Theoretical Estimation of Nucleosome Density for Gene Sequences of Different Orthologs upon Euchromatic and Heterochromatic Locations

V. B. Fedoseyeva

Matematičeskaâ biologiâ i bioinformatika, Tome 9 (2014) no. 1, pp. 273-285.

Résumé

A comparison is carried out for orthologs of some genes localized at heterochromatic and euchromatic portions in different Drosophila species by using computer methods for calculation of nucleosome preference and estimation of cluster dimensions of the preference and their inter-distances. It was elucidated that average level of nucleosome location is lower in the case of euchromatin as well as specters of linear dimensions of nucleosome preference are different. In the case of heterochromatin location light, concertina genes incorporate introns that are enriched by short regions of strong nucleosome preferences. The presence of large peaks of nucleosome binding is associated with the numerous repeats of LINE and LTR classes in the introns of heterochromatic gene whereas euchromatic ortholog doesn’t include corresponding repeats and so long introns. In the latter case the local peaks characteristic of nucleosome binding potential are fussy and of smaller amplitude. Upon the heterochromatin location concertina gene characterized by the highest average signal of the nucleosome positioning expresses at the embryonic stage, while light gene with lower average value is viable for different stages of fly development.

Bibliographie

[1] Weiler K. S., Wakimoto V. T., “Heterochromatin and gene expression in Drosophila”, Annu. Rev. Genet., 29 (1995), 577–605 | DOI

[2] Schotta G., Ebert A., Dorn R., Reuter G., “Position-effect variegation and the genetic dissection of chromatin regulation in Drosophila”, Semin. Cell Dev. Biol., 14 (2003), 67–75 | DOI

[3] Hower M., Dimitri P., Berloco M., Wakimoto B., “Cis-effects of heterochromatin on heterochromatic and euchromatic gene activity in Drosophila melanogaster”, Genetics, 140 (1995), 1033–1045

[4] Sun F.-L., Cuaycong M. H., Elgin S. C. R., “Long-range nucleosome ordering is associated with gene silencing in Drosophila melanogaster pericentric heterochromatin”, Mol. Cell. Biol., 21 (2001), 2867–2879 | DOI

[5] Noma K., Allis C. D., Grewal S. I., “Transitions in distinct histone H3 methylation patterns at the heterochromatin domain boundaries”, Science, 293 (2001), 1150–1155 | DOI

[6] Verschure P., Van der Kraan I., De Leeuw W., Van der Vlag J., Carpenter A. E., Belmont A. S., Van Drier R., “In vivo HP1 targeting causes large-scale chromatin condensation and enhanced histone lysine methylation”, Mol. Cell. Biol., 25 (2005), 4552–4564 | DOI

[7] Stewart M. D., Li J., Wong J., “Relationship between histone H3 lysine 9 methylation, transcription repression and heterochromatin protein1 recruitment”, Mol. Cell. Biol., 25 (2005), 2525–2538 | DOI

[8] Jacob S. A., Khorasanizadeh S., “Structure of HP1 chromodomain bound to lysine 9-methylated histone H3 tail”, Science, 295 (2002), 2080–2083 | DOI

[9] Nielsen P. R., Nietlespach D., Mott H. R., Callaghan J., Bannister A., Kouzarides T., Murzin A. G., Mursin N. V., Laue E. D., “Structure of the HP1 chromodomain bound to histone h3 methylated at lysine 9”, Nature, 416 (2002), 103–107 | DOI

[10] De Wit E., Greil F., van Steensel B., “High-resolution mapping reveals links of HP1 with active and inactive chromatin components”, PLoS Genetics, 3:3 (2007), e38 | DOI

[11] Riddle N. C., Monoda A., Kharchenko P. V., Alekseyenko A. A., Schwartz Y. B., Tolstorukov M. Y., Gorchakov A. A., Jaffe J. D., Kennedy C., Linder-Basso D. et al., “Plasticity in patterns of histone modifications and chromosomal proteins in Drosophila heterochromatin”, Genome Research, 21 (2011), 147–163 | DOI

[12] Pal-Bhadra M., Leibovitch B. A., Gandhi S. G., Chikka M. R., Bhadra U., Birchler J. A., Elgin S. C., “Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery”, Science, 303 (2004), 669–672 | DOI

[13] Fagegaltier D., Bouge A.-L., Berry B., Poisot E., Sismeiro O., Coppee J.-Y., Theodore L., Voinnet O., Antoniewski C., “The endogenous siRNA pathway is involved in heterochromatin formation in Drosophila”, Proc. Natl. Acad. Sci. USA, 106 (2009), 21258–21263 | DOI

[14] Aravin A. A., Lagos-Quintana M., Yalcin A., Zavolan M., Marks D., Snyder D., Gaasterland T., Meyer J., Tuschl T., “The small RNA profile during Drosophila melanogaster development”, Dev. Cell., 5 (2003), 337–350 | DOI

[15] Reihart B. J., Bratel D. P., “Small RNAs correspond to centromere heterochromatin repeats”, Science, 297 (2002), 1831–1838 | DOI

[16] Fedoseyeva V. B., Alexandrov A. A., “Large-scale periodicity of nucleosome positioning signal in pericentric regions of chromosomes (Drosophila melanogaster)”, J. Biomol. Struct. Dynam., 2013 | DOI

[17] Devlin R. H., Brendan B., Wakimoto B. T., “The organization and expression of the light gene, a heterochromatic gene of Drosophila”, Genetics, 123 (1990), 129–140

[18] Yasuhara J. C., DeCrease C. H., Wakimoto B. T., “Evolution of heterochromatic genes of Drosophila”, Proc. Natl. Acad. Sci. USA, 102 (2005), 10958–10963 | DOI

[19] 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: implication for nucleosome positioning”, J. Mol. Biol., 371 (2007), 725–738 | DOI

[20] Wang D., Ulyanov N. B., Zhurkin V. B., “Sequence-dependent kink-and-slide deformations of nucleosome DNA facilitated by histone arginines bound in the minor groove”, J. Biomol. Struct. Dynam., 27 (2010), 843–859 | DOI

[21] Lahm A., Suck D., “DNase I-induced DNA conformation 2A structure of the DNase I-octamer comple”, J. Mol. Biol., 222 (1991), 645–667 | DOI

[22] Suck D., “DNA recognition by DNase I”, J. Mol. Recognit., 7 (1994), 65–70 | DOI

[23] Weston S. A., Lahm A., Suck D., “X-ray structure of the DNase I-d(GGTATACC)2 complex at 2.3 A resolution”, J. Mol. Biol., 226 (1992), 1237–1256 | DOI

[24] Luger K., Mader A. W., Richmond R. K., Sargent D. F., Richmond T. J., “Crystal structure of nucleosome core particle 2.8 Å resolution”, Nature, 389 (1997), 251–260 | DOI

[25] Oguel C., Foloppe N., Hartmann B., “Understanding the sequence dependence of DNA groove dimentions: implications for DNA interactions”, PLoS One, 5 (2010), e15931 | DOI

[26] Drew H. R., Travers A. A., “DNA structural variations in the E.coli tyrT promoter”, Cell, 37 (1984), 491–502 | DOI

[27] Drew H. R., Travers A. A., “DNA bending and its relation to nucleosome positioning”, J. Mol. Biol., 186 (1985), 773–790 | DOI

[28] Lomonossoff G. P., Butler P. J. G., Klug A., “Sequence dependent variation in the conformation of DNA”, J. Mol. Biol., 149 (1984), 745–760 | DOI

[29] Bruckner I., Sanchez R., Suck D., Pondor S., “Sequence-dependent bending propensity of DNA as revealed by DNase I: parameters for trinucleotides”, EMBO J., 114 (1995), 1812–1818

[30] Satchwell S. C., Drew H. R., Travers A. A., “Sequence periodicities in chicken nucleosome”, J. Mol. Biol., 191 (1986), 659–675 | DOI

[31] Fedoseyeva V. B., Alexandrov A. A., “Analysis and development of the computer methods of nucleosome localization on DNA fragments with different AT-content”, J. Biomol. Struct. Dynam., 24 (2007), 481–488 | DOI

[32] Bruckner I., Sanchez R., Suck D., Pongor S., “Trinucleotide models for DNA bending propensity: comparison of models based on DNase I digestion and nucleosome packaging data”, J. Biomol. Struct. Dynam., 13 (1995), 309–317 | DOI

[33] Martinez-Garcia J. F., Estruch E., Perez-Ortin J. E., “Chromatin structure of the 5' flanking region of the yeast LEU2 gene”, Mol. Gen. Genet., 217 (1989), 464–470 | DOI

[34] Shimizu M., Roth S. Y., Szent-Gyorgui C., Simpson R. T., “Nucleosomes are positioned with base pair precision adjacent to the alpha 2 operator in Saccharomyces cerevisiae”, EMBO J., 10 (1991), 3033–3041

[35] Roberson A., Wolffe A. P., Hauserans L. J., Olins D. E., “The 5S RNA gene minichromosome of Euplotes”, Nucl. Acids Res., 17 (1989), 4699–4712 | DOI

[36] Levy-Wilson B., Fortier C., Blackhart B. D., McCarthy, “DNase I and micrococcal nuclease-hypersensitive sites in the human apolipoprotein B gene are tissue specific”, Mol. Cell Biol., 8 (1988), 71–80

[37] Thoma F., Bergman L. W., Simpson R. T., “Nuclease digestion of circular TRP1ARS1 chromatin reveals positioned nucleosomes separated by nuclease-sensitive regions”, J. Mol. Biol., 177 (1984), 715–733 | DOI

[38] Thoma F., “Protein-DNA interactions and nuclease-sensitive regions determine nucleosome positions on yeast plasmid chromatin”, J. Mol. Biol., 190 (1986), 177–190 | DOI

[39] Drew H. R., Calladine C. R., “Sequence-specific positioning of core histones on an 860 base-pair DNA. Experiment and theory”, J. Mol. Biol., 195 (1987), 143–173 | DOI

[40] Almer A., Horz W., “Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the PHO5/PHO3 locus in yeast”, EMBO J., 5 (1986), 2681–2687

[41] Almer A., Rudolph H., Hinnen A., Horz W., “Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements”, EMBO J., 5 (1986), 2689–2696

[42] Capranico G., Jaxel C., Roberge M., Kohn K. W., Pommier T., “Nucleosome positioning as a critical determinant for the DNA cleavage sites of mammalian DNA topoisomerase II in reconstituted simian virus 40 chromatin”, Nucl. Acids Res., 18 (1990), 4553–4559 | DOI

[43] Stein A., “Unique positioning of reconstituted nucleosomes occurs in one region of simian virus 40 DNA”, J. Biol. Chem., 262 (1987), 3872–3879

[44] Tanaka S., Livingstone-Zatchej M., Thoma F., “Chromatin structure of the yeast URA3 gene at high resolution provides insight into structure and positioning of nucleosomes in the chromosomal context”, J. Mol. Biol., 257 (1996), 929–934 | DOI

[45] Mengeritsky G., Trifonov E. N., “Nucleotide sequence-directed mapping of the nucleosomes”, Nucl. Acids Res., 11 (1983), 3833–3851 | DOI

[46] Levitsky V. G., Ponomarenko M. P., Ponomarenko J. V., Frolov A. C., Kolchanov N. A., “Nucleosomal DNA property database”, Bioinformatics, 15 (1999), 582–592 | DOI

[47] Levitsky V. G., Podkolodnaya O. A., Kolchanov N. A., Podkolodny N. I., “Nucleosome formation potential of eukaryotic DNA: calculation and promoters analysis”, Bioinformatics, 17 (2001), 998–1010 | DOI

[48] Segal E., Fondufe-Mittendorf V., Chen L., Thasstrom A., Field Y., More I. K., Wang J. P., Widom J., “A genomic code for nucleosome positioning”, Nature, 442 (2006), 772–778 | DOI

[49] Ioshikhes I. P., Albert I., Zanton S. J., Pugh B. F., “Nucleosome positions predicted through comparative genomics”, Nat. Genet., 38 (2006), 1210–1215 | DOI

[50] Lee W., Tillo D., Bray N., Morse R. H., Davis R. W., Hughes T. R., Nislow C., “A high-resolution atlas of nucleosome occupancy in yeast”, Nature Genetics, 39 (2007), 1235–1244 | DOI

[51] Yuan G.-C., Lui Y.-J., Dion M. F., Clack M. D., Wu L. F., Altschuler S. J., Rando O. J., “Genome-scale identification of nucleosome positions in S.cerevisiae”, Science, 309 (2005), 626–630 | DOI

[52] Shruhl K., “Naturally occurring poly(dA-dT) sequences are upstream promoter elements for constitutive transcription in yeast”, Proc. Natl. Acad. Sci. USA, 82 (1985), 8419–8423 | DOI

[53] Yuan G. C., Lui J. S., “Genomic sequence is highly predictive of local nucleosome depletion”, PLoS Comput. Biol., 4 (2008), e13 | DOI

[54] Barski A., Cuddapah S., Cui K., Roh T. Y., Schones D. E., Wang Z., Wei G., Chepelev I., Zhao K., “High resolution profiling of histone methylations in the human genome”, Cell, 129 (2007), 823–837 | DOI

[55] Albert I., Mavrich T. N., Tomsho L. P., Qi J., Zanton S. J., Schuster S. C., Pugh B. F., “Translational and notational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome”, Nature, 446 (2007), 572–576 | DOI

[56] Mavrich T. N., Jiang V., Ioshikhes I. P., Li X., Venters B. J., Zanton S. J., Tomsho L. P., Qi J., Glasen R., Schuster S. C. et al., “Nucleosome organization in the Drosophila genome”, Nature, 453 (2008), 358–362 | DOI

[57] Schones D. E., Cui K., Cuddapah S., Roh T. Y., Barski A., Wang Z., Wei G., Zhao K., “Dynamic regulation of nucleosomes positioning in the human genome”, Cell, 132 (2008), 887–898 | DOI

[58] Field Y., Kaplan N., Fondufe-Mittendorf Y., Moore I. K., Sharon E., Lubling Y., Widom J., Segal E., “Distinct modes of regulation by chromatin encoded through nucleosome positioning signals”, PLoS Comput. Biol., 4 (2008), e1000216 | DOI

[59] Schwabish M. A., Struhl K., “Evidence for eviction and rapid deposition of histones upon transcription elongation by RNA polymerase II”, Mol. Cell Biol., 24 (2004), 10111–10117 | DOI

[60] Schnitzler R., “Control of nucleosome position by DNA sequence and remodeling machine”, Cell Biochem. Biophys., 51 (2008), 6780–6788 | DOI

[61] UCSC Genome Bioinformatics Site (data obrascheniya: 18.01.2012) http://www.genome.ucsc.edu

[62] Peckham H. E., Thurman R. E., Fu Y., Stamatoyannopoulos J. A., Noble W. S., Struhl K., Weng Z., “Nucleosome positioning signals in genomic DNA”, Genome Res., 17 (2007), 1170–1177 | DOI

[63] National Center for Biotechnology Information (data obrascheniya: 18.01.2012) http://www.ncbi.nlm.nih.gov

[64] Penn State Genome Cartography Project (data obrascheniya: 21.05.2013) http://atlas.bx.psu.edu/project/drosophila.html

[65] Khesin R. V., Leibovitch B., “Influence of deficiency of the histone gene-containing 38B-40 region on X-chromosome template activity and the white gene position effect variegation in Drosophila melanogaster”, Mol. Gen. Genet., 162 (1978), 323–328 | DOI

[66] A Database of Drosophila Genes Genomes (data obrascheniya: 8.02.2012) http://flybase.org

[67] Wakimoto B. I., Hearn M. G., “The effect of chromosome rearrangements on the expression of heterochromatic genes in chromosome 2L of Drosophila melanogaster”, Genetics, 125 (1990), 141–154