Enhanced Identification of Transcriptional Enhancers Provides Mechanistic Insights into Diseases

Trends in Genetics

Volumn 32, Issue 2, 2016, Pages 76-88

  Murakawa, Yasuhiro ^a,b   Yoshihara, Masahito ^b,c   Kawaji, Hideya ^a,b   Nishikawa, Miki ^a   Zayed, Hatem ^d   Suzuki, Harukazu ^b   Hayashizaki, Yoshihide ^a  

^a Wako Hospital   (Japan)

^b RIKEN   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d QATAR UNIVERSITY   (Qatar)

Author keywords

CAGE; Enhancer; ERNA; FANTOM

Indexed keywords

FUNCTIONAL ANNOTATION OF THE MAMMALIAN GENOME 5; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; RNA;

ACUTE LYMPHOBLASTIC LEUKEMIA; AGE RELATED MACULAR DEGENERATION; CANCER GENETICS; CHROMATIN; COLORECTAL CANCER; DISEASES; ENHANCER REGION; GENE EXPRESSION REGULATION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HIGH THROUGHPUT SEQUENCING; HISTONE MODIFICATION; HUMAN; NEXT GENERATION SEQUENCING; PRIORITY JOURNAL; REGULATOR GENE; REVIEW; RNA SEQUENCE; SOMATIC MUTATION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETIC VARIATION; GENETICS; MOLECULAR GENETICS; MUTATION; PROCEDURES;

DISEASE; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIATION; HUMANS; MOLECULAR SEQUENCE ANNOTATION; MUTATION; RNA; TRANSCRIPTION, GENETIC;

EID: 84958618144     PISSN: 01689525     EISSN: 13624555     Source Type: Journal    
DOI: 10.1016/j.tig.2015.11.004     Document Type: Review

References (100)

1. Epstein D.J. Cis-regulatory mutations in human disease. Brief. Funct. Genomic. Proteomic. 2009, 8:310-316.
2. Mathelier A., et al. Identification of altered cis-regulatory elements in human disease. Trends Genet. 2015, 31:67-76.
3. Schwanhausser B., et al. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
4. Juven-Gershon T., Kadonaga J.T. Regulation of gene expression via the core promoter and the basal transcriptional machinery. Dev. Biol. 2010, 339:225-229.
5. Ong C.T., Corces V.G. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat. Rev. Genet. 2011, 12:283-293.
6. Shlyueva D., et al. Transcriptional enhancers: from properties to genome-wide predictions. Nat. Rev. Genet. 2014, 15:272-286.
7. Banerji J., et al. Expression of a beta-globin gene is enhanced by remote SV40 DNA sequences. Cell 1981, 27:299-308.
8. Moreau P., et al. The SV40 72 base repair repeat has a striking effect on gene expression both in SV40 and other chimeric recombinants. Nucleic Acids Res. 1981, 9:6047-6068.
9. Banerji J., et al. A lymphocyte-specific cellular enhancer is located downstream of the joining region in immunoglobulin heavy chain genes. Cell 1983, 33:729-740.
10. Gillies S.D., et al. A tissue-specific transcription enhancer element is located in the major intron of a rearranged immunoglobulin heavy chain gene. Cell 1983, 33:717-728.
11. Mercola M., et al. Transcriptional enhancer elements in the mouse immunoglobulin heavy chain locus. Science 1983, 221:663-665.
12. Spitz F., Furlong E.E. Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 2012, 13:613-626.
13. Buecker C., Wysocka J. Enhancers as information integration hubs in development: lessons from genomics. Trends Genet. 2012, 28:276-284.
14. Kagey M.H., et al. Mediator and cohesin connect gene expression and chromatin architecture. Nature 2010, 467:430-435.
15. Thurman R.E., et al. The accessible chromatin landscape of the human genome. Nature 2012, 489:75-82.
16. Zhou V.W., et al. Charting histone modifications and the functional organization of mammalian genomes. Nat. Rev. Genet. 2011, 12:7-18.
17. Calo E., Wysocka J. Modification of enhancer chromatin: what, how, and why?. Mol. Cell 2013, 49:825-837.
18. Hnisz D., et al. Super-enhancers in the control of cell identity and disease. Cell 2013, 155:934-947.
19. Loven J., et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 2013, 153:320-334.
20. Whyte W.A., et al. Master transcription factors and Mediator establish super-enhancers at key cell identity genes. Cell 2013, 153:307-319.
21. Pott S., Lieb J.D. What are super-enhancers?. Nat. Genet. 2015, 47:8-12.
22. Woolfe A., et al. Highly conserved non-coding sequences are associated with vertebrate development. PLoS Biol. 2005, 3:e7.
23. Pennacchio L.A., et al. In vivo enhancer analysis of human conserved non-coding sequences. Nature 2006, 444:499-502.
24. Visel A., et al. Ultraconservation identifies a small subset of extremely constrained developmental enhancers. Nat. Genet. 2008, 40:158-160.
25. Visel A., et al. Enhancer identification through comparative genomics. Semin. Cell Dev. Biol. 2007, 18:140-152.
26. Hardison R.C., Taylor J. Genomic approaches towards finding cis-regulatory modules in animals. Nat. Rev. Genet. 2012, 13:469-483.
27. Visel A., et al. VISTA Enhancer Browser - a database of tissue-specific human enhancers. Nucleic Acids Res. 2007, 35:D88-D92.
28. Visel A., et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
29. Buenrostro J.D., et al. Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin DNA-binding proteins and nucleosome position. Nat. Methods 2013, 10:1213-1218.
30. Tsompana M., Buck M.J. Chromatin accessibility: a window into the genome. Epigenetics Chromatin 2014, 7:33.
31. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. ENCODE Project Consortium.
32. Wang J., et al. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res. 2012, 22:1798-1812.
33. Ernst J., et al. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 2011, 473:43-49.
34. Zentner G.E., Henikoff S. Surveying the epigenomic landscape, one base at a time. Genome Biol. 2012, 13:250.
35. Dogan N., et al. Occupancy by key transcription factors is a more accurate predictor of enhancer activity than histone modifications or chromatin accessibility. Epigenetics Chromatin 2015, 8:16.
36. Kim T.K., et al. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
37. Tuan D., et al. Transcription of the hypersensitive site HS2 enhancer in erythroid cells. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:11219-11223.
38. Lam M.T., et al. Enhancer RNAs and regulated transcriptional programs. Trends Biochem. Sci. 2014, 39:170-182.
39. Koch F., et al. Transcription initiation platforms and GTF recruitment at tissue-specific enhancers and promoters. Nat. Struct. Mol. Biol. 2011, 18:956-963.
40. Djebali S., et al. Landscape of transcription in human cells. Nature 2012, 489:101-108.
41. Andersson R., et al. An atlas of active enhancers across human cell types and tissues. Nature 2014, 507:455-461.
42. Pefanis E., et al. RNA exosome-regulated long non-coding RNA transcription controls super-enhancer activity. Cell 2015, 161:774-789.
43. Melo C.A., et al. eRNAs are required for p53-dependent enhancer activity and gene transcription. Mol. Cell 2013, 49:524-535.
44. Li W., et al. Functional roles of enhancer RNAs for oestrogen-dependent transcriptional activation. Nature 2013, 498:516-520.
45. Mousavi K., et al. eRNAs promote transcription by establishing chromatin accessibility at defined genomic loci. Mol. Cell 2013, 51:606-617.
46. Schaukowitch K., et al. Enhancer RNA facilitates NELF release from immediate early genes. Mol. Cell 2014, 56:29-42.
47. Pnueli L., et al. RNA transcribed from a distal enhancer is required for activating the chromatin at the promoter of the gonadotropin alpha-subunit gene. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:4369-4374.
48. Shiraki T., et al. Cap analysis gene expression for high-throughput analysis of transcriptional starting point and identification of promoter usage. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:15776-15781.
49. Andersson R., et al. A unified architecture of transcriptional regulatory elements. Trends Genet. 2015, 31:426-433.
50. Yao P., et al. Coexpression networks identify brain region-specific enhancer RNAs in the human brain. Nat. Neurosci. 2015, 18:1168-1174.
51. Yamashita R., et al. Genome-wide characterization of transcriptional start sites in humans by integrative transcriptome analysis. Genome Res. 2011, 21:775-789.
52. Ni T., et al. A paired-end sequencing strategy to map the complex landscape of transcription initiation. Nat. Methods 2010, 7:521-527.
53. Melgar M.F., et al. Discovery of active enhancers through bidirectional expression of short transcripts. Genome Biol. 2011, 12:R113.
54. Core L.J., et al. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 2008, 322:1845-1848.
55. Kwak H., et al. Precise maps of RNA polymerase reveal how promoters direct initiation and pausing. Science 2013, 339:950-953.
56. Nechaev S., et al. Global analysis of short RNAs reveals widespread promoter-proximal stalling and arrest of Pol II in Drosophila. Science 2010, 327:335-338.
57. Scruggs B.S., et al. Bidirectional transcription arises from two distinct hubs of transcription factor binding and active chromatin. Mol. Cell 2015, 58:1101-1112.
58. Mayer A., et al. Native elongating transcript sequencing reveals human transcriptional activity at nucleotide resolution. Cell 2015, 161:541-554.
59. Churchman L.S., Weissman J.S. Nascent transcript sequencing visualizes transcription at nucleotide resolution. Nature 2011, 469:368-373.
60. Nojima T., et al. Mammalian NET-seq reveals genome-wide nascent transcription coupled to RNA processing. Cell 2015, 161:526-540.
61. Parker S.C., et al. Chromatin stretch enhancer states drive cell-specific gene regulation and harbor human disease risk variants. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:17921-17926.
62. Farh K.K., et al. Genetic and epigenetic fine mapping of causal autoimmune disease variants. Nature 2015, 518:337-343.
63. Huang F.W., et al. Highly recurrent TERT promoter mutations in human melanoma. Science 2013, 339:957-959.
64. Fredriksson N.J., et al. Systematic analysis of noncoding somatic mutations and gene expression alterations across 14 tumor types. Nat. Genet. 2014, 46:1258-1263.
65. Weinhold N., et al. Genome-wide analysis of noncoding regulatory mutations in cancer. Nat. Genet. 2014, 46:1160-1165.
66. Melton C., et al. Recurrent somatic mutations in regulatory regions of human cancer genomes. Nat. Genet. 2015, 47:710-716.
67. Puente X.S., et al. Non-coding recurrent mutations in chronic lymphocytic leukaemia. Nature 2015, 526:519-524.
68. Mansour M.R., et al. Oncogene regulation An oncogenic super-enhancer formed through somatic mutation of a noncoding intergenic element. Science 2014, 346:1373-1377.
69. Brown L., et al. Site-specific recombination of the tal-gene is a common occurrence in human T cell leukemia. EMBO J. 1990, 9:3343-3351.
70. Tomlinson I., et al. A genome-wide association scan of tag SNPs identifies a susceptibility variant for colorectal cancer at 8q24.21. Nat. Genet. 2007, 39:984-988.
71. Yeager M., et al. Genome-wide association study of prostate cancer identifies a second risk locus at 8q24. Nat. Genet. 2007, 39:645-649.
72. Tuupanen S., et al. The common colorectal cancer predisposition SNP rs6983267 at chromosome 8q24 confers potential to enhanced Wnt signaling. Nat. Genet. 2009, 41:885-890.
73. Pomerantz M.M., et al. The 8q24 cancer risk variant rs6983267 shows long-range interaction with MYC in colorectal cancer. Nat. Genet. 2009, 41:882-884.
74. Sur I.K., et al. Mice lacking a Myc enhancer that includes human SNP rs6983267 are resistant to intestinal tumors. Science 2012, 338:1360-1363.
75. Forbes S.A., et al. COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res. 2011, 39:D945-D950.
76. Houlston R.S., et al. Meta-analysis of genome-wide association data identifies four new susceptibility loci for colorectal cancer. Nat. Genet. 2008, 40:1426-1435.
77. Takahashi K., et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007, 131:861-872.
78. Kamao H., et al. Characterization of human induced pluripotent stem cell-derived retinal pigment epithelium cell sheets aiming for clinical application. Stem Cell Rep. 2014, 2:205-218.
79. Cyranoski D. Japanese woman is first recipient of next-generation stem cells. Nature 2014, Published online September 12, 2014. 10.1038/nature.2014.15915.
80. Okano H., Yamanaka S. iPS cell technologies: significance and applications to CNS regeneration and disease. Mol. Brain 2014, 7:22.
81. Mayshar Y., et al. Identification and classification of chromosomal aberrations in human induced pluripotent stem cells. Cell Stem Cell 2010, 7:521-531.
82. Gore A., et al. Somatic coding mutations in human induced pluripotent stem cells. Nature 2011, 471:63-67.
83. Sugiura M., et al. Induced pluripotent stem cell generation-associated point mutations arise during the initial stages of the conversion of these cells. Stem Cell Rep. 2014, 2:52-63.
84. Wasserman W.W., Fickett J.W. Identification of regulatory regions which confer muscle-specific gene expression. J. Mol. Biol. 1998, 278:167-181.
85. Chen X., et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008, 133:1106-1117.
86. Zinzen R.P., et al. Combinatorial binding predicts spatio-temporal cis-regulatory activity. Nature 2009, 462:65-70.
87. May D., et al. Large-scale discovery of enhancers from human heart tissue. Nat. Genet. 2012, 44:89-93.
88. Dorschner M.O., et al. High-throughput localization of functional elements by quantitative chromatin profiling. Nat. Methods 2004, 1:219-225.
89. Giresi P.G., et al. FAIRE (formaldehyde-assisted isolation of regulatory elements) isolates active regulatory elements from human chromatin. Genome Res. 2007, 17:877-885.
90. Heintzman N.D., et al. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007, 39:311-318.
91. van Steensel B., Dekker J. Genomics tools for unraveling chromosome architecture. Nat. Biotechnol. 2010, 28:1089-1095.
92. Li G., et al. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 2012, 148:84-98.
93. Melnikov A., et al. Systematic dissection and optimization of inducible enhancers in human cells using a massively parallel reporter assay. Nat. Biotechnol. 2012, 30:271-277.
94. Arnold C.D., et al. Genome-wide quantitative enhancer activity maps identified by STARR-seq. Science 2013, 339:1074-1077.
95. Lai F., et al. Integrator mediates the biogenesis of enhancer RNAs. Nature 2015, 525:399-403.
96. Rosenbloom K.R., et al. ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res. 2013, 41:D56-D63.
97. de Hoon M., et al. Paradigm shifts in genomics through the FANTOM projects. Mamm. Genome 2015, 26:391-402.
98. Arner E., et al. Gene regulation Transcribed enhancers lead waves of coordinated transcription in transitioning mammalian cells. Science 2015, 347:1010-1014.
99. The FANTOM Consortium and the RIKEN PMI and CLST (DGT), et al. A promoter-level mammalian expression atlas. Nature 2014, 507:462-470.
100. Zhao T., et al. Immunogenicity of induced pluripotent stem cells. Nature 2011, 474:212-215.