Discriminative prediction of mammalian enhancers from DNA sequence

Genome Research

Volumn 21, Issue 12, 2011, Pages 2167-2180

  Lee, Dongwon ^a   Karchin, Rachel ^a,b   Beer, Michael A ^a,c  

^a Johns Hopkins University   (United States)

^b Johns Hopkins University   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEASE I;

ANIMAL TISSUE; ARTICLE; DISCRIMINANT ANALYSIS; DNA SEQUENCE; ENHANCER REGION; GENETIC IDENTIFICATION; GENOME ANALYSIS; MAMMAL; MOUSE; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; SUPPORT VECTOR MACHINE;

ANIMALS; CEREBRAL CORTEX; CREB-BINDING PROTEIN; GENOME; GENOME-WIDE ASSOCIATION STUDY; MICE; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; RESPONSE ELEMENTS; SEQUENCE ANALYSIS, DNA;

EID: 83055181959     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.121905.111     Document Type: Article

References (79)

1. Bailey T, Elkan C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28-36.
2. Banerji J. 1981. Expression of a b-globin gene is enhanced by remote SV40 DNA sequences. Cell 27: 299-308. (Pubitemid 12200499)
3. Beer MA, Tavazoie S. 2004. Predicting gene expression from sequence. Cell 117: 185-198. (Pubitemid 38496239)
4. Ben-Hur A, Ong CS, Sonnenburg S, Schölkopf B, Rätsch G. 2008. Support vector machines and kernels for computational biology. PLoS Comput Biol 4: e1000173. doi: 10.1371/journal.pcbi.1000173.
5. Berger MF, Badis G, Gehrke AR, Talukder S, Philippakis AA, Peña-Castillo L, Alleyne TM, Mnaimneh S, Botvinnik OB, Chan ET, et al. 2008. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 133: 1266-1276. (Pubitemid 351852913)
6. Bertrand N, Castro DS, Guillemot F. 2002. Proneural genes and the specification of neural cell types. Nat Rev Neurosci 3: 517-530. (Pubitemid 135706662)
7. Blackwood EM, Kadonaga JT. 1998. Going the distance: A current view of enhancer action. Science 281: 60-63. (Pubitemid 28354042)
8. Boser BE, Guyon IM, Vapnik VN. 1992. A training algorithm for optimal margin classifiers. In Proceedings of the Fifth Annual Workshop on Computational Learning Theory. Association for Computing Machinery (ACM), New York.
9. Bryne JC, Valen E, TangME, Marstrand T,Winther O, da Piedade I, Krogh A, Lenhard B, Sandelin A. 2008. JASPAR, the open access database of transcription factor-binding profiles: New content and tools in the 2008 update. Nucleic Acids Res 36: D102-D106. (Pubitemid 351149704)
10. Bulfone A, Puelles L, PorteusM, FrohmanM,Martin G, Rubenstein J. 1993. Spatially restricted expression of Dlx-1, Dlx-2 (Tes-1), Gbx-2, and Wnt-3 in the embryonic day 12.5 mouse forebrain defines potential transverse and longitudinal segmental boundaries. J Neurosci 13: 3155-3172. (Pubitemid 23199240)
11. Carter D, Chakalova L, Osborne CS, Dai Y, Fraser P. 2002. Long-range chromatin regulatory interactions in vivo. Nat Genet 32: 623-626. (Pubitemid 35435174)
12. Chan HM, La Thangue NB. 2001. P300/CBP proteins: HATs for transcriptional bridges and scaffolds. J Cell Sci 114: 2363-2373. (Pubitemid 32684792)
13. Chen X, Xu H, Yuan P, Fang F, Huss M, Vega VB,Wong E, Orlov YL, ZhangW, Jiang J, et al. 2008. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133: 1106-1117. (Pubitemid 351787745)
14. Demarque M, Spitzer NC. 2010. Activity-dependent expression of Lmx1b regulates specification of serotonergic neurons modulating swimming behavior. Neuron 67: 321-334.
15. Elnitski L, Hardison RC, Li J, Yang S, Kolbe D, Eswara P, O'Connor MJ, Schwartz S, Miller W, Chiaromonte F. 2003. Distinguishing regulatory DNA from neutral sites. Genome Res 13: 64-72.
16. ENCODE Project Consortium. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447: 799-816.
17. Erives A, Levine M. 2004. Coordinate enhancers share common organizational features in the Drosophila genome. Proc Natl Acad Sci 101: 3851-3856. (Pubitemid 38381066)
18. Fisher S, Grice EA, Vinton RM, Bessling SL, McCallion AS. 2006. Conservation of RET regulatory function from human to zebrafish without sequence similarity. Science 312: 276-279.
19. Flavell SW, Greenberg ME. 2008. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 31: 563-590.
20. Frietze S, Lan X, Jin VX, FarnhamPJ. 2010. Genomic targets of the KRAB and SCAN domain-containing zinc finger protein 263. J Biol Chem 285: 1393-1403.
21. Furey TS, Cristianini N, Duffy N, Bednarski DW, Schummer M, Haussler D. 2000. Support vector machine classification and validation of cancer tissue samples usingmicroarray expression data. Bioinformatics 16: 906-914.
22. Ghanem N, Jarinova O, Amores A, Long Q, Hatch G, Park BK, Rubenstein JLR, Ekker M. 2003. Regulatory roles of conserved intergenic domains in vertebrate Dlx bigene clusters. Genome Res 13: 533-543. (Pubitemid 36511913)
23. Gotea V, Visel A,Westlund JM, Nobrega MA, Pennacchio LA, Ovcharenko I. 2010. Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res 20: 565-577.
24. Gupta S, Stamatoyannopoulos JA, Bailey TL, Noble W. 2007. Quantifying similarity between motifs. Genome Biol 8: R24. doi: 10.1186/gb-2007-8- 2-r24.
25. Hallikas O, Palin K, Sinjushina N, Rautiainen R, Partanen J, Ukkonen E, Taipale J. 2006. Genome-wide prediction ofmammalian enhancers based on analysis of transcription-factor binding affinity. Cell 124: 47-59. (Pubitemid 43069309)
26. Heintzman ND, Stuart RK, Hon G, Fu Y, ChingCW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, et al. 2007. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39: 311-318. (Pubitemid 46328487)
27. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, Harp LF, Ye Z, Lee LK, Stuart RK, Ching CW, et al. 2009. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459: 108-112.
28. Hughes JD, Estep PW, Tavazoie S, Church GM. 2000. Computational identification of Cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae. J Mol Biol 296: 1205-1214.
29. Joachims T. 1999. Making large-scale support vector machine learning practical. In Advances in kernal methods, pp. 169-184. MIT Press, Cambridge, MA.
30. John S, Sabo PJ, Thurman RE, Sung M-H, Biddie SC, Johnson TA, Hager GL, Stamatoyannopoulos JA. 2011. Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat Genet 43: 264-268.
31. Johnson DS, Mortazavi A, Myers RM,Wold B. 2007. Genome-wide mapping of in vivo protein-DNA interactions. Science 316: 1497-1502. (Pubitemid 46906620)
32. Kadonaga JT. 2004. Regulation of RNA polymerase II transcription by sequence-specific DNA binding factors. Cell 116: 247-257. (Pubitemid 38173000)
33. Karchin R, Karplus K, Haussler D. 2002. Classifying G-protein coupled receptors with support vector machines. Bioinformatics 18: 147-159. (Pubitemid 34145043)
34. Karolchik D, Kuhn RM, Baertsch R, Barber GP, Clawson H, Diekhans M, Giardine B, Harte RA, Hinrichs AS, Hsu F, et al. 2008. The UCSC Genome Browser Database: 2008 update. Nucleic Acids Res 36: D773-D779. (Pubitemid 351149822)
35. Keilwagen J, Grau J, Paponov IA, Posch S, Strickert M, Grosse I. 2011. Denovo discovery of differentially abundant transcription factor binding sites including their positional preference. PLoS Comput Biol 7: e1001070. doi: 10.1371/journal.pcbi.1001070.
36. Kim T, Hemberg M,Gray JM,CostaAM, BearDM,Wu J, HarminDA, Laptewicz M, Barbara-Haley K, Kuersten S, et al. 2010.Widespread transcription at neuronal activity-regulated enhancers. Nature 465: 182-187.
37. King DC, Taylor J, Elnitski L, Chiaromonte F, Miller W, Hardison RC. 2005. Evaluation of regulatory potential and conservation scores for detecting cis-regulatory modules in aligned mammalian genome sequences. Genome Res 15: 1051-1060. (Pubitemid 41126860)
38. Koh K, Kim S-J, Boyd S. 2007. An interior-point method for large-scale l1- regularized logistic regression. J Mach Learn Res 8: 1519-1555. (Pubitemid 47210273)
39. Kurokawa D, Kiyonari H, Nakayama R, Kimura-Yoshida C, Matsuo I, Aizawa S. 2004. Regulation of Otx2 expression and its functions in mouse forebrain and midbrain. Development 131: 3319-3331. (Pubitemid 39139879)
40. Lee JE. 1997. Basic helix-loop-helix genes in neural development. Curr Opin Neurobiol 7: 13-20. (Pubitemid 27096238)
41. Leslie C, Eskin E, Noble WS. 2002. The spectrum kernel: A string kernel for SVM protein classification. Pac Symp Biocomput 7: 564-575.
42. Leslie C, Eskin E,Cohen A,Weston J,NobleWS. 2004. Mismatchstring kernels for discriminative protein classification. Bioinformatics 20: 467-476. (Pubitemid 38344326)
43. Leung G, Eisen MB. 2009. Identifying cis-regulatory sequences by word profile similarity. PLoS ONE 4: e6901. doi: 10.1371/journal.pone. 0006901.
44. Maniatis T, Falvo JV, Kim TH, Kim TK, Lin CH, Parekh BS, Wathelet MG. 1998. Structure and function of the interferon-β enhanceosome. Cold Spring Harb Symp Quant Biol 63: 609-620.
45. Mason S, Piper M, Gronostajski RM, Richards LJ. 2008. Nuclear factor one transcription factors in CNS development. Mol Neurobiol 39: 10-23.
46. Matsuo I, Kuratani S, Kimura C, Takeda N, Aizawa S. 1995. Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev 9: 2646-2658.
47. Matys V, Fricke E, Geffers R, Gossling E, Haubrock M, Hehl R, Hornischer K, Karas D, Kel AE, Kel-Margoulis OV, et al. 2003. TRANSFAC(R): Transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31: 374-378. (Pubitemid 36150406)
48. McGaughey DM, Vinton RM, Huynh J, Al-Saif A, Beer MA, McCallion AS. 2008. Metrics of sequence constraint overlook regulatory sequences in an exhaustive analysis at phox2b. Genome Res 18: 252-260. (Pubitemid 351240735)
49. Megraw M, Pereira F, Jensen ST, Ohler U, Hatzigeorgiou AG. 2009. A transcription factor affinity-based code for mammalian transcription initiation. Genome Res 19: 644-656.
50. Meinicke P, Tech M, Morgenstern B, Merkl R. 2004. Oligo kernels for datamining on biological sequences: A case study on prokaryotic translation initiation sites. BMC Bioinformatics 5: 169. doi: 10.1186/ 1471-2105-5-169.
51. Narlikar L, Sakabe NJ, Blanski AA, Arimura FE, Westlund JM, Nobrega MA, Ovcharenko I. 2010. Genome-wide discovery of human heart enhancers. Genome Res 20: 381-392.
52. Newburger DE, Bulyk ML. 2009. UniPROBE: An online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res 37: D77-D82.
53. Noonan JP, McCallion AS. 2010. Genomics of long-range regulatory elements. Annu Rev Genomics Hum Genet 11: 1-23.
54. Pavesi G, Mauri G, Pesole G. 2001. An algorithm for finding signals of unknown length in DNA sequences. Bioinformatics 17 (Suppl 1): S207-S214. (Pubitemid 33793512)
55. PeckhamHE, Thurman RE, Fu Y, Stamatoyannopoulos JA, Noble WS, Struhl K, Weng Z. 2007. Nucleosome positioning signals in genomic DNA. Genome Res 17: 1170-1177. (Pubitemid 47204860)
56. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, Shoukry M, Minovitsky S, Dubchak I, Holt A, Lewis KD, et al. 2006. In vivo enhancer analysis of human conserved noncoding sequences. Nature 444: 499-502. (Pubitemid 44809068)
57. Rätsch G, Sonnenburg S, Schölkopf B. 2005. RASE: Recognition of alternatively spliced exons in C. elegans. Bioinformatics 21 (Suppl 1): i369-i377. (Pubitemid 41794510)
58. Robertson G, Hirst M, Bainbridge M, Bilenky M, Zhao Y, Zeng T, Euskirchen G, Bernier B, Varhol R, Delaney A, et al. 2007. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat Methods 4: 651-657. (Pubitemid 47202477)
59. Ross SE, Greenberg ME, Stiles CD. 2003. Basic helix-loop-helix factors in cortical development. Neuron 39: 13-25. (Pubitemid 36830945)
60. Schölkopf B, Tsuda K, Vert JP. 2004. Kernel methods in computational biology. MIT Press, Cambridge, MA.
61. Schultheiss SJ. 2010. Kernel-based identification of regulatory modules. In Computational biology of transcription factor binding (ed. I. Ladunga), Vol. 674, pp. 213-223. Humana Press, Totowa, NJ.
62. Schultheiss SJ, Busch W, Lohmann JU, Kohlbacher O, Rätsch G. 2009. KIRMES: Kernel-based identification of regulatory modules in euchromatic sequences. Bioinformatics 25: 2126-2133.
63. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, Rosenbloom K, Clawson H, Spieth J, Hillier LW, Richards S, et al. 2005. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050. (Pubitemid 41126859)
64. Sonnenburg S, Rätsch G, Schäfer C, Schölkopf B. 2006a. Large scale multiple kernel learning. J Mach Learn Res 7: 1531-1565. (Pubitemid 44373694)
65. Sonnenburg S, Zien A, Ratsch G. 2006b. ARTS: Accurate recognition of transcription starts in human. Bioinformatics 22: e472-e480. (Pubitemid 44288318)
66. Sonnenburg S, Schweikert G, Philips P, Behr J, Ratsch G. 2007. Accurate splice site prediction using support vectormachines. BMC Bioinformatics 8: S7. doi: 10.1186/1471-2105-8-S10-S7.
67. Sonnenburg S, Zien A, Philips P, Ratsch G. 2008. POIMs: positional oligomer importance matrices-understanding support vector machine-based signal detectors. Bioinformatics 24: i6-i14. (Pubitemid 351911652)
68. Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proc Natl Acad Sci 100: 9440-9445. (Pubitemid 37033947)
69. Su J, Teichmann SA, Down TA. 2010. Assessing computational methods of cis-regulatory module prediction. PLoS Comput Biol 6: e1001020. doi: 10.1371/journal.pcbi.1001020.
70. Thanos D, Maniatis T. 1995. Virus induction of human IFNb gene expression requires the assembly of an enhanceosome. Cell 83: 1091-1100. (Pubitemid 26007801)
71. Vandewalle C, Roy F, Berx G. 2008. The role of the ZEB family of transcription factors in development and disease. Cell Mol Life Sci 66: 773-787.
72. Vapnik VN. 1995. The nature of statistical learning theory. Springer, New York.
73. Visel A, Prabhakar S, Akiyama JA, Shoukry M, Lewis KD, Holt A, Plajzer-Frick I, Afzal V, Rubin EM, Pennacchio LA. 2008. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat Genet 40: 158-160.
74. Visel A, Blow MJ, Zhang T, Akiyama JA, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, et al. 2009. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457: 854-858.
75. Wigle JT, Eisenstat DD. 2008. Homeobox genes in vertebrate forebrain development and disease. Clin Genet 73: 212-226. (Pubitemid 351228504)
76. Wilson M, Koopman P. 2002. Matching SOX: Partner proteins and cofactors of the SOX family of transcriptional regulators. Curr Opin Genet Dev 12: 441-446. (Pubitemid 34722924)
77. Wilson MD, Barbosa-Morais NL, Schmidt D, Conboy CM, Vanes L, Tybulewicz VLJ, Fisher EMC, Tavare S, Odom DT. 2008. Species-specific transcription in mice carrying human chromosome 21. Science 322: 434-438.
78. Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK, Vavouri T, Smith SF, North P, Callaway H, Kelly K, et al. 2004. Highly conserved noncoding sequences are associated with vertebrate development. PLoS Biol 3: e7. doi: 10.1371/journal.pbio.0030007.
79. Zerucha T, Stühmer T, Hatch G, Park BK, Long Q, Yu G, Gambarotta A, Schultz JR, Rubenstein JLR, Ekker M. 2000. A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain. J Neurosci 20: 709-721. (Pubitemid 30225573)