Skip to main content

On the Relationship between DNA Periodicity and Local Chromatin Structure

  • Conference paper
Research in Computational Molecular Biology (RECOMB 2009)

Part of the book series: Lecture Notes in Computer Science ((LNBI,volume 5541))

Abstract

DNA periodicity and its relationship to the formation of nucleosomes has been investigated extensively using autocorrelation and Fourier transform methods. We provide a precise treatment of the mathematical foundation for this type of analysis, and we apply the resulting method to quantify dinucleotide periodicity in several datasets. We begin by demonstrating, via simulation, the sensitivity of our method relative to previous methods. We then provide evidence of pervasive ~10 bp periodicity in S. cerevisiae, with stronger periodicity in sequences associated with positioned nucleosomes. In human, although repeat-masked sequences do not exhibit significant periodicity on average, we find that experimentally determined nucleosome positions show a periodicity of the AA dinucleotide similar to that found in S. cerevisiae. Furthermore, transcription start sites in the human genome are marked by a sharp drop in the 10 bp periodicity of the AA dinucleotide, while occupied CTCF sites are surrounded by a local increase.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Crick, F.H.C., Klug, A.: Kinky helix. Nature 255, 530–533 (1975)

    Article  CAS  PubMed  Google Scholar 

  2. Trifonov, E.N., Sussman, J.L.: The pitch of chromatin DNA is reflected in its nucleotide sequence. Proceedings of the National Academy of Sciences of the United States of America 77, 3816–3820 (1980)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Herzel, H., Trifonov, E.N., Weiss, O., Grosse, I.: Interpreting correlations in biosequences. Physica A 249, 449–459 (1998)

    Article  CAS  Google Scholar 

  4. Satchwell, S.C., Drew, H.R., Travers, A.A.: Sequence periodicities in chicken nucleosome core DNA. Journal of Molecular Biology 191, 659–675 (1986)

    Article  CAS  PubMed  Google Scholar 

  5. Drew, H.R., Travers, A.A.: DNA bending and its relation to nucleosome positioning. Journal of Molecular Biology 186, 773–790 (1985)

    Article  CAS  PubMed  Google Scholar 

  6. Shrader, T., Crothers, D.: Artificial nucleosome positioning sequences. Proceedings of the National Academy of Sciences of the United States of America 86, 7418–7422 (1989)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Widom, J.: Short-range order in two eukaryotic genomes: relation to chromatin structure. Journal of Molecular Biology 259, 579–588 (1996)

    Article  CAS  PubMed  Google Scholar 

  8. Segal, E., Fondufe-Mittendorf, Y., Chen, L., Thȧström, A., Field, Y., Moore, I.K., Wang, J.Z., Widom, J.: A genomic code for nucleosome positioning. Nature 44, 772–778 (2006)

    Article  Google Scholar 

  9. Fire, A., Alcazar, R., Tan, F.: Unusual DNA structures associated with germline genetic activity in Caenorhabditis elegans. Genetics 173, 1259–1273 (2006)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Packer, M.J., Dauncey, M.P., Hunter, C.A.: Sequence-dependent DNA structure: dinucleotide conformational maps. Journal of Molecular Biology 295, 71–83 (2000)

    Article  CAS  PubMed  Google Scholar 

  11. Packer, M.J., Dauncey, M.P., Hunter, C.A.: Sequence-dependent DNA structure: tetranucleotide conformational maps. Journal of Molecular Biology 295, 85–103 (2000)

    Article  CAS  PubMed  Google Scholar 

  12. Beveridge, D.L., Dixit, S.B., Barreiro, G., Thayer, K.M.: Molecular dynamics simulations of DNA curvature and flexibility: helix phasing and premelting. Biopolymers 73, 380–403 (2004)

    Article  CAS  PubMed  Google Scholar 

  13. Gabrielian, A., Simoncsits, A., Pongor, S.: Distribution of bending propensity in DNA sequences. FEBS Letters 393, 125–140 (1996)

    Google Scholar 

  14. Bomble, Y.J., Case, D.A.: Multiscale modeling of nucleic acids: insights into DNA flexibility. Biopolymers 89, 722–731 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Travers, A.A.: The structural basis of DNA flexibility. Philosophical Transactions of the Royal Society of London. Series A Mathematical, Physical and Engineering Sciences. 362, 1423–1438 (2004)

    Article  CAS  Google Scholar 

  16. Thȧström, A., Lowary, P.T., Widlund, H.R., Cao, H., Kubista, M., Widom, J.: Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. Journal of Molecular Biology 288, 213–229 (1999)

    Article  PubMed  Google Scholar 

  17. Bailey, K.A., Pereira, S.L., Widom, J., Reeve, J.N.: Archaeal histone selection of nucleosome positioning sequences and the procaryotic origin of histone-dependent genome evolution. Journal of Molecular Biology 303, 25–34 (2000)

    Article  CAS  PubMed  Google Scholar 

  18. Holste, D., Grosse, I., Beirer, S., Schieg, P., Herzel, H.: Repeats and correlations in human DNA sequences. Physical Review E 67 (2003)

    Google Scholar 

  19. Hosid, S., Trifonov, E.N., Bolshoy, A.: Sequence periodicity of Escherichia coli is concentrated in intergenic regions. BMC Molecular Biology 5, 14 (2004)

    Article  PubMed  PubMed Central  Google Scholar 

  20. Schieg, P., Herzel, H.: Periodicities of 10-11 bp as indicators of the supercoiled state of genomic DNA. Journal of Molecular Biology 343, 891–901 (2004)

    Article  CAS  PubMed  Google Scholar 

  21. Grimmett, G.R., Stirzaker, D.R.: Probability and Random Processes. Oxford University Press, USA (2001)

    Google Scholar 

  22. Jenkins, G.M., Watts, D.: Spectral Analysis and Its Applications. Emerson-Adams Press, USA (1998)

    Google Scholar 

  23. Baldi, P., Brunak, S., Chauvin, Y., Englebrecht, J., Krogh, A.: Periodic sequence patterns in human exons. In: ISMB, pp. 30–38 (1995)

    Google Scholar 

  24. Baldi, P., Brunak, S., Chauvin, Y., Krogh, A.: Naturally occurring nucleosome positioning signals in human exons and introns. Journal of Molecular Biology 263, 503–510 (1996)

    Article  CAS  PubMed  Google Scholar 

  25. Kharchenko, P.V., Woo, C.J., Tolstorukov, M.Y., Kingston, R.E., Park, P.J.: Nucleosome positioning in human HOX gene clusters. Genome Research 18, 1554–1561 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kornberg, R.: The location of nucleosomes in chromatin: specific or statistical. Nature 292, 579–580 (1981)

    Article  CAS  PubMed  Google Scholar 

  27. Kornberg, R.D., Lorch, Y.: Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromasome. Cell 98, 285–294 (1999)

    Article  CAS  PubMed  Google Scholar 

  28. Reynolds, S.M., Käll, L., Bilmes, J.A., Noble, W.S.: Transmembrane topology and signal peptide prediction using dynamic Bayesian networks. PLoS Computational Biology 4, 11 (2008)

    Article  Google Scholar 

  29. Takasuka, T.E., Cioffi, A., Stein, A.: Sequence information encoded in DNA that influence long-range chromatin structure correlates with human chromosome functions. PLoS ONE 3, 7 (2008)

    Article  Google Scholar 

  30. Wang, Y.H.: Chromatin structure of repeating CTG/CAG and CGG/CCG sequences in human disease. Front Bioscience 122, 4731–4741 (2007)

    Article  Google Scholar 

  31. Albert, I., Mavrich, T.N., Tomsho, L.P., Qi, J., Zanton, S.J., Schuster, S.C., Pugh, B.F.: Translational and rotational settings of H2A. Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446, 572–576 (2007)

    Article  CAS  PubMed  Google Scholar 

  32. Mavrich, T.N., Ioshikhes, I.P., Venters, B.J., Jiang, C., Tomsho, L.P., Qi, J., Schuster, S.C., Albert, I., Pugh, B.F.: A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Research 18, 1073–1083 (2008)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Richmond, T.J., Davey, C.A.: The structure of DNA in the nucleosome core. Nature 423, 145–150 (2007)

    Article  Google Scholar 

  34. Tolstorukov, M.Y., Colasanti, A.V., McCandlish, D.M., Olson, W.K., Zhurkin, V.B.: A novel roll-and-slide mechanism of DNA folding in chromatin: implications for nucleosome positioning. Journal of Molecular Biology 371, 725–738 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. ENCODE Consortium: The ENCODE (ENcyclopedia Of DNA Elements) Project. Science. 306, 636–640 (2004)

    Google Scholar 

  36. Xie, X., Mikkelsen, T.S., Gnirke, A., Lindblad-Toh, K., Kellis, M., Lander, E.S.: Systematic discovery of regulatory motifs in conserved regions of the human genome, including thousands of CTCF insulator sites. Proceedings of the National Academy of Sciences of the United States of America 104, 7145–7150 (2007)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Fu, Y., Sinha, M., Peterson, C.L., Weng, Z.: The insulator binding protein CTCF positions 20 nucleosomes around its binding sites across the human genome. PLoS Genetics 4, 7 (2008)

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this paper

Cite this paper

Reynolds, S.M., Bilmes, J.A., Noble, W.S. (2009). On the Relationship between DNA Periodicity and Local Chromatin Structure. In: Batzoglou, S. (eds) Research in Computational Molecular Biology. RECOMB 2009. Lecture Notes in Computer Science(), vol 5541. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02008-7_31

Download citation

  • DOI: https://doi.org/10.1007/978-3-642-02008-7_31

  • Publisher Name: Springer, Berlin, Heidelberg

  • Print ISBN: 978-3-642-02007-0

  • Online ISBN: 978-3-642-02008-7

  • eBook Packages: Computer ScienceComputer Science (R0)

Publish with us

Policies and ethics