Transcriptional enhancers in protein-coding exons of vertebrate developmental genes

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Ritter, Deborah I ^a,c   Dong, Zhiqiang ^b   Guo, Su ^b   Chuang, Jeffrey H ^a  

^a BOSTON COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GREEN FLUORESCENT PROTEIN; HISTONE;

ARTICLE; AUTOREGULATION; CONTROLLED STUDY; DEVELOPMENTAL GENE; EMBRYO; EXON; GENE EXPRESSION; GENE SEQUENCE; GENETIC CODE; GENETIC CONSERVATION; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; NONHUMAN; PROMOTER REGION; TISSUE SPECIFICITY; TRANSPOSON; ZEBRA FISH; ANIMAL; ENHANCER REGION; GENETICS; HUMAN; VERTEBRATE;

DANIO RERIO; VERTEBRATA;

ANIMALS; ENHANCER ELEMENTS, GENETIC; EXONS; GENES, DEVELOPMENTAL; HUMANS; VERTEBRATES; ZEBRAFISH;

EID: 84860469898     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035202     Document Type: Article

References (90)

1. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, et al. (2004) Ultraconserved elements in the human genome. Science 304 (5675): 1321-1325.
2. Pennacchio LA, Loots GG, Nobrega MA, Ovcharenko I, (2007) Predicting tissue-specific enhancers in the human genome. Genome Res 17 (2): 201-211.
3. Li Q, Ritter D, Yang N, Dong Z, Li H, et al. (2010) A systematic approach to identify functional motifs within vertebrate developmental enhancers. Dev Biol 337 (2): 484-495.
4. Loots GG, (2008) Chapter 10 genomic identification of regulatory elements by evolutionary sequence comparison and functional analysis. Adv Genet 61: 269-293.
5. Woolfe A, Goodson M, Goode DK, Snell P, McEwen GK, et al. (2005) Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol 3 (1): e7.
6. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15 (8): 1034-1050.
7. Navratilova P, Fredman D, Hawkins TA, Turner K, Lenhard B, et al. (2009) Systematic human/zebrafish comparative identification of cis-regulatory activity around vertebrate developmental transcription factor genes. Dev Biol 327 (2): 526-540.
8. Muller F, Chang B, Albert S, Fischer N, Tora L, et al. (1999) Intronic enhancers control expression of zebrafish sonic hedgehog in floor plate and notochord. Development 126 (10): 2103-2116.
9. Itzkovitz S, Alon U, (2007) The genetic code is nearly optimal for allowing additional information within protein-coding sequences. Genome Res 17 (4): 405-412.
10. Kural D, Ding Y, Wu J, Korpi AM, Chuang JH, (2009) COMIT: Identification of noncoding motifs under selection in coding sequences. Genome Biol 10 (11): R133.
11. Goren A, Ram O, Amit M, Keren H, Lev-Maor G, et al. (2006) Comparative analysis identifies exonic splicing regulatory sequences-the complex definition of enhancers and silencers. Mol Cell 22 (6): 769-781.
12. Cawley S, Bekiranov S, Ng HH, Kapranov P, Sekinger EA, et al. (2004) Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 116 (4): 499-509.
13. Macquarrie KL, Fong AP, Morse RH, Tapscott SJ, (2011) Genome-wide transcription factor binding: Beyond direct target regulation. Trends Genet.
14. Visel A, Blow MJ, Li Z, Zhang T, Akiyama JA, et al. (2009) ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457 (7231): 854-858.
15. Li XY, MacArthur S, Bourgon R, Nix D, Pollard DA, et al. (2008) Transcription factors bind thousands of active and inactive regions in the drosophila blastoderm. PLoS Biol 6 (2): e27.
16. 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 (7118): 499-502.
17. Barthel KK, Liu X, (2008) A transcriptional enhancer from the coding region of ADAMTS5. PLoS One 3 (5): e2184.
18. Chen HP, Lin A, Bloom JS, Khan AH, Park CC, et al. (2008) Screening reveals conserved and nonconserved transcriptional regulatory elements including an E3/E4 allele-dependent APOE coding region enhancer. Genomics 92 (5): 292-300.
19. Lang G, Gombert WM, Gould HJ, (2005) A transcriptional regulatory element in the coding sequence of the human bcl-2 gene. Immunology 114 (1): 25-36.
20. Tumpel S, Cambronero F, Sims C, Krumlauf R, Wiedemann LM, (2008) A regulatory module embedded in the coding region of Hoxa2 controls expression in rhombomere 2. Proc Natl Acad Sci U S A 105 (51): 20077-20082.
21. Lampe X, Samad OA, Guiguen A, Matis C, Remacle S, et al. (2008) An ultraconserved hox-pbx responsive element resides in the coding sequence of Hoxa2 and is active in rhombomere 4. Nucleic Acids Res 36 (10): 3214-3225.
22. Suzuki R, Saitou N, (2011) Exploration for functional nucleotide sequence candidates within coding regions of mammalian genes. DNA Res 18 (3): 177-187.
23. Kimura M, (1979) The neutral theory of molecular evolution. Sci Am 241(5) 98-100, 102, 108 passim.
24. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A, (2010) Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20 (1): 110-121.
25. Shin JT, Priest JR, Ovcharenko I, Ronco A, Moore RK, et al. (2005) Human-zebrafish non-coding conserved elements act in vivo to regulate transcription. Nucleic Acids Res 33 (17): 5437-5445.
26. 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 (5771): 276-279.
27. Kikuta H, Kawakami K, (2009) Transient and stable transgenesis using tol2 transposon vectors. Methods Mol Biol 546: 69-84.
28. Reinhard E, Nedivi E, Wegner J, Skene JH, Westerfield M, (1994) Neural selective activation and temporal regulation of a mammalian GAP-43 promoter in zebrafish. Development 120 (7): 1767-1775.
29. Hufton AL, Mathia S, Braun H, Georgi U, Lehrach H, et al. (2009) Deeply conserved chordate noncoding sequences preserve genome synteny but do not drive gene duplicate retention. Genome Res 19 (11): 2036-2051.
30. Fort A, Fish RJ, Attanasio C, Dosch R, Visel A, et al. (2011) A liver enhancer in the fibrinogen gene cluster. Blood 117 (1): 276-282.
31. Ritter DI, Li Q, Kostka D, Pollard KS, Guo S, et al. (2010) The importance of being cis: Evolution of orthologous fish and mammalian enhancer activity. Mol Biol Evol 27 (10): 2322-2332.
32. Sanges R, Kalmar E, Claudiani P, D'Amato M, Muller F, et al. (2006) Shuffling of cis-regulatory elements is a pervasive feature of the vertebrate lineage. Genome Biol 7 (7): R56.
33. Navratilova P, Fredman D, Lenhard B, Becker TS, (2010) Regulatory divergence of the duplicated chromosomal loci sox11a/b by subpartitioning and sequence evolution of enhancers in zebrafish. Mol Genet Genomics 283 (2): 171-184.
34. McGaughey DM, Vinton RM, Huynh J, Al-Saif A, Beer MA, et al. (2008) Metrics of sequence constraint overlook regulatory sequences in an exhaustive analysis at phox2b. Genome Res 18 (2): 252-260.
35. Sprague J, Bayraktaroglu L, Clements D, Conlin T, Fashena D, et al. (2006) The zebrafish information network: The zebrafish model organism database. Nucleic Acids Res 34(Database issue) pp. D581-5.
36. Wang K, Diskin SJ, Zhang H, Attiyeh EF, Winter C, et al. (2011) Integrative genomics identifies LMO1 as a neuroblastoma oncogene. Nature 469 (7329): 216-220.
37. Eagleson GW, Theisen S, (2008) Stage-specific effects of retinoic acid on gene expression during forebrain development. Brain Res Bull 75 (2-4): 281-288.
38. McGrath MF, de Bold AJ, (2009) Transcriptional analysis of the mammalian heart with special reference to its endocrine function. BMC Genomics 10: 254.
39. Cao F, Wagner RA, Wilson KD, Xie X, Fu JD, et al. (2008) Transcriptional and functional profiling of human embryonic stem cell-derived cardiomyocytes. PLoS One 3 (10): e3474.
40. de Pater E, Clijsters L, Marques SR, Lin YF, Garavito-Aguilar ZV, et al. (2009) Distinct phases of cardiomyocyte differentiation regulate growth of the zebrafish heart. Development 136 (10): 1633-1641.
41. Jopling C, Sleep E, Raya M, Marti M, Raya A, et al. (2010) Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation. Nature 464 (7288): 606-609.
42. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, et al. (2010) Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 107 (50): 21931-21936.
43. Heintzman ND, Hon GC, Hawkins RD, Kheradpour P, Stark A, et al. (2009) Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459 (7243): 108-112.
44. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, et al. (2007) Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 39 (3): 311-318.
45. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, et al. (2010) A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol 8 (5): e1000384.
46. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, et al. (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465 (7295): 182-187.
47. Hon GC, Hawkins RD, Ren B, (2009) Predictive chromatin signatures in the mammalian genome. Hum Mol Genet 18 (R2): R195-201.
48. Aday AW, Zhu LJ, Lakshmanan A, Wang J, Lawson ND, (2011) Identification of cis regulatory features in the embryonic zebrafish genome through large-scale profiling of H3K4me1 and H3K4me3 binding sites. Dev Biol.
49. Pruitt KD, Harrow J, Harte RA, Wallin C, Diekhans M, et al. (2009) The consensus coding sequence (CCDS) project: Identifying a common protein-coding gene set for the human and mouse genomes. Genome Res 19 (7): 1316-1323.
50. ENCODE Project Consortium, Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, et al. (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447 (7146): 799-816.
51. Grogan SP, Olee T, Hiraoka K, Lotz MK, (2008) Repression of chondrogenesis through binding of notch signaling proteins HES-1 and HEY-1 to N-box domains in the COL2A1 enhancer site. Arthritis Rheum 58 (9): 2754-2763.
52. Li AG, Piluso LG, Cai X, Gadd BJ, Ladurner AG, et al. (2007) An acetylation switch in p53 mediates holo-TFIID recruitment. Mol Cell 28 (3): 408-421.
53. Euskirchen GM, Auerbach RK, Davidov E, Gianoulis TA, Zhong G, et al. (2011) Diverse roles and interactions of the SWI/SNF chromatin remodeling complex revealed using global approaches. PLoS Genet 7 (3): e1002008.
54. Tang H, Sharp PA, (1999) Transcriptional regulation of the murine 3′ IgH enhancer by OCT-2. Immunity 11 (5): 517-526.
55. Wood LJ, Mukherjee M, Dolde CE, Xu Y, Maher JF, et al. (2000) HMG-I/Y, a new c-myc target gene and potential oncogene. Mol Cell Biol 20 (15): 5490-5502.
56. Winkler C, Elmasri H, Klamt B, Volff JN, Gessler M, (2003) Characterization of hey bHLH genes in teleost fish. Dev Genes Evol 213 (11): 541-553.
57. Pelengaris S, Khan M, Evan G, (2002) c-MYC: More than just a matter of life and death. Nat Rev Cancer 2 (10): 764-776.
58. Maile T, Kwoczynski S, Katzenberger RJ, Wassarman DA, Sauer F, (2004) TAF1 activates transcription by phosphorylation of serine 33 in histone H2B. Science 304 (5673): 1010-1014.
59. Singhal N, Graumann J, Wu G, Arauzo-Bravo MJ, Han DW, et al. (2010) Chromatin-remodeling components of the BAF complex facilitate reprogramming. Cell 141 (6): 943-955.
60. Phillips K, Luisi B, (2000) The virtuoso of versatility: POU proteins that flex to fit. J Mol Biol 302 (5): 1023-1039.
61. Lareau LF, Inada M, Green RE, Wengrod JC, Brenner SE, (2007) Unproductive splicing of SR genes associated with highly conserved and ultraconserved DNA elements. Nature 446 (7138): 926-929.
62. Dong X, Navratilova P, Fredman D, Drivenes O, Becker TS, et al. (2010) Exonic remnants of whole-genome duplication reveal cis-regulatory function of coding exons. Nucleic Acids Res 38 (4): 1071-1085.
63. Fox AK, Tuch BB, Chuang JH, (2008) Measuring the prevalence of regional mutation rates: An analysis of silent substitutions in mammals, fungi, and insects. BMC Evol Biol 8: 186.
64. Birnbaum RY, Clowney EJ, Agamy O, Kim MJ, Zhao J, et al. (3546) 111.
65. Ng PC, Henikoff S, (2006) Predicting the effects of amino acid substitutions on protein function. Annu Rev Genomics Hum Genet 7: 61-80.
66. Guo HH, Choe J, Loeb LA, (2004) Protein tolerance to random amino acid change. Proc Natl Acad Sci U S A 101 (25): 9205-9210.
67. Friedli M, (2010) A systematic enhancer screen using lentivector transgenesis identifies conserved and non-conserved functional elements at the Olig1 and Olig2 locus ONE Alerts. 10.1371/journal.pone.0015741. Available: www.refworks.com via the Internet.
68. Schattner P, Diekhans M, (2006) Regions of extreme synonymous codon selection in mammalian genes. Nucleic Acids Res 34 (6): 1700-1710.
69. Rubinstein ND, Doron-Faigenboim A, Mayrose I, Pupko T, (2011) Evolutionary models accounting for layers of selection in protein-coding genes and their impact on the inference of positive selection. Mol Biol Evol 28 (12): 3297-3308.
70. Berman BP, Pfeiffer BD, Laverty TR, Salzberg SL, Rubin GM, et al. (2004) Computational identification of developmental enhancers: Conservation and function of transcription factor binding-site clusters in drosophila melanogaster and drosophila pseudoobscura. Genome Biol 5 (9): R61.
71. Lee D, Karchin R, Beer MA, (2011) Discriminative prediction of mammalian enhancers from DNA sequence. Genome Res 21 (12): 2167-2180.
72. Oulion S, Debiais-Thibaud M, d'Aubenton-Carafa Y, Thermes C, Da Silva C, et al. (2010) Evolution of hox gene clusters in gnathostomes: Insights from a survey of a shark (scyliorhinus canicula) transcriptome. Mol Biol Evol 27 (12): 2829-2838.
73. Kudla G, Murray AW, Tollervey D, Plotkin JB, (2009) Coding-sequence determinants of gene expression in escherichia coli. Science 324 (5924): 255-258.
74. Kikuta H, Laplante M, Navratilova P, Komisarczuk AZ, Engstrom PG, et al. (2007) Genomic regulatory blocks encompass multiple neighboring genes and maintain conserved synteny in vertebrates. Genome Res 17 (5): 545-555.
75. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, et al. (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143 (1): 46-58.
76. Brest P, Lapaquette P, Souidi M, Lebrigand K, Cesaro A, et al. (2011) A synonymous variant in IRGM alters a binding site for miR-196 and causes deregulation of IRGM-dependent xenophagy in crohn's disease. Nat Genet 43 (3): 242-245.
77. Ho PA, Kuhn J, Gerbing RB, Pollard JA, Zeng R, et al. (2011) WT1 synonymous single nucleotide polymorphism rs16754 correlates with higher mRNA expression and predicts significantly improved outcome in favorable-risk pediatric acute myeloid leukemia: A report from the children's oncology group. J Clin Oncol 29 (6): 704-711.
78. Fung KL, Gottesman MM, (2009) A synonymous polymorphism in a common MDR1 (ABCB1) haplotype shapes protein function. Biochim Biophys Acta 1794 (5): 860-871.
79. Flicek P, Amode MR, Barrell D, Beal K, Brent S, et al. (2011) Ensembl 2011. Nucleic Acids Res 39(Database issue) pp. D800-6.
80. Fujita PA, Rhead B, Zweig AS, Hinrichs AS, Karolchik D, et al. (2011) The UCSC genome browser database: Update 2011. Nucleic Acids Res 39(Database issue) pp. D876-82.
81. Goecks J, Nekrutenko A, Taylor J, Galaxy Team (2010) Galaxy: A comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11 (8): R86.
82. Rozen S, Skaletsky H, (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132: 365-386.
83. Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, et al. (2004) A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 7 (1): 133-144.
84. Delporte FM, Pasque V, Devos N, Manfroid I, Voz ML, et al. (2008) Expression of zebrafish pax6b in pancreas is regulated by two enhancers containing highly conserved cis-elements bound by PDX1, PBX and PREP factors. BMC Dev Biol 8: 53.
85. Balciunas D, Wangensteen KJ, Wilber A, Bell J, Geurts A, et al. (2006) Harnessing a high cargo-capacity transposon for genetic applications in vertebrates. PLoS Genet 2 (11): e169.
86. Urasaki A, Asakawa K, Kawakami K, (2008) Efficient transposition of the Tol2 transposable element from a single-copy donor in zebrafish. Proc Natl Acad Sci U S A 105 (50): 19827-19832.
87. Chen L, Zheng J, Yang N, Li H, Guo S, (2011) Genomic selection identifies vertebrate transcription factor Fezf2 binding sites and target genes. J Biol Chem 286 (21): 18641-18649.
88. Fisher S, Grice EA, Vinton RM, Bessling SL, Urasaki A, et al. (2006) Evaluating the biological relevance of putative enhancers using Tol2 transposon-mediated transgenesis in zebrafish. Nat Protoc 1 (3): 1297-1305.
89. R Development Core Team (2008) R: A language and environment for statistical computing.
90. Quinlan AR, Hall IM, (2010) BEDTools: A flexible suite of utilities for comparing genomic features. Bioinformatics 26 (6): 841-842.