A simple metric of promoter architecture robustly predicts expression breadth of human genes suggesting that most transcription factors are positive regulators

Genome Biology

Volumn 15, Issue 7, 2014, Pages

  Hurst, Laurence D ^a   Sachenkova, Oxana ^b,c   Daub, Carsten ^c   Forrest, Alistair R R ^d   Huminiecki, Lukasz ^b,c,e,f,g  

^a University of Bath   (United Kingdom)

^b STOCKHOLM UNIVERSITY   (Sweden)

^c SCIENCE FOR LIFE LABORATORY   (Sweden)

^d RIKEN   (Japan)

^e KAROLINSKA INSTITUTE   (Sweden)

^f Bioinformatics Infrastructure for Life Sciences (BILS)   (Sweden)

^g UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; CONTROLLED STUDY; EUKARYOTE; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MACHINE LEARNING; PREDICTION; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; BIOLOGICAL MODEL; BIOLOGY; GENETIC DATABASE; GENETICS; MOLECULAR EVOLUTION; PROCEDURES; SUPPORT VECTOR MACHINE;

BINDING SITES; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; EVOLUTION, MOLECULAR; GENE EXPRESSION REGULATION; HUMANS; MODELS, GENETIC; PROMOTER REGIONS, GENETIC; SUPPORT VECTOR MACHINE; TRANSCRIPTION FACTORS;

EID: 84956964144     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-014-0413-3     Document Type: Article

References (56)

1. Makova KD, Li WH: Divergence in the spatial pattern of gene expression between human duplicate genes. Genome Res 2003, 13:1638-1645.
2. Huminiecki L, Wolfe KH: Divergence of spatial gene expression profiles following species-specific gene duplications in human and mouse. Genome Res 2004, 14:1870-1879.
3. Struhl K: Fundamentally different logic of gene regulation in eukaryotes and prokaryotes. Cell 1999, 98:1-4.
4. Ptashne MGA: Genes and signals. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press; 2002.
5. Segal E, Raveh-Sadka T, Schroeder M, Unnerstall U, Gaul U: Predicting expression patterns from regulatory sequence in Drosophila segmentation. Nature 2008, 451:535-540.
6. Tirosh I, Weinberger A, Bezalel D, Kaganovich M, Barkai N: On the relation between promoter divergence and gene expression evolution. Mol Syst Biol 2008, 4:159.
7. Ge Y, Porse BT: The functional consequences of intron retention: Alternative splicing coupled to NMD as a regulator of gene expression. Bioessays 2013, 36:236-243.
8. Stroynowska-Czerwinska A, Fiszer A, Krzyzosiak WJ: The panorama of miRNA-mediated mechanisms in mammalian cells. Cell Mol Life Sci 2014, 71:2253-2270.
9. Cheadle C, Fan J, Cho-Chung YS, Werner T, Ray J, Do L, Gorospe M, Becker KG: Control of gene expression during T cell activation: alternate regulation of mRNA transcription and mRNA stability. BMC Genomics 2005, 6:75.
10. Gilbert N, Boyle S, Fiegler H, Woodfine K, Carter NP, Bickmore WA: Chromatin architecture of the human genome: Gene-rich domains are enriched in open chromatin fibers. Cell 2004, 118:555-566.
11. Chen T, Dent SY: Chromatin modifiers and remodellers: regulators of cellular differentiation. Nat Rev Genet 2014, 15:93-106.
12. Agalioti T, Chen G, Thanos D: Deciphering the transcriptional histone acetylation code for a human gene. Cell 2002, 111:381-392.
13. Gierman HJ, Indemans MH, Koster J, Goetze S, Seppen J, Geerts D, van Driel R, Versteeg R: Domain-wide regulation of gene expression in the human genome. Genome Res 2007, 17:1286-1295.
14. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S: Stochastic mRNA synthesis in mammalian cells. Plos Biology 2006, 4:e309.
15. Ebisuya M, Yamamoto T, Nakajima M, Nishida E: Ripples from neighbouring transcription. Nat Cell Biol 2008, 10:1106-1113.
16. Batada NN, Urrutia AO, Hurst LD: Chromatin remodelling is a major source of coexpression of linked genes in yeast. Trends Genet: TIG 2007, 23:480-484.
17. Park J, Xu K, Park T, Yi SV: What are the determinants of gene expression levels and breadths in the human genome?. Hum Mol Genet 2012, 21:46-56.
18. Illingworth RS, Bird AP: CpG islands -'a rough guide'. FEBS Lett 2009, 583:1713-1720.
19. Borneman AR, Gianoulis TA, Zhang ZD, Yu H, Rozowsky J, Seringhaus MR, Wang LY, Gerstein M, Snyder M: Divergence of transcription factor binding sites across related yeast species. Science 2007, 317:815-819.
20. Park C, Makova KD: Coding region structural heterogeneity and turnover of transcription start sites contribute to divergence in expression between duplicate genes. Genome Biol 2009, 10:R10.
21. Zhang Z, Gu J, Gu X: How much expression divergence after yeast gene duplication could be explained by regulatory motif evolution? Trends Genet 2004, 20:403-407.
22. Papp B, Pal C, Hurst LD: Evolution of cis-regulatory elements in duplicated genes of yeast. Trends Genet 2003, 19:417-422.
23. Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F, Epstein CB, Frietze S, Harrow J, Kaul R, Khatun J, Lajoie BR, Landt SG, Lee BK, Pauli F, Rosenbloom KR, Sabo P, Safi A, Sanyal A, Shoresh N, Simon JM, Song L, Trinklein ND, Altshuler RC, Birney E, Brown JB, Cheng C, Djebali S, Dong X, Ernst J, et al: An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74.
24. Landt SG, Marinov GK, Kundaje A, Kheradpour P, Pauli F, Batzoglou S, Bernstein BE, Bickel P, Brown JB, Cayting P, Chen Y, DeSalvo G, Epstein C, Fisher-Aylor KI, Euskirchen G, Gerstein M, Gertz J, Hartemink AJ, Hoffman MM, Iyer VR, Jung YL, Karmakar S, Kellis M, Kharchenko PV, Li Q, Liu T, Liu XS, Ma L, Milosavljevic A, Myers RM, et al: ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res 2012, 22:1813-1831.
25. ENCODE-TfbsV2. [http://hgdownload.cse.ucsc.edu/goldenPath/hg19/encode DCC/wgEncodeRegTfbsClustered/wgEncodeRegTfbsClusteredV2.bed]
26. ENCODE-TfbsV3. [http://hgdownload.cse.ucsc.edu/goldenPath/hg19/encode DCC/wgEncodeRegTfbsClustered/wgEncodeRegTfbsClusteredV3.bed]
27. Forrest AR, Kawaji H, Rehli M, Baillie JK, de Hoon MJ, Lassmann T, Itoh M, Summers KM, Suzuki H, Daub CO, Kawai J, Heutink P, Hide W, Freeman TC, Lenhard B, Bajic VB, Taylor MS, Makeev VJ, Sandelin A, Hume DA, Carninci P, Hayashizaki Y: A promoter-level mammalian expression atlas. Nature 2014, 507:462-470.
28. Velculescu VE, Madden SL, Zhang L, Lash AE, Yu J, Rago C, Lal A, Wang CJ, Beaudry GA, Ciriello KM, Cook BP, Dufault MR, Ferguson AT, Gao Y, He TC, Hermeking H, Hiraldo SK, Hwang PM, Lopez MA, Luderer HF, Mathews B, Petroziello JM, Polyak K, Zawel L, Kinzler KW: Analysis of human transcriptomes. Nat Genet 1999, 23:387-388.
29. Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, Greven MC, Pierce BG, Dong X, Kundaje A, Cheng Y, Rando OJ, Birney E, Myers RM, Noble WS, Snyder M, Weng Z: Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res 2012, 22:1798-1812.
30. Spivakov M, Akhtar J, Kheradpour P, Beal K, Girardot C, Koscielny G, Herrero J, Kellis M, Furlong EE, Birney E: Analysis of variation at transcription factor binding sites in Drosophila and humans. Genome Biol 2012, 13:R49.
31. ENCODE-InputsV2. [http://hgdownload.cse.ucsc.edu/goldenPath/hg19/encode DCC/wgEncodeRegTfbsClustered/wgEncodeRegTfbsClusteredInputs.tab.gz]
32. ENCODE-InputsV3. [http://hgdownload.cse.ucsc.edu/goldenPath/hg19/encodeDCC/wgEncodeRegTfbsClustered/wgEncodeRegTfbsClustered InputsV3.tab.gz]
33. Jordan IK, Marino-Ramirez L, Koonin EV: Evolutionary significance of gene expression divergence. Gene 2005, 345:119-126.
34. Pereira V, Waxman D, Eyre-Walker A: A problem with the correlation coefficient as a measure of gene expression divergence. Genetics 2009, 183:1597-1600.
35. Piasecka B, Robinson-Rechavi M, Bergmann S: Correcting for the bias due to expression specificity improves the estimation of constrained evolution of expression between mouse and human. Bioinformatics 2012, 28:1865-1872.
36. He X, Zhang J: Higher duplicability of less important genes in yeast genomes. Mol Biol Evol 2006, 23:144-151.
37. Woods S, Coghlan A, Rivers D, Warnecke T, Jeffries SJ, Kwon T, Rogers A, Hurst LD, Ahringer J: Duplication and Retention Biases of Essential and Non-Essential Genes Revealed by Systematic Knockdown Analyses. Plos Genetics 2013, 9:e1003330.
38. Gu Z, Nicolae D, Lu HH, Li WH: Rapid divergence in expression between duplicate genes inferred from microarray data. Trends Genet 2002, 18:609-613.
39. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, Wong KY, Sung KW, Lee CW, Zhao XD, Chiu KP, Lipovich L, Kuznetsov VA, Robson P, Stanton LW, Wei CL, Ruan Y, Lim B, Ng HH: The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 2006, 38:431-440.
40. Gause M, Schaaf CA, Dorsett D: Cohesin and CTCF: cooperating to control chromosome conformation? Bioessays 2008, 30:715-718.
41. Wendt KS, Peters JM: How cohesin and CTCF cooperate in regulating gene expression. Chromosome Res 2009, 17:201-214.
42. Factorbook. [http://www.factorbook.org/mediawiki/index.php/Welcome_to_factorbook]
43. Su AI, Cooke MP, Ching KA, Hakak Y, Walker JR, Wiltshire T, Orth AP, Vega RG, Sapinoso LM, Moqrich A, Patapoutian A, Hampton GM, Schultz PG, Hogenesch JB: Large-scale analysis of the human and mouse transcriptomes. Proc Natl Acad Sci U S A 2002, 99:4465-4470.
44. WP4 expression tables. [https://fantom5-collaboration.gsc.riken.jp/files/data/shared/contrib/110120-gene_expression_table-WP4/UPDATE_011/]
45. Primary FANTOM5 CAGE data. [http://fantom.gsc.riken.jp/5/datafiles/phase1.0/basic/]
46. Dnase sites slustered. [http://hgdownload.cse.ucsc.edu/goldenPath/hg19/encodeDCC/wgEncodeRegDnaseClustered/wgEncodeRegDnaseClusteredV2.bed.gz]
47. Dnase-Inputs. [http://hgdownload.cse.ucsc.edu/goldenPath/hg19/encode DCC/wgEncodeRegDnaseClustered/wgEncodeRegDnaseClusteredInputsV2.tab.gz]
48. Methylation in HeLa. [http://hgdownload.cse.ucsc.edu/goldenPath/hg19/encodeDCC/wgEncodeHaibMethyl450/wgEncodeHaibMethyl450Helas3Sites Rep1.bed.gz]
49. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB: A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci U S A 2004, 101:6062-6067.
50. Favorov A, Mularoni L, Cope LM, Medvedeva Y, Mironov AA, Makeev VJ, Wheelan SJ: Exploring massive, genome scale datasets with the GenometriCorr package. PLoS Comput Biol 2012, 8:e1002529.
51. Quinlan AR, Hall IM: BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 2010, 26:841-842.
52. Li H, Coghlan A, Ruan J, Coin LJ, Heriche JK, Osmotherly L, Li R, Liu T, Zhang Z, Bolund L, Wong GK, Zheng W, Dehal P, Wang J, Durbin R: TreeFam: a curated database of phylogenetic trees of animal gene families. Nucleic Acids Res 2006, 34:D572-D580.
53. Huminiecki L, Goldovsky L, Freilich S, Moustakas A, Ouzounis C, Heldin CH: Emergence, development and diversification of the TGF-beta signalling pathway within the animal kingdom. BMC Evol Biol 2009, 9:28.
54. Huminiecki L, Heldin CH: 2R and remodeling of vertebrate signal transduction engine. BMC Biol 2010, 8:146.
55. Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
56. The Duplicator. [https://github.com/LukaszHuminiecki/bioCode/tree/master/duplicator]