Decoding enhancers using massively parallel reporter assays

Genomics

Volumn 106, Issue 3, 2015, Pages 159-164

  Inoue, Fumitaka ^a   Ahituv, Nadav ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Enhancer; Massively parallel reporter assays; Transcriptional regulation

Indexed keywords

TRANSCRIPTION FACTOR;

ASSAY; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; DNA BARCODING; DNA METHYLATION; ENHANCER REGION; EXON; GENE EXPRESSION; HIGH THROUGHPUT SEQUENCING; HUMAN; INSULATOR ELEMENT; MASSIVELY PARALLEL REPORTER ASSAY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY SEQUENCE; REPORTER GENE; REVIEW; SATURATION MUTAGENESIS; SILENCER ELEMENT; TRANSCRIPTION REGULATION; TRANSPOSON; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENETICS; GENOMICS; PROCEDURES;

BINDING SITES; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION; GENOMICS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS;

EID: 84939255435     PISSN: 08887543     EISSN: 10898646     Source Type: Journal    
DOI: 10.1016/j.ygeno.2015.06.005     Document Type: Review

References (50)

1. Birnbaum R.Y., Clowney E.J., Agamy O., Kim M.J., Zhao J., Yamanaka T., Pappalardo Z., Clarke S.L., Wenger A.M., Nguyen L., Gurrieri F., Everman D.B., Schwartz C.E., Birk O.S., Bejerano G., Lomvardas S., Ahituv N. Coding exons function as tissue-specific enhancers of nearby genes. Genome Res. 2012, 22:1059-1068.
2. Birnbaum R.Y., Patwardhan R.P., Kim M.J., Findlay G.M., Martin B., Zhao J., Bell R.J., Smith R.P., Ku A.A., Shendure J., Ahituv N. Systematic dissection of coding exons at single nucleotide resolution supports an additional role in cell-specific transcriptional regulation. PLoS Genet. 2014, 10:e1004592.
3. Lomvardas S., Barnea G., Pisapia D.J., Mendelsohn M., Kirkland J., Axel R. Interchromosomal interactions and olfactory receptor choice. Cell 2006, 126:403-413.
4. Sanyal A., Lajoie B.R., Jain G., Dekker J. The long-range interaction landscape of gene promoters. Nature 2012, 489:109-113.
5. Andersson R., Gebhard C., Miguel-Escalada I., Hoof I., Bornholdt J., Boyd M., Chen Y., Zhao X., Schmidl C., Suzuki T., Ntini E., Arner E., Valen E., Li K., Schwarzfischer L., Glatz D., Raithel J., Lilje B., Rapin N., Bagger F.O., Jorgensen M., Andersen P.R., Bertin N., Rackham O., Burroughs A.M., Baillie J.K., Ishizu Y., Shimizu Y., Furuhata E., Maeda S., Negishi Y., Mungall C.J., Meehan T.F., Lassmann T., Itoh M., Kawaji H., Kondo N., Kawai J., Lennartsson A., Daub C.O., Heutink P., Hume D.A., Jensen T.H., Suzuki H., Hayashizaki Y., Muller F., Forrest A.R., Carninci P., Rehli M., Sandelin A. An atlas of active enhancers across human cell types and tissues. Nature 2014, 507:455-461.
6. Kim T.K., Hemberg M., Gray J.M., Costa A.M., Bear D.M., Wu J., Harmin D.A., Laptewicz M., Barbara-Haley K., Kuersten S., Markenscoff-Papadimitriou E., Kuhl D., Bito H., Worley P.F., Kreiman G., Greenberg M.E. Widespread transcription at neuronal activity-regulated enhancers. Nature 2010, 465:182-187.
7. Lam M.T., Li W., Rosenfeld M.G., Glass C.K. Enhancer RNAs and regulated transcriptional programs. Trends Biochem. Sci. 2014, 39:170-182.
8. Carroll S.B. Evolution at two levels: on genes and form. PLoS Biol. 2005, 3:e245.
9. Ahituv N. Gene Regulatory Sequences and Human Disease 2012, Springer, New York, (pp. x, 283 pp.).
10. Welter D., MacArthur J., Morales J., Burdett T., Hall P., Junkins H., Klemm A., Flicek P., Manolio T., Hindorff L., Parkinson H. The NHGRI GWAS Catalog, a curated resource of SNP-trait associations. Nucleic Acids Res. 2014, 42:D1001-D1006.
11. Hindorff L.A., Sethupathy P., Junkins H.A., Ramos E.M., Mehta J.P., Collins F.S., Manolio T.A. Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9362-9367.
12. Gotea V., Visel A., Westlund J.M., Nobrega M.A., Pennacchio L.A., Ovcharenko I. Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Res. 2010, 20:565-577.
13. Levy S., Hannenhalli S., Workman C. Enrichment of regulatory signals in conserved non-coding genomic sequence. Bioinformatics 2001, 17:871-877.
14. Pennacchio L.A., Ahituv N., Moses A.M., Prabhakar S., Nobrega M.A., Shoukry M., Minovitsky S., Dubchak I., Holt A., Lewis K.D., Plajzer-Frick I., Akiyama J., De Val S., Afzal V., Black B.L., Couronne O., Eisen M.B., Visel A., Rubin E.M. In vivo enhancer analysis of human conserved non-coding sequences. Nature 2006, 444:499-502.
15. Pennacchio L.A., Loots G.G., Nobrega M.A., Ovcharenko I. Predicting tissue-specific enhancers in the human genome. Genome Res. 2007, 17:201-211.
16. Creyghton M.P., Cheng A.W., Welstead G.G., Kooistra T., Carey B.W., Steine E.J., Hanna J., Lodato M.A., Frampton G.M., Sharp P.A., Boyer L.A., Young R.A., Jaenisch R. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:21931-21936.
17. Heintzman N.D., Hon G.C., Hawkins R.D., Kheradpour P., Stark A., Harp L.F., Ye Z., Lee L.K., Stuart R.K., Ching C.W., Ching K.A., Antosiewicz-Bourget J.E., Liu H., Zhang X., Green R.D., Lobanenkov V.V., Stewart R., Thomson J.A., Crawford G.E., Kellis M., Ren B. Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 2009, 459:108-112.
18. Rada-Iglesias A., Bajpai R., Swigut T., Brugmann S.A., Flynn R.A., Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 2011, 470:279-283.
19. Heintzman N.D., Stuart R.K., Hon G., Fu Y., Ching C.W., Hawkins R.D., Barrera L.O., Van Calcar S., Qu C., Ching K.A., Wang W., Weng Z., Green R.D., Crawford G.E., Ren B. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 2007, 39:311-318.
20. Boyle A.P., Davis S., Shulha H.P., Meltzer P., Margulies E.H., Weng Z., Furey T.S., Crawford G.E. High-resolution mapping and characterization of open chromatin across the genome. Cell 2008, 132:311-322.
21. Song L., Zhang Z., Grasfeder L.L., Boyle A.P., Giresi P.G., Lee B.K., Sheffield N.C., Graf S., Huss M., Keefe D., Liu Z., London D., McDaniell R.M., Shibata Y., Showers K.A., Simon J.M., Vales T., Wang T., Winter D., Zhang Z., Clarke N.D., Birney E., Iyer V.R., Crawford G.E., Lieb J.D., Furey T.S. Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res. 2011, 21:1757-1767.
22. Thurman R.E., Rynes E., Humbert R., Vierstra J., Maurano M.T., Haugen E., Sheffield N.C., Stergachis A.B., Wang H., Vernot B., Garg K., John S., Sandstrom R., Bates D., Boatman L., Canfield T.K., Diegel M., Dunn D., Ebersol A.K., Frum T., Giste E., Johnson A.K., Johnson E.M., Kutyavin T., Lajoie B., Lee B.K., Lee K., London D., Lotakis D., Neph S., Neri F., Nguyen E.D., Qu H., Reynolds A.P., Roach V., Safi A., Sanchez M.E., Sanyal A., Shafer A., Simon J.M., Song L., Vong S., Weaver M., Yan Y., Zhang Z., Zhang Z., Lenhard B., Tewari M., Dorschner M.O., Hansen R.S., Navas P.A., Stamatoyannopoulos G., Iyer V.R., Lieb J.D., Sunyaev S.R., Akey J.M., Sabo P.J., Kaul R., Furey T.S., Dekker J., Crawford G.E., Stamatoyannopoulos J.A. The accessible chromatin landscape of the human genome. Nature 2012, 489:75-82.
23. Buenrostro J.D., Giresi P.G., Zaba L.C., Chang H.Y., Greenleaf W.J. 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.
24. Kheradpour P., Ernst J., Melnikov A., Rogov P., Wang L., Zhang X., Alston J., Mikkelsen T.S., Kellis M. Systematic dissection of regulatory motifs in 2000 predicted human enhancers using a massively parallel reporter assay. Genome Res. 2013, 23:800-811.
25. Melnikov A., Murugan A., Zhang X., Tesileanu T., Wang L., Rogov P., Feizi S., Gnirke A., Callan C.G., Kinney J.B., Kellis M., Lander E.S., Mikkelsen T.S. Systematic dissection and optimization of inducible enhancers in human cells using a massively parallel reporter assay. Nat. Biotechnol. 2012, 30:271-277.
26. Patwardhan R.P., Hiatt J.B., Witten D.M., Kim M.J., Smith R.P., May D., Lee C., Andrie J.M., Lee S.I., Cooper G.M., Ahituv N., Pennacchio L.A., Shendure J. Massively parallel functional dissection of mammalian enhancers in vivo. Nat. Biotechnol. 2012, 30:265-270.
27. Kwasnieski J.C., Fiore C., Chaudhari H.G., Cohen B.A. High-throughput functional testing of ENCODE segmentation predictions. Genome Res. 2014, 24:1595-1602.
28. Kwasnieski J.C., Mogno I., Myers C.A., Corbo J.C., Cohen B.A. Complex effects of nucleotide variants in a mammalian cis-regulatory element. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:19498-19503.
29. White M.A., Myers C.A., Corbo J.C., Cohen B.A. Massively parallel in vivo enhancer assay reveals that highly local features determine the cis-regulatory function of ChIP-seq peaks. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:11952-11957.
30. Arnold C.D., Gerlach D., Spies D., Matts J.A., Sytnikova Y.A., Pagani M., Lau N.C., Stark A. Quantitative genome-wide enhancer activity maps for five Drosophila species show functional enhancer conservation and turnover during cis-regulatory evolution. Nat. Genet. 2014, 46:685-692.
31. Arnold C.D., Gerlach D., Stelzer C., Boryn L.M., Rath M., Stark A. Genome-wide quantitative enhancer activity maps identified by STARR-seq. Science 2013, 339:1074-1077.
32. Shlyueva D., Stelzer C., Gerlach D., Yanez-Cuna J.O., Rath M., Boryn L.M., Arnold C.D., Stark A. Hormone-responsive enhancer-activity maps reveal predictive motifs, indirect repression, and targeting of closed chromatin. Mol. Cell 2014, 54:180-192.
33. Akhtar W., de Jong J., Pindyurin A.V., Pagie L., Meuleman W., de Ridder J., Berns A., Wessels L.F., van Lohuizen M., van Steensel B. Chromatin position effects assayed by thousands of reporters integrated in parallel. Cell 2013, 154:914-927.
34. Murtha M., Tokcaer-Keskin Z., Tang Z., Strino F., Chen X., Wang Y., Xi X., Basilico C., Brown S., Bonneau R., Kluger Y., Dailey L. FIREWACh: high-throughput functional detection of transcriptional regulatory modules in mammalian cells. Nat. Methods 2014, 11:559-565.
35. Dickel D.E., Zhu Y., Nord A.S., Wylie J.N., Akiyama J.A., Afzal V., Plajzer-Frick I., Kirkpatrick A., Gottgens B., Bruneau B.G., Visel A., Pennacchio L.A. Function-based identification of mammalian enhancers using site-specific integration. Nat. Methods 2014, 11:566-571.
36. Patwardhan R.P., Lee C., Litvin O., Young D.L., Pe'er D., Shendure J. High-resolution analysis of DNA regulatory elements by synthetic saturation mutagenesis. Nat. Biotechnol. 2009, 27:1173-1175.
37. Kim M.J., Ahituv N. The hydrodynamic tail vein assay as a tool for the study of liver promoters and enhancers. Methods Mol. Biol. 2013, 1015:279-289.
38. Smith R.P., Taher L., Patwardhan R.P., Kim M.J., Inoue F., Shendure J., Ovcharenko I., Ahituv N. Massively parallel decoding of mammalian regulatory sequences supports a flexible organizational model. Nat. Genet. 2013, 45:1021-1028.
39. Sharon E., Kalma Y., Sharp A., Raveh-Sadka T., Levo M., Zeevi D., Keren L., Yakhini Z., Weinberger A., Segal E. Inferring gene regulatory logic from high-throughput measurements of thousands of systematically designed promoters. Nat. Biotechnol. 2012, 30:521-530.
40. Kinney J.B., Murugana A., Callan C.G., Cox E.C. Using deep sequencing to characterize the biophysical mechanism of a transcriptional regulatory sequence. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:9158-9163.
41. Hiatt J.B., Patwardhan R.P., Turner E.H., Lee C., Shendure J. Parallel, tag-directed assembly of locally derived short sequence reads. Nat. Methods 2010, 7:119-122.
42. Hupe M., Li M.X., Gertow Gillner K., Adams R.H., Stenman J.M. Evaluation of TRAP-sequencing technology with a versatile conditional mouse model. Nucleic Acids Res. 2014, 42:e14.
43. Findlay G.M., Boyle E.A., Hause R.J., Klein J.C., Shendure J. Saturation editing of genomic regions by multiplex homology-directed repair. Nature 2014, 513:120-123.
44. Kosuri S., Goodman D.B., Cambray G., Mutalik V.K., Gao Y., Arkin A.P., Endy D., Church G.M. Composability of regulatory sequences controlling transcription and translation in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:14024-14029.
45. Zhao W., Pollack J.L., Blagev D.P., Zaitlen N., McManus M.T., Erle D.J. Massively parallel functional annotation of 3' untranslated regions. Nat. Biotechnol. 2014, 32:387-391.
46. Visel A., Blow M.J., Li Z., Zhang T., Akiyama J.A., Holt A., Plajzer-Frick I., Shoukry M., Wright C., Chen F., Afzal V., Ren B., Rubin E.M., Pennacchio L.A. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 2009, 457:854-858.
47. Visel A., Taher L., Girgis H., May D., Golonzhka O., Hoch R.V., McKinsey G.L., Pattabiraman K., Silberberg S.N., Blow M.J., Hansen D.V., Nord A.S., Akiyama J.A., Holt A., Hosseini R., Phouanenavong S., Plajzer-Frick I., Shoukry M., Afzal V., Kaplan T., Kriegstein A.R., Rubin E.M., Ovcharenko I., Pennacchio L.A., Rubenstein J.L. A high-resolution enhancer atlas of the developing telencephalon. Cell 2013, 152:895-908.
48. Carroll S.B. Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 2008, 134:25-36.
49. Wittkopp P.J., Kalay G. Cis-regulatory elements: molecular mechanisms and evolutionary processes underlying divergence. Nat. Rev. Genet. 2012, 13:59-69.
50. Wray G.A. The evolutionary significance of cis-regulatory mutations. Nat. Rev. Genet. 2007, 8:206-216.