Nonconsensus Protein Binding to Repetitive DNA Sequence Elements Significantly Affects Eukaryotic Genomes

PLoS Computational Biology

Volumn 11, Issue 8, 2015, Pages

  Afek, Ariel ^a   Cohen, Hila ^a   Barber Zucker, Shiran ^a   Gordân, Raluca ^b   Lukatsky, David B ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BINDING SITES; BIOCHIPS; DNA; FREE ENERGY; GENE ENCODING; PROTEINS; STATISTICAL MECHANICS;

BINDING EVENTS; BINDING-SITES; CONSENSUS MOTIF; EUKARYOTIC GENOME; IN-VITRO; NUCLEOSOMES; PROTEIN-BINDING; PROTEIN-DNA BINDING; TRANSCRIPTION FACTOR BINDING; TRANSCRIPTION FACTOR BINDING SITES;

DNA SEQUENCES;

TRANSCRIPTION FACTOR; DNA; DNA BINDING PROTEIN; PROTEIN BINDING;

ARTICLE; BINDING ASSAY; CAENORHABDITIS ELEGANS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA DETERMINATION; DNA SEQUENCE; DROSOPHILA MELANOGASTER; GENOME ANALYSIS; HIGH THROUGHPUT SEQUENCING; IN VITRO STUDY; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOSOME; PREDICTION; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; ANIMAL; BINDING SITE; BIOLOGICAL MODEL; BIOLOGY; CHEMISTRY; GENETICS; GENOME; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE REPEAT; NUCLEOTIDE SEQUENCE; THERMODYNAMICS;

ANIMALS; BASE SEQUENCE; BINDING SITES; CAENORHABDITIS ELEGANS; COMPUTATIONAL BIOLOGY; DNA; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; GENOME; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; REPETITIVE SEQUENCES, NUCLEIC ACID; THERMODYNAMICS; TRANSCRIPTION FACTORS;

EID: 84940778387     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1004429     Document Type: Article

References (69)

1. Iyer V, Struhl K, Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 1995;14(11):2570–9. Epub 1995/06/01. 7781610
2. Gerstein MB, Lu ZJ, Van Nostrand EL, Cheng C, Arshinoff BI, Liu T, et al. Integrative analysis of the Caenorhabditis elegans genome by the modENCODE project. Science. 2010;330(6012):1775–87. Epub 2010/12/24. doi: 10.1126/science.1196914 21177976
3. Niu W, Lu ZJ, Zhong M, Sarov M, Murray JI, Brdlik CM, et al. Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans. Genome Research. 2011;21(2):245–54. doi: 10.1101/gr.114587.110 21177963
4. Ercan S, Lubling Y, Segal E, Lieb JD, High nucleosome occupancy is encoded at X-linked gene promoters in C. elegans. Genome Res. 2011;21(2):237–44. Epub 2010/12/24. doi: 10.1101/gr.115931.110 21177966
5. Liu T, Rechtsteiner A, Egelhofer TA, Vielle A, Latorre I, Cheung MS, et al. Broad chromosomal domains of histone modification patterns in C. elegans. Genome Res. 2011;21(2):227–36. Epub 2010/12/24. doi: 10.1101/gr.115519.110 21177964
6. Harris TW, Antoshechkin I, Bieri T, Blasiar D, Chan J, Chen WJ, et al. WormBase: a comprehensive resource for nematode research. Nucleic Acids Res. 2010;38(Database issue):D463–7. Epub 2009/11/17. doi: 10.1093/nar/gkp952 19910365
7. Spencer WC, Zeller G, Watson JD, Henz SR, Watkins KL, McWhirter RD, et al. A spatial and temporal map of C. elegans gene expression. Genome Research. 2011;21(2):325–41. doi: 10.1101/gr.114595.110 21177967
8. Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, Eaton ML, et al. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science. 2010;330(6012):1787–97. doi: 10.1126/science.1198374 21177974
9. Roy S, Ernst J, Kharchenko PV, Kheradpour P, Negre N, Eaton ML, et al. Identification of functional elements and regulatory circuits by Drosophila modENCODE. Science. 2010;330(6012):1787–97. Epub 2010/12/24. doi: 10.1126/science.1198374 21177974
10. Negre N, Brown CD, Ma L, Bristow CA, Miller SW, Wagner U, et al. A cis-regulatory map of the Drosophila genome. Nature. 2011;471(7339):527–31. Epub 2011/03/25. doi: 10.1038/nature09990 21430782
11. Sela I, Lukatsky DB, DNA sequence correlations shape nonspecific transcription factor-DNA binding affinity. Biophysical Journal. 2011;101(1):160–6. Epub 2011/07/05. doi: 10.1016/j.bpj.2011.04.037 21723826
12. Afek A, Sela I, Musa-Lempel N, Lukatsky DB, Nonspecific transcription-factor-DNA binding influences nucleosome occupancy in yeast. Biophysical Journal. 2011;101(10):2465–75. Epub 2011/11/22. doi: 10.1016/j.bpj.2011.10.012 22098745
13. Afek A, Lukatsky DB, Nonspecific protein-DNA binding is widespread in the yeast genome. Biophysical Journal. 2012;102(8):1881–8. Epub 2012/07/10. doi: 10.1016/j.bpj.2012.03.044 22768944
14. Afek A, Lukatsky DB, Genome-Wide Organization of Eukaryotic Preinitiation Complex Is Influenced by Nonconsensus Protein-DNA Binding. Biophysical Journal. 2013;104(5):1107–15. Epub 2013/03/12. doi: 10.1016/j.bpj.2013.01.038 23473494
15. Afek A, Schipper JL, Horton J, Gordan R, Lukatsky DB, Protein-DNA binding in the absence of specific base-pair recognition. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(48):17140–5. doi: 10.1073/pnas.1410569111 25313048
16. von Hippel PH, Revzin A, Gross CA, Wang AC, Non-specific DNA binding of genome regulating proteins as a biological control mechanism: I. The lac operon: equilibrium aspects. Proc Natl Acad Sci U S A. 1974;71(12):4808–12. Epub 1974/12/01. 4612528
17. Berg OG, Winter RB, von Hippel PH, Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry. 1981;20(24):6929–48. Epub 1981/11/24. 7317363
18. Berg OG, von Hippel PH, Selection of DNA binding sites by regulatory proteins. Statistical-mechanical theory and application to operators and promoters. J Mol Biol. 1987;193(4):723–50. 3612791
19. von Hippel PH, Berg OG, On the specificity of DNA-protein interactions. Proc Natl Acad Sci U S A. 1986;83(6):1608–12. Epub 1986/03/01. 3456604
20. von Hippel PH, Berg OG, Facilitated target location in biological systems. J Biol Chem. 1989;264(2):675–8. Epub 1989/01/15. 2642903
21. von Hippel PH, From "simple" DNA-protein interactions to the macromolecular machines of gene expression. Annu Rev Biophys Biomol Struct. 2007;36:79–105. Epub 2007/05/05. 17477836
22. Slutsky M, Mirny LA, Kinetics of protein-DNA interaction: facilitated target location in sequence-dependent potential. Biophys J. 2004;87(6):4021–35. Epub 2004/10/07. 15465864
23. Wunderlich Z, Mirny LA, Different gene regulation strategies revealed by analysis of binding motifs. Trends Genet. 2009;25(10):434–40. Epub 2009/10/10. doi: 10.1016/j.tig.2009.08.003 19815308
24. Elf J, Li GW, Xie XS, Probing transcription factor dynamics at the single-molecule level in a living cell. Science. 2007;316(5828):1191–4. Epub 2007/05/26. 17525339
25. Hammar P, Leroy P, Mahmutovic A, Marklund EG, Berg OG, Elf J, The lac repressor displays facilitated diffusion in living cells. Science. 2012;336(6088):1595–8. Epub 2012/06/23. doi: 10.1126/science.1221648 22723426
26. Liebesny P, Goyal S, Dunlap D, Family F, Finzi L, Determination of the number of proteins bound non-specifically to DNA. J Phys Condens Matter. 2010;22(41):414104. Epub 2011/03/10. doi: 10.1088/0953-8984/22/41/414104 21386587
27. Manzo C, Zurla C, Dunlap DD, Finzi L, The effect of nonspecific binding of lambda repressor on DNA looping dynamics. Biophys J. 2012;103(8):1753–61. Epub 2012/10/23. doi: 10.1016/j.bpj.2012.09.006 23083719
28. Zurla C, Manzo C, Dunlap D, Lewis DE, Adhya S, Finzi L, Direct demonstration and quantification of long-range DNA looping by the lambda bacteriophage repressor. Nucleic Acids Res. 2009;37(9):2789–95. Epub 2009/03/12. doi: 10.1093/nar/gkp134 19276206
29. Wang YM, Austin RH, Cox EC, Single molecule measurements of repressor protein 1D diffusion on DNA. Phys Rev Lett. 2006;97(4):048302. Epub 2006/08/16. 16907618
30. Blainey PC, Luo G, Kou SC, Mangel WF, Verdine GL, Bagchi B, et al. Nonspecifically bound proteins spin while diffusing along DNA. Nat Struct Mol Biol. 2009;16(12):1224–9. Epub 2009/11/10. doi: 10.1038/nsmb.1716 19898474
31. Tafvizi A, Huang F, Leith JS, Fersht AR, Mirny LA, van Oijen AM, Tumor suppressor p53 slides on DNA with low friction and high stability. Biophys J. 2008;95(1):L01–3. Epub 2008/04/22. doi: 10.1529/biophysj.108.134122 18424488
32. Mavrich TN, Jiang C, Ioshikhes IP, Li X, Venters BJ, Zanton SJ, et al. Nucleosome organization in the Drosophila genome. Nature. 2008;453(7193):358–62. Epub 2008/04/15. doi: 10.1038/nature06929 18408708
33. Grove CA, De Masi F, Barrasa MI, Newburger DE, Alkema MJ, Bulyk ML, et al. A multiparameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell. 2009;138(2):314–27. Epub 2009/07/28. doi: 10.1016/j.cell.2009.04.058 19632181
34. Badis G, Berger MF, Philippakis AA, Talukder S, Gehrke AR, Jaeger SA, et al. Diversity and complexity in DNA recognition by transcription factors. Science. 2009;324(5935):1720–3. Epub 2009/05/16. doi: 10.1126/science.1162327 19443739
35. Berger MF, Bulyk ML, Universal protein-binding microarrays for the comprehensive characterization of the DNA-binding specificities of transcription factors. Nat Protoc. 2009;4(3):393–411. Epub 2009/03/07. doi: 10.1038/nprot.2008.195 19265799
36. Afek A, Shakhnovich EI, Lukatsky DB, Multi-scale sequence correlations increase proteome structural disorder and promiscuity. J Mol Biol. 2011;409(3):439–49. Epub 2011/04/06. doi: 10.1016/j.jmb.2011.03.056 21463640
37. Lukatsky DB, Afek A, Shakhnovich EI, Sequence correlations shape protein promiscuity. J Chem Phys. 2011;135(6):065104. Epub 2011/08/17. doi: 10.1063/1.3624332 21842953
38. Elkin M, Andre I, Lukatsky DB, Energy Fluctuations Shape Free Energy of Nonspecific Biomolecular Interactions. Journal of Statistical Physics. 2012;146(4):870–7.
39. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ, Crystal structure of the nucleosome core particle at 2.8 angstrom resolution. Nature. 1997;389(6648):251–60. 9305837
40. Liu X, Bushnell DA, Wang D, Calero G, Kornberg RD, Structure of an RNA polymerase II-TFIIB complex and the transcription initiation mechanism. Science. 2010;327(5962):206–9. Epub 2009/12/08. doi: 10.1126/science.1182015 19965383
41. Kasinathan S, Orsi GA, Zentner GE, Ahmad K, Henikoff S, High-resolution mapping of transcription factor binding sites on native chromatin. Nature methods. 2014;11(2):203–9. doi: 10.1038/nmeth.2766 24336359
42. Valouev A, Ichikawa J, Tonthat T, Stuart J, Ranade S, Peckham H, et al. A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res. 2008;18(7):1051–63. Epub 2008/05/15. doi: 10.1101/gr.076463.108 18477713
43. 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(6032):977–80. Epub 2011/05/21. doi: 10.1126/science.1200508 21596991
44. Zhang Y, Moqtaderi Z, Rattner BP, Euskirchen G, Snyder M, Kadonaga JT, et al. Intrinsic histone-DNA interactions are not the major determinant of nucleosome positions in vivo. Nat Struct Mol Biol. 2009;16(8):847–52. Epub 2009/07/22. doi: 10.1038/nsmb.1636 19620965
45. Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature. 2009;458(7236):362–6. Epub 2008/12/19. doi: 10.1038/nature07667 19092803
46. Lorch Y, Maier-Davis B, Kornberg RD, Role of DNA sequence in chromatin remodeling and the formation of nucleosome-free regions. Genes Dev. 2014;28(22):2492–7. Epub 2014/11/19. doi: 10.1101/gad.250704.114 25403179
47. Berger MF, Philippakis AA, Qureshi AM, He FS, Estep PW, 3rdBulyk ML, Compact, universal DNA microarrays to comprehensively determine transcription-factor binding site specificities. Nat Biotechnol. 2006;24(11):1429–35. Epub 2006/09/26. 16998473
48. Mukherjee S, Berger MF, Jona G, Wang XS, Muzzey D, Snyder M, et al. Rapid analysis of the DNA-binding specificities of transcription factors with DNA microarrays. Nat Genet. 2004;36(12):1331–9. Epub 2004/11/16. 15543148
49. Gordan R, Shen N, Dror I, Zhou T, Horton J, Rohs R, et al. Genomic regions flanking E-box binding sites influence DNA binding specificity of bHLH transcription factors through DNA shape. Cell Rep. 2013;3(4):1093–104. Epub 2013/04/09. doi: 10.1016/j.celrep.2013.03.014 23562153
50. Berger MF, Badis G, Gehrke AR, Talukder S, Philippakis AA, Pena-Castillo L, et al. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell. 2008;133(7):1266–76. Epub 2008/07/01. doi: 10.1016/j.cell.2008.05.024 18585359
51. Mirny LA, Nucleosome-mediated cooperativity between transcription factors. Proc Natl Acad Sci U S A. 2010;107(52):22534–9. Epub 2010/12/15. doi: 10.1073/pnas.0913805107 21149679
52. Teif VB, Rippe K, Nucleosome mediated crosstalk between transcription factors at eukaryotic enhancers. Phys Biol. 2011;8(4):044001. doi: 10.1088/1478-3975/8/4/044001 21666293
53. Elfving N, Chereji RV, Bharatula V, Bjorklund S, Morozov AV, Broach JR, A dynamic interplay of nucleosome and Msn2 binding regulates kinetics of gene activation and repression following stress. Nucleic Acids Res. 2014;42(9):5468–82. doi: 10.1093/nar/gku176 24598258
54. Bailey T, Krajewski P, Ladunga I, Lefebvre C, Li Q, Liu T, et al. Practical guidelines for the comprehensive analysis of ChIP-seq data. PLoS Comput Biol. 2013;9(11):e1003326. Epub 2013/11/19. doi: 10.1371/journal.pcbi.1003326 24244136
55. Grewal SI, Elgin SC, Transcription and RNA interference in the formation of heterochromatin. Nature. 2007;447(7143):399–406. 17522672
56. Bulut-Karslioglu A, Perrera V, Scaranaro M, de la Rosa-Velazquez IA, van de Nobelen S, Shukeir N, et al. A transcription factor-based mechanism for mouse heterochromatin formation. Nat Struct Mol Biol. 2012;19(10):1023–30. Epub 2012/09/18. doi: 10.1038/nsmb.2382 22983563
57. Ezer D, Zabet NR, Adryan B, Homotypic clusters of transcription factor binding sites: A model system for understanding the physical mechanics of gene expression. Computational and structural biotechnology journal. 2014;10(17):63–9. doi: 10.1016/j.csbj.2014.07.005 25349675
58. Kolomeisky AB, Physics of protein—DNA interactions: mechanisms of facilitated target search. Physical Chemistry Chemical Physics. 2011;13(6):2088–95. doi: 10.1039/c0cp01966f 21113556
59. Shimamoto N, One-dimensional diffusion of proteins along DNA Its biological and chemical significance revealed by single-molecule measurements. Journal of Biological Chemistry. 1999;274(22):15293–6. 10336412
60. Esadze A, Kemme CA, Kolomeisky AB, Iwahara J, Positive and negative impacts of nonspecific sites during target location by a sequence-specific DNA-binding protein: origin of the optimal search at physiological ionic strength. Nucleic acids research. 2014:gku418.
61. Weindl J, Dawy Z, Hanus P, Zech J, Mueller JC, Modeling promoter search by E. coli RNA polymerase: One-dimensional diffusion in a sequence-dependent energy landscape. Journal of theoretical biology. 2009;259(3):628–34. doi: 10.1016/j.jtbi.2009.05.006 19463831
62. Mirny L, Slutsky M, Wunderlich Z, Tafvizi A, Leith J, Kosmrlj A, How a protein searches for its site on DNA: the mechanism of facilitated diffusion. Journal of Physics A: Mathematical and Theoretical. 2009;42(43):434013.
63. Zhang C, Xuan Z, Otto S, Hover JR, McCorkle SR, Mandel G, et al. A clustering property of highly-degenerate transcription factor binding sites in the mammalian genome. Nucleic acids research. 2006;34(8):2238–46. 16670430
64. Afek A, Schipper JL, Horton J, Gordân R, Lukatsky DB, Protein− DNA binding in the absence of specific base-pair recognition. Proceedings of the National Academy of Sciences. 2014;111(48):17140–5.
65. Smith T, Husbands P, Layzell P, O'Shea M, Fitness landscapes and evolvability. Evolutionary computation. 2002;10(1):1–34. 11911781
66. Weirauch MT, Yang A, Albu M, Cote AG, Montenegro-Montero A, Drewe P, et al. Determination and inference of eukaryotic transcription factor sequence specificity. Cell. 2014;158(6):1431–43. Epub 2014/09/13. doi: 10.1016/j.cell.2014.08.009 25215497
67. Yook K, Harris TW, Bieri T, Cabunoc A, Chan J, Chen WJ, et al. WormBase 2012: more genomes, more data, new website. Nucleic Acids Res. 2012;40(Database issue):D735–41. Epub 2011/11/10. doi: 10.1093/nar/gkr954 22067452
68. Halford S, An end to 40 years of mistakes in DNA-protein association kinetics? Biochemical Society Transactions. 2009;37(2):343.
69. Bonnet I, Biebricher A, Porté P-L, Loverdo C, Bénichou O, Voituriez R, et al. Sliding and jumping of single EcoRV restriction enzymes on non-cognate DNA. Nucleic acids research. 2008;36(12):4118–27. doi: 10.1093/nar/gkn376 18544605