and their sequence preferences. Svozil D, Kalina J, Omelka M, Schneider B. Nucleic Acids Res 36 3690-3706 (2008)
  3. An ensemble of B-DNA dinucleotide geometries lead to characteristic nucleosomal DNA structure and provide plasticity required for gene expression. Marathe A, Bansal M. BMC Struct Biol 11 1 (2011)
  4. Geometry of the nucleosomal DNA superhelix. Bishop TC. Biophys J 95 1007-1017 (2008)
  5. DNA architecture, deformability, and nucleosome positioning. Xu F, Olson WK. J Biomol Struct Dyn 27 725-739 (2010)
  6. Mechanism of cohesin loading onto chromosomes: a conformational dynamics study. Kurkcuoglu O, Bates PA. Biophys J 99 1212-1220 (2010)
  7. Surprising Twists in Nucleosomal DNA with Implication for Higher-order Folding. Todolli S, Young RT, Watkins AS, Bu Sha A, Yager J, Olson WK. J Mol Biol 433 167121 (2021)
  8. SMOG 2 and OpenSMOG: Extending the limits of structure-based models. de Oliveira AB, Contessoto VG, Hassan A, Byju S, Wang A, Wang Y, Dodero-Rojas E, Mohanty U, Noel JK, Onuchic JN, Whitford PC. Protein Sci 31 158-172 (2022)
  9. Statistical investigation of position-specific deformation pattern of nucleosome DNA based on multiple conformational properties. Yang X, Yan Y. Bioinformation 7 120-124 (2011)


Reviews citing this publication (22)

  1. Regulated nucleosome mobility and the histone code. Cosgrove MS, Boeke JD, Wolberger C. Nat Struct Mol Biol 11 1037-1043 (2004)
  2. Post-translational modifications of histones that influence nucleosome dynamics. Bowman GD, Poirier MG. Chem Rev 115 2274-2295 (2015)
  3. Nucleosome structure(s) and stability: variations on a theme. Andrews AJ, Luger K. Annu Rev Biophys 40 99-117 (2011)
  4. Histone structure and nucleosome stability. Mariño-Ramírez L, Kann MG, Shoemaker BA, Landsman D. Expert Rev Proteomics 2 719-729 (2005)
  5. Mechanisms for ATP-dependent chromatin remodelling: farewell to the tuna-can octamer? Flaus A, Owen-Hughes T. Curr Opin Genet Dev 14 165-173 (2004)
  6. Dynamic nucleosomes. Luger K. Chromosome Res 14 5-16 (2006)
  7. How does the histone code work? Cosgrove MS, Wolberger C. Biochem Cell Biol 83 468-476 (2005)
  8. The tale beyond the tail: histone core domain modifications and the regulation of chromatin structure. Mersfelder EL, Parthun MR. Nucleic Acids Res 34 2653-2662 (2006)
  9. Chromatin architecture. Woodcock CL. Curr Opin Struct Biol 16 213-220 (2006)
  10. Nucleosome structural studies. Tan S, Davey CA. Curr Opin Struct Biol 21 128-136 (2011)
  11. Mechanism of transcription through a nucleosome by RNA polymerase II. Kulaeva OI, Hsieh FK, Chang HW, Luse DS, Studitsky VM. Biochim Biophys Acta 1829 76-83 (2013)
  12. Mechanisms of ATP-dependent nucleosome sliding. Bowman GD. Curr Opin Struct Biol 20 73-81 (2010)
  13. Histone exchange and histone modifications during transcription and aging. Das C, Tyler JK. Biochim Biophys Acta 1819 332-342 (2013)
  14. Histone proteomics and the epigenetic regulation of nucleosome mobility. Cosgrove MS. Expert Rev Proteomics 4 465-478 (2007)
  15. Repair of UV lesions in nucleosomes--intrinsic properties and remodeling. Thoma F. DNA Repair (Amst) 4 855-869 (2005)
  16. Physicochemical analysis of electrostatic foundation for DNA-protein interactions in chromatin transformations. Korolev N, Vorontsova OV, Nordenskiöld L. Prog Biophys Mol Biol 95 23-49 (2007)
  17. Structure and dynamic properties of nucleosome core particles. Chakravarthy S, Park YJ, Chodaparambil J, Edayathumangalam RS, Luger K. FEBS Lett 579 895-898 (2005)
  18. Molecular traffic jams on DNA. Finkelstein IJ, Greene EC. Annu Rev Biophys 42 241-263 (2013)
  19. Current progress on structural studies of nucleosomes containing histone H3 variants. Kurumizaka H, Horikoshi N, Tachiwana H, Kagawa W. Curr Opin Struct Biol 23 109-115 (2013)
  20. Histone H2B Mutations in Cancer. Wan YCE, Chan KM. Biomedicines 9 694 (2021)
  21. Histone 3.3-related chromatinopathy: missense variants throughout H3-3A and H3-3B cause a range of functional consequences across species. Bryant L, Sangree A, Clark K, Bhoj E. Hum Genet (2023)
  22. Structural studies of functional nucleosome complexes with transacting factors. Kurumizaka H. Proc Jpn Acad Ser B Phys Biol Sci 98 1-14 (2022)

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