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Structural insight into the sequence dependence of nucleosome positioning.

Wu B, Mohideen K, Vasudevan D, Davey CA
Structure 18 528-36 (2010)
Cited: 32 times
EuropePMC logo PMID: 20399189

Abstract

Nucleosome positioning displays sequence dependency and contributes to genomic regulation in a site-specific manner. We solved the structures of nucleosome core particle composed of strong positioning TTTAA elements flanking the nucleosome center. The positioning strength of the super flexible TA dinucleotide is consistent with its observed central location within minor groove inward regions, where it can contribute maximally to energetically challenging minor groove bending, kinking and compression. The marked preference for TTTAA and positioning power of the site 1.5 double helix turns from the nucleosome center relates to a unique histone protein motif at this location, which enforces a sustained, extremely narrow minor groove via a hydrophobic "sugar clamp." Our analysis sheds light on the basis of nucleosome positioning and indicates that the histone octamer has evolved not to fully minimize sequence discrimination in DNA binding.

Reviews - 3lel mentioned but not cited (1)

  1. Nucleosome structural studies. Tan S, Davey CA. Curr Opin Struct Biol 21 128-136 (2011)

Articles - 3lel mentioned but not cited (4)

  1. Biodamage via shock waves initiated by irradiation with ions. Surdutovich E, Yakubovich AV, Solov'yov AV. Sci Rep 3 1289 (2013)
  2. Modeling DNA-bending in the nucleosome: role of AA periodicity. Prytkova TR, Zhu X, Widom J, Schatz GC. J Phys Chem B 115 8638-8644 (2011)
  3. The genome of a prasinoviruses-related freshwater virus reveals unusual diversity of phycodnaviruses. Chen H, Zhang W, Li X, Pan Y, Yan S, Wang Y. BMC Genomics 19 49 (2018)
  4. 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 (9)

  1. On the sequence-directed nature of human gene mutation: the role of genomic architecture and the local DNA sequence environment in mediating gene mutations underlying human inherited disease. Cooper DN, Bacolla A, Férec C, Vasquez KM, Kehrer-Sawatzki H, Chen JM. Hum Mutat 32 1075-1099 (2011)
  2. Dps biomineralizing proteins: multifunctional architects of nature. Zeth K. Biochem J 445 297-311 (2012)
  3. Nucleosome dynamics: Sequence matters. Eslami-Mossallam B, Schiessel H, van Noort J. Adv Colloid Interface Sci 232 101-113 (2016)
  4. Working the kinks out of nucleosomal DNA. Olson WK, Zhurkin VB. Curr Opin Struct Biol 21 348-357 (2011)
  5. Yeast HMO1: Linker Histone Reinvented. Panday A, Grove A. Microbiol Mol Biol Rev 81 e00037-16 (2017)
  6. Contributions of Sequence to the Higher-Order Structures of DNA. Todolli S, Perez PJ, Clauvelin N, Olson WK. Biophys J 112 416-426 (2017)
  7. Protein/DNA interactions in complex DNA topologies: expect the unexpected. Noy A, Sutthibutpong T, A Harris S. Biophys Rev 8 233-243 (2016)
  8. Protein/DNA interactions in complex DNA topologies: expect the unexpected. Noy A, Sutthibutpong T, A Harris S. Biophys Rev 8 145-155 (2016)
  9. Collaboration through chromatin: motors of transcription and chromatin structure. Gamarra N, Narlikar GJ. J Mol Biol 433 166876 (2021)

Articles citing this publication (18)

  1. Crystal structures of nucleosome core particles containing the '601' strong positioning sequence. Vasudevan D, Chua EYD, Davey CA. J Mol Biol 403 1-10 (2010)
  2. The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association. Allahverdi A, Yang R, Korolev N, Fan Y, Davey CA, Liu CF, Nordenskiöld L. Nucleic Acids Res 39 1680-1691 (2011)
  3. The mechanics behind DNA sequence-dependent properties of the nucleosome. Chua EY, Vasudevan D, Davey GE, Wu B, Davey CA. Nucleic Acids Res 40 6338-6352 (2012)
  4. Perturbations in nucleosome structure from heavy metal association. Mohideen K, Muhammad R, Davey CA. Nucleic Acids Res 38 6301-6311 (2010)
  5. X-ray structure of the MMTV-A nucleosome core. Frouws TD, Duda SC, Richmond TJ. Proc Natl Acad Sci U S A 113 1214-1219 (2016)
  6. Combined micrococcal nuclease and exonuclease III digestion reveals precise positions of the nucleosome core/linker junctions: implications for high-resolution nucleosome mapping. Nikitina T, Wang D, Gomberg M, Grigoryev SA, Zhurkin VB. J Mol Biol 425 1946-1960 (2013)
  7. Specific DNA structural attributes modulate platinum anticancer drug site selection and cross-link generation. Wu B, Davey GE, Nazarov AA, Dyson PJ, Davey CA. Nucleic Acids Res 39 8200-8212 (2011)
  8. An Organometallic Compound which Exhibits a DNA Topology-Dependent One-Stranded Intercalation Mode. Ma Z, Palermo G, Adhireksan Z, Murray BS, von Erlach T, Dyson PJ, Rothlisberger U, Davey CA. Angew Chem Int Ed Engl 55 7441-7444 (2016)
  9. Hydroxyl-radical footprinting combined with molecular modeling identifies unique features of DNA conformation and nucleosome positioning. Shaytan AK, Xiao H, Armeev GA, Wu C, Landsman D, Panchenko AR. Nucleic Acids Res 45 9229-9243 (2017)
  10. Simulations Meet Experiment to Reveal New Insights into DNA Intrinsic Mechanics. Ben Imeddourene A, Elbahnsi A, Guéroult M, Oguey C, Foloppe N, Hartmann B. PLoS Comput Biol 11 e1004631 (2015)
  11. Finding optimal interaction interface alignments between biological complexes. Cui X, Naveed H, Gao X. Bioinformatics 31 i133-41 (2015)
  12. Stereochemical control of nucleosome targeting by platinum-intercalator antitumor agents. Chua EY, Davey GE, Chin CF, Dröge P, Ang WH, Davey CA. Nucleic Acids Res 43 5284-5296 (2015)
  13. High-resolution biophysical analysis of the dynamics of nucleosome formation. Hatakeyama A, Hartmann B, Travers A, Nogues C, Buckle M. Sci Rep 6 27337 (2016)
  14. RNAHelix: computational modeling of nucleic acid structures with Watson-Crick and non-canonical base pairs. Bhattacharyya D, Halder S, Basu S, Mukherjee D, Kumar P, Bansal M. J Comput Aided Mol Des 31 219-235 (2017)
  15. Reading sequence-directed computational nucleosome maps. Nibhani R, Trifonov EN. J Biomol Struct Dyn 33 1558-1566 (2015)
  16. Role of transcription factor-mediated nucleosome disassembly in PHO5 gene expression. Kharerin H, Bhat PJ, Marko JF, Padinhateeri R. Sci Rep 6 20319 (2016)
  17. Slow motions in A·T rich DNA sequence. Ben Imeddourene A, Zargarian L, Buckle M, Hartmann B, Mauffret O. Sci Rep 10 19005 (2020)
  18. Letter Does the nucleosome break its own rules? Davey CA. Curr Opin Struct Biol 23 311-313 (2013)


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