Contribution of histone sequence preferences to nucleosome organization: Proposed definitions and methodology

Genome Biology

Volumn 11, Issue 11, 2010, Pages

  Kaplan, Noam ^a   Hughes, Timothy R ^b,c   Lieb, Jason D ^d   Widom, Jonathan ^e   Segal, Eran ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b UNIVERSITY OF TORONTO   (Canada)

^c Banting and Best Department of Medical Research   (Canada)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

^e NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; MICROCOCCAL NUCLEASE;

ARTICLE; BASE PAIRING; CELLULAR DISTRIBUTION; DNA BASE COMPOSITION; DNA MICROARRAY; DNA SEQUENCE; GENE MAPPING; GENOME; NUCLEOSOME; STEREOSPECIFICITY; BIOLOGICAL MODEL; CHEMISTRY; CHROMATIN; CLASSIFICATION; GENETICS; METABOLISM; NOMENCLATURE;

CHROMATIN; HISTONES; MODELS, BIOLOGICAL; NUCLEOSOMES; SEQUENCE ANALYSIS, DNA; TERMINOLOGY AS TOPIC;

EID: 78650576256     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2010-11-11-140     Document Type: Article

References (56)

1. Wittig B, Wittig S. A phase relationship associates tRNA structural gene sequences with nucleosome cores. Cell 1979, 18:1173-1183. 10.1016/0092-8674(79)90230-7, 519765.
2. Lam FH, Steger DJ, O'Shea EK. Chromatin decouples promoter threshold from dynamic range. Nature 2008, 453:246-250. 10.1038/nature06867, 2435410, 18418379.
3. Miller JA, Widom J. Collaborative competition mechanism for gene activation in vivo. Mol Cell Biol 2003, 23:1623-1632. 10.1128/MCB.23.5.1623-1632.2003, 151720, 12588982.
4. Han M, Grunstein M. Nucleosome loss activates yeast downstream promoters in vivo. Cell 1988, 55:1137-1145. 10.1016/0092-8674(88)90258-9, 2849508.
5. Field Y, Fondufe-Mittendorf Y, Moore IK, Mieczkowski P, Kaplan N, Lubling Y, Lieb JD, Widom J, Segal E. Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization. Nat Genet 2009, 41:438-445. 10.1038/ng.324, 2744203, 19252487.
6. Gencheva M, Boa S, Fraser R, Simmen MW, A Whitelaw CB, Allan J. In vivo and in vitro nucleosome positioning on the ovine beta-lactoglobulin gene are related. J Mol Biol 2006, 361:216-230. 10.1016/j.jmb.2006.06.039, 16859709.
7. Thåström A, Bingham LM, Widom J. Nucleosomal locations of dominant DNA sequence motifs for histone-DNA interactions and nucleosome positioning. J Mol Biol 2004, 338:695-709. 10.1016/j.jmb.2004.03.032, 15099738.
8. Lowary PT, Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 1998, 276:19-42. 10.1006/jmbi.1997.1494, 9514715.
9. Segal E, Fondufe-Mittendorf Y, Chen L, Thåström A, Field Y, Moore IK, Wang JZ, Widom J. A genomic code for nucleosome positioning. Nature 2006, 442:772-778. 10.1038/nature04979, 2623244, 16862119.
10. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, Leproust EM, Hughes TR, Lieb JD, Widom J, Segal E. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 2009, 458:362-366. 10.1038/nature07667, 2658732, 19092803.
11. Valouev A, Ichikawa J, Tonthat T, Stuart J, Ranade S, Peckham H, Zeng K, Malek JA, Costa G, McKernan K, Sidow A, Fire A, Johnson SM. A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res 2008, 18:1051-1063. 10.1101/gr.076463.108, 2493394, 18477713.
12. Zhang Y, Moqtaderi Z, Rattner BP, Euskirchen G, Snyder M, Kadonaga JT, Liu XS, Struhl K. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol 2009, 16:847-852. 10.1038/nsmb.1636, 2823114, 19620965.
13. Lee W, Tillo D, Bray N, Morse RH, Davis RW, Hughes TR, Nislow C. A high-resolution atlas of nucleosome occupancy in yeast. Nat Genet 2007, 39:1235-1244. 10.1038/ng2117, 17873876.
14. Whitehouse I, Rando OJ, Delrow J, Tsukiyama T. Chromatin remodelling at promoters suppresses antisense transcription. Nature 2007, 450:1031-1035. 10.1038/nature06391, 18075583.
15. Yuan G, Liu Y, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 2005, 309:30.
16. Ozsolak F, Song JS, Liu XS, Fisher DE. High-throughput mapping of the chromatin structure of human promoters. Nat Biotechnol 2007, 25:244-248. 10.1038/nbt1279, 17220878.
17. Albert I, Mavrich TN, Tomsho LP, Qi J, Zanton SJ, Schuster SC, Pugh BF. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 2007, 446:572-576. 10.1038/nature05632, 17392789.
18. Field Y, Kaplan N, Fondufe-Mittendorf Y, Moore IK, Sharon E, Lubling Y, Widom J, Segal E. Distinct modes of regulation by chromatin encoded through nucleosome positioning signals. PLoS Comput Biol 2008, 4:e1000216. 10.1371/journal.pcbi.1000216, 2570626, 18989395.
19. Mavrich TN, Ioshikhes IP, Venters BJ, Jiang C, Tomsho LP, Qi J, Schuster SC, Albert I, Pugh BF. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res 2008, 18:1073-1083. 10.1101/gr.078261.108, 2493396, 18550805.
20. Weiner A, Hughes A, Yassour M, Rando OJ, Friedman N. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome Res 2010, 20:90-100. 10.1101/gr.098509.109, 2798834, 19846608.
21. Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, Zanton SJ, Tomsho LP, Qi J, Glaser RL, Schuster SC, Gilmour DS, Albert I, Pugh BF. Nucleosome organization in the Drosophila genome. Nature 2008, 453:358-362. 10.1038/nature06929, 2735122, 18408708.
22. Nishida H, Motoyama T, Yamamoto S, Aburatani H. Genome-wide maps of mono- and di-nucleosomes of Aspergillus fumigatus. Bioinformatics 2009, 25:2295-2297. 10.1093/bioinformatics/btp413, 19570804.
23. Johnson SM, Tan FJ, McCullough HL, Riordan DP, Fire AZ. Flexibility and constraint in the nucleosome core landscape of Caenorhabditis elegans chromatin. Genome Res 2006, 16:1505-1516. 10.1101/gr.5560806, 1665634, 17038564.
24. Schones DE, Cui K, Cuddapah S, Roh T, Barski A, Wang Z, Wei G, Zhao K. Dynamic regulation of nucleosome positioning in the human genome. Cell 2008, 132:887-898. 10.1016/j.cell.2008.02.022, 18329373.
25. Hörz W, Altenburger W. Sequence specific cleavage of DNA by micrococcal nuclease. Nucleic Acids Res 1981, 9:2643-2658. 10.1093/nar/9.12.2643, 326882, 7279658.
26. Harismendy O, Ng PC, Strausberg RL, Wang X, Stockwell TB, Beeson KY, Schork NJ, Murray SS, Topol EJ, Levy S, Frazer KA. Evaluation of next generation sequencing platforms for population targeted sequencing studies. Genome Biol 2009, 10:R32. 10.1186/gb-2009-10-3-r32, 2691003, 19327155.
27. Johnson WE, Li W, Meyer CA, Gottardo R, Carroll JS, Brown M, Liu XS. Model-based analysis of tiling-arrays for ChIP-chip. Proc Natl Acad Sci USA 2006, 103:12457-12462. 10.1073/pnas.0601180103, 1567901, 16895995.
28. Richmond TJ, Finch JT, Rushton B, Rhodes D, Klug A. Structure of the nucleosome core particle at 7 Å resolution. Nature 1984, 311:532-537. 10.1038/311532a0, 6482966.
29. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389:251-260. 10.1038/38444, 9305837.
30. Finch JT, Noll M, Kornberg RD. Electron microscopy of defined lengths of chromatin. Proc Natl Acad Sci USA 1975, 72:3320-3322. 10.1073/pnas.72.9.3320, 432983, 1059115.
31. Segal E, Widom J. Poly(dA:dT) tracts: major determinants of nucleosome organization. Curr Opin Struct Biol 2009, 19:65-71. 10.1016/j.sbi.2009.01.004, 2673466, 19208466.
32. Keene MA, Elgin SC. Micrococcal nuclease as a probe of DNA sequence organization and chromatin structure. Cell 1981, 27:57-64. 10.1016/0092-8674(81)90360-3, 6799212.
33. Flick JT, Eissenberg JC, Elgin SC. Micrococcal nuclease as a DNA structural probe: its recognition sequences, their genomic distribution and correlation with DNA structure determinants. J Mol Biol 1986, 190:619-633. 10.1016/0022-2836(86)90247-0, 3097328.
34. Keene MA, Elgin SC. Patterns of DNA structural polymorphism and their evolutionary implications. Cell 1984, 36:121-129. 10.1016/0092-8674(84)90080-1, 6319004.
35. Visnapuu M, Greene EC. Single-molecule imaging of DNA curtains reveals intrinsic energy landscapes for nucleosome deposition. Nat Struct Mol Biol 2009, 16:1056-1062. 10.1038/nsmb.1655, 2779460, 19734899.
36. Milani P, Chevereau G, Vaillant C, Audit B, Haftek-Terreau Z, Marilley M, Bouvet P, Argoul F, Arneodo A. Nucleosome positioning by genomic excluding-energy barriers. Proc Natl Acad Sci USA 2009, 106:22257-22262. 10.1073/pnas.0909511106, 2799728, 20018700.
37. Cartwright IL, Elgin SC. Chemical footprinting of 5 S RNA chromatin in embryos of Drosophila melanogaster. EMBO J 1984, 3:3101-3108. 557824, 6084593.
38. Cartwright IL, Hertzberg RP, Dervan PB, Elgin SC. Cleavage of chromatin with methidiumpropyl-EDTA. iron(II). Proc Natl Acad Sci USA 1983, 80:3213-3217. 10.1073/pnas.80.11.3213, 394010, 6407008.
39. Cartwright IL, Elgin SC. Analysis of chromatin structure and DNA sequence organization: use of the 1,10-phenanthroline-cuprous complex. Nucleic Acids Res 1982, 10:5835-5852. 10.1093/nar/10.19.5835, 320934, 6292854.
40. Flaus A, Richmond TJ. Base-pair resolution mapping of nucleosomes in vitro. Methods Mol Biol 1999, 119:45-60.
41. Kassabov SR, Bartholomew B. Site-directed histone-DNA contact mapping for analysis of nucleosome dynamics. Methods Enzymol 2004, 375:193-192. full_text, 14870668.
42. Widlak P, Garrard WT. Unique features of the apoptotic endonuclease DFF40/CAD relative to micrococcal nuclease as a structural probe for chromatin. Biochem Cell Biol 2006, 84:405-410. 10.1139/O06-063, 16936813.
43. Yuan G, Liu JS. Genomic sequence is highly predictive of local nucleosome depletion. PLoS Comput Biol 2008, 4:e13. 10.1371/journal.pcbi.0040013, 2211532, 18225943.
44. Peckham HE, Thurman RE, Fu Y, Stamatoyannopoulos JA, Noble WS, Struhl K, Weng Z. Nucleosome positioning signals in genomic DNA. Genome Res 2007, 17:1170-1177. 10.1101/gr.6101007, 1933512, 17620451.
45. Hanley JA, McNeil BJ. The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 1982, 143:29-36.
46. Gupta S, Dennis J, Thurman RE, Kingston R, Stamatoyannopoulos JA, Noble WS. Predicting human nucleosome occupancy from primary sequence. PLoS Comput Biol 2008, 4:e1000134. 10.1371/journal.pcbi.1000134, 2515632, 18725940.
47. Ioshikhes IP, Albert I, Zanton SJ, Pugh BF. Nucleosome positions predicted through comparative genomics. Nat Genet 2006, 38:1210-1215. 10.1038/ng1878, 16964265.
48. Tillo D, Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Field Y, Lieb JD, Widom J, Segal E, Hughes TR. High nucleosome occupancy is encoded at human regulatory sequences. PloS ONE 2010, 5:e9129. 10.1371/journal.pone.0009129, 2817738, 20161746.
49. Kaplan N, Moore I, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, Hughes TR, Lieb JD, Widom J, Segal E. Nucleosome sequence preferences influence in vivo nucleosome organization. Nat Struct Mol Biol 2010, 17:918-920. 10.1038/nsmb0810-918, 2969171, 20683473.
50. Satchwell SC, Drew HR, Travers AA. Sequence periodicities in chicken nucleosome core DNA. J Mol Biol 1986, 191:659-675. 10.1016/0022-2836(86)90452-3, 3806678.
51. Levitsky VG. RECON: a program for prediction of nucleosome formation potential. Nucleic Acids Res 2004, 32:W346-W349. 10.1093/nar/gkh482, 441620, 15215408.
52. Levitsky VG, Podkolodnaya OA, Kolchanov NA. DNA: calculation and promoters analysis. Bioinformatics 2001, 17:998-1010. 10.1093/bioinformatics/17.11.998, 11724728.
53. Tillo D, Hughes TR. G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics 2009, 10:442. 10.1186/1471-2105-10-442, 2808325, 20028554.
54. Kornberg RD, Stryer L. Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res 1988, 16:6677-6690. 10.1093/nar/16.14.6677, 338322, 3399412.
55. Kornberg R. The location of nucleosomes in chromatin: specific or statistical?. Nature 1981, 292:579-580. 10.1038/292579a0, 7254354.
56. Stein A, Takasuka TE, Collings CK. Are nucleosome positions in vivo primarily determined by histone-DNA sequence preferences?. Nucleic Acids Res 2010, 38:709-719. 10.1093/nar/gkp1043, 2817465, 19934265.