Regulation of the Nucleosome Repeat Length In Vivo by the DNA Sequence, Protein Concentrations and Long-Range Interactions

PLoS Computational Biology

Volumn 10, Issue 7, 2014, Pages

  Beshnova, Daria A ^a   Cherstvy, Andrey G ^b   Vainshtein, Yevhen ^a   Teif, Vladimir B ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF POTSDAM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOMES; DNA; MAMMALS; PROTEINS; YEAST;

BIOLOGICAL FUNCTIONS; CHROMATIN PROTEINS; IN-VIVO; LENGTH DEPENDENCE; LONG RANGE INTERACTIONS; LONGER-RANGE INTERACTION; NUCLEOSOMES; PERIOD OF OSCILLATION; PROPERTY; PROTEIN CONCENTRATIONS;

DNA SEQUENCES;

RNA POLYMERASE; CHROMATIN; DNA; HISTONE; NUCLEOSOME;

ANIMAL CELL; ANURA; ARTICLE; BINDING AFFINITY; CELL INTERACTION; CHROMATIN; CONSTITUTIVE HETEROCHROMATIN; CONTROLLED STUDY; DNA HISTONE INTERACTION; DNA SEQUENCE; EMBRYO; ENTROPY; GENETIC ASSOCIATION; IN VIVO STUDY; MOUSE; NONHUMAN; NUCLEOSOME REPEAT LENGTH; PROMOTER REGION; PROTEIN CONTENT; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; RIBOSWITCH; VARIABLE NUMBER OF TANDEM REPEAT; YEAST; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; CHEMISTRY; METABOLISM; NUCLEOSOME;

ANIMALS; ANURA; CHROMATIN; COMPUTATIONAL BIOLOGY; DNA; HISTONES; MICE; MODELS, BIOLOGICAL; NUCLEOSOMES; YEASTS;

EID: 84905484605     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003698     Document Type: Article

References (82)

1. van Holde KE (1989) Chromatin. New York: Springer-Verlag. 497 p.
2. Olins AL, Olins DE, (1974) Spheroid chromatin units (v bodies). Science 183: 330-332.
3. Kornberg RD, (1974) Chromatin structure: a repeating unit of histones and DNA. Science 184: 868-871.
4. Lohr D, Tatchell K, Van Holde KE, (1977) On the occurrence of nucleosome phasing in chromatin. Cell 12: 829-836.
5. Gottesfeld JM, Melton DA, (1978) The length of nucleosome-associated DNA is the same in both transcribed and nontranscribed regions of chromatin. Nature 273: 317-319.
6. Trifonov EN, Sussman JL, (1980) The pitch of chromatin DNA is reflected in its nucleotide sequence. Proc Natl Acad Sci U S A 77: 3816-3820.
7. Chereji RV, Morozov AV, (2014) Ubiquitous nucleosome unwrapping in the yeast genome. Proc Natl Acad Sci U S A Early Edition DOI:10.1073/pnas.1321001111.
8. Vaillant C, Palmeira L, Chevereau G, Audit B, d'Aubenton-Carafa Y, et al. (2010) A novel strategy of transcription regulation by intragenic nucleosome ordering. Genome Res 20: 59-67.
9. Schwab DJ, Bruinsma RF, Rudnick J, Widom J, (2008) Nucleosome switches. Phys Rev Lett 100: 228105.
10. Mobius W, Osberg B, Tsankov AM, Rando OJ, Gerland U, (2013) Toward a unified physical model of nucleosome patterns flanking transcription start sites. Proc Natl Acad Sci U S A 110: 5719-5724.
11. Morozov AV, Fortney K, Gaykalova DA, Studitsky VM, Widom J, et al. (2009) Using DNA mechanics to predict in vitro nucleosome positions and formation energies. Nucleic Acids Res 37: 4707-4722.
12. Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, et al. (2006) A genomic code for nucleosome positioning. Nature 442: 772-778.
13. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, et al. (2009) The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 458: 362-366.
14. Teif VB, Rippe K, (2011) Nucleosome mediated crosstalk between transcription factors at eukaryotic enhancers. Phys Biol 8: 04400.
15. Teif VB, Rippe K, (2010) Statistical-mechanical lattice models for protein-DNA binding in chromatin. J Phys: Condens Matter 22: 414105.
16. Teif VB, Ettig R, Rippe K, (2010) A lattice model for transcription factor access to nucleosomal DNA. Biophys J 99: 2597-2607.
17. Wang JP, Fondufe-Mittendorf Y, Xi L, Tsai GF, Segal E, et al. (2008) Preferentially quantized linker DNA lengths in Saccharomyces cerevisiae. PLoS Comput Biol 4: e1000175.
18. Lubliner S, Segal E, (2009) Modeling interactions between adjacent nucleosomes improves genome-wide predictions of nucleosome occupancy. Bioinformatics 25: i348-355.
19. Florescu AM, Schiessel H, Blossey R, (2012) Kinetic control of nucleosome displacement by ISWI/ACF chromatin remodelers. Phys Rev Lett 109: 118103.
20. Teif VB, Rippe K, (2009) Predicting nucleosome positions on the DNA: combining intrinsic sequence preferences and remodeler activities. Nucleic Acids Res 37: 5641-5655.
21. Afek A, Sela I, Musa-Lempel N, Lukatsky DB, (2011) Nonspecific transcription-factor-DNA binding influences nucleosome occupancy in yeast. Biophys J 101: 2465-2475.
22. Mirny LA, (2010) Nucleosome-mediated cooperativity between transcription factors. Proc Natl Acad Sci U S A 107: 22534-22539.
23. Gabdank I, Barash D, Trifonov EN, (2010) FineStr: a web server for single-base-resolution nucleosome positioning. Bioinformatics 26: 845-846.
24. Chevereau G, Palmeira L, Thermes C, Arneodo A, Vaillant C, (2009) Thermodynamics of intragenic nucleosome ordering. Phys Rev Lett 103: 188103.
25. Reynolds SM, Bilmes JA, Noble WS, (2010) Learning a weighted sequence model of the nucleosome core and linker yields more accurate predictions in Saccharomyces cerevisiae and Homo sapiens. PLoS Comput Biol 6: e1000834.
26. Weintraub H, (1978) The nucleosome repeat length increases during erythropoiesis in the chick. Nucleic Acids Res 5: 1179-1188.
27. Valouev A, Johnson SM, Boyd SD, Smith CL, Fire AZ, et al. (2011) Determinants of nucleosome organization in primary human cells. Nature 474: 516-520.
28. Teif VB, Vainstein E, Marth K, Mallm J-P, Caudron-Herger M, et al. (2012) Genome-wide nucleosome positioning during embryonic stem cell development. Nat Struct Mol Biol 19: 1185-1192.
29. Zhang Z, Wippo CJ, Wal M, Ward E, Korber P, et al. (2011) A packing mechanism for nucleosome organization reconstituted across a eukaryotic genome. Science 332: 977-980.
30. Celona B, Weiner A, Di Felice F, Mancuso FM, Cesarini E, et al. (2011) Substantial histone reduction modulates genomewide nucleosomal occupancy and global transcriptional output. PLoS Biol 9: e1001086.
31. Hennig BP, Bendrin K, Zhou Y, Fischer T, (2012) Chd1 chromatin remodelers maintain nucleosome organization and repress cryptic transcription. EMBO Rep 13: 997-1003.
32. Mobius W, Gerland U, (2010) Quantitative test of the barrier nucleosome model for statistical positioning of nucleosomes up- and downstream of transcription start sites. PLoS Comput Biol 6: e1000891.
33. Oberg C, Izzo A, Schneider R, Wrange O, Belikov S, (2012) Linker histone subtypes differ in their effect on nucleosomal spacing in vivo. J Mol Biol 419: 183-197.
34. Woodcock CL, Skoultchi AI, Fan Y, (2006) Role of linker histone in chromatin structure and function: H1 stoichiometry and nucleosome repeat length. Chromosome Res 14: 17-25.
35. Cherstvy AG, Teif VB, (2014) Electrostatic effect of H1 histone binding on the nucleosome repeat length. Accepted.
36. Blank TA, Becker PB, (1995) Electrostatic mechanism of nucleosome spacing. J Mol Biol 252: 305-313.
37. Nalabothula N, McVicker G, Maiorano J, Martin R, Pritchard JK, et al. (2014) The chromatin architectural proteins HMGD1 and H1 bind reciprocally and have opposite effects on chromatin structure and gene regulation. BMC Genomics 15: 92.
38. Skene PJ, Illingworth RS, Webb S, Kerr AR, James KD, et al. (2010) Neuronal MeCP2 is expressed at near histone-octamer levels and globally alters the chromatin state. Mol Cell 37: 457-468.
39. Routh A, Sandin S, Rhodes D, (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc Natl Acad Sci U S A 105: 8872-8877.
40. Teif VB, Rippe K, (2012) Calculating transcription factor binding maps for chromatin. Brief Bioinform 13: 187-201.
41. Ising E, (1925) Beitrag zur Theorie des Ferromagnetismus. Z Phys 31: 253-258.
42. Epstein IR, (1978) Cooperative and noncooperative binding of large ligands to a finite one-dimensional lattice. A model for ligand-oligonucleotide interactions. Biophys Chem 8: 327-339.
43. Kornberg RD, Stryer L, (1988) Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res 16: 6677-6690.
44. McGhee JD, von Hippel PH, (1974) Theoretical aspects of DNA-protein interactions: co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice. J Mol Biol 86: 469-489.
45. Nechipurenko YD, (1988) Anticooperative interactions between the nearest neighbor chromatosomes. Biofizika 33: 580-583.
46. Chereji RV, Tolkunov D, Locke G, Morozov AV, (2011) Statistical mechanics of nucleosome ordering by chromatin-structure-induced two-body interactions. Phys Rev E Stat Nonlin Soft Matter Phys 83: 050903.
47. Chou T, (2007) Peeling and sliding in nucleosome repositioning. Phys Rev Lett 99: 058105.
48. Kulic IM, Schiessel H, (2004) DNA spools under tension. Phys Rev Lett 92: 228101.
49. Schiessel H, (2003) The physics of chromatin. Journal of Physics: Condensed Matter 15: R699.
50. Cherstvy AG, Winkler RG, (2005) Simple model for overcharging of a sphere by a wrapped oppositely charged asymmetrically neutralized polyelectrolyte: Possible effects of helical charge distribution. J Phys Chem B 109: 2962-2969.
51. Meersseman G, Pennings S, Bradbury EM, (1992) Mobile nucleosomes-a general behavior. EMBO J 11: 2951-2959.
52. Längst G, Teif VB, Rippe K (2011) Chromatin Remodeling and Nucleosome Positioning. In: Rippe K, editor. Genome Organization and Function in the Cell Nucleus. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA. pp. 111-138.
53. Teif VB, Erdel F, Beshnova DA, Vainshtein Y, Mallm JP, et al. (2013) Taking into account nucleosomes for predicting gene expression. Methods 62: 26-38.
54. Teif VB, Haroutiunian SG, Vorob'ev VI, Lando DY, (2002) Short-range interactions and size of ligands bound to DNA strongly influence adsorptive phase transition caused by long-range interactions. J Biomol Struct Dynam 19: 1093-1100.
55. Lando DY, Teif VB, (2000) Long-range interactions between ligands bound to a DNA molecule give rise to adsorption with the character of phase transition of the first kind. J Biomol Struct Dyn 17: 903-911.
56. Zhou BR, Feng H, Kato H, Dai L, Yang Y, et al. (2013) Structural insights into the histone H1-nucleosome complex. Proc Natl Acad Sci U S A 110: 19390-19395.
57. Teif VB, (2007) General transfer matrix formalism to calculate DNA-protein-drug binding in gene regulation: application to OR operator of phage λ. Nucleic Acids Res 35: e80.
58. Korber P, (2012) Active nucleosome positioning beyond intrinsic biophysics is revealed by in vitro reconstitution. Biochem Soc Trans 40: 377-382.
59. Teif VB, Bohinc K, (2011) Condensed DNA: condensing the concepts. Progr Biophys Mol Biol 105: 199-213.
60. Riposo J, Mozziconacci J, (2012) Nucleosome positioning and nucleosome stacking: two faces of the same coin. Mol Biosyst 8: 1172-1178.
61. Rube TH, Song JS, (2014) Quantifying the role of steric constraints in nucleosome positioning. Nucleic Acids Res 42: 2147-2158.
62. Harshman SW, Young NL, Parthun MR, Freitas MA, (2013) H1 histones: current perspectives and challenges. Nucleic Acids Res 41: 9593-9609.
63. Puig S, Matallana E, Perez-Ortin JE, (1999) Stochastic nucleosome positioning in a yeast chromatin region is not dependent on histone H1. Curr Microbiol 39: 168-172.
64. Patterton HG, Landel CC, Landsman D, Peterson CL, Simpson RT, (1998) The biochemical and phenotypic characterization of Hho1p, the putative linker histone H1 of Saccharomyces cerevisiae. J Biol Chem 273: 7268-7276.
65. Lantermann AB, Straub T, Stralfors A, Yuan GC, Ekwall K, et al. (2010) Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae. Nat Struct Mol Biol 17: 251-257.
66. Clapier CR, Cairns BR, (2009) The biology of chromatin remodeling complexes. Annu Rev Biochem 78: 273-304.
67. Cherstvy AG, Teif VB, (2013) Structure-driven homology pairing of chromatin fibers: the role of electrostatics and protein-induced bridging. Journal of Biological Physics 39: 363-385.
68. Cherstvy AG, Everaers R, (2006) Layering, bundling, and azimuthal orientations in dense phases of nucleosome core particles. Journal of Physics: Condensed Matter 18: 11429.
69. Kepper N, Foethke D, Stehr R, Wedemann G, Rippe K, (2008) Nucleosome geometry and internucleosomal interactions control the chromatin fiber conformation. Biophys J 95: 3692-3705.
70. Pachov GV, Gabdoulline RR, Wade RC, (2011) On the structure and dynamics of the complex of the nucleosome and the linker histone. Nucleic Acids Res 39: 5255-5263.
71. Korolev N, Vorontsova OV, Nordenskiold L, (2007) Physicochemical analysis of electrostatic foundation for DNA-protein interactions in chromatin transformations. Prog Biophys Mol Biol 95: 23-49.
72. Parmar JJ, Marko JF, Padinhateeri R, (2013) Nucleosome positioning and kinetics near transcription-start-site barriers are controlled by interplay between active remodeling and DNA sequence. Nucleic Acids Res 42: 128-136.
73. Zhang Y, Vastenhouw NL, Feng J, Fu K, Wang C, et al. (2014) Canonical nucleosome organization at promoters forms during genome activation. Genome Res 24: 260-266.
74. Shen Y, Yue F, McCleary DF, Ye Z, Edsall L, et al. (2012) A map of the cis-regulatory sequences in the mouse genome. Nature 488: 116-120.
75. Tolstorukov MY, Choudhary V, Olson WK, Zhurkin VB, Park PJ, (2008) nuScore: a web-interface for nucleosome positioning predictions. Bioinformatics 24: 1456-1458.
76. Van Bortle K, Corces VG, (2013) The role of chromatin insulators in nuclear architecture and genome function. Curr Opin Genet Dev 23: 212-218.
77. Teif VB, Beshnova DA, Vainshtein Y, Marth C, Mallm JP, et al. (2014) Nucleosome repositioning links DNA (de)methylation and differential CTCF binding during stem cell development. Genome Research Published online May 8, 2014.
78. Salih B, Tripathi V, Trifonov EN, (2013) Visible periodicity of strong nucleosome DNA sequences. J Biomol Struct Dyn DOI:10.1080/07391102.2013.855143.
79. Salih B, Teif VB, Tripathi V, Trifonov EN, (2014) Strong nucleosomes of mouse genome in recovered centromeric sequences. J. Biomol. Struct. & Dynam. In press.
80. Zhang XY, Horz W, (1984) Nucleosomes are positioned on mouse satellite DNA in multiple highly specific frames that are correlated with a diverged subrepeat of nine base-pairs. J Mol Biol 176: 105-129.
81. Levitsky VG, Babenko VN, Vershinin AV, (2014) The roles of the monomer length and nucleotide context of plant tandem repeats in nucleosome positioning. J Biomol Struct Dyn 32: 115-126.
82. Langmead B, Trapnell C, Pop M, Salzberg SL, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.