Mapping nucleosome positions using DNase-seq

Genome Research

Volumn 26, Issue 3, 2016, Pages 351-364

  Zhong, Jianling ^a,b   Luo, Kaixuan ^a,b   Winter, Peter S ^a,c   Crawford, Gregory E ^a,c   Iversen, Edwin S ^a,d   Hartemink, Alexander J ^a,b,d  

^a DUKE UNIVERSITY   (United States)

^b Duke University   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d Duke University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I; DNA; TRANSCRIPTION FACTOR; CHROMATIN; NUCLEOSOME; PROTEIN BINDING;

ARTICLE; BINDING SITE; CONSENSUS SEQUENCE; DNA CLEAVAGE; GENE MAPPING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION AND TRANSLATION; HUMAN; HUMAN GENOME; IN VITRO STUDY; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS; YEAST CELL; BIOLOGY; CHROMATIN; CHROMOSOMAL MAPPING; FUNGAL GENOME; GENETICS; GENOMICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; NUCLEOTIDE MOTIF; PROCEDURES;

BINDING SITES; CHROMATIN; CHROMOSOME MAPPING; COMPUTATIONAL BIOLOGY; DEOXYRIBONUCLEASE I; DNA; GENOME, FUNGAL; GENOME, HUMAN; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; NUCLEOSOMES; NUCLEOTIDE MOTIFS; PROTEIN BINDING; TRANSCRIPTION FACTORS;

EID: 84960345101     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.195602.115     Document Type: Article

References (71)

1. Albert I, Mavrich TN, Tomsho LP, Qi J, Zanton SJ, Schuster SC, Pugh BF. 2007. Translational and rotational settingsof H2A. Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446:572-576.
2. Allan J, Fraser RM, Owen-Hughes T, Keszenman-Pereyra D. 2012. Micrococcal nuclease does not substantially bias nucleosome mapping. J Mol Biol 417:152-164.
3. Bai L, Morozov A. 2010. Gene regulation by nucleosome positioning. Trends Genet 26:476-483.
4. Boyle AP, Davis S, Shulha HP, Meltzer P, Margulies EH, Weng Z, Furey TS, Crawford GE. 2008. High-resolution mapping and characterization of open chromatin across the genome. Cell 132:311-322.
5. Brogaard K, Xi L, Wang J-P, Widom J. 2012. A map of nucleosome positions in yeast at base-pair resolution. Nature 486:496-501.
6. Buenrostro JD, Giresi PG, Zaba LC, Chang HY, Greenleaf WJ. 2013. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nat Methods 10:1213-1218.
7. Carlin BP, Louis TA. 1997. Bayes and empirical Bayes methods for data analysis. Stat Comput 7:153-154.
8. Chung H, Dunkel I, Heise F, Linke C, Krobitsch S, Ehrenhofer-Murray A, Sperling S, Vingron M. 2010. The effect of micrococcal nuclease digestion on nucleosome positioning data. PLOS ONE 5:e15754.
9. Cleveland WS. 1979. Robust locally weighted regression and smoothing scatterplots. J Am Stat Assoc 74:829-836.
10. Cousins D, Islam S, Sanderson M, Proykova Y, Crane-Robinson C, Staynov D. 2004. Redefinitionof the cleavage sitesof DNaseI on the nucleosome core particle. J Mol Biol 335:1199-1211.
11. Crawford GE, Davis S, Scacheri PC, Renaud G, Halawi MJ, Erdos MR, Green R, Meltzer PS, Wolfsberg TG, Collins FS, et al. 2006. DNase-chip: a highresolution method to identify DNase I hypersensitive sites using tiled microarrays. Nat Methods 3:503-509.
12. Cui F, Zhurkin VB. 2014. Rotational positioning of nucleosomes facilitates selective binding of p53 to response elements associated with cell cycle arrest. Nucleic Acids Res 42:836-847.
13. Degner JF, Pai AA, Pique-Regi R, Veyrieras J-B, Gaffney DJ, Pickrell JK, De Leon S, Michelini K, Lewellen N, Crawford GE, et al. 2012. DNase I sensitivity QTLs are a major determinant of human expression variation. Nature 482:390-394.
14. Dorn ES, Cook JG. 2011. Nucleosomes in the neighborhood. Epigenetics 6:552-559.
15. Eaton ML, Galani K, Kang S, Bell SP, MacAlpine DM. 2010. Conserved nucleosome positioning defines replication origins. Genes Dev 24:748-753.
16. Ehrenhofer-Murray AE. 2004. Chromatin dynamics at DNA replication, transcription and repair. Eur J Biochem 271:2335-2349.
17. The ENCODE Project Consortium. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447:799-816.
18. The ENCODE Project Consortium. 2011. A user's guide to the encyclopedia of DNA elements (ENCODE). PLOS Biol 9:e1001046.
19. 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.
20. 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.
21. Gordân R, Hartemink AJ, Bulyk ML. 2009. Distinguishing direct versus indirect transcription factor-DNA interactions. Genome Res 19:2090-2100.
22. Gordân R, Murphy KF, McCord RP, Zhu C, Vedenko A, Bulyk ML. 2011. Curated collection of yeast transcription factor DNA binding specificity data reveals novel structural and gene regulatory insights. Genome Biol 12:R125.
23. Henikoff J, Belsky J, Krassovsky K, MacAlpine D, Henikoff S. 2011. Epigenome characterization at single base-pair resolution. Proc Natl Acad Sci 108:18318-18323.
24. Hesselberth J, Chen X, Zhang Z, Sabo P, Sandstrom R, Reynolds A, Thurman R, Neph S, Kuehn M, Noble W, et al. 2009. Global mapping of protein-DNA interactions in vivo by digital genomic footprinting. Nat Methods 6:283-289.
25. Hoffman M, Buske O, Wang J, Weng Z, Bilmes J, Noble W. 2012. Unsupervised pattern discovery in human chromatin structure through genomic segmentation. Nat Methods 9:473-476.
26. Hörz W, Altenburger W. 1981. Sequence specific cleavage of DNA by micrococcal nuclease. Nucleic Acids Res 9:2643-2658.
27. Jiang C, Pugh BF. 2009a. A compiled and systematic reference map of nucleosome positions across the Saccharomyces cerevisiae genome. Genome Biol 10:R109.
28. Jiang C, Pugh BF. 2009b. Nucleosome positioning and gene regulation: advances through genomics. Nat Rev Genet 10:161-172.
29. Koerber RT, Rhee HS, Jiang C, Pugh BF. 2009. Interaction of transcriptional regulators with specific nucleosomes across the Saccharomyces genome. Mol Cell 35:889-902.
30. Kornberg RD, Lorch Y. 1999. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98:285-294.
31. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memoryefficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25.
32. Lee W, 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.
33. Li G, Widom J. 2004. Nucleosomes facilitate their own invasion. Nat Struct Mol Biol 11:763-769.
34. Li Q, Wrange O. 1995. Accessibility of a glucocorticoid response element in a nucleosome depends on its rotational positioning. Mol Cell Biol 15:4375-4384.
35. Li G, Levitus M, Bustamante C, Widom J. 2005. Rapid spontaneous accessibility of nucleosomal DNA. Nat Struct Mol Biol 12:46-53.
36. Li B, Carey M, Workman JL. 2007. The role of chromatin during transcription. Cell 128:707-719.
37. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. 1997. Crystal structureof the nucleosome core particleat2.8 Åresolution. Nature 389:251-260.
38. Luo K, Hartemink AJ. 2013. Using DNase digestion data to accurately identify transcription factor binding sites. In Pacific symposium on biocomputing, pp. 80-91. World Scientific, Hackensack, NJ.
39. Lutter LC. 1978. Kinetic analysis of deoxyribonuclease I cleavages in the nucleosome core: evidence for a DNA superhelix. J Mol Biol 124:391-420.
40. Lutter LC. 1979. Precise location of DNase I cutting sites in the nucleosome core determined by high resolution gel electrophoresis. Nucleic Acids Res 6:41-56.
41. MacIsaac K, Wang T, Gordon D, Gifford D, Stormo G, Fraenkel E. 2006. An improved map of conserved regulatory sites for Saccharomyces cerevisiae. BMC Bioinformatics 7:113.
42. Mao C, Brown CR, Griesenbeck J, Boeger H. 2011. Occlusion of regulatory sequences by promoter nucleosomes in vivo. PLOS ONE 6:e17521.
43. Martinez-Campa C, Politis P, Moreau J-L, Kent N, Goodall J, Mellor J, Goding CR. 2004. Precise nucleosome positioning and the TATA box dictate requirements for the histone H4 tail and the bromodomain factor Bdf1. Mol Cell 15:69-81.
44. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, Arenillas DJ, Buchman S, Chen CY, Chou A, Ienasescu H, et al. 2014. Jaspar 2014:an extensively expanded and updated open-access databaseof transcription factor binding profiles. Nucleic Acids Res 42:D142-D147.
45. Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, Qi J, Schuster SC, Albert I, Pugh BF. 2008. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 18:1073-1083.
46. Méchali M. 2010. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat Rev Mol Cell Biol 11:728-738.
47. Nagy PL, Cleary ML, Brown PO, Lieb JD. 2003. Genomewide demarcation of RNA polymerase II transcription units revealed by physical fractionation of chromatin. Proc Natl Acad Sci 100:6364-6369.
48. Narlikar L, Gordân R, Hartemink A. 2007. A nucleosome-guided map of transcription factor binding sites in yeast. PLOS Comput Biol 3:e215.
49. Neph S, Vierstra J, Stergachis AB, Reynolds AP, Haugen E, Vernot B, Thurman RE, John S, Sandstrom R, Johnson AK, et al. 2012. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 489:83-90.
50. Noll M. 1974. Internal structure of the chromatin subunit. Nucleic Acids Res 1:1573-1578.
51. Prado R, West M. 2010. Time series: modeling, computation, and inference, 1st ed. Chapman and Hall/CRC Texts in Statistical Science. Chapman and Hall/CRC, Boca Raton, FL.
52. Prunell A, Kornberg R, Lutter L, Klug A, Levitt M, Crick F. 1979. Periodicity of deoxyribonuclease I digestion of chromatin. Science 204:855-858.
53. Radman-Livaja M, Rando OJ. 2010. Nucleosome positioning: how is it established, and why does it matter? Dev Biol 339:258-266.
54. Raveh-Sadka T, Levo M, Segal E. 2009. Incorporating nucleosomes into thermodynamic models of transcription regulation. Genome Res 19:1480-1496.
55. Rhee HS, Pugh BF. 2012. Genome-wide structure and organization of eukaryotic pre-initiation complexes. Nature 483:295-301.
56. Satchwell SC, Drew HR, Travers AA. 1986. Sequence periodicities in chicken nucleosome core DNA. J Mol Biol 191:659-675.
57. Schones DE, Cui K, Cuddapah S, Roh T-Y, Barski A, Wang Z, Wei G, Zhao K. 2008. Dynamic regulation of nucleosome positioning in the human genome. Cell 132:887-898.
58. Segal E, Fondufe-Mittendorf Y, Chen L, Thåström A, Field Y, Moore IK, Wang J-P, Widom J. 2006. A genomic code for nucleosome positioning. Nature 442:772-778.
59. Sekiya T, Muthurajan UM, Luger K, Tulin AV, Zaret KS. 2009. Nucleosomebinding affinity as a primary determinant of the nuclear mobility of the pioneer transcription factor FoxA. Genes Dev 23:804-809.
60. Sherwood RI, Hashimoto T, O'Donnell CW, Lewis S, Barkal AA, Van Hoff JP, Karun V, Jaakkola T, Gifford DK. 2014. Discovery of directional and nondirectional pioneer transcription factors by modeling DNase profile magnitude and shape. Nat Biotechnol 32:171-178.
61. Shivaswamy S, Bhinge A, Zhao Y, Jones S, Hirst M, Iyer VR. 2008. Dynamic remodeling ofindividual nucleosomes across a eukaryotic genome inresponse to transcriptional perturbation. PLOS Biol 6:e65.
62. Simpson RT, Stafford DW. 1983. Structural features of a phased nucleosome core particle. Proc Natl Acad Sci 80:51-55.
63. Song L, Crawford GE. 2010. DNase-seq: A high-resolution technique for mapping active gene regulatory elements across the genome from mammalian cells. Cold Spring Harb Protoc 2010: pdb.prot5384.
64. Song L, Zhang Z, Grasfeder LL, Boyle AP, Giresi PG, Lee B-K, Sheffield NC, Gräf S, Huss M, Keefe D, et al. 2011. Open chromatin defined by DNase I and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res 21:1757-1767.
65. Suck D, Lahm A, Oefner C. 1988. Structure refined to 2Å of a nicked DNA octanucleotide complex with DNase I. Nature 332:464-468.
66. Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, et al. 2012. The accessible chromatin landscape of the human genome. Nature 489:75-82.
67. Vierstra J, Wang H, John S, Sandstrom R, Stamatoyannopoulos JA. 2014. Coupling transcription factor occupancy to nucleosome architecture with DNase-FLASH. Nat Methods 11:66-72.
68. Wasson T, Hartemink AJ. 2009. An ensemble model of competitive multifactor binding of the genome. Genome Res 19:2101-2012.
69. Winter DR, Song L, Mukherjee S, Furey TS, Crawford GE. 2013. DNase-seq predicts regionsof rotational nucleosome stability across diverse human cell types. Genome Res 23:1118-1129.
70. 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.
71. Zhong J, Wasson T, Hartemink AJ. 2014. Learning protein-DNA interaction landscapes by integrating experimental data through computational models. Bioinformatics 30:2868-2874.