The transcriptional regulatory code of eukaryotic cells - insights from genome-wide analysis of chromatin organization and transcription factor binding

Current Opinion in Cell Biology

Volumn 18, Issue 3, 2006, Pages 291-298

  Barrera, Leah O ^a   Ren, Bing ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HISTONE; OCTAMER TRANSCRIPTION FACTOR 4; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SOX2;

ACETYLATION; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; CPG ISLAND; DNA MICROARRAY; EUKARYOTIC CELL; GENE CONTROL; GENE EXPRESSION; GENE LOCUS; GENE MAPPING; GENE SEQUENCE; GENOME ANALYSIS; HUMAN; MOLECULAR INTERACTION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN MODIFICATION; PROTEIN VARIANT; REVIEW; TRANSCRIPTION REGULATION;

ANIMALS; BASE SEQUENCE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME MAPPING; DNA-BINDING PROTEINS; EUKARYOTIC CELLS; GENE EXPRESSION REGULATION; HISTONES; HUMANS; MICROARRAY ANALYSIS; NUCLEOSOMES; PROMOTER REGIONS (GENETICS); TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EUKARYOTA;

EID: 33646502826     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2006.04.002     Document Type: Review

References (58)

1. Bertone P., Stolc V., Royce T.E., Rozowsky J.S., Urban A.E., Zhu X., Rinn J.L., Tongprasit W., Samanta M., Weissman S., et al. Global identification of human transcribed sequences with genome tiling arrays. Science 306 (2004) 2242-2246
2. Carninci P., Kasukawa T., Katayama S., Gough J., Frith M.C., Maeda N., Oyama R., Ravasi T., Lenhard B., Wells C., et al. The transcriptional landscape of the mammalian genome. Science 309 (2005) 1559-1563
3. Cheng J., Kapranov P., Drenkow J., Dike S., Brubaker S., Patel S., Long J., Stern D., Tammana H., Helt G., et al. Transcriptional maps of 10 human chromosomes at 5-nucleotide resolution. Science 308 (2005) 1149-1154
4. Kimura K., Wakamatsu A., Suzuki Y., Ota T., Nishikawa T., Yamashita R., Yamamoto J., Sekine M., Tsuritani K., Wakaguri H., et al. Diversification of transcriptional modulation: large-scale identification and characterization of putative alternative promoters of human genes. Genome Res 16 (2006) 55-65
5. Su A.I., Wiltshire T., Batalov S., Lapp H., Ching K.A., Block D., Zhang J., Soden R., Hayakawa M., Kreiman G., et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 101 (2004) 6062-6067
6. International Human Genome Sequencing Consortium. Finishing the euchromatic sequence of the human genome. Nature 431 (2004) 931-945
7. Project Consortium ENCODE. The ENCODE (ENCyclopedia Of DNA Elements) Project. Science 306 (2004) 636-640
8. Sakaki Y., and Awaya A. Genome network project: a national project in post-sequence era. Tanpakushitsu Kakusan Koso 49 (2004) 2986-2992
9. Kamakaka R.T., and Biggins S. Histone variants: deviants?. Genes Dev 19 (2005) 295-310
10. Henikoff S., and Ahmad K. Assembly of variant histones into chromatin. Annu Rev Cell Dev Biol 21 (2005) 133-153
11. Ren B., and Dynlacht B.D. Use of chromatin immunoprecipitation assays in genome-wide location analysis of mammalian transcription factors. Methods Enzymol 376 (2004) 304-315
12. Weinmann A.S., and Farnham P.J. Identification of unknown target genes of human transcription factors using chromatin immunoprecipitation. Methods 26 (2002) 37-47
13. Kim T.H., Barrera L.O., Zheng M., Qu C., Singer M.A., Richmond T.A., Wu Y., Green R.D., and Ren B. A high-resolution map of active promoters in the human genome. Nature 436 (2005) 876-880. With arrays tiling all non-repetitive human DNA at 100-bp resolution, the authors use ChIP-chip against the TAF1 subunit of the general transcription factor IID to create a high-resolution map of active promoters in human fibroblast cells at steady-state. Pol II occupancy and active chromatin modifications are also assessed by ChIP-chip at these promoters, resulting in a global view of active promoter structure and their correlation with detected expression states via mRNA expression profiling.
14. Pokholok D.K., Harbison C.T., Levine S., Cole M., Hannett N.M., Lee T.I., Bell G.W., Walker K., Rolfe P.A., Herbolsheimer E., et al. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122 (2005) 517-527. Yeast genome-wide tiling arrays (266 bp resolution) are used to perform ChIP-chip for eight histone modifications (H3K9ac, H3K14ac, H4ac, H3K4me3, H3K4me2, H3K4me1, H3K36me3, H3K79me3) and two core histones (H3 and H4). This study resolves methylation events to the beginning, middle and end of actively transcribed regions and generally associates acetylation events with the start of active genes.
15. Cawley S., Bekiranov S., Ng H.H., Kapranov P., Sekinger E.A., Kampa D., Piccolboni A., Sementchenko V., Cheng J., Williams A.J., et al. Unbiased mapping of transcription factor binding sites along human chromosomes 21 and 22 points to widespread regulation of noncoding RNAs. Cell 116 (2004) 499-509
16. Buck M.J., Nobel A.B., and Lieb J.D. ChIPOTle: a user-friendly tool for the analysis of ChIP-chip data. Genome Biol 6 (2005) R97
17. Gibbons F.D., Proft M., Struhl K., and Roth F.P. Chipper: discovering transcription-factor targets from chromatin immunoprecipitation microarrays using variance stabilization. Genome Biol 6 (2005) R96
18. Li W., Meyer C.A., and Liu X.S. A hidden Markov model for analyzing ChIP-chip experiments on genome tiling arrays and its application to p53 binding sequences. Bioinformatics 21 Suppl 1 (2005) i274-i282
19. Zheng M., Barrera L.O., Ren B., and Wu Y. ChIP-chip: Data, Model, and Analysis. Proceedings of the American Statistical Association, Statistical Computing Section (2005), American Statistical Association, Alexandria, VA
20. van Steensel B., Delrow J., and Henikoff S. Chromatin profiling using targeted DNA adenine methyltransferase. Nat Genet 27 (2001) 304-308
21. Roh T.Y., Ngau W.C., Cui K., Landsman D., and Zhao K. High-resolution genome-wide mapping of histone modifications. Nat Biotechnol 22 (2004) 1013-1016
22. Impey S., McCorkle S.R., Cha-Molstad H., Dwyer J.M., Yochum G.S., Boss J.M., McWeeney S., Dunn J.J., Mandel G., and Goodman R.H. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 119 (2004) 1041-1054
23. Kim J., Bhinge A.A., Morgan X.C., and Iyer V.R. Mapping DNA-protein interactions in large genomes by sequence tag analysis of genomic enrichment. Nat Methods 2 (2005) 47-53
24. Wei C.L., Wu Q., Vega V.B., Chiu K.P., Ng P., Zhang T., Shahab A., Yong H.C., Fu Y., Weng Z., et al. A global map of p53 transcription-factor binding sites in the human genome. Cell 124 (2006) 207-219
25. Kim T.H., and Ren B. Genome-wide analysis of protein-DNA interactions. Annu Rev Genomics Hum Genet (2006) 7
26. Bernstein B.E., Liu C.L., Humphrey E.L., Perlstein E.O., and Schreiber S.L. Global nucleosome occupancy in yeast. Genome Biol 5 (2004) R62
27. Lee C.K., Shibata Y., Rao B., Strahl B.D., and Lieb J.D. Evidence for nucleosome depletion at active regulatory regions genome-wide. Nat Genet 36 (2004) 900-905
28. Yuan G.C., Liu Y.J., Dion M.F., Slack M.D., Wu L.F., Altschuler S.J., and Rando O.J. Genome-scale identification of nucleosome positions in S. cerevisiae. Science 309 (2005) 626-630. This study describes the use of a pioneering assay combining the use of high-resolution microarray detection with micrococcal nuclease digestion of yeast genomic DNA to define genomic regions occupied by nucleosomes or linkers. It provides a view of a large fraction of yeast genome at mononucleosomal level and resolves previously suggested regions of nucleosome depletion at promoters to a ∼150 bp region ∼200 bp upstream of the start codon.
29. Bernstein B.E., Kamal M., Lindblad-Toh K., Bekiranov S., Bailey D.K., Huebert D.J., McMahon S., Karlsson E.K., Kulbokas III E.J., Gingeras T.R., et al. Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120 (2005) 169-181. The authors describe unbiased mapping of active histone modifications in human by ChIP-chip against H3K9/K14ac and H3K4me2 and H3K4me3 over chromosomes 21 and 22. By performing ChIP-chip for H3K4me2 over orthologous human and mouse gene loci, they also suggest a role for methylation in the maintenance of active chromatin domains.
30. Kurdistani S.K., Tavazoie S., and Grunstein M. Mapping global histone acetylation patterns to gene expression. Cell 117 (2004) 721-733
31. •] probing 12 histone modifications in yeast at the mononucleosomal level. The authors use antibodies against individual modification states for H3 and H4 acetylation to define transcription-dependent and transcription-independent acetylation states. The study suggests that patterns of acetylation and methylation occur in few independent combinations and are often the result rather than the cause of transcription.
32. Liang G., Lin J.C., Wei V., Yoo C., Cheng J.C., Nguyen C.T., Weisenberger D.J., Egger G., Takai D., Gonzales F.A., et al. Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc Natl Acad Sci USA 101 (2004) 7357-7362
33. Roh T.Y., Cuddapah S., and Zhao K. Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 19 (2005) 542-552
34. Schubeler D., MacAlpine D.M., Scalzo D., Wirbelauer C., Kooperberg C., van Leeuwen F., Gottschling D.E., O'Neill L.P., Turner B.M., Delrow J., et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev 18 (2004) 1263-1271
35. Ng H.H., Robert F., Young R.A., and Struhl K. Targeted recruitment of Set1 histone methylase by elongating Pol II provides a localized mark and memory of recent transcriptional activity. Mol Cell 11 (2003) 709-719
36. Zhang H., Roberts D.N., and Cairns B.R. Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed/basal promoters for activation through histone loss. Cell 123 (2005) 219-231
37. Guillemette B., Bataille A.R., Gevry N., Adam M., Blanchette M., Robert F., and Gaudreau L. Variant histone H2A.Z is globally localized to the promoters of inactive yeast genes and regulates nucleosome positioning. PLoS Biol 3 (2005) e384
38. Raisner R.M., Hartley P.D., Meneghini M.D., Bao M.Z., Liu C.L., Schreiber S.L., Rando O.J., and Madhani H.D. Histone variant H2A.Z marks the 5′ ends of both active and inactive genes in euchromatin. Cell 123 (2005) 233-248
39. Lieb J.D., and Clarke N.D. Control of transcription through intragenic patterns of nucleosome composition. Cell 123 (2005) 1187-1190. This review posits a model of transcription control through intragenic patterns of nucleosome composition by highlighting recent findings regarding the link between histone H3 lysine 36 methylation and histone deacetylation towards the 3′ end of coding regions, as well as recent findings regarding the localization of the H2A.Z variant, which flanks nucleosome-free regions at the 5′ ends of genes.
40. Mito Y., Henikoff J.G., and Henikoff S. Genome-scale profiling of histone H3.3 replacement patterns. Nat Genet 37 (2005) 1090-1097. This study describes the genome-scale distribution of a histone variant in higher eukaryotes by using biotin-tagged histone H3 and H3.3 variants and a streptavidin pulldown system to isolate protein-DNA nucleosomal complexes in an adaptation of ChIP-chip with genomic tiling arrays in Drosophila. H3.3 is found to be enriched upstream and downsteam of nucleosome-depleted promoter regions in actively transcribed genes in Drosophila.
41. Kim T.H., Barrera L.O., Qu C., Van Calcar S., Trinklein N.D., Cooper S.J., Luna R.M., Glass C.K., Rosenfeld M.G., Myers R.M., et al. Direct isolation and identification of promoters in the human genome. Genome Res 15 (2005) 830-839
42. Brodsky A.S., Meyer C.A., Swinburne I.A., Hall G., Keenan B.J., Liu X.S., Fox E.A., and Silver P.A. Genomic mapping of RNA polymerase II reveals sites of co-transcriptional regulation in human cells. Genome Biol 6 (2005) R64
43. Guenther M.G., Jenner R.G., Chevalier B., Nakamura T., Croce C.M., Canaani E., and Young R.A. Global and hox-specific roles for the MLL1 methyltransferase. Proc Natl Acad Sci USA 102 (2005) 8603-8608
44. Greil F., van der Kraan I., Delrow J., Smothers J.F., de Wit E., Bussemaker H.J., van Driel R., Henikoff S., and van Steensel B. Distinct HP1 and Su(var)3-9 complexes bind to sets of developmentally coexpressed genes depending on chromosomal location. Genes Dev 17 (2003) 2825-2838
45. Kirmizis A., Bartley S.M., Kuzmichev A., Margueron R., Reinberg D., Green R., and Farnham P.J. Silencing of human polycomb target genes is associated with methylation of histone H3 Lys 27. Genes Dev 18 (2004) 1592-1605
46. Blais A., Tsikitis M., Acosta-Alvear D., Sharan R., Kluger Y., and Dynlacht B.D. An initial blueprint for myogenic differentiation. Genes Dev 19 (2005) 553-569
47. Boyer L.A., Lee T.I., Cole M.F., Johnstone S.E., Levine S.S., Zucker J.P., Guenther M.G., Kumar R.M., Murray H.L., Jenner R.G., et al. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122 (2005) 947-956. Localization of binding sites of known human embryonic stem cell (hESC) transcription factors - Oct4, Sox2, and Nanog - shows that they form interconnected autoregulatory and feed-forward loops. The model for the core transcriptional regulatory network based on the binding of these factors highlights their collaborative roles in maintaining hESC self-renewal and pluripotency.
48. Li Z., Van Calcar S., Qu C., Cavenee W.K., Zhang M.Q., and Ren B. A global transcriptional regulatory role for c-Myc in Burkitt's lymphoma cells. Proc Natl Acad Sci USA 100 (2003) 8164-8169
49. Odom D.T., Zizlsperger N., Gordon D.B., Bell G.W., Rinaldi N.J., Murray H.L., Volkert T.L., Schreiber J., Rolfe P.A., Gifford D.K., et al. Control of pancreas and liver gene expression by HNF transcription factors. Science 303 (2004) 1378-1381
50. Lee T.I., Rinaldi N.J., Robert F., Odom D.T., Bar-Joseph Z., Gerber G.K., Hannett N.M., Harbison C.T., Thompson C.M., Simon I., et al. Transcriptional regulatory networks in Saccharomyces cerevisiae. Science 298 (2002) 799-804
51. Simon I., Barnett J., Hannett N., Harbison C.T., Rinaldi N.J., Volkert T.L., Wyrick J.J., Zeitlinger J., Gifford D.K., Jaakkola T.S., et al. Serial regulation of transcriptional regulators in the yeast cell cycle. Cell 106 (2001) 697-708
52. Zhang X., Odom D.T., Koo S.H., Conkright M.D., Canettieri G., Best J., Chen H., Jenner R., Herbolsheimer E., Jacobsen E., et al. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc Natl Acad Sci USA 102 (2005) 4459-4464. This detailed study of CREB occupancy and phosphorylation state at gene promoters in different tissues demonstrates that binding is not sufficient to explain tissue-specific regulation of target genes, and that binding of the histone acetyltransferase/co-activator CREB-binding protein (CBP) mediated by additional regulatory partners is required.
53. Harbison C.T., Gordon D.B., Lee T.I., Rinaldi N.J., Macisaac K.D., Danford T.W., Hannett N.M., Tagne J.B., Reynolds D.B., Yoo J., et al. Transcriptional regulatory code of a eukaryotic genome. Nature 431 (2004) 99-104
54. Euskirchen G., Royce T.E., Bertone P., Martone R., Rinn J.L., Nelson F.K., Sayward F., Luscombe N.M., Miller P., Gerstein M., et al. CREB binds to multiple loci on human chromosome 22. Mol Cell Biol 24 (2004) 3804-3814
55. Martone R., Euskirchen G., Bertone P., Hartman S., Royce T.E., Luscombe N.M., Rinn J.L., Nelson F.K., Miller P., Gerstein M., et al. Distribution of NF-κB-binding sites across human chromosome 22. Proc Natl Acad Sci USA 100 (2003) 12247-12252
56. Carroll J.S., Liu X.S., Brodsky A.S., Li W., Meyer C.A., Szary A.J., Eeckhoute J., Shao W., Hestermann E.V., Geistlinger T.R., et al. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122 (2005) 33-43. Unbiased mapping of estrogen receptor (ER) over human chromosomes 21 and 22 shows limited binding of ER and that the binding that does occur is at sites that are far from transcription start sites of regulated genes. In addition to deducing the requirement for the binding of a Forkhead factor co-activator protein by motif-analysis, the authors use ChIP for Pol II occupancy and a chromosome capture assay for promoter-enhancer interaction to evaluate the functionality of the sites identified.
57. Alberts B., Johnson A., Lewis J., Raff M., Roberts K., and Walter P. Molecular Biology of the Cell. edn 4 (2002), Garland Publishing, New York
58. Dekker J., Rippe K., Dekker M., and Kleckner N. Capturing chromosome conformation. Science 295 (2002) 1306-1311