Naturally Occurring Nucleosome Positioning Signals in Human Exons and Introns

Baldi, Pierre; Brunak, Søren; Chauvin, Yves; Krogh, Anders

doi:10.1006/jmbi.1996.0592

Cited by 67 publications

(66 citation statements)

References 38 publications

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“…This particularity might be related to the constraints exerted on the evolution of these sequences by their protein coding contents. This result extends the possibility that the formation of nucleosomes in exonic regions can involve sequence patterns that differ from those of intronic regions, as already suggested by Baldi and collaborators [22].…”

Section: To What Mechanisms Of the Eukaryotic Cells Are Related The Ssupporting

confidence: 88%

“…So far, such constraints have been evidenced to favour the formation and positioning of nucleosomes [15,16,17,18,19]. These structural properties depend upon the local nucleotides composition and therefore can be seen as statistical features of the DNA primary structure [20,21,22,23,24,25,26]. The actual challenge is thus to find a way to extract these structural informations from an appropriate reading of the DNA text.…”

Section: Introductionmentioning

confidence: 99%

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Wavelet Analysis of DNA Bending Profiles reveals Structural Constraints on the Evolution of Genomic Sequences

Audit

Vaillant

Arnéodo

et al. 2004

Journal of Biological Physics

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Abstract. Analyses of genomic DNA sequences have shown in previous works that base pairs are correlated at large distances with scale-invariant statistical properties. We show in the present study that these correlations between nucleotides (letters) result in fact from long-range correlations (LRC) between sequence-dependent DNA structural elements (words) involved in the packaging of DNA in chromatin. Using the wavelet transform technique, we perform a comparative analysis of the DNA text and of the corresponding bending profiles generated with curvature tables based on nucleosome positioning data. This exploration through the optics of the so-called 'wavelet transform microscope' reveals a characteristic scale of 100 − 200 bp that separates two regimes of different LRC. We focus here on the existence of LRC in the small-scale regime ( 200 bp). Analysis of genomes in the three kingdoms reveals that this regime is specifically associated to the presence of nucleosomes. Indeed, small scale LRC are observed in eukaryotic genomes and to a less extent in archaeal genomes, in contrast with their absence in eubacterial genomes. Similarly, this regime is observed in eukaryotic but not in bacterial viral DNA genomes. There is one exception for genomes of Poxviruses, the only animal DNA viruses that do not replicate in the cell nucleus and do not present small scale LRC. Furthermore, no small scale LRC are detected in the genomes of all examined RNA viruses, with one exception in the case of retroviruses. Altogether, these results strongly suggest that small-scale LRC are a signature of the nucleosomal structure. Finally, we discuss possible interpretations of these small-scale LRC in terms of the mechanisms that govern the positioning, the stability and the dynamics of the nucleosomes along the DNA chain. This paper is maily devoted to a pedagogical presentation of the theoretical concepts and physical methods which are well suited to perform a statistical analysis of genomic sequences. We review the results obtained with the so-called waveletbased multifractal analysis when investigating the DNA sequences of various organisms in the three kingdoms. Some of these results have been announced in B. Audit et al. [1,2].

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Section: To What Mechanisms Of the Eukaryotic Cells Are Related The Ssupporting

confidence: 88%

Section: Introductionmentioning

confidence: 99%

Wavelet Analysis of DNA Bending Profiles reveals Structural Constraints on the Evolution of Genomic Sequences

Audit

Vaillant

Arnéodo

et al. 2004

Journal of Biological Physics

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“…However, knowledge of how nucleosomes and histone modifications are distributed relative to other genomic features could result in valuable and novel insights into other biological processes, such as DNA replication and mRNA splicing (Allemand et al 2008;Bres et al 2008;Gottipati and Helleday 2009). It has been previously suggested that intron/exon junctions contain DNA sequences that promote nucleosome positioning (Beckmann and Trifonov 1991;Baldi et al 1996;Kogan and Trifonov 2005). Positioned nucleosomes at these junctions were proposed to protect splice sites at exon starts from mutations (Kogan and Trifonov 2005).…”

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confidence: 99%

Nucleosomes are well positioned in exons and carry characteristic histone modifications

Andersson¹,

Enroth²,

et al. 2009

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The genomes of higher organisms are packaged in nucleosomes with functional histone modifications. Until now, genomewide nucleosome and histone modification studies have focused on transcription start sites (TSSs) where nucleosomes in RNA polymerase II (RNAPII) occupied genes are well positioned and have histone modifications that are characteristic of expression status. Using public data, we here show that there is a higher nucleosome-positioning signal in internal human exons and that this positioning is independent of expression. We observed a similarly strong nucleosome-positioning signal in internal exons of Caenorhabditis elegans. Among the 38 histone modifications analyzed in man, H3K36me3, H3K79me1, H2BK5me1, H3K27me1, H3K27me2, and H3K27me3 had evidently higher signals in internal exons than in the following introns and were clearly related to exon expression. These observations are suggestive of roles in splicing. Thus, exons are not only characterized by their coding capacity, but also by their nucleosome organization, which seems evolutionarily conserved since it is present in both primates and nematodes.

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“…It is frequently assumed that the underlying DNA sequence plays an important role in defining some fraction of nucleosome positions across a genome. Several rather different nucleosome DNA sequence patterns have been suggested (Mengeritsky and Trifonov 1983;Zhurkin 1983;Drew and Travers 1985;Calladine and Drew 1986;Satchwell et al 1986;Uberbacher et al 1988;Ioshikhes et al 1992;Baldi et al 1996;Ioshikhes et al 1996;Lowary and Widom 1998;Kogan et al 2006;Segal et al 2006;Albert et al 2007;Salih et al 2007;Mavrich et al 2008a). The observation of the periodical appearance of some dinucleotides, primarily AA and TT, along eukaryotic DNA sequences with a period close to that of the DNA helical repeat (;10 bp) was long ago spelled out as a nucleotide sequence pattern that may facilitate anisotropic DNA bendability and nucleosome formation (Trifonov and Sussman 1980).…”

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confidence: 99%

Variety of genomic DNA patterns for nucleosome positioning

Ioshikhes¹,

Hosid²,

Pugh³

2011

Genome Res.

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Precise positioning of nucleosomes along DNA is important for a variety of gene regulatory processes. Among the factors directing nucleosome positioning, the DNA sequence is highly important. Two main classes of nucleosome positioning sequence (NPS) patterns have previously been described. In the first class, AA, TT, and other WW dinucleotides (where W is A or T) tend to occur together (in-phase) in the major groove of DNA closest to the histone octamer surface, while SS dinucleotides (where S is G or C) are predominantly positioned in the major groove facing outward. In the second class, AA and TT are structurally separated (AA backbone near the histone octamer, and TT backbone further away), but grouped with other RR (where R is purine A or G) and YY (where Y is pyrimidine C or T) dinucleotides. As a result, the RR/YY pattern includes counter-phase AA/TT distributions. We describe here anti-NPS patterns, which are inverse to the conventional NPS patterns: WW runs inverse to SS, and RR inverse to YY. Evidence for the biological relevance of anti-NPS patterns is presented.

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Naturally Occurring Nucleosome Positioning Signals in Human Exons and Introns

Cited by 67 publications

References 38 publications

Wavelet Analysis of DNA Bending Profiles reveals Structural Constraints on the Evolution of Genomic Sequences

Wavelet Analysis of DNA Bending Profiles reveals Structural Constraints on the Evolution of Genomic Sequences

Nucleosomes are well positioned in exons and carry characteristic histone modifications

Variety of genomic DNA patterns for nucleosome positioning

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