Chromatin-Specific Regulation of Mammalian rDNA Transcription by Clustered TTF-I Binding Sites
Enhancers and promoters often contain multiple binding sites for the same transcription factor, suggesting that homotypic clustering of binding sites may serve a role in transcription regulation. Here we show that clustering of binding sites for the transcription termination factor TTF-I downstream of the pre-rRNA coding region specifies transcription termination, increases the efficiency of transcription initiation and affects the three-dimensional structure of rRNA genes. On chromatin templates, but not on free rDNA, clustered binding sites promote cooperative binding of TTF-I, loading TTF-I to the downstream terminators before it binds to the rDNA promoter. Interaction of TTF-I with target sites upstream and downstream of the rDNA transcription unit connects these distal DNA elements by forming a chromatin loop between the rDNA promoter and the terminators. The results imply that clustered binding sites increase the binding affinity of transcription factors in chromatin, thus influencing the timing and strength of DNA-dependent processes.
Vyšlo v časopise:
Chromatin-Specific Regulation of Mammalian rDNA Transcription by Clustered TTF-I Binding Sites. PLoS Genet 9(9): e32767. doi:10.1371/journal.pgen.1003786
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1003786
Souhrn
Enhancers and promoters often contain multiple binding sites for the same transcription factor, suggesting that homotypic clustering of binding sites may serve a role in transcription regulation. Here we show that clustering of binding sites for the transcription termination factor TTF-I downstream of the pre-rRNA coding region specifies transcription termination, increases the efficiency of transcription initiation and affects the three-dimensional structure of rRNA genes. On chromatin templates, but not on free rDNA, clustered binding sites promote cooperative binding of TTF-I, loading TTF-I to the downstream terminators before it binds to the rDNA promoter. Interaction of TTF-I with target sites upstream and downstream of the rDNA transcription unit connects these distal DNA elements by forming a chromatin loop between the rDNA promoter and the terminators. The results imply that clustered binding sites increase the binding affinity of transcription factors in chromatin, thus influencing the timing and strength of DNA-dependent processes.
Zdroje
1. BergOG, Hippel vonPH (1987) Selection of DNA binding sites by regulatory proteins. Statistical-mechanical theory and application to operators and promoters. Journal of Molecular Biology 193: 723–750.
2. BergOG, Hippel vonPH, Hippel vonPH (1988) Selection of DNA binding sites by regulatory proteins. Trends in Biochemical Sciences 13: 207–211.
3. GoteaV, ViselA, WestlundJM, NobregaMA, PennacchioLA, et al. (2010) Homotypic clusters of transcription factor binding sites are a key component of human promoters and enhancers. Genome Research 20: 565–577.
4. DavidsonEH (2002) A Genomic Regulatory Network for Development. Science 295: 1669–1678.
5. SchroederMD, PearceM, FakJ, FanH, UnnerstallU, et al. (2004) Transcriptional Control in the Segmentation Gene Network of Drosophila. PLoS Biol 2 (9) e271.
6. ErivesA, LevineM (2004) Coordinate enhancers share common organizational features in the Drosophila genome. Proc Natl Acad Sci USA 101: 3851–3856.
7. RheeHS, PughBF (2011) Comprehensive Genome-wide Protein-DNA Interactions Detected at Single-Nucleotide Resolution. Cell 147: 1408–1419.
8. SauerF, HansenSK, TjianR (1995) Multiple TAFIIs directing synergistic activation of transcription. Science 270: 1783–1788.
9. SauerF, HansenSK, TjianR (1995) DNA template and activator-coactivator requirements for transcriptional synergism by Drosophila bicoid. Science 270: 1825–1828.
10. HertelKJ, LynchKW, ManiatisT (1997) Common themes in the function of transcription and splicing enhancers. Current Opinion in Cell Biology 9: 350–357.
11. VasheeS, MelcherK, MelcherK, DingWV, et al. (1998) Evidence for two modes of cooperative DNA binding in vivo that do not involve direct protein-protein interactions. Current biology : CB 8: 452–458.
12. GrummtI, RosenbauerH, NiedermeyerI, MaierU, OhrleinA (1986) A repeated 18 bp sequence motif in the mouse rDNA spacer mediates binding of a nuclear factor and transcription termination. Cell 45: 837–846.
13. GrummtI, MaierU, OhrleinA, HassounaN, BachellerieJP (1985) Transcription of mouse rDNA terminates downstream of the 3″ end of 28S RNA and involves interaction of factors with repeated sequences in the 3″ spacer. Cell 43: 801–810.
14. La VolpeA, SimeoneA, SimeoneA, D'EspositoM, et al. (1985) Molecular analysis of the heterogeneity region of the human ribosomal spacer. Journal of Molecular Biology 183: 213–223.
15. BartschI, SchonebergC, GrummtI (1987) Evolutionary changes of sequences and factors that direct transcription termination of human and mouse ribsomal genes. Molecular and Cellular Biology 7: 2521–2529.
16. ClosJ, NormannA, OhrleinA, GrummtI (1986) The core promoter of mouse rDNA consists of two functionally distinct domains. Nucleic Acids Research 14: 7581–7595.
17. StrohnerR, NemethA, NemethA, JansaP, et al. (2001) NoRC–a novel member of mammalian ISWI-containing chromatin remodeling machines. The EMBO Journal 20: 4892–4900.
18. SantoroR, LiJ, GrummtI (2002) The nucleolar remodeling complex NoRC mediates heterochromatin formation and silencing of ribosomal gene transcription. Nature Genetics 32: 393–396.
19. YuanX, FengW, ImhofA, GrummtI, ZhouY (2007) Activation of RNA Polymerase I Transcription by Cockayne Syndrome Group B Protein and Histone Methyltransferase G9a. Molecular Cell 27: 585–595.
20. XieW, LingT, ZhouY, FengW, ZhuQ, et al. (2012) The chromatin remodeling complex NuRD establishes the poised state of rRNA genes characterized by bivalent histone modifications and altered nucleosome positions. Proceedings of the National Academy of Sciences 109: 8161–8166.
21. SanderEE, GrummtI (1997) Oligomerization of the transcription termination factor TTF-I: implications for the structural organization of ribosomal transcription units. Nucleic Acids Research 25: 1142–1147.
22. NémethA, GuibertS, TiwariVK, OhlssonR, LängstG (2008) Epigenetic regulation of TTF-I-mediated promoter–terminator interactions of rRNA genes. The EMBO Journal 27: 1255–1265.
23. DenissovS, LessardF, MayerC, StefanovskyV, van DrielM, et al. (2011) A model for the topology of active ribosomal RNA genes. EMBO reports 12 (3) 231–7 doi:10.1038/embor.2011.8
24. NémethA, LängstG (2011) Genome organization in and around the nucleolus. Trends in Genetics 27: 149–156.
25. GerberJK, GögelE, BergerC, WallischM, MüllerF, et al. (1997) Termination of mammalian rDNA replication: polar arrest of replication fork movement by transcription termination factor TTF-I. Cell 90: 559–567.
26. ZillnerK, Jerabek-WillemsenM, DuhrS, BraunD, LängstG, et al. (2012) Microscale thermophoresis as a sensitive method to quantify protein: nucleic acid interactions in solution. Methods Mol Biol 815: 241–252.
27. ColemanRA, PughBF (1995) Evidence for functional binding and stable sliding of the TATA binding protein on nonspecific DNA. J Biol Chem 270: 13850–13859.
28. MaerklSJ, QuakeSR (2007) A Systems Approach to Measuring the Binding Energy Landscapes of Transcription Factors. Science 315: 233–237.
29. BaaskeP, WienkenCJ, ReineckP, DuhrS, BraunD (2010) Optical Thermophoresis for Quantifying the Buffer Dependence of Aptamer Binding. Angew Chem Int Ed 49: 2238–2241.
30. BeckerPB, WuC (1992) Cell-free system for assembly of transcriptionally repressed chromatin from Drosophila embryos. Molecular and Cellular Biology 12: 2241–2249.
31. LangstG, BlankA, BeckerPB, GrummtI (1997) RNA polymerase I transcription on nucleosomal templates: the transcription termination factor TTF-I induces chromatin remodeling and relieves transcriptional repression. The EMBO Journal 16: 760–768.
32. LangstG, BeckerPB, GrummtI (1998) TTF-I determines the chromatin architecture of the active rDNA promoter. The EMBO Journal 17: 3135–3145.
33. ShiueC-N, BerksonRG, WrightAPH (2009) c-Myc induces changes in higher order rDNA structure on stimulation of quiescent cells. 28: 1833–1842.
34. LingJQ, LiT, HuJF, VuTH, ChenHL, QiuXW, CherryAM, HoffmanAR (2006) CTCF Mediates Interchromosomal Colocalization Between Igf2/H19 and Wsb1/Nf1. Science 312: 269–272.
35. StanojevicD, SmallS, LevineM (1991) Regulation of a segmentation stripe by overlapping activators and repressors in the Drosophila embryo. Science 254: 1385–1387.
36. ArnoneMI, DavidsonEH (1997) The hardwiring of development: organization and function of genomic regulatory systems. Development 124: 1851–1864.
37. PapatsenkoDA, MakeevVJ, LifanovAP, RegnierM, NazinaAG, et al. (2002) Extraction of Functional Binding Sites from Unique Regulatory Regions: The Drosophila Early Developmental Enhancers. Genome Research 12: 470–481.
38. BermanBP, NibuY, PfeifferBD, TomancakP, CelnikerSE, et al. (2002) Exploiting transcription factor binding site clustering to identify cis-regulatory modules involved in pattern formation in the Drosophila genome. Proc Natl Acad Sci USA 99: 757–762.
39. HalfonMS, GradY, ChurchGM, MichelsonAM (2002) Computation-based discovery of related transcriptional regulatory modules and motifs using an experimentally validated combinatorial model. Genome Research 12: 1019–1028.
40. RyeM, SætromP, HåndstadT, DrabløsF (2011) Clustered ChIP-Seq-defined transcription factor binding sites and histone modifications map distinct classes of regulatory elements. BMC Biology 9: 80.
41. VavouriT, ElgarG (2005) Prediction of cis-regulatory elements using binding site matrices — the successes, the failures and the reasons for both. Current Opinion in Genetics & Development 15: 395–402.
42. SommaMP, PisanoC, LaviaP (1991) The housekeeping promoter from the mouse CpG island HTF9 contains multiple protein-binding elements that are functionally redundant. Nucleic Acids Research 19: 2817–2824.
43. GinigerE, PtashneM (1988) Cooperative DNA binding of the yeast transcriptional activator GAL4. Proc Natl Acad Sci USA 85: 382–386.
44. LinYS, CareyM, PtashneM, GreenMR (1990) How different eukaryotic transcriptional activators can cooperate promiscuously. Nature 345: 359–361.
45. AndersonGM, FreytagSO (1991) Synergistic activation of a human promoter in vivo by transcription factor Sp1. Molecular and Cellular Biology 11: 1935–1943.
46. HeX, SameeMAH, BlattiC, SinhaS (2010) Thermodynamics-Based Models of Transcriptional Regulation by Enhancers: The Roles of Synergistic Activation, Cooperative Binding and Short-Range Repression. PLoS Comput Biol 6: e1000935.
47. VicentGP, ZaurinR, NachtAS, Font-MateuJ, Le DilyF, et al. (2010) Nuclear Factor 1 Synergizes with Progesterone Receptor on the Mouse Mammary Tumor Virus Promoter Wrapped around a Histone H3/H4 Tetramer by Facilitating Access to the Central Hormone-responsive Elements. Journal of Biological Chemistry 285: 2622–2631.
48. AdamsCC, WorkmanJL (1995) Binding of disparate transcriptional activators to nucleosomal DNA is inherently cooperative. Molecular and Cellular Biology 15: 1405–1421.
49. Kempers-VeenstraAE, OliemansJ, OffenbergH, DekkerAF, PiperPW, et al. (1986) 3′-End formation of transcripts from the yeast rRNA operon. The EMBO Journal 5: 2703.
50. CookPR (2003) Nongenic transcription, gene regulation and action at a distance. Journal of Cell Science 116: 4483–4491.
51. Lykke-AndersenS, MapendanoCK, Heick JensenT (2011) An ending is a new beginning: transcription termination supports re-initiation. Cell Cycle 10: 863–865.
52. ZentnerGE, SaiakhovaA, ManaenkovP, AdamsMD, ScacheriPC (2011) Integrative genomic analysis of human ribosomal DNA. Nucleic Acids Res 39: 4949–4960.
53. NémethA, StrohnerR, GrummtI, LängstG (2004) The chromatin remodeling complex NoRC and TTF-I cooperate in the regulation of the mammalian rRNA genes in vivo. Nucleic Acids Research 32: 4091–4099.
54. SeitherP, ZatsepinaO, HoffmannM, et al. (1997) Constitutive and strong association of PAF53 with RNA polymerase I. Chromosoma 106: 216–225.
55. NémethA, ConesaA, Santoyo-LopezJ, MedinaI, MontanerD, et al. (2010) Initial Genomics of the Human Nucleolus. PLoS Genet 6: e1000889 doi:10.1371/journal.pgen.1000889.g004
56. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25.
57. HeinzS, BennerC, SpannN, BertolinoE, LinYC, et al. (2010) Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities. Molecular Cell 38: 576–589.
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2013 Číslo 9
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- A Genome-Wide Systematic Analysis Reveals Different and Predictive Proliferation Expression Signatures of Cancerous vs. Non-Cancerous Cells
- Recent Acquisition of by Baka Pygmies
- The Condition-Dependent Transcriptional Landscape of
- Histone Chaperone NAP1 Mediates Sister Chromatid Resolution by Counteracting Protein Phosphatase 2A