A comparative evaluation on prediction methods of nucleosome positioning

Nucleosome positioning plays an essential role in cellular processes by modulating accessibility of DNA to proteins. Many computational models have been developed to predict genome-wide nucleosome positions from DNA sequences. Comparative analysis of predicted and experimental nucleosome positioning maps facilitates understanding the regulatory mechanisms of transcription and DNA replication. Therefore, a comprehensive evaluation of existing computational methods is important and useful for biologists to choose appropriate ones in their research. In this article, we carried out a performance comparison among eight widely used computational methods on four species including yeast, fruitfly, mouse and human. In particular, we compared these methods on different regions of each species such as gene sequences, promoters and 5'UTR exons. The experimental results show that the performances of the two latest versions of the thermodynamic model are relatively steadier than the other four methods. Moreover, these methods are workable on four species, but their performances decrease gradually from yeast to human, indicating that the fundamental mechanism of nucleosome positioning is conserved through the evolution process, but more and more factors participate in the determination of nucleosome positions, which leads to sophisticated regulation mechanisms.

[1]  Geoffrey J. Barton,et al.  A Role for Snf2-Related Nucleosome-Spacing Enzymes in Genome-Wide Nucleosome Organization , 2011, Science.

[2]  M. Pellegrini,et al.  Relationship between nucleosome positioning and DNA methylation , 2010, Nature.

[3]  Cizhong Jiang,et al.  Nucleosome positioning and gene regulation: advances through genomics , 2009, Nature Reviews Genetics.

[4]  Srinivasan Parthasarathy,et al.  Predicting functionality of protein–DNA interactions by integrating diverse evidence , 2009, Bioinform..

[5]  Jerome Percus,et al.  Model for density variation at a fluid surface , 1976 .

[6]  Alexandre V. Morozov,et al.  Using DNA mechanics to predict in vitro nucleosome positions and formation energies , 2009, Nucleic acids research.

[7]  Bryan J Venters,et al.  A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. , 2008, Genome research.

[8]  C. Allis,et al.  Translating the Histone Code , 2001, Science.

[9]  Lei Xia,et al.  Predicting nucleosome positioning using a duration Hidden Markov Model , 2010, BMC Bioinformatics.

[10]  K. Struhl,et al.  Determinants of nucleosome positioning , 2013, Nature Structural &Molecular Biology.

[11]  C. Peterson,et al.  Histones and histone modifications , 2004, Current Biology.

[12]  I. Albert,et al.  Nucleosome positions predicted through comparative genomics , 2006, Nature Genetics.

[13]  Kevin Struhl,et al.  A functional evolutionary approach to identify determinants of nucleosome positioning: a unifying model for establishing the genome-wide pattern. , 2012, Molecular cell.

[14]  L. Hurst,et al.  The Impact of the Nucleosome Code on Protein-Coding Sequence Evolution in Yeast , 2008, PLoS genetics.

[15]  Naama Barkai,et al.  On the relation between promoter divergence and gene expression evolution , 2008, Molecular systems biology.

[16]  D. Timm,et al.  Asymmetries in the nucleosome core particle at 2.5 A resolution. , 2000, Acta crystallographica. Section D, Biological crystallography.

[17]  N. Barkai,et al.  Two strategies for gene regulation by promoter nucleosomes. , 2008, Genome research.

[18]  Ronald W. Davis,et al.  A high-resolution atlas of nucleosome occupancy in yeast , 2007, Nature Genetics.

[19]  Andrew V. Colasanti,et al.  A novel roll-and-slide mechanism of DNA folding in chromatin: implications for nucleosome positioning. , 2007, Journal of molecular biology.

[20]  Irene K. Moore,et al.  The DNA-encoded nucleosome organization of a eukaryotic genome , 2009, Nature.

[21]  Clifford A. Meyer,et al.  Nucleosome Dynamics Define Transcriptional Enhancers , 2010, Nature Genetics.

[22]  Carlos Bustamante,et al.  Nucleosomal Fluctuations Govern the Transcription Dynamics of RNA Polymerase II , 2009, Science.

[23]  Michael G. Poirier,et al.  DYNAMICS AND FUNCTION OF COMPACT NUCLEOSOME ARRAYS , 2009, Nature Structural &Molecular Biology.

[24]  Alain Arneodo,et al.  A novel strategy of transcription regulation by intragenic nucleosome ordering. , 2010, Genome research.

[25]  Christoforos Nikolaou,et al.  Structural constraints revealed in consistent nucleosome positions in the genome of S. cerevisiae , 2010, Epigenetics & Chromatin.

[26]  Lani F. Wu,et al.  Genome-Scale Identification of Nucleosome Positions in S. cerevisiae , 2005, Science.

[27]  Stephan C. Schuster,et al.  Nucleosome organization in the Drosophila genome , 2008, Nature.

[28]  Jonathan Schug,et al.  The Nucleosome Map of the Mammalian Liver , 2011, Nature Structural &Molecular Biology.

[29]  Wei Chen,et al.  iNuc-PhysChem: A Sequence-Based Predictor for Identifying Nucleosomes via Physicochemical Properties , 2012, PloS one.

[30]  Peter J. Park,et al.  nuScore: a web-interface for nucleosome positioning predictions , 2008, Bioinform..

[31]  Steven M. Johnson,et al.  A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. , 2008, Genome research.

[32]  Yaniv Lubling,et al.  Distinct Modes of Regulation by Chromatin Encoded through Nucleosome Positioning Signals , 2008, PLoS Comput. Biol..

[33]  J. Lieb,et al.  Evidence for nucleosome depletion at active regulatory regions genome-wide , 2004, Nature Genetics.

[34]  Danny Barash,et al.  FineStr: a web server for single-base-resolution nucleosome positioning , 2010, Bioinform..

[35]  K. Struhl,et al.  Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo , 2009, Nature Structural &Molecular Biology.

[36]  Terrence S. Furey,et al.  The UCSC Table Browser data retrieval tool , 2004, Nucleic Acids Res..

[37]  Xiao Sun,et al.  Notice of RetractionDynamic Nucleosome Positioning around Functional Transcription Factor Binding Sites in the Promoters of Inducible NF-kappaB Target Genes , 2011, 2011 5th International Conference on Bioinformatics and Biomedical Engineering.

[38]  K. Struhl,et al.  High-throughput sequencing reveals a simple model of nucleosome energetics , 2010, Proceedings of the National Academy of Sciences.

[39]  Vincent Miele,et al.  DNA physical properties determine nucleosome occupancy from yeast to fly , 2008, Nucleic acids research.

[40]  Irene K. Moore,et al.  A genomic code for nucleosome positioning , 2006, Nature.

[41]  Oliver J. Rando,et al.  Chromatin remodelling at promoters suppresses antisense transcription , 2007, Nature.

[42]  C. Logie,et al.  Sequence-based prediction of single nucleosome positioning and genome-wide nucleosome occupancy , 2012, Proceedings of the National Academy of Sciences.

[43]  Taichi E. Takasuka,et al.  Are nucleosome positions in vivo primarily determined by histone–DNA sequence preferences? , 2009, Nucleic acids research.

[44]  Dustin E. Schones,et al.  Dynamic Regulation of Nucleosome Positioning in the Human Genome , 2008, Cell.

[45]  William Stafford Noble,et al.  Nucleosome positioning signals in genomic DNA. , 2007, Genome research.

[46]  Young-Joon Kim,et al.  Intrinsic variability of gene expression encoded in nucleosome positioning sequences , 2009, Nature Genetics.

[47]  Eran Segal,et al.  Evidence against a genomic code for nucleosome positioning? , 2010 .

[48]  T. Richmond,et al.  The structure of DNA in the nucleosome core , 2003, Nature.

[49]  T. Richmond,et al.  Crystal structure of the nucleosome core particle at 2.8 Å resolution , 1997, Nature.

[50]  Alexander J. Hartemink,et al.  Nucleosome Occupancy Information Improves de novo Motif Discovery , 2007, RECOMB.

[51]  Christoforos Nikolaou,et al.  Nucleosome positioning as a determinant of exon recognition , 2009, Nature Structural &Molecular Biology.

[52]  Kevin Struhl,et al.  Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. , 2005, Molecular cell.

[53]  Zhenhai Zhang,et al.  A Packing Mechanism for Nucleosome Organization Reconstituted Across a Eukaryotic Genome , 2011, Science.

[54]  Guo-Cheng Yuan,et al.  Genomic Sequence Is Highly Predictive of Local Nucleosome Depletion , 2007, PLoS Comput. Biol..

[55]  Kevin Struhl,et al.  Evidence against a genomic code for nucleosome positioning Reply to “Nucleosome sequence preferences influence in vivo nucleosome organization” , 2010, Nature Structural &Molecular Biology.

[56]  R. Kornberg,et al.  Twenty-Five Years of the Nucleosome, Fundamental Particle of the Eukaryote Chromosome , 1999, Cell.

[57]  B. Blencowe,et al.  Regulation of Alternative Splicing by Histone Modifications , 2010, Science.