Three enhancements to the inference of statistical protein-DNA potentials

Proteins: Structure, Function and Bioinformatics

Volumn 81, Issue 3, 2013, Pages 426-442

  Alquraishi, Mohammed ^a   Mcadams, Harley H ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Biophysics; DNA binding sites; DNA motifs; Energy potentials; Machine learning; Protein DNA binding; Structural biology

Indexed keywords

ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; DNA BINDING; DNA PROTEIN COMPLEX; DNA STRUCTURE; PREDICTION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN STRUCTURE;

ALGORITHMS; ARTIFICIAL INTELLIGENCE; BASE SEQUENCE; BINDING SITES; CONSENSUS SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DATA INTERPRETATION, STATISTICAL; DNA; DNA-BINDING PROTEINS; ENTROPY; MODELS, MOLECULAR; MODELS, STATISTICAL; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEINS; SENSITIVITY AND SPECIFICITY;

EID: 84873091407     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24201     Document Type: Article

References (81)

1. Latchman DS. Gene control, Vol. 16. New York: Garland Science; 2010. 430 p.
2. Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P. Molecular biology of the cell, Vol. 33. New York: Garland Science; 2008. 1601, 1690 p.
3. Angarica VE, Perez AG, Vasconcelos AT, Collado-Vides J, Contreras-Moreira B. Prediction of TF target sites based on atomistic models of protein-DNA complexes. BMC Bioinform 2008; 9: 436.
4. Donald JE, Chen WW, Shakhnovich EI. Energetics of protein-DNA interactions. Nucleic Acids Res 2007; 35: 1039-1047.
5. Kaplan T, Friedman N, Margalit H. Ab initio prediction of transcription factor targets using structural knowledge. PLoS Comput Biol 2005; 1: e1.
6. Moroni E, Caselle M, Fogolari F. Identification of DNA-binding protein target sequences by physical effective energy functions: free energy analysis of lambda repressor-DNA complexes. BMC Struct Biol 2007; 7: 61.
7. Morozov AV, Havranek JJ, Baker D, Siggia ED. Protein-DNA binding specificity predictions with structural models. Nucleic Acids Res 2005; 33: 5781-5798.
8. AlQuraishi M, McAdams HH. Direct inference of protein-DNA interactions using compressed sensing methods. Proc Natl Acad Sci U S A 2011; 108: 14819-14824.
9. Pande VS. (Compressed) sensing and sensibility. Proc Natl Acad Sci U S A 2011; 108: 14713-14714.
10. Kono H, Sarai A. Structure-based prediction of DNA target sites by regulatory proteins. Proteins 1999; 35: 114-131.
11. Jorgensen WL, Tirado-Rives J. Potential energy functions for atomic-level simulations of water and organic and biomolecular systems. Proc Natl Acad Sci U S A 2005; 102: 6665-6670.
12. Zhou Y, Zhou HY, Zhang C, Liu S. What is a desirable statistical energy function for proteins and how can it be obtained? Cell Biochem Biophys 2006; 46: 165-174.
13. Zhao HY, Yang YD, Zhou YQ. Structure-based prediction of DNA-binding proteins by structural alignment and a volume-fraction corrected DFIRE-based energy function. Bioinformatics 2010; 26: 1857-1863.
14. Zhou H, Zhou Y. Distance-scaled, finite ideal-gas reference state improves structure-derived potentials of mean force for structure selection and stability prediction. Prot Sci 2002; 11: 2714-2726.
15. Xu BS, Yang YD, Liang HJ, Zhou YQ. An all-atom knowledge-based energy function for protein-DNA threading, docking decoy discrimination, and prediction of transcription-factor binding profiles. Prot Struct Funct Bioinform 2009; 76: 718-730.
16. Kussell E, Shimada J, Shakhnovich EI. A structure-based method for derivation of all-atom potentials for protein folding. Proc Natl Acad Sci U S A 2002; 99: 5343-5348.
17. Chen WW, Shakhnovich EI. Lessons from the design of a novel atomic potential for protein folding. Prot Sci 2005; 14: 1741-1752.
18. Hubner IA, Deeds EJ, Shakhnovich EI. High-resolution protein folding with a transferable potential. Proc Natl Acad Sci U S A 2005; 102: 18914-18919.
19. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. The protein data bank. Nucleic Acids Res 2000; 28: 235-242.
20. Vaquerizas JM, Kummerfeld SK, Teichmann SA, Luscombe NM. A census of human transcription factors: function, expression and evolution. Nat Rev Genet 2009; 10: 252-263.
21. Gajiwala KS, Burley SK. Winged helix proteins. Curr Opin Struct Biol 2000; 10: 110-116.
22. Mo Y, Vaessen B, Johnston K, Marmorstein R. Structure of the elk-1-DNA complex reveals how DNA-distal residues affect ETS domain recognition of DNA. Nat Struct Biol 2000; 7: 292-297.
23. Lu XJ, Olson WK. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucl Acids Res 2003; 31: 5108-5121.
24. Lu XJ, Olson WK. 3DNA: a versatile, integrated software system for the analysis, rebuilding and visualization of three-dimensional nucleic-acid structures. Nat Protoc 2008; 3: 1213-1227.
25. Badis G, Berger MF, Philippakis AA, Talukder S, Gehrke AR, Jaeger SA, Chan ET, Metzler G, Vedenko A, Chen XY, Kuznetsov H, Wang CF, Coburn D, Newburger DE, Morris Q, Hughes TR, Bulyk ML. Diversity and complexity in DNA recognition by transcription factors. Science 2009; 324: 1720-1723.
26. Berg OG, Vonhippel PH. Selection of DNA-binding sites by regulatory proteins-statistical-mechanical theory and application to operators and promoters. J Mol Biol 1987; 193: 723-743.
27. Kullback S, Leibler RA. On information and sufficiency. Ann Math Stat 1951; 22: 79-86.
28. Mirny LA, Gelfand MS. Structural analysis of conserved base pairs in protein-DNA complexes. Nucleic Acids Res 2002; 30: 1704-1711.
29. Hoglund A, Kohlbacher O. From sequence to structure and back again: approaches for predicting protein-DNA binding. Proteome Sci 2004; 2: 3.
30. Eisen M. All motifs are NOT created equal: structural properties of transcription factor-DNA interactions and the inference of sequence specificity. Genome Biol 2005; 6: P7.
31. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre-Dirrie A, Reuter I, Chekmenev D, Krull M, Hornischer K, Voss N, Stegmaier P, Lewicki-Potapov B, Saxel H, Kel AE, Wingender E. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 2006; 34( Database issue): D108-D110.
32. Kazakov AE, Cipriano MJ, Novichkov PS, Minovitsky S, Vinogradov DV, Arkin A, Mironov AA, Gelfand MS, Dubchak I. RegTransBase-a database of regulatory sequences and interactions in a wide range of prokaryotic genomes. Nucleic Acids Res 2007; 35: D407-D412.
33. Halfon MS, Gallo SM, Bergman CM. REDfly 2.0: an integrated database of cis-regulatory modules and transcription factor binding sites in Drosophila. Nucleic Acids Res 2008; 36( Database issue): D594-D598.
34. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, Valen E, Yusuf D, Lenhard B, Wasserman WW, Sandelin A. JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 2010; 38( Database issue): D105-D110.
35. Newburger DE, Bulyk ML. UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res 2009; 37: D77-D82.
36. Munch R, Hiller K, Barg H, Heldt D, Linz S, Wingender E, Jahn D. PRODORIC: prokaryotic database of gene regulation. Nucleic Acids Res 2003; 31: 266-269.
37. Gama-Castro S, Jimenez-Jacinto V, Peralta-Gil M, Santos-Zavaleta A, Penaloza-Spinola MI, Contreras-Moreira B, Segura-Salazar J, Muniz-Rascado L, Martinez-Flores I, Salgado H, Bonavides-Martinez C, Abreu-Goodger C, Rodriguez-Penagos C, Miranda-Rios J, Morett E, Merino E, Huerta AM, Trevino-Quintanilla L, Collado-Vides J. RegulonDB (version 6.0): gene regulation model of Escherichia coli K-12 beyond transcription, active (experimental) annotated promoters and Textpresso navigation. Nucleic Acids Res 2008; 36( Database issue): D120-D124.
38. Sierro N, Makita Y, de Hoon M, Nakai K. DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information. Nucleic Acids Res 2008; 36( Database issue): D93-D96.
39. Jagannathan V, Roulet E, Delorenzi M, Bucher P. HTPSELEX-a database of high-throughput SELEX libraries for transcription factor binding sites. Nucleic Acids Res 2006; 34( Database issue): D90-D94.
40. Down TA, Bergman CM, Su J, Hubbard TJ. Large-scale discovery of promoter motifs in Drosophila melanogaster. PLoS Comput Biol 2007; 3: e7.
41. Palaniswamy SK, James S, Sun H, Lamb RS, Davuluri RV, Grotewold E. AGRIS and AtRegNet. A platform to link cis-regulatory elements and transcription factors into regulatory networks. Plant Physiol 2006; 140: 818-829.
42. Bulow L, Engelmann S, Schindler M, Hehl R. AthaMap, integrating transcriptional and post-transcriptional data. Nucleic Acids Res 2009; 37( Database issue): D983-D986.
43. Kumar MDS, Bava KA, Gromiha MM, Prabakaran P, Kitajima K, Uedaira H, Sarai A. ProTherm and ProNIT: thermodynamic databases for proteins and protein-nucleic acid interactions. Nucleic Acids Res 2006; 34: D204-D206.
44. Yellaboina S, Ranjan S, Chakhaiyar P, Hasnain SE, Ranjan A. Prediction of DtxR regulon: identification of binding sites and operons controlled by Diphtheria toxin repressor in Corynebacterium diphtheriae. BMC Microbiol 2004; 4: 38.
45. Franks AH, Griffiths AA, Wake RG. Identification and characterization of new DNA-replication terminators in Bacillus subtilis. Mol Microbiol 1995; 17: 13-23.
46. Griffiths AA, Wake RG. Search for additional replication terminators in the Bacillus subtilis 168 chromosome. J Bacteriol 1997; 179: 3358-3361.
47. Griffiths AA, Andersen PA, Wake RG. Replication terminator protein-based replication fork-arrest systems in various Bacillus species. J Bacteriol 1998; 180: 3360-3367.
48. Sugisaki H, Kanazawa S. New restriction endonucleases from Flavobacterium okeanokoites (FokI) and Micrococcus luteus (MluI). Gene 1981; 16: 73-78.
49. Falvey E, Grindley NDF. Contacts between gamma-delta-resolvase and the gamma-delta-res site. Embo J 1987; 6: 815-821.
50. Moskowitz IP, Heichman KA, Johnson RC. Alignment of recombination sites in Hin-mediated site-specific DNA recombination. Genes Dev 1991; 5: 1635-1645.
51. Rosandic M, Paar V, Basar I, Gluncic M, Pavin N, Pilas I. CENP-B box and pJ alpha sequence distribution in human alpha satellite higher-order repeats (HOR). Chromosome Res 2006; 14: 735-753.
52. Tronche F, Yaniv M. HNF1, a homeoprotein member of the hepatic transcription regulatory network. Bioessays 1992; 14: 579-587.
53. Liston DR, Johnson PJ. Analysis of a ubiquitous promoter element in a primitive eukaryote: early evolution of the initiator element. Mol Cell Biol 1999; 19: 2380-2388.
54. Shen WF, Montgomery JC, Rozenfeld S, Moskow JJ, Lawrence HJ, Buchberg AM, Largman C. AbdB-like Hox proteins stabilize DNA binding by the Meis1 homeodomain proteins. Mol Cell Biol 1997; 17: 6448-6458.
55. Kostelidou K, Thomas CM. The hierarchy of KorB binding at its 12 binding sites on the broad-host-range plasmid RK2 and modulation of this binding by IncC1 protein. J Mol Biol 2000; 295: 411-422.
56. Garcia-Castellanos R, Mallorqui-Fernandez G, Marrero A, Potempa J, Coll M, Gomis-Ruth FX. On the transcriptional regulation of methicillin resistance-MecI repressor in complex with its operator. J Biol Chem 2004; 279: 17888-17896.
57. Colloms SD, van Luenen HG, Plasterk RH. DNA binding activities of the Caenorhabditis elegans Tc3 transposase. Nucleic Acids Res 1994; 22: 5548-5554.
58. Prakash P, Yellaboina S, Ranjan A, Hasnain SE. Computational prediction and experimental verification of novel IdeR binding sites in the upstream sequences of Mycobacterium tuberculosis open reading frames. Bioinformatics 2005; 21: 2161-2166.
59. Wilson DS, Guenther B, Desplan C, Kuriyan J. High resolution crystal structure of a paired (Pax) class cooperative homeodomain dimer on DNA. Cell 1995; 82: 709-719.
60. Hughes KT, Gaines PCW, Karlinsey JE, Vinayak R, Simon MI. Sequence-specific interaction of the Salmonella Hin recombinase in both major and minor grooves of DNA. EMBO J 1992; 11: 2695-2705.
61. Hoey T, Levine M. Divergent homeo box proteins recognize similar DNA sequences in Drosophila. Nature 1988; 332: 858-861.
62. White CE, Winans SC. The quorum-sensing transcription factor TraR decodes its DNA binding site by direct contacts with DNA bases and by detection of DNA flexibility. Mol Microbiol 2007; 64: 245-256.
63. Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW, Hannett NM, Tagne JB, Reynolds DB, Yoo J, Jennings EG, Zeitlinger J, Pokholok DK, Kellis M, Rolfe PA, Takusagawa KT, Lander ES, Gifford DK, Fraenkel E, Young RA. Transcriptional regulatory code of a eukaryotic genome. Nature 2004; 431: 99-104.
64. Chen SF, Gunasekera A, Zhang XP, Kunkel TA, Ebright RH, Berman HM. Indirect readout of DNA sequence at the primary-kink site in the CAP-DNA complex: alteration of DNA binding specificity through alteration of DNA kinking. J Mol Biol 2001; 314: 75-82.
65. Koudelka GB, Lam CY. Differential recognition of OR1 and OR3 by bacteriophage 434 repressor and Cro. J Biol Chem 1993; 268: 23812-23817.
66. Koudelka GB, Harrison SC, Ptashne M. Effect of non-contacted bases on the affinity of 434 operator for 434 repressor and Cro. Nature 1987; 326: 886-888.
67. Schumacher MA, Lau AOT, Johnson PJ. Structural basis of core promoter recognition in a primitive eukaryote. Cell 2003; 115: 413-424.
68. Smale ST, Jain A, Kaufmann J, Emami KH, Lo K, Garraway IP. The initiator element: a paradigm for core promoter heterogeneity within metazoan protein-coding genes. Cold Spring Harb Symp Quant Biol 1998; 63: 21-31.
69. Lo K, Smale ST. Generality of a functional initiator consensus sequence. Gene 1996; 182: 13-22.
70. Javahery R, Khachi A, Lo K, Zenziegregory B, Smale ST. DNA-sequence requirements for transcriptional initiator activity in mammalian-cells. Mol Cell Biol 1994; 14: 116-127.
71. Huerta AM, Francino MP, Morett E, Collado-Vides J. Selection for unequal densities of sigma(70) promoter-like signals in different regions of large bacterial genomes. Plos Genet 2006; 2: 1740-1750.
72. Fischer SEJ, van Luenen HGAM, Plasterk RHA. Cis requirements for transposition of Tc1-like transposons in C. elegans. Mol Gen Genet 1999; 262: 268-274.
73. Rodgers DW, Harrison SC. The complex between phage 434 repressor DNA-binding domain and operator site OR3: structural differences between consensus and non-consensus half-sites. Structure 1993; 1: 227-240.
74. van Luenen HGAM, Plasterk RHA. Target site choice of the related transposable elements Tc1 and Tc3 of Caenorhabditis elegans. Nucleic Acids Res 1994; 22: 262-269.
75. Wintjens R, Rooman M. Structural classification of HTH DNA-binding domains and protein-DNA interaction modes. J Mol Biol 1996; 262: 294-313.
76. Suzuki M, Gerstein M. Binding geometry of alpha-helices that recognize DNA. Prot Struct Funct Genet 1995; 23: 525-535.
77. Pabo CO, Nekludova L. Geometric analysis and comparison of protein-DNA interfaces: why is there no simple code for recognition? J Mol Biol 2000; 301: 597-624.
78. Bell RM, Koren Y. Lessons from the netflix prize challenge. SIGKDD Explor Newsl 2007; 9: 75-79.
79. Dietterich TG. Ensemble methods in machine learning. Lect Notes Comput Sci 2000; 1857: 1-15.
80. Bulyk ML, Gentalen E, Lockhart DJ, Church GM. Quantifying DNA-protein interactions by double-stranded DNA arrays. Nat Biotechnol 1999; 17: 573-577.
81. Stormo GD, Zhao Y. Determining the specificity of protein-DNA interactions. Nat Rev Genet 2010; 11: 751-760.