A DNA-Centric Protein Interaction Map of Ultraconserved Elements Reveals Contribution of Transcription Factor Binding Hubs to Conservation

Cell Reports

Volumn 5, Issue 2, 2013, Pages 531-545

  Viturawong, Tar ^a   Meissner, Felix ^a   Butter, Falk ^a   Mann, Matthias ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANALYTIC METHOD; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; DNA STRUCTURE; FINITE ELEMENT ANALYSIS; GENE MAPPING; GENETIC CONSERVATION; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DNA INTERACTION; PROTEIN PURIFICATION; QUANTITATIVE STUDY; STABLE ISOTOPE LABELING BY AMINO ACID IN CELL CULTURE; TRANSCRIPTION REGULATION; ULTRACONSERVED ELEMENT SEQUENCE; CHEMISTRY; CHROMATIN; GENETICS; HELA CELL LINE; ISOTOPE LABELING; MASS SPECTROMETRY; METABOLISM; MUTAGENESIS; NUCLEOTIDE SEQUENCE; PROTEIN PROTEIN INTERACTION;

CHROMATIN; DNA; PEPTIDE; PROTEIN BINDING; TRANSCRIPTION FACTOR;

BASE SEQUENCE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONSERVED SEQUENCE; DNA; HELA CELLS; HUMANS; ISOTOPE LABELING; MASS SPECTROMETRY; MUTAGENESIS; PEPTIDES; PROTEIN BINDING; PROTEIN INTERACTION MAPS; TRANSCRIPTION FACTORS;

EID: 84887021003     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2013.09.022     Document Type: Article

References (58)

1. Aalfs J.D., Narlikar G.J., Kingston R.E. Functional differences between the human ATP-dependent nucleosome remodeling proteins BRG1 and SNF2H. J.Biol. Chem. 2001, 276:34270-34278.
2. Ahituv N., Zhu Y., Visel A., Holt A., Afzal V., Pennacchio L.A., Rubin E.M. Deletion of ultraconserved elements yields viable mice. PLoS Biol. 2007, 5:e234.
3. Arbab M., Mahony S., Cho H., Chick J.M., Rolfe P.A., van Hoff J.P., Morris V.W., Gygi S.P., Maas R.L., Gifford D.K., Sherwood R.I. A multi-parametric flow cytometric assay to analyze DNA-protein interactions. Nucleic Acids Res. 2013, 41:e38.
4. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., Davis A.P., Dolinski K., Dwight S.S., Eppig J.T., et al. Gene ontology: tool for the unification of biology. Nat. Genet. 2000, 25:25-29. The Gene Ontology Consortium.
5. Bateman A., Coin L., Durbin R., Finn R.D., Hollich V., Griffiths-Jones S., Khanna A., Marshall M., Moxon S., Sonnhammer E.L., et al. The Pfam protein families database. Nucleic Acids Res. 2004, 32(Database issue):D138-D141.
6. Bejerano G., Pheasant M., Makunin I., Stephen S., Kent W.J., Mattick J.S., Haussler D. Ultraconserved elements in the human genome. Science 2004, 304:1321-1325.
7. Benjamini Y., Hochberg Y. Controlling the false discovery rate-a practical and powerful approach to multiple testing. J.Roy. Stat. Soc. B Met. 1995, 57:289-300.
8. Berman B.P., Pfeiffer B.D., Laverty T.R., Salzberg S.L., Rubin G.M., Eisen M.B., Celniker S.E. Computational identification of developmental enhancers: conservation and function of transcription factor binding-site clusters in Drosophila melanogaster and Drosophila pseudoobscura. Genome Biol. 2004, 5:R61.
9. Bernstein B.E., Mikkelsen T.S., Xie X., Kamal M., Huebert D.J., Cuff J., Fry B., Meissner A., Wernig M., Plath K., et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006, 125:315-326.
10. Bernstein B.E., Birney E., Dunham I., Green E.D., Gunter C., Snyder M. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. ENCODE Project Consortium.
11. Bryne J.C., Valen E., Tang M.H., Marstrand T., Winther O., da Piedade I., Krogh A., Lenhard B., Sandelin A. JASPAR, the open access database of transcription factor-binding profiles: new content and tools in the 2008 update. Nucleic Acids Res. 2008, 36(Database issue):D102-D106.
12. Butter F., Davison L., Viturawong T., Scheibe M., Vermeulen M., Todd J.A., Mann M. Proteome-wide analysis of disease-associated SNPs that show allele-specific transcription factor binding. PLoS Genet. 2012, 8:e1002982.
13. Cao R., Wang L., Wang H., Xia L., Erdjument-Bromage H., Tempst P., Jones R.S., Zhang Y. Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 2002, 298:1039-1043.
14. Collins D.W., Jukes T.H. Rates of transition and transversion in coding sequences since the human-rodent divergence. Genomics 1994, 20:386-396.
15. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 2008, 26:1367-1372.
16. Déjardin J., Kingston R.E. Purification of proteins associated with specific genomic Loci. Cell 2009, 136:175-186.
17. Dignam J.D., Lebovitz R.M., Roeder R.G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983, 11:1475-1489.
18. Dohm J.C., Lottaz C., Borodina T., Himmelbauer H. Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Res. 2008, 36:e105.
19. Eberl H.C., Spruijt C.G., Kelstrup C.D., Vermeulen M., Mann M. A map of general and specialized chromatin readers in mouse tissues generated by label-free interaction proteomics. Mol. Cell 2013, 49:368-378.
20. Hermsen R., Tans S., ten Wolde P.R. Transcriptional regulation by competing transcription factor modules. PLoS Comput. Biol. 2006, 2:e164.
21. Hoshino A., Fujii H. Insertional chromatin immunoprecipitation: a method for isolating specific genomic regions. J.Biosci. Bioeng. 2009, 108:446-449.
22. Jin C., Felsenfeld G. Nucleosome stability mediated by histone variants H3.3 and H2A.Z. Genes Dev. 2007, 21:1519-1529.
23. Koyama-Nasu R., David G., Tanese N. The F-box protein Fbl10 is a novel transcriptional repressor of c-Jun. Nat. Cell Biol. 2007, 9:1074-1080.
24. Ku M., Koche R.P., Rheinbay E., Mendenhall E.M., Endoh M., Mikkelsen T.S., Presser A., Nusbaum C., Xie X., Chi A.S., et al. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 2008, 4:e1000242.
25. Licastro D., Gennarino V.A., Petrera F., Sanges R., Banfi S., Stupka E. Promiscuity of enhancer, coding and non-coding transcription functions in ultraconserved elements. BMC Genomics 2010, 11:151.
26. Lu X., Wontakal S.N., Emelyanov A.V., Morcillo P., Konev A.Y., Fyodorov D.V., Skoultchi A.I. Linker histone H1 is essential for Drosophila development, the establishment of pericentric heterochromatin, and a normal polytene chromosome structure. Genes Dev. 2009, 23:452-465.
27. Martínez F., Monfort S., Roselló M., Oltra S., Blesa D., Quiroga R., Mayo S., Orellana C. Enrichment of ultraconserved elements among genomic imbalances causing mental delay and congenital anomalies. BMC Med. Genomics 2010, 3:54.
28. Mendenhall E.M., Koche R.P., Truong T., Zhou V.W., Issac B., Chi A.S., Ku M., Bernstein B.E. GC-rich sequence elements recruit PRC2 in mammalian ES cells. PLoS Genet. 2010, 6:e1001244.
29. Meyer L.R., Zweig A.S., Hinrichs A.S., Karolchik D., Kuhn R.M., Wong M., Sloan C.A., Rosenbloom K.R., Roe G., Rhead B., et al. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res. 2013, 41(Database issue):D64-D69.
30. Michalski A., Damoc E., Hauschild J.P., Lange O., Wieghaus A., Makarov A., Nagaraj N., Cox J., Mann M., Horning S. Mass spectrometry-based proteomics using Q Exactive, a high-performance benchtop quadrupole Orbitrap mass spectrometer. Mol. Cell. Proteomics 2011, 10. M111.011015.
31. Mirzaei H., Knijnenburg T.A., Kim B., Robinson M., Picotti P., Carter G.W., Li S., Dilworth D.J., Eng J.K., Aitchison J.D., et al. Systematic measurement of transcription factor-DNA interactions by targeted mass spectrometry identifies candidate gene regulatory proteins. Proc. Natl. Acad. Sci. USA 2013, 110:3645-3650.
32. Mittler G., Butter F., Mann M. A SILAC-based DNA protein interaction screen that identifies candidate binding proteins to functional DNA elements. Genome Res. 2009, 19:284-293.
33. Ngondo-Mbongo R.P., Myslinski E., Aster J.C., Carbon P. Modulation of gene expression via overlapping binding sites exerted by ZNF143, Notch1 and THAP11. Nucleic Acids Res. 2013, 41:4000-4014.
34. Ni J.Z., Grate L., Donohue J.P., Preston C., Nobida N., O'Brien G., Shiue L., Clark T.A., Blume J.E., Ares M. Ultraconserved elements are associated with homeostatic control of splicing regulators by alternative splicing and nonsense-mediated decay. Genes Dev. 2007, 21:708-718.
35. Ong S.E., Blagoev B., Kratchmarova I., Kristensen D.B., Steen H., Pandey A., Mann M. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1:376-386.
36. Palmer S.J., Tay E.S., Santucci N., Cuc Bach T.T., Hook J., Lemckert F.A., Jamieson R.V., Gunnning P.W., Hardeman E.C. Expression of Gtf2ird1, the Williams syndrome-associated gene, during mouse development. Gene Expr. Patterns 2007, 7:396-404.
37. Palmer S.J., Santucci N., Widagdo J., Bontempo S.J., Taylor K.M., Tay E.S., Hook J., Lemckert F., Gunning P.W., Hardeman E.C. Negative autoregulation of GTF2IRD1 in Williams-Beuren syndrome via a novel DNA binding mechanism. J.Biol. Chem. 2010, 285:4715-4724.
38. Pasini D., Malatesta M., Jung H.R., Walfridsson J., Willer A., Olsson L., Skotte J., Wutz A., Porse B., Jensen O.N., Helin K. Characterization of an antagonistic switch between histone H3 lysine 27 methylation and acetylation in the transcriptional regulation of Polycomb group target genes. Nucleic Acids Res. 2010, 38:4958-4969.
39. Pennacchio L.A., Ahituv N., Moses A.M., Prabhakar S., Nobrega M.A., Shoukry M., Minovitsky S., Dubchak I., Holt A., Lewis K.D., et al. Invivo enhancer analysis of human conserved non-coding sequences. Nature 2006, 444:499-502.
40. Perry M.W., Boettiger A.N., Bothma J.P., Levine M. Shadow enhancers foster robustness of Drosophila gastrulation. Curr. Biol. 2010, 20:1562-1567.
41. Poitras L., Yu M., Lesage-Pelletier C., Macdonald R.B., Gagné J.P., Hatch G., Kelly I., Hamilton S.P., Rubenstein J.L., Poirier G.G., Ekker M. An SNP in an ultraconserved regulatory element affects Dlx5/Dlx6 regulation in the forebrain. Development 2010, 137:3089-3097.
42. Rai T.S., Puri A., McBryan T., Hoffman J., Tang Y., Pchelintsev N.A., van Tuyn J., Marmorstein R., Schultz D.C., Adams P.D. Human CABIN1 is a functional member of the human HIRA/UBN1/ASF1a histone H3.3 chaperone complex. Mol. Cell. Biol. 2011, 31:4107-4118.
43. Scaruffi P. The transcribed-ultraconserved regions: a novel class of long noncoding RNAs involved in cancer susceptibility. ScientificWorldJournal 2011, 11:340-352.
44. Schwanhäusser B., Busse D., Li N., Dittmar G., Schuchhardt J., Wolf J., Chen W., Selbach M. Global quantification of mammalian gene expression control. Nature 2011, 473:337-342.
45. Siepel A., Bejerano G., Pedersen J.S., Hinrichs A.S., Hou M., Rosenbloom K., Clawson H., Spieth J., Hillier L.W., Richards S., et al. Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res. 2005, 15:1034-1050.
46. 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.
47. Spitz F., Furlong E.E. Transcription factors: from enhancer binding to developmental control. Nat. Rev. Genet. 2012, 13:613-626.
48. Tacheny A., Michel S., Dieu M., Payen L., Arnould T., Renard P. Unbiased proteomic analysis of proteins interacting with the HIV-1 5'LTR sequence: role of the transcription factor Meis. Nucleic Acids Res. 2012, 40:e168.
49. Thoma F., Koller T. Influence of histone H1 on chromatin structure. Cell 1977, 12:101-107.
50. Thompson P.D., Webb M., Beckett W., Hinsley T., Jowitt T., Sharrocks A.D., Tassabehji M. GTF2IRD1 regulates transcription by binding an evolutionarily conserved DNA motif 'GUCE'. FEBS Lett. 2007, 581:1233-1242.
51. Tie F., Banerjee R., Stratton C.A., Prasad-Sinha J., Stepanik V., Zlobin A., Diaz M.O., Scacheri P.C., Harte P.J. CBP-mediated acetylation of histone H3 lysine 27 antagonizes Drosophila Polycomb silencing. Development 2009, 136:3131-3141.
52. Tillo D., Hughes T.R. G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics 2009, 10:442.
53. Udugama M., Sabri A., Bartholomew B. The INO80 ATP-dependent chromatin remodeling complex is a nucleosome spacing factor. Mol. Cell. Biol. 2011, 31:662-673.
54. Visel A., Minovitsky S., Dubchak I., Pennacchio L.A. VISTA Enhancer Browser-a database of tissue-specific human enhancers. Nucleic Acids Res. 2007, 35(Database issue):D88-D92.
55. Williamson I., Hill R.E., Bickmore W.A. Enhancers: from developmental genetics to the genetics of common human disease. Dev. Cell 2011, 21:17-19.
56. Wilson M.D., Barbosa-Morais N.L., Schmidt D., Conboy C.M., Vanes L., Tybulewicz V.L., Fisher E.M., Tavaré S., Odom D.T. Species-specific transcription in mice carrying human chromosome 21. Science 2008, 322:434-438.
57. Xie W., Ling T., Zhou Y., Feng W., Zhu Q., Stunnenberg H.G., Grummt I., Tao W. The chromatin remodeling complex NuRD establishes the poised state of rRNA genes characterized by bivalent histone modifications and altered nucleosome positions. Proc. Natl. Acad. Sci. USA 2012, 109:8161-8166.
58. Yang R., Frank B., Hemminki K., Bartram C.R., Wappenschmidt B., Sutter C., Kiechle M., Bugert P., Schmutzler R.K., Arnold N., et al. SNPs in ultraconserved elements and familial breast cancer risk. Carcinogenesis 2008, 29:351-355.