Effects on the transcriptome upon deletion of a distal element cannot be predicted by the size of the H3K27Ac peak in human cells

Nucleic Acids Research

Volumn 44, Issue 9, 2016, Pages 4123-4133

  Tak, Yu Gyoung ^a   Hung, Yuli ^a   Yao, Lijing ^a   Grimmer, Matthew R ^a   Do, Albert ^a   Bhakta, Mital S ^b   O'Geen, Henriette ^b   Segal, David J ^b   Farnham, Peggy J ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

H3K27AC; HISTONE; NUCLEASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; PROTEIN E7;

ARTICLE; CANCER RISK; COLORECTAL CANCER; CONTROLLED STUDY; CRISPR CAS SYSTEM; DOWN REGULATION; EPIGENETICS; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENOME-WIDE ASSOCIATION STUDY; HCT116 CELL LINE; HEK293 CELL LINE; HISTONE MODIFICATION; HUMAN; HUMAN CELL; ONCOGENE MYC; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; ACETYLATION; CELL PROLIFERATION; COLORECTAL TUMOR; ENHANCER REGION; GENETICS; HCT 116 CELL LINE; METABOLISM; PROTEIN PROCESSING;

ACETYLATION; CELL PROLIFERATION; COLORECTAL NEOPLASMS; ENHANCER ELEMENTS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOME-WIDE ASSOCIATION STUDY; HCT116 CELLS; HEK293 CELLS; HISTONES; HUMANS; PAPILLOMAVIRUS E7 PROTEINS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE DELETION; TRANSCRIPTOME;

EID: 84960185948     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1530     Document Type: Article

References (55)

1. Yao,L., Tak,Y.G., Berman,B.P. and Farnham,P.J. (2014) Functional annotation of colon cancer risk SNPs. Nat. Commun., 5, 5114.
2. Panne,D. (2008) The enhanceosome. Curr. Opin. Struct. Biol., 18, 236-242.
3. Maniatis,T., Falvo,J.V., Kim,T.H., Lin,C.H., Parekh,B.S. and Wathelet,M.G. (1998) Structure and function of the interferon-B enhanceosome. Cold Spring Harb. Symp. Quant. Biol., 63, 609-620.
4. ENCODE Project Consortium. (2012) An integrated encyclopedia of DNA elements in the human genome. Nature, 489, 57-74.
5. RoadmapEpigenomicsConsortium. (2015) Integrative analysis of 111 reference human epigenomes. Nature, 19, 317-330.
6. Corradin,O. and Scacheri,P.C. (2014) Enhancer variants: evaluating functions in common disease. Genome Med., 6, 85.
7. Mali,P., Yang,L., Esvelt,K.M., Aach,J., Guell,M., DiCarlo,J.E., Norville,J.E. and Church,G.M. (2013) RNA-guided human genome engineering via Cas9. Science, 339, 823-826.
8. Trapnell,C., Pachter,L. and Salzberg,S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111.
9. Anders,S., Pyl,P.T. and Huber,W. (2015) HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics, 31, 166-169.
10. Robinson,M.D., McCarthy,D.J. and Smyth,G.K. (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26, 139-140.
11. Blahnik,K.R., Dou,L., Echipare,L., Iyengar,S., O'Geen,H., Sanchez,E., Zhao,Y., Marra,M.A., Hirst,M., Costello,J.F. et al. (2011) Characterization of the contradictory chromatin signatures at the 3 exons of zinc finger genes. PLoS One, 6, e17121.
12. Blahnik,K.R., Dou,L., O'Geen,H., McPhillips,T., Xu,X., Cao,A.R., Iyengar,S., Nicolet,C.M., Ludaescher,B., Korf,I. et al. (2010) Sole-search: an integrated analysis program for peak detection and functional annotation using ChIP-seq data. Nucleic Acids Res., 38, e13.
13. O'Geen,H., Echipare,L. and Farnham,P.J. (2011) Using ChIP-seq technology to generate high-resolution profiles of histone modifications. Methods Mol. Biol., 791, 265-286.
14. Zhang,Y., Lin,Y.H., Johnson,T.D., Rozek,L.S. and Sartor,M.A. (2014) PePr: a peak-calling prioritization pipeline to identify consistent or differential peaks from replicated ChIP-Seq data. Bioinformatics, 30, 2568-2575.
15. Frietze,S., Wang,R., Yao,L., Tak,Y.G., Ye,Z., Gaddis,M., Witt,H., Farnham,P.J. and Jin,V.X. (2012) Cell type-specific binding patterns reveal that TCF7L2 can be tethered to the genome by association with GATA3. Genome Biol., 13, R52.
16. Blattler,A., Yao,L., Witt,H., Guo,Y., Nicolet,C.M., Berman,B.P. and Farnham,P.J. (2014) Global loss of DNA methylation uncovers intronic enhancers in genes showing expression changes. Genome Biol., 15, 469.
17. Schork,A.J., Thompson,W.K., Pham,P., Torkamani,A., Roddey,J.C., Sullivan,P.F., Kelsoe,J.R., O'Donovan,M.C., Furberg,H., Schork,N.J. et al. (2013) All SNPs are not created equal: genome-wide association studies reveal a consistent pattern of enrichment among functionally annotated SNPs. PLoS Genet., 9, e1003449.
18. Ma,G., Gu,D., Lv,C., Chu,H., Xu,Z., Tong,N., Wang,M., Tang,C., Xu,Y., Zhang,Z. et al. (2015) Genetic variant in 8q24 is associated with prognosis for gastric cancer in a Chinese population. J. Gastroenterol. Hepatol., 30, 689-695.
19. Sagai,T., Hosoya,M., Mizushina,Y., Tamura,M. and Shiroishi,T. (2005) Elimination of a long-range cis-regulatory module causes complete loss of limb-specific Shh expression and truncation of the mouse limb. Development, 132, 797-803.
20. Zhou,H.Y., Katsman,Y., Dhaliwal,N.K., Davidson,S., Macpherson,N.N., Sakthidevi,M., Collura,F. and Mitchell,J.A. (2014) A Sox2 distal enhancer cluster regulates embryonic stem cell differentiation potential. Genes Dev., 28, 2699-2711.
21. Sanyal,A., Lajoie,B.R., Jain,G. and Dekker,J. (2012) The long-range interaction landscape of gene promoters. Nature, 489, 109-113.
22. Farnham,P.J. (2009) Insights from genomic profiling of transcription factors. Nat. Rev. Genet., 10, 605-616.
23. Li,G., Ruan,X., Auerbach,R.K., Sandhu,K.S., Zheng,M., Wang,P., Poh,H.M., Goh,Y., Lim,J., Zhang,J. et al. (2012) Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell, 148, 84-98.
24. Yao,L., Berman,B.P. and Farnham,P.J. (2015) Demystifying the secret mission of enhancers: linking distal regulatory elements to target genes. Crit. Rev. Biochem. Mol. Biol., 50, 550-573.
25. Segditsas,S. and Tomlinson,I. (2006) Colorectal cancer and genetic alterations in the Wnt pathway. Oncogene, 25, 7531-7537.
26. Bright-Thomas,R.M. and Hargest,R. (2003) APC, beta-Catenin and hTCF-4; an unholy trinity in the genesis of colorectal cancer. Eur. J. Surg. Oncol., 29, 107-117.
27. Gaddis,M., Gerrard,D., Frietze,S. and Farnham,P.J. (2015) Altering cancer transcriptomes using epigenomic inhibitors. Epigenet. Chromatin, 8,9.
28. Clevers,H. (2004) Wnt breakers in colon cancer. Cancer Cell, 5, 5-6.
29. Clevers,H. (2006) Wnt/beta-catenin signaling in development and disease. Cell, 127, 469-480.
30. Holwerda,S.J. and de Laat,W. (2013) CTCF: the protein, the binding partners, the binding sites and their chromatin loops. Philos. Trans. R. Soc. Lond. B. Biol. Sci., 368, 20120369.
31. Narendra,V., Rocha,P.P., An,D., Raviram,R., Skok,J.A., Mazzoni,E.O. and Reinberg,D. (2015) Transcription. CTCF establishes discrete functional chromatin domains at the Hox clusters during differentiation. Science, 347, 1017-1021.
32. Ong,C.T. and Corces,V.G. (2014) CTCF: an architectural protein bridging genome topology and function. Nat. Rev. Genet., 15, 234-246.
33. Splinter,E., Heath,H., Kooren,J., Palstra,R.-J., Klous,P., Grosveld,F., Galjart,N. and de Laat,W. (2006) CTCF mediates long-range chromatin looping and local histone modification in the beta-globin locus. Genes Dev., 20, 2349-2354.
34. Vietri Rudan,M., Barrington,C., Henderson,S., Ernst,C., Odom,D.T., Tanay,A. and Hadjur,S. (2015) Comparative Hi-C reveals that CTCF underlies evolution of chromosomal domain architecture. Cell Rep., 10, 1297-1309.
35. Gabay,M., Li,Y. and Felsher,D.W. (2014) MYC activation is a hallmark of cancer initiation and maintenance. Cold Spring Harb. Perspect. Med., 4, a014241.
36. McKeown,M.R. and Bradner,J.E. (2014) Therapeutic strategies to inhibit MYC. Cold Spring Harb. Perspect. Med., 4, a014266.
37. Diolaiti,D., McFerrin,L., Carroll,P.A. and Eisenman,R.N. (2014) Functional interactions among members of the MAX and MLX transcriptional network during oncogenesis. Biochim. Biophys. Acta, S1874-S9399.
38. Freedman,M.L., Monteiro,A.N., Gayther,S.A., Coetzee,G.A., Risch,A., Plass,C., Casey,G., De Biasi,M., Carlson,C., Duggan,D. et al. (2011) Principles for the post-GWAS functional characterization of cancer risk loci. Nat. Genet., 43, 513-518.
39. Coetzee,G.A., Jia,L., Frenkel,B., Henderson,B.E., Tanay,A., Haiman,C.A. and Freedman,M.L. (2010) A systematic approach to understand the functional consequences of non-protein coding risk regions. Cell Cycle, 9, 256-259.
40. Jin,F., Li,Y., Dixon,J.R., Selvaraj,S., Ye,Z., Lee,A.Y., Yen,C.A., Schmitt,A.D., Espinoza,C.A. and Ren,B. (2013) A high-resolution map of the three-dimensional chromatin interactome in human cells. Nature, 503, 290-294.
41. Pomerantz,M.M., Ahmadiyeh,N., Jia,L., Herman,P., Verzi,M.P., Doddapaneni,H., Beckwith,C.A., Chan,J.A., Hills,A., Davis,M. et al. (2009) The 8q24 cancer risk variant rs6983267 shows long-range interaction with MYC in colorectal cancer. Nat. Genet., 41, 882-884.
42. Wright,J.B., Brown,S.J. and Cole,M.D. (2010) Upregulation of c-MYC in cis through a large chromatin loop linked to a cancer risk-associated single-nucleotide polymorphism in colorectal cancer cells. Mol. Cell. Biol., 30, 1411-1420.
43. Ahmadiyeh,N., Pomerantz,M.M., Grisanzio,C., Herman,P., Jia,L., Almendro,V., He,H.H., Brown,M., Liu,X.S., Davis,M. et al. (2010) 8q24 prostate, breast, and colon cancer risk loci show tissue-specific long-range interaction with MYC. Proc. Natl. Acad. Sci. U.S.A., 107, 9742-9746.
44. Jager,R., Migliorini,G., Henrion,M., Kandaswamy,R., Speedy,H.E., Heindl,A., Whiffin,N., Carnicer,M.J., Broome,L., Dryden,N. et al. (2015) Capture Hi-C identifies the chromatin interactome of colorectal cancer risk loci. Nat. Commun., 6, 6178.
45. Du,M., Yuan,T., Schilter,K.F., Dittmar,R.L., Mackinnon,A., Huang,X., Tschannen,M.,Worthey,E., Jacob,H., Xia,S. et al. (2015) Prostate cancer risk locus at 8q24 as a regulatory hub by physical interactions with multiple genomic loci across the genome. Hum. Mol. Genet., 24, 154-166.
46. Dryden,N.H., Broome,L.R., Dudbridge,F., Johnson,N., Orr,N., Schoenfelder,S., Nagano,T., Andrews,S.,Wingett,S., Kozarewa,I. et al. (2014) Unbiased analysis of potential targets of breast cancer susceptibility loci by Capture Hi-C. Genome Res., 24, 1854-1868.
47. Xiang,J.F., Yin,Q.F., Chen,T., Zhang,Y., Zhang,X.O., Wu,Z., Zhang,S., Wang,H.B., Ge,J., Lu,X. et al. (2014) Human colorectal cancer-specific CCAT1-L lncRNA regulates long-range chromatin interactions at the MYC locus. Cell Res., 24, 513-531.
48. Williamson,I., Berlivet,S., Eskeland,R., Boyle,S., Illingworth,R.S., Paquette,D., Dostie,J. and Bickmore,W.A. (2014) Spatial genome organization: contrasting views from chromosome conformation capture and fluorescence in situ hybridization. Genes Dev., 28, 2778-2791.
49. Conacci-Sorrell,M., McFerrin,L. and Eisenman,R.N. (2014) An overview of MYC and its interactome. Cold Spring Harb. Perspect. Med., 4, a014357.
50. Sur,I.K., Hallikas,O., Vaharautio,A., Yan,J., Turunen,M., Enge,M., Taipale,M., Karhu,A., Aaltonen,L.A. and Taipale,J. (2012) Mice lacking a Myc enhancer that includes human SNP rs6983267 are resistant to intestinal tumors. Science, 338, 1360-1363.
51. Grandori,C., Cowley,S.M., James,L.P. and Eisenman,R.N. (2000) The Myc/Max/Mad network and the transcriptional control of cell behavior. Annu. Rev. Cell Dev. Biol., 16, 653-699.
52. Tseng,Y.Y., Moriarity,B.S., Gong,W., Akiyama,R., Tiwari,A., Kawakami,H., Ronning,P., Reuland,B., Guenther,K., Beadnell,T.C. et al. (2014) PVT1 dependence in cancer with MYC copy-number increase. Nature, 512, 82-86.
53. Kwasnieski,J.C., Fiore,C., Chaudhari,H.G. and Cohen,B.A. (2014) High-throughput functional testing of ENCODE segmentation predictions. Genome Res., 24, 1595-1602.
54. Sanborn,A.L., Rao,S.S., Huang,S.C., Durand,N.C., Huntley,M.H., Jewett,A.I., Bochkov,I.D., Chinnappan,D., Cutkosky,A., Li,J. et al. (2015) Chromatin extrusion explains key features of loop and domain formation in wild-type and engineered genomes. Proc. Natl. Acad. Sci. U.S.A., 112, E6456-E6465.
55. de Wit,E., Vos,E., Holwerda,S.J., Valdes-Quezada,C., Verstegen,M.J., Teunissen,H., Splinter,E., Wijchers,P.J., Kriger,P.H. and de Laat,W. (2015) CTCF binding polarity determines chromatin looping. Mol. Cell, 60, 676-684.