Validation of skeletal muscle cis-regulatory module predictions reveals nucleotide composition bias in functional enhancers

PLoS Computational Biology

Volumn 7, Issue 12, 2011, Pages

  Kwon, Andrew T ^a   Chou, Alice Yi ^a   Arenillas, David J ^a   Wasserman, Wyeth W ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; FORECASTING; GENE EXPRESSION; NUCLEOTIDES;

C2C12 MYOBLASTS; CIS-REGULATORY MODULES; COMPUTATIONAL PREDICTIONS; FUNCTIONAL SEQUENCES; MYOTUBES; NUCLEOTIDE COMPOSITION; REGULATORY SEQUENCES; REPORTER-GENE EXPRESSION; SEQUENCE CONSERVATION; SKELETAL MUSCLE;

MUSCLE;

MYOD PROTEIN; NUCLEOTIDE; HISTONE;

ANIMAL CELL; ARTICLE; CELL STRAIN 3T3; CONTROLLED STUDY; DNA FLANKING REGION; FIBROBLAST CULTURE; FUNCTIONAL GENOMICS; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; HISTONE MODIFICATION; HUMAN GENOME; MOUSE; MYOBLAST; MYOTUBE; NONHUMAN; NUCLEOTIDE MOTIF; NUCLEOTIDE SEQUENCE; PREDICTION; REGULATORY SEQUENCE; REPORTER GENE; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; VALIDATION PROCESS; ANIMAL; BIOLOGICAL MODEL; BIOLOGY; CHROMATIN IMMUNOPRECIPITATION; COMPUTER SIMULATION; DNA BASE COMPOSITION; DNA SEQUENCE; GENETICS; GENOME; HUMAN; METHODOLOGY; PHYLOGENY; PHYSIOLOGY; REPRODUCIBILITY; STATISTICAL MODEL;

ANIMALS; BASE COMPOSITION; CHROMATIN IMMUNOPRECIPITATION; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; CONSERVED SEQUENCE; GENOME; HISTONES; HUMANS; MICE; MODELS, GENETIC; MODELS, STATISTICAL; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MYOD PROTEIN; NIH 3T3 CELLS; PHYLOGENY; REGULATORY SEQUENCES, NUCLEIC ACID; REPRODUCIBILITY OF RESULTS; SEQUENCE ANALYSIS, DNA;

EID: 84855272659     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002256     Document Type: Article

References (68)

1. Arnone MI, Davidson EH, (1997) The hardwiring of development: organization and function of genomic regulatory systems. Development 124: 1851-1864.
2. Shimizu S, Miyamoto Y, Hayashi M, (2002) Cell-type dependency of two Foxa/HNF3 sites in the regulation of vitronectin promoter activity. Biochim Biophys Acta 1574: 337-344.
3. McBride DJ, Kleinjan DA, (2004) Rounding up active cis-elements in the triple C corral: combining conservation, cleavage and conformation capture for the analysis of regulatory gene domains. Brief Funct Genomic Proteomic 3: 267-279.
4. Ilnytska O, Sözen MA, Dauterive R, Argyropoulos G, (2009) Control elements in the neighboring ATPase gene influence spatiotemporal expression of the human agouti-related protein. J Mol Biol 388: 239-251.
5. Ling J, Ainol L, Zhang L, Yu X, Pi W, et al. (2004) HS2 enhancer function is blocked by a transcriptional terminator inserted between the enhancer and the promoter. J Biol Chem 279: 51704-51713.
6. Miele A, Dekker J, (2008) Long-range chromosomal interactions and gene regulation. Mol Biosyst 4: 1046-1057.
7. Frech K, Quandt K, Werner T, (1997) Finding protein-binding sites in DNA sequences: the next generation. Trends Biochem Sci 22: 103-104.
8. Look AT, (1997) Oncogenic Transcription Factors in the Human Acute Leukemias. Science 278: 1059-1064.
9. Lee J, Ahnn J, Bae S-C, (2004) Homologs of RUNX and CBF beta/PEBP2 beta in C. elegans. Oncogene 23: 4346-4352.
10. Arnold HH, Winter B, (1998) Muscle differentiation: more complexity to the network of myogenic regulators. Curr Opin Genet Dev 8: 539-544.
11. Gramolini AO, Jasmin BJ, (1999) Expression of the utrophin gene during myogenic differentiation. Nucleic Acids Res 27: 3603-3609.
12. Braun T, Bober E, Rudnicki M, Jaenisch R, Arnold H, (1994) MyoD expression marks the onset of skeletal myogenesis in Myf-5 mutant mice. Development 120: 3083-3092.
13. Rudnicki M, Jaenisch R, (1995) The MyoD family of transcription factors and skeletal myogenesis. BioEssays 17: 203-209.
14. Naya FJ, Olson E, (1999) MEF2: a transcriptional target for signaling pathways controlling skeletal muscle growth and differentiation. Curr Opin Cell Biol 11: 683-688.
15. Wasserman WW, Fickett JW, (1998) Identification of regulatory regions which confer muscle-specific gene expression. J Mol Biol 278: 167-181.
16. Angus LM, Chan RY, Jasmin BJ, (2001) Role of intronic E- and N-box motifs in the transcriptional induction of the acetylcholinesterase gene during myogenic differentiation. J Biol Chem 276: 17603-17609.
17. Zheng Z, Wang Z-M, Delbono O, (2002) Charge movement and transcription regulation of L-type calcium channel 1S in skeletal muscle cells. J Physiol 540: 397-409.
18. Alkema WB, Johansson O, Lagergren J, Wasserman WW, (2004) MSCAN: identification of functional clusters of transcription factor binding sites. Nucleic Acids Res 32: W195-W198.
19. Frith MC, Li MC, Weng Z, (2003) Cluster-Buster: Finding dense clusters of motifs in DNA sequences. Nucleic Acids Res 31: 3666-3668.
20. Blanchette M, Tompa M, (2002) Discovery of regulatory elements by a computational method for phylogenetic footprinting. Genome Res 12: 739-748.
21. Sinha S, Liang Y, Siggia E, (2006) Stubb: a program for discovery and analysis of cis-regulatory modules. Nucleic Acids Res 34: W555-W559.
22. Warner JB, Philippakis AA, Jaeger SA, He FS, Lin J, et al. (2008) Systematic identification of mammalian regulatory motifs' target genes and functions. Nat Methods 5: 347-353.
23. Gumucio DL, Heilstedt-Williamson H, Gray TA, Tarlé SA, Shelton DA, et al. (1992) Phylogenetic footprinting reveals a nuclear protein which binds to silencer sequences in the human gamma and epsilon globin genes. Mol Cell Biol 12: 4919-4929.
24. Shelton DA, Stegman L, Hardison R, Miller W, Bock JH, et al. (1997) Phylogenetic footprinting of hypersensitive site 3 of the beta-globin locus control region. Blood 89: 3457-3469.
25. Chalfie M, Tu Y, Euskirchen G, Ward WW, Prasher DC, (1994) Green fluorescent protein as a marker for gene expression. Science 263: 802-805.
26. Cooper SJ, Trinklein ND, Anton ED, Nguyen L, Myers RM, (2006) Comprehensive analysis of transcriptional promoter structure and function in 1% of the human genome. Genome Res 16: 1-10.
27. Pennacchio LA, Ahituv N, Moses AM, Prabhakar S, Nobrega MA, et al. (2006) In vivo enhancer analysis of human conserved non-coding sequences. Nature 444: 499-502.
28. Kappen C, Salbaum JM, (2009) Identification of regulatory elements in the Isl1 gene locus. Int J Dev Biol 53: 935-946.
29. Portales-Casamar E, Swanson DJ, Liu L, de Leeuw CN, Banks KG, et al. (2010) A regulatory toolbox of MiniPromoters to drive selective expression in the brain. Proc Natl Acad Sci U S A 107: 16589-16594.
30. Ho Sui SJ, Mortimer JR, Arenillas DJ, Brumm J, Walsh CJ, et al. (2005) oPOSSUM: identification of over-represented transcription factor binding sites in co-expressed genes. Nucleic Acids Res 33: 3154-3164.
31. Kawaji H, Kasukawa T, Fukuda S, Katayama S, Kai C, et al. (2006) CAGE Basic/Analysis Databases: the CAGE resource for comprehensive promoter analysis. Nucleic Acids Res 34: D632-D636.
32. Sandelin A, Alkema WB, Engström P, Wasserman WW, Lenhard B, (2004) JASPAR: an open-access database for eukaryotic transcription factor binding profiles. Nucleic Acids Res 32: D91-D94.
33. Karolchik D, Kuhn RM, Baertsch R, Barber GP, Clawson H, et al. (2008) The UCSC Genome Browser Database: 2008 update. Nucleic Acids Res 36: D773-D779.
34. Cao Y, Yao Z, Sarkar D, Lawrence M, Sanchez GJ, et al. (2010) Genome-wide MyoD binding in skeletal muscle cells: a potential for broad cellular reprogramming. Dev Cell 18: 662-674.
35. Asp P, Blum R, Vethantham V, Parisi F, Micsinai M, et al. (2011) Genome-wide remodeling of the epigenetic landscape during myogenic differentiation. Proc Natl Acad Sci U S A 108: E149-58.
36. Sandelin A, Höglund A, Lenhard B, Wasserman WW, (2003) Integrated analysis of yeast regulatory sequences for biologically linked clusters of genes. Funct Integr Genomics 3: 125-134.
37. Rozen S, Skaletsky H, (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
38. R Development Core TeamTeam RDC, editor (2008) R: A Language and Environment for Statistical Computing. Vienna, Austria R Foundation for Statistical Computing.
39. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M, (2002) Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18: S96-S104.
40. Tusher VG, Tibshirani R, Chu G, (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
41. Kolbe D, Taylor J, Elnitski L, Eswara P, Li J, et al. (2004) Regulatory Potential Scores From Genome-Wide Three-Way Alignments of Human, Mouse, and Rat. Genome Res 14: 700-707 doi:10.1101/gr.1976004.mouse.
42. Moran JL, Li Y, Hill AA, Mounts WM, Miller CP, (2002) Gene expression changes during mouse skeletal myoblast differentiation revealed by transcriptional profiling. Physiol Genomics 10: 103-111.
43. Tomczak KK, Marinescu VD, Ramoni MF, Sanoudou D, Montanaro F, et al. (2004) Expression profiling and identification of novel genes involved in myogenic differentiation. FASEB J 18: 403-405.
44. Blais A, Tsikitis M, Acosta-Alvear D, Sharan R, Kluger Y, et al. (2005) An initial blueprint for myogenic differentiation. Genes Dev 19: 553-569.
45. Kislinger T, Gramolini AO, Pan Y, Rahman K, MacLennan DH, et al. (2005) Proteome dynamics during C2C12 myoblast differentiation. Mol Cell Proteomics 4: 887-901.
46. Li Z, Marchand P, Humbert J, Babinet C, Paulin D, (1993) Desmin sequence elements regulating skeletal muscle-specific expression in transgenic mice. Development 117: 947-959.
47. Gao J, Li Z, Paulin D, (1998) A novel site, Mt, in the human desmin enhancer is necessary for maximal expression in skeletal muscle. J Biol Chem 273: 6402-6409.
48. Mullen a J, Barton PJ, (2000) Structural characterization of the human fast skeletal muscle troponin I gene (TNNI2). Gene 242: 313-320.
49. Chen K-J, Chao H-K, Hsiao K-J, Su T-S, (2002) Identification and characterization of a novel liver-specific enhancer of the human phenylalanine hydroxylase gene. Hum Genet 110: 235-243.
50. Pan D, Courey AJ, (1992) The same dorsal binding site mediates both activation and repression in a context-dependent manner. EMBO J 11: 1837-1842.
51. Brown L, Baer R, (1994) HEN1 encodes a 20-kilodalton phosphoprotein that binds an extended E-box motif as a homodimer. Mol Cell Biol 14: 1245-1255.
52. Thiagalingam A, De Bustros A, Borges M, Jasti R, Compton D, et al. (1996) RREB-1, a novel zinc finger protein, is involved in the differentiation response to Ras in human medullary thyroid carcinomas. Mol Cell Biol 16: 5335-5345.
53. Portales-Casamar E, Kirov S, Lim J, Lithwick S, Swanson MI, et al. (2007) PAZAR: a framework for collection and dissemination of cis-regulatory sequence annotation. Genome Biol 8: R207.
54. Sing T, Sander O, Beerenwinkel N, Lengauer T, (2005) ROCR: visualizing classifier performance in R. Bioinformatics 21: 3940-3941.
55. Saxonov S, Berg P, Brutlag DL, (2006) A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters. Proc Natl Acad Sci U S A 103: 1412-1417.
56. Cheng Y, King DC, Dore LC, Zhang X, Zhou Y, et al. (2008) Transcriptional enhancement by GATA1-occupied DNA segments is strongly associated with evolutionary constraint on the binding site motif. Genome Res 18: 1896-1905.
57. Stankunas K, Shang C, Twu KY, Kao S-C, Jenkins Na, et al. (2008) Pbx/Meis deficiencies demonstrate multigenetic origins of congenital heart disease. Circ Res 103: 702-709.
58. Goecks J, Nekrutenko A, Taylor J, Galaxy Team T (2010) Galaxy: a comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11: R86.
59. Fischer JJ, Toedling J, Krueger T, Schueler M, Huber W, et al. (2008) Combinatorial effects of four histone modifications in transcription and differentiation. Genomics 91: 41-51.
60. Francastel C, Schübeler D, Martin DI, Groudine M, (2000) Nuclear compartmentalization and gene activity. Nat Rev Mol Cell Biol 1: 137-143.
61. Gregory PD, (2001) Transcription and chromatin converge: lessons from yeast genetics. Curr Opin Genet Dev 11: 142-147.
62. Georgel PT, (2002) Chromatin structure of eukaryotic promoters: a changing perspective. Biochem Cell Biol 80: 295-300.
63. Fischle W, Wang Y, Allis CD, Ã WF, Ã YW, (2003) Histone and chromatin cross-talk. Curr Opin Cell Biol 15: 172-183.
64. Bina M, Wyss P, Lazarus SA, Shah SR, Ren W, et al. (2009) Discovering sequences with potential regulatory characteristics. Genomics 93: 314-322.
65. Evans KJ, (2010) Most transcription factor binding sites are in a few mosaic classes of the human genome. BMC Genomics 11: 286.
66. Hannenhalli S, Levy S, (2001) Promoter prediction in the human genome. Bioinformatics 17 (Suppl 1): S90-S96.
67. Kiełbasa SM, Klein H, Roider HG, Vingron M, Blüthgen N, (2010) TransFind-predicting transcriptional regulators for gene sets. Nucleic Acids Res 38: W275-W280.
68. He X, Ling X, Sinha S, (2009) Alignment and prediction of cis-regulatory modules based on a probabilistic model of evolution. PLoS Comput Biol 5: e1000299.