DNA-guided establishment of nucleosome patterns within coding regions of a eukaryotic genome

Genome Research

Volumn 25, Issue 11, 2015, Pages 1727-1738

  Beh, Leslie Y ^a   Müller, Manuel M ^a   Muir, Tom W ^a   Kaplan, Noam ^b   Landweber, Laura F ^a  

^a PRINCETON UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DINUCLEOTIDE; DNA; TRANS ACTING FACTOR; NUCLEOSOME; PROTOZOAL DNA;

AMINO ACID COMPOSITION; ARTICLE; AT RICH SEQUENCE; CODON USAGE; DNA BASE COMPOSITION; DNA SEQUENCE; EUKARYOTIC CELL; GC RICH SEQUENCE; GENETIC CODE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; TETRAHYMENA THERMOPHILA; TRANSCRIPTION INITIATION SITE; CHROMOSOMAL MAPPING; GENETIC ASSOCIATION STUDY; GENETIC TRANSCRIPTION; GENETICS; GENOME; OPEN READING FRAME;

CHROMOSOME MAPPING; DNA, PROTOZOAN; GENETIC ASSOCIATION STUDIES; GENOME, PROTOZOAN; NUCLEOSOMES; OPEN READING FRAMES; SEQUENCE ANALYSIS, DNA; TETRAHYMENA THERMOPHILA; TRANSCRIPTION, GENETIC;

EID: 84946565962     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.188516.114     Document Type: Article

References (56)

1. Allan J, Fraser RM, Owen-Hughes T, Docherty K, Singh V. 2013. A comparison of in vitro nucleosome positioning mapped with chicken, frog and a variety of yeast core histones. J Mol Biol 425: 4206-4222.
2. Blankenberg D, Von Kuster G, Coraor N, Ananda G, Lazarus R, Mangan M, Nekrutenko A, Taylor J. 2010. Galaxy: a web-based genome analysis tool for experimentalists. Curr Protoc Mol Biol 19: 19.10.1-21.
3. Chang GS, Noegel AA, Mavrich TN, Müller R, Tomsho L, Ward E, Felder M, Jiang C, Eichinger L, Glöckner G, et al. 2012. Unusual combinatorial involvement of poly-A/T tracts in organizing genes and chromatin in Dictyostelium. Genome Res 22: 1098-1106.
4. Chen X, Chen Z, Chen H, Su Z, Yang J, Lin F, Shi S, He X. 2012. Nucleosomes suppress spontaneous mutations base-specifically in eukaryotes. Science 335: 1235-1238.
5. Chen K, Xi Y, Pan X, Li Z, Kaestner K, Tyler J, Dent S, He X, Li W. 2013a. DANPOS: dynamic analysis of nucleosome position and occupancy by sequencing. Genome Res 23: 341-351.
6. Chen RA-J, Down TA, Stempor P, Chen QB, Egelhofer TA, Hillier LW, Jeffers TE, Ahringer J. 2013b. The landscape of RNA polymerase II transcription initiation in C. elegans reveals promoter and enhancer architectures. Genome Res 23: 1339-1347.
7. Coyne RS, Stover NA, MiaoW. 2012. Whole genome studies of Tetrahymena. Methods Cell Biol 109: 53-81.
8. Eisen JA, Coyne RS, Wu M, Wu D, Thiagarajan M, Wortman JR, Badger JH, Ren Q, Amedeo P, Jones KM, et al. 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol 4: e286.
9. Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, Lubling Y, Widom J, Segal E. 2008. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol 4: e1000216.
10. Fredrick K, Ibba M. 2010. How the sequence of a gene can tune its translation. Cell 141: 227-229.
11. Gaffney DJ, McVicker G, Pai AA, Fondufe-Mittendorf YN, Lewellen N, Michelini K, Widom J, Gilad Y, Pritchard JK. 2012. Controls of nucleosome positioning in the human genome. PLoS Genet 8: e1003036.
12. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, et al. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
13. Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, Zhang Y, Blankenberg D, Albert I, Taylor J, et al. 2005. Galaxy: a platform for interactive large-scale genome analysis. Genome Res 15: 1451-1455.
14. Gkikopoulos T, Schofield P, Singh V, Pinskaya M, Mellor J, Smolle M, Workman JL, Barton GJ, Owen-Hughes T. 2011. A role for Snf2-related nucleosome-spacing enzymes in genome-wide nucleosome organization. Science 333: 1758-1760.
15. Goecks J, Nekrutenko A, Taylor J. 2010. Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86.
16. GorovskyMA, Glover C, Johmann CA, Keevert JB, Mathis DJ, Samuelson M. 1978. Histones and chromatin structure in Tetrahymena macro- and micronuclei. Cold Spring Harb Symp Quant Biol 42 Pt (1): 493-503.
17. Huff JT, Zilberman D. 2014. Dnmt1-independent CG methylation contributes to nucleosome positioning in diverse eukaryotes. Cell 156: 1286-1297.
18. Hughes AL, Jin Y, Rando OJ, Struhl K. 2012. A functional evolutionary approach to identify determinants of nucleosome positioning: a unifying model for establishing the genome-wide pattern. Mol Cell 48: 5-15.
19. Jacob NK, Stout AR, Price CM. 2004. Modulation of telomere length dynamics by the subtelomeric region of Tetrahymena telomeres. Mol Biol Cell 15: 3719-3728.
20. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, LeProust EM, Hughes TR, Lieb JD, Widom J, et al. 2009. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362-366.
21. Kaplan N, Hughes TR, Lieb JD, Widom J, Segal E. 2010a. Contribution of histone sequence preferences to nucleosome organization: proposed definitions and methodology. Genome Biol 11: 140.
22. Kaplan N, Moore I, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, Hughes TR, Lieb JD, Widom J, Segal E. 2010b. Nucleosome sequence preferences influence in vivo nucleosome organization. Nat Struct Mol Biol 17: 918-920.
23. Kornberg RD, Stryer L. 1988. Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res 16: 6677-6690.
24. Lam FH, Steger DJ, O'Shea EK. 2008. Chromatin decouples promoter threshold from dynamic range. Nature 453: 246-250.
25. Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9; 357-359
26. Lantermann AB, Straub T, Strålfors A, Yuan G-C, Ekwall K, Korber P. 2010. Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae. Nat Struct Mol Biol 17: 251-257.
27. LeeW, Tillo D, Bray N, Morse RH, Davis RW, Hughes TR, Nislow C. 2007. A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 39: 1235-1244.
28. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Crystal structure of the nucleosome core particle at 2.8 Å resolution. Nature 389: 251-260.
29. Luger K, Rechsteiner TJ, Richmond TJ. 1999. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol 304: 3-19.
30. Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, Qi J, Schuster SC, Albert I, Pugh BF. 2008a. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18: 1073-1083.
31. Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, Zanton SJ, Tomsho LP, Qi J, Glaser RL, Schuster SC, et al. 2008b. Nucleosome organization in the Drosophila genome. Nature 453: 358-362.
32. Nelson HC, Finch JT, Luisi BF, Klug A. 1987. The structure of an oligo (dA)·oligo(dT) tract and its biological implications. Nature 330: 221-226.
33. Palen TE, Cech TR. 1984. Chromatin structure at the replication origins and transcription-initiation regions of the ribosomal RNA genes of Tetrahymena. Cell 36: 933-942.
34. Parmley JL, Hurst LD. 2007. Exonic splicing regulatory elements skew synonymous codon usage near intron-exon boundaries in mammals. Mol Biol Evol 24: 1600-1603.
35. Parmley JL, Chamary JV, Hurst LD. 2006. Evidence for purifying selection against synonymous mutations in mammalian exonic splicing enhancers. Mol Biol Evol 23: 301-309.
36. Piña B, Brüggemeier U, Beato M. 1990. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell 60: 719-731.
37. Ponts N, Harris EY, Prudhomme J, Wick I, Eckhardt-Ludka C, Hicks GR, Hardiman G, Lonardi S, Le Roch KG. 2010. Nucleosome landscape and control of transcription in the human malaria parasite. Genome Res 20: 228-238.
38. Radman-Livaja M, Rando OJ. 2010. Nucleosome positioning: How is it established, and why does it matter? Dev Biol 339: 258-66.
39. Segal E, Widom J. 2009. Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol 19: 65-71.
40. Shabalina SA, Ogurtsov AY, Spiridonov NA. 2006. A periodic pattern of mRNA secondary structure created by the genetic code. Nucleic Acids Res 34: 2428-2437.
41. Shivaswamy S, Bhinge A, Zhao Y, Jones S, Hirst M, Iyer VR. 2008. Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation. PLoS Biol 6: e65.
42. Stergachis AB, Haugen E, Shafer A, FuW, Vernot B, Reynolds A, Raubitschek A, Ziegler S, LeProust EM, Akey JM, et al. 2013. Exonic transcription factor binding directs codon choice and affects protein evolution. Science 342: 1367-1372.
43. Struhl K, Segal E. 2013. Determinants of nucleosome positioning. Nat Struct Mol Biol 20: 267-273.
44. Suter B, Schnappauf G, Thoma F. 2000. Poly(dA·dT) sequences exist as rigid DNA structures in nucleosome-free yeast promoters in vivo. Nucleic Acids Res 28: 4083-4089.
45. Teves SS, Weber CM, Henikoff S. 2014. Transcribing through the nucleosome. Trends Biochem Sci 39: 577-586.
46. Tillo D, Hughes TR. 2009. G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics 10: 442.
47. Valouev A, Johnson SM, Boyd SD, Smith CL, Fire AZ, Sidow A. 2011. Determinants of nucleosome organization in primary human cells. Nature 474: 516-520.
48. Wiley EA, Mizzen CA, Allis CD. 2000. Isolation and characterization of in vivo modified histones and an activity gel assay for identification of histone acetyltransferases. Methods Cell Biol 62: 379-394.
49. Xiong J, Lu X, Zhou Z, Chang Y, Yuan D, Tian M, Zhou Z, Wang L, Fu C, Orias E, et al. 2012. Transcriptome analysis of the model protozoan, Tetrahymena thermophila, using deep RNA sequencing. PLoS One 7: e30630.
50. Yen K, Vinayachandran V, Batta K, Koerber RT, Pugh BF. 2012. Genomewide nucleosome specificity and directionality of chromatin remodelers. Cell 149: 1461-1473.
51. Yuan G-C, Liu Y-J, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ. 2005. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309: 626-630.
52. Zhang Z, Pugh BF. 2011. High-resolution genome-wide mapping of the primary structure of chromatin. Cell 144: 175-186.
53. Zhang Y, Moqtaderi Z, Rattner BP, Euskirchen G, Snyder M, Kadonaga JT, Liu XS, Struhl K. 2009. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol 16: 847-852.
54. Zhang L, Ma H, Pugh BF. 2011a. Stable and dynamic nucleosome states during a meiotic developmental process. Genome Res 21: 875-884.
55. Zhang Z, Wippo CJ, Wal M, Ward E, Korber P, Pugh BF. 2011b. A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332: 977-980.
56. Zhang Y, Vastenhouw NL, Feng J, Fu K, Wang C, Ge Y, Pauli A, van Hummelen P, Schier AF, Liu XS. 2014. Canonical nucleosome organization at promoters forms during genome activation. Genome Res 24: 260-266.