Physical properties of naked DNA influence nucleosome positioning and correlate with transcription start and termination sites in yeast

BMC Genomics

Volumn 12, Issue , 2011, Pages

  Deniz, Özgen ^a   Flores, Oscar ^a   Battistini, Federica ^a   Pérez, Alberto ^b   Soler López, Montserrat ^a   Orozco, Modesto ^a,c  

^a BARCELONA SUPERCOMPUTING CENTER   (Spain)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Chromatin structure; Dna physical properties; Gene regulation; Mnase digestion; Molecular dynamics; Nucleosome positioning

Indexed keywords

FUNGAL DNA; MICROCOCCAL NUCLEASE; NAKED DNA; NUCLEOSOMAL DNA; UNCLASSIFIED DRUG; DEOXYRIBONUCLEASE; DNA;

ARTICLE; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA CONFORMATION; DNA STRUCTURE; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENETIC ASSOCIATION; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOSOME; TRANSCRIPTION INITIATION; TRANSCRIPTION INITIATION SITE; TRANSCRIPTION TERMINATION; TRANSCRIPTION TERMINATION SITE; YEAST; DNA SEQUENCE; GENETICS; METABOLISM; PHYSIOLOGY; REGULATOR GENE; SACCHAROMYCES CEREVISIAE;

EUKARYOTA;

DEOXYRIBONUCLEASES; DNA; MOLECULAR DYNAMICS SIMULATION; NUCLEOSOMES; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS, DNA; TERMINATOR REGIONS, GENETIC; TRANSCRIPTION INITIATION SITE;

EID: 80053471251     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-12-489     Document Type: Article

References (70)

1. Gilbert N, Boyle S, Fiegler H, Woodfine K, Carter NP, Bickmore WA. Chromatin architecture of the human genome: gene-rich domains are enriched in open chromatin fibers. Cell 2004, 118:555-566. 10.1016/j.cell.2004.08.011, 15339661.
2. Holde K, Zlatanova J. Unusual DNA structures, chromatin and transcription. BioEssays : news and reviews in molecular, cellular and developmental biology 1994, 16:59-68.
3. Jiang C, Pugh BF. Nucleosome positioning and gene regulation: advances through genomics. Nature reviews Genetics 2009, 10:161-72.
4. Lodhi N, Ranjan A, Singh M, Srivastava R, Singh SP, Chaturvedi CP, Ansari SA, Sawant SV, Tuli R. Interactions between upstream and core promoter sequences determine gene expression and nucleosome positioning in tobacco PR-1a promoter. Biochimica et biophysica acta 2008, 1779:634-44.
5. Choi JK, Kim Y-J. Intrinsic variability of gene expression encoded in nucleosome positioning sequences. Nature genetics 2009, 41:498-503. 10.1038/ng.319, 19252489.
6. Schwartz S, Ast G. Chromatin density and splicing destiny: on the cross-talk between chromatin structure and splicing. The EMBO journal 2010, 29:1629-1636. 10.1038/emboj.2010.71, 2876972, 20407423.
7. Boyle AP, Davis S, Shulha HP, Meltzer P, Margulies EH, Weng Z, Furey TS, Crawford GE. High-resolution mapping and characterization of open chromatin across the genome. Cell 2008, 132:311-22. 10.1016/j.cell.2007.12.014, 2669738, 18243105.
8. Ling G, Sugathan A, Mazor T, Fraenkel E, Waxman DJ. Unbiased, Genome-wide in vivo Mapping of Transcriptional Regulatory Elements Reveals Sex Differences in Chromatin Structure Associated with Sex-specific Liver Gene Expression. Molecular and cellular biology 2010, MCB.00601-10-.
9. Micheli E, Martufi M, Cacchione S, Santis P, Savino M. Self-organization of G-quadruplex structures in the hTERT core promoter stabilized by polyaminic side chain perylene derivatives. Biophysical chemistry 2010,
10. Ioshikhes IP, Albert I, Zanton SJ, Pugh BF. Nucleosome positions predicted through comparative genomics. Nature genetics 2006, 38:1210-5. 10.1038/ng1878, 16964265.
11. 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, 458:362-6. 10.1038/nature07667, 2658732, 19092803.
12. Chung H-R, Vingron M. Sequence-dependent nucleosome positioning. Journal of molecular biology 2009, 386:1411-22. 10.1016/j.jmb.2008.11.049, 19070622.
13. Cui F, Zhurkin VB. Structure-based analysis of DNA sequence patterns guiding nucleosome positioning in vitro. Journal of biomolecular structure & dynamics 2010, 27:821-41.
14. Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389:251-60. 10.1038/38444, 9305837.
15. Richmond TJ, Davey CA. The structure of DNA in the nucleosome core. Nature 2003, 423:145-50. 10.1038/nature01595, 12736678.
16. Hall MA, Shundrovsky A, Bai L, Fulbright RM, Lis JT, Wang MD. High-resolution dynamic mapping of histone-DNA interactions in a nucleosome. Nature structural & molecular biology 2009, 16:124-9. 10.1038/nsmb.1526, 21983966.
17. Makde RD, England JR, Yennawar HP, Tan S. Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 2010, 467:562-566. 10.1038/nature09321, 3168546, 20739938.
18. 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. Nature structural & molecular biology 2009, 16:847-52. 10.1038/nsmb.1636, 21983966.
19. Lowary PT, Widom J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. Journal of molecular biology 1998, 276:19-42. 10.1006/jmbi.1997.1494, 9514715.
20. Tolstorukov MY, Colasanti AV, McCandlish DM, Olson WK, Zhurkin VB. A novel roll-and-slide mechanism of DNA folding in chromatin: implications for nucleosome positioning. Journal of molecular biology 2007, 371:725-38. 10.1016/j.jmb.2007.05.048, 2000845, 17585938.
21. De Santis P, Morosetti S, Scipioni A. Prediction of nucleosome positioning in genomes: limits and perspectives of physical and bioinformatic approaches. Journal of biomolecular structure & dynamics 2010, 27:747-64.
22. Trifonov EN, Sussman JL. The pitch of chromatin DNA is reflected in its nucleotide sequence. Proceedings of the National Academy of Sciences of the United States of America 1980, 77:3816-20. 10.1073/pnas.77.7.3816, 349717, 6933438.
23. Xu F, Olson WK. DNA architecture, deformability, and nucleosome positioning. Journal of biomolecular structure & dynamics 2010, 27:725-39.
24. Rohs R, West SM, Sosinsky A, Liu P, Mann RS, Honig B. The role of DNA shape in protein-DNA recognition. Nature 2009, 461:1248-53. 10.1038/nature08473, 2793086, 19865164.
25. Travers A, Hiriart E, Churcher M, Caserta M, Di Mauro E. The DNA sequence-dependence of nucleosome positioning in vivo and in vitro. Journal of biomolecular structure & dynamics 2010, 27:713-24.
26. Arya G, Maitra A, Grigoryev SA. A structural perspective on the where, how, why, and what of nucleosome positioning. Journal of biomolecular structure & dynamics 2010, 27:803-20.
27. Trifonov EN. Nucleosome positioning by sequence, state of the art and apparent finale. Journal of biomolecular structure & dynamics 2010, 27:741-6.
28. Abeel T, Saeys Y, Bonnet E, Rouzé P, Van de Peer Y. Generic eukaryotic core promoter prediction using structural features of DNA. Genome research 2008, 18:310-23. 10.1101/gr.6991408, 2203629, 18096745.
29. Goñi JR, Fenollosa C, Pérez A, Torrents D, Orozco M. DNAlive: a tool for the physical analysis of DNA at the genomic scale. Bioinformatics (Oxford, England) 2008, 24:1731-2.
30. Miele V, Vaillant C, D Aubenton-Carafa Y, Thermes C, Grange T. DNA physical properties determine nucleosome occupancy from yeast to fly. Nucleic acids research 2008, 36:3746-56. 10.1093/nar/gkn262, 2441789, 18487627.
31. Goñi JR, Pérez A, Torrents D, Orozco M. Determining promoter location based on DNA structure first-principles calculations. Genome biology 2007, 8:R263. 10.1186/gb-2007-8-12-r263, 2246265, 18072969.
32. Lankas F, Sponer J, Langowski J, Cheatham TE. DNA basepair step deformability inferred from molecular dynamics simulations. Biophysical journal 2003, 85:2872-83. 10.1016/S0006-3495(03)74710-9, 1303568, 14581192.
33. Morozov AV, Fortney K, Gaykalova DA, Studitsky VM, Widom J, Siggia ED. Using DNA mechanics to predict in vitro nucleosome positions and formation energies. Nucleic acids research 2009, 37:4707-22. 10.1093/nar/gkp475, 2724288, 19509309.
34. Olson WK. DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. Proceedings of the National Academy of Sciences 1998, 95:11163-11168.
35. Araúzo-Bravo MJ, Fujii S, Kono H, Ahmad S, Sarai A. Sequence-dependent conformational energy of DNA derived from molecular dynamics simulations: toward understanding the indirect readout mechanism in protein-DNA recognition. Journal of the American Chemical Society 2005, 127:16074-89. 10.1021/ja053241l, 16287294.
36. Yamasaki S, Terada T, Shimizu K, Kono H, Sarai A. A generalized conformational energy function of DNA derived from molecular dynamics simulations. Nucleic acids research 2009, 37:e135. 10.1093/nar/gkp718, 2777435, 19729512.
37. Fujii S, Kono H, Takenaka S, Go N, Sarai A. Sequence-dependent DNA deformability studied using molecular dynamics simulations. Nucleic acids research 2007, 35:6063-74. 10.1093/nar/gkm627, 2094071, 17766249.
38. 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. Journal of molecular biology 1986, 190:619-33. 10.1016/0022-2836(86)90247-0, 3097328.
39. Hörz W, Altenburger W. Sequence specific cleavage of DNA by micrococcal nuclease. Nucleic acids research 1981, 9:2643-58. 10.1093/nar/9.12.2643, 326882, 7279658.
40. Alexander M, Heppel LA, Hurwitz J. The purification and properties of micrococcal nuclease. The Journal of biological chemistry 1961, 236:3014-9.
41. Pérez A, Lankas F, Luque FJ, Orozco M. Towards a molecular dynamics consensus view of B-DNA flexibility. Nucleic acids research 2008, 36:2379-94. 10.1093/nar/gkn082, 2367714, 18299282.
42. Lavery R, Zakrzewska K, Beveridge D, Bishop TC, Case DA, Cheatham T, Dixit S, Jayaram B, Lankas F, Laughton C, Maddocks JH, Michon A, Osman R, Orozco M, Perez A, Singh T, Spackova N, Sponer J. A systematic molecular dynamics study of nearest-neighbor effects on base pair and base pair step conformations and fluctuations in B-DNA. Nucleic acids research 2010, 38:299-313. 10.1093/nar/gkp834, 2800215, 19850719.
43. Ozsolak F, Song JS, Liu XS, Fisher DE. High-throughput mapping of the chromatin structure of human promoters. Nature biotechnology 2007, 25:244-8. 10.1038/nbt1279, 17220878.
44. 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 computational biology 2008, 4:e1000216. 10.1371/journal.pcbi.1000216, 2570626, 18989395.
45. Bai L, Morozov AV. Gene regulation by nucleosome positioning. Trends in genetics TIG 2010, 26:476-83. 10.1016/j.tig.2010.08.003, 21982512.
46. 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 research 2008, 18:1073-83. 10.1101/gr.078261.108, 2493396, 18550805.
47. Segal E, Fondufe-Mittendorf Y, Chen L, Thåström A, Field Y, Moore IK, Wang J-PZ, Widom J. A genomic code for nucleosome positioning. Nature 2006, 442:772-8. 10.1038/nature04979, 2623244, 16862119.
48. Lee W, Tillo D, Bray N, Morse RH, Davis RW, Hughes TR, Nislow C. A high-resolution atlas of nucleosome occupancy in yeast. Nature genetics 2007, 39:1235-44. 10.1038/ng2117, 17873876.
49. 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, 446:572-6. 10.1038/nature05632, 17392789.
50. Yuan G-C, Liu Y-J, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ. Genome-scale identification of nucleosome positions in S. cerevisiae. Science (New York, N.Y.) 2005, 309:626-30.
51. Yuan GC, Liu YJ, Dion MF, Slack MD, Wu LF, Altschuler SJ, Rando OJ. Genome-scale identification of nucleosome positions in S. cerevisiae. Science (New York, N.Y.) 2005, 309:626-3010. 1126/science.1112178.
52. Lee W, Tillo D, Bray N, Morse RH, Davis RW, Hughes TR, Nislow C. A high-resolution atlas of nucleosome occupancy in yeast. Nature genetics 2007, 39. 1235-4410.1038/ng2117.
53. 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 computational biology 2008, 4:e100021610. 1371/journal.pcbi.1000216.
54. 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, 446:572-610.1038/nature05632. 10.1038/nature05632, 17392789.
55. 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, 458:362-610. 1038/nature07667, 10.1038/nature07667, 2658732, 19092803.
56. Chung H-R, Dunkel I, Heise F, Linke C, Krobitsch S, Ehrenhofer-Murray AE, Sperling SR, Vingron M. The effect of micrococcal nuclease digestion on nucleosome positioning data. PloS one 2010, 5:e1575410. 1371/journal.pone.0015754.
57. Rando OJ, Ahmad K. Rules and regulation in the primary structure of chromatin. Current opinion in cell biology 2007, 19:250-6. 10.1016/j.ceb.2007.04.006, 17466507.
58. Rohs R, Jin X, West SM, Joshi R, Honig B, Mann RS. Origins of specificity in protein-DNA recognition. Annual review of biochemistry 2010, 79:233-69. 10.1146/annurev-biochem-060408-091030, 20334529.
59. Peckham HE, Thurman RE, Fu Y, Stamatoyannopoulos JA, Noble WS, Struhl K, Weng Z. Nucleosome positioning signals in genomic DNA. Genome research 2007, 17:1170-7. 10.1101/gr.6101007, 1933512, 17620451.
60. Weiner A, Hughes A, Yassour M, Rando OJ, Friedman N. High-resolution nucleosome mapping reveals transcription-dependent promoter packaging. Genome research 2010, 20:90-100. 10.1101/gr.098509.109, 2798834, 19846608.
61. Locke G, Tolkunov D, Moqtaderi Z, Struhl K, Morozov AV. High-throughput sequencing reveals a simple model of nucleosome energetics. Proceedings of the National Academy of Sciences 2010, 1003838107.
62. Segal E, Widom J. From DNA sequence to transcriptional behaviour: a quantitative approach. Nature reviews Genetics 2009, 10:443-56. 2719885, 19506578.
63. Fan X, Moqtaderi Z, Jin Y, Zhang Y, Liu XS, Struhl K. Nucleosome depletion at yeast terminators is not intrinsic and can occur by a transcriptional mechanism linked to 3'-end formation. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:17945-50. 10.1073/pnas.1012674107, 2964211, 20921369.
64. Zhang Z, Wippo CJ, Wal M, Ward E, Korber P, Pugh BF. A Packing Mechanism for Nucleosome Organization Reconstituted Across a Eukaryotic Genome. Science 2011, 332:977-98010. 1126/science.1200508, 10.1126/science.1200508, 21596991.
65. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature genetics 2000, 25:25-9. 10.1038/75556, 3037419, 10802651.
66. 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, 453:358-62. 10.1038/nature06929, 2735122, 18408708.
67. 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, 453:358-6210. 1038/nature06929, 10.1038/nature06929, 2735122, 18408708.
68. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome biology 2009, 10:R25. 10.1186/gb-2009-10-3-r25, 2690996, 19261174.
69. Flores O, Orozco M. nucleR: a package for non-parametric nucleosome positioning. Bioinformatics (Oxford, England) 2011, 27:2149-215010. 1093/bioinformatics/btr345.
70. Pérez A, Marchán I, Svozil D, Sponer J, Cheatham TE, Laughton CA, Orozco M. Refinement of the AMBER force field for nucleic acids: improving the description of alpha/gamma conformers. Biophysical journal 2007, 92:3817-29. 10.1529/biophysj.106.097782, 1868997, 17351000.