GAGA Factor Maintains Nucleosome-Free Regions and Has a Role in RNA Polymerase II Recruitment to Promoters

PLoS Genetics

Volumn 11, Issue 3, 2015, Pages

  Fuda, Nicholas J ^a,c   Guertin, Michael J ^a,d   Sharma, Sumeet ^a,e   Danko, Charles G ^a,b   Martins, André L ^b   Siepel, Adam ^b,f   Lis, John T ^a  

^a Department of Obstetrics Gynecology   (United States)

^b Program on Infrastructure Policy   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f Simons Center for Quantitative Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAGA FACTOR; REGULATOR PROTEIN; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR M1BP; UNCLASSIFIED DRUG; BEAF-32 PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; EYE PROTEIN; M1BP PROTEIN, DROSOPHILA; NUCLEOSOME; TRL PROTEIN, DROSOPHILA;

ANIMAL CELL; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA; GENE MAPPING; GENE SEQUENCE; INSECT CELL; INSECT GENETICS; NONHUMAN; NUCLEOSOME; PROMOTER REGION; RNA INTERFERENCE; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; DROSOPHILA MELANOGASTER; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

ANIMALS; BINDING SITES; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE PROTEINS; GENE KNOCKDOWN TECHNIQUES; NUCLEOSOMES; PROMOTER REGIONS, GENETIC; RNA POLYMERASE II; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84926306750     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005108     Document Type: Article

References (63)

1. Fuda NJ, Ardehali MB, Lis JT, (2009) Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature 461: 186–192. doi: 10.1038/nature08449 19741698
2. Adelman K, Lis JT, (2012) Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat Rev Genet 13: 720–731. doi: 10.1038/nrg3293 22986266
3. Lis JT, Mason P, Peng J, Price DH, Werner J, (2000) P-TEFb kinase recruitment and function at heat shock loci. Genes Dev 14: 792–803. 10766736
4. Lee C, Li X, Hechmer A, Eisen M, Biggin MD, et al. (2008) NELF and GAGA factor are linked to promoter-proximal pausing at many genes in Drosophila. Mol Cell Biol 28: 3290–3300. doi: 10.1128/MCB.02224-07 18332113
5. Wilkins RC, Lis JT, (1998) GAGA factor binding to DNA via a single trinucleotide sequence element. Nucleic Acids Res 26: 2672–2678. 9592153
6. Omichinski JG, Pedone P V, Felsenfeld G, Gronenborn AM, Clore GM, (1997) The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode. Nat Struct Biol 4: 122–132. 9033593
7. Farkas G, Gausz J, Galloni M, Reuter G, Gyurkovics H, et al. (1994) The Trithorax-like gene encodes Drosophila GAGA factor. Nature 371: 806–808. 7935842
8. Hagstrom K, Muller M, Schedl P, (1997) A Polycomb and GAGA dependent silencer adjoins the Fab-7 boundary in the Drosophila bithorax complex. Genetics 146: 1365–1380. 9258680
9. Horard B, Tatout C, Poux S, Pirrotta V, (2000) Structure of a polycomb response element and in vitro binding of polycomb group complexes containing GAGA factor. Mol Cell Biol 20: 3187–3197. 10757803
10. Pedone P V, Ghirlando R, Clore GM, Gronenborn a M, Felsenfeld G, et al. (1996) The single Cys2-His2 zinc finger domain of the GAGA protein flanked by basic residues is sufficient for high-affinity specific DNA binding. Proc Natl Acad Sci U S A 93: 2822–2826. 8610125
11. Van Steensel B, Delrow J, Bussemaker HJ, (2003) Genomewide analysis of Drosophila GAGA factor target genes reveals context-dependent DNA binding. Proc Natl Acad Sci U S A 100: 2580–2585. 12601174
12. Omelina ES, Baricheva EM, Oshchepkov DY, Merkulova TI, (2011) Analysis and recognition of the GAGA transcription factor binding sites in Drosophila genes. Comput Biol Chem 35: 363–370. doi: 10.1016/j.compbiolchem.2011.10.008 22099633
13. Katsani KR, Hajibagheri MAN, Verrijzer CP, (1999) Co-operative DNA binding by GAGA transcription factor requires the conserved BTB/POZ domain and reorganizes promoter topology. EMBO J 18: 698–708. 9927429
14. Espinás ML, Jiménez-García E, Vaquero a, Canudas S, Bernués J, et al. (1999) The N-terminal POZ domain of GAGA mediates the formation of oligomers that bind DNA with high affinity and specificity. J Biol Chem 274: 16461–16469. 10347208
15. Read D, Butte MJ, Dernburg AF, Frasch M, Kornberg TB, (2000) Functional studies of the BTB domain in the Drosophila GAGA and Mod(mdg4) proteins. Nucleic Acids Res 28: 3864–3870. 11024164
16. Pagans S, Ortiz-Lombardía M, Espinás ML, Bernués J, Azorín F, (2002) The Drosophila transcription factor tramtrack (TTK) interacts with Trithorax-like (GAGA) and represses GAGA-mediated activation. Nucleic Acids Res 30: 4406–4413. 12384587
17. Schwendemann A, Lehmann M, (2002) Pipsqueak and GAGA factor act in concert as partners at homeotic and many other loci. Proc Natl Acad Sci U S A 99: 12883–12888. 12271134
18. Vaquero a, Espinás ML, Azorin F, Bernueś J, (2000) Functional mapping of the GAGA factor assigns its transcriptional activity to the C-terminal glutamine-rich domain. J Biol Chem 275: 19461–19468. 10764754
19. Vaquero A, Blanch M, Espinás ML, Bernués J, (2008) Activation properties of GAGA transcription factor. Biochim Biophys Acta 1779: 312–317. doi: 10.1016/j.bbagrm.2008.02.005 18394434
20. Wilkins RC, Lis JT, (1999) DNA distortion and multimerization: novel functions of the glutamine-rich domain of GAGA factor. J Mol Biol 285: 515–525. 9878426
21. Agianian B, Leonard K, Bonte E, Van der Zandt H, Becker PB, et al. (1999) The glutamine-rich domain of the Drosophila GAGA factor is necessary for amyloid fibre formation in vitro, but not for chromatin remodelling. J Mol Biol 285: 527–544. 9878427
22. Granok H, Leibovitch BA, Elgin SC, (2001) A heat-shock-activated cDNA encoding GAGA factor rescues some lethal mutations in the Drosophila melanogaster Trithorax-like gene. Genet Res 78: 13–21. 11556133
23. Nègre N, Brown CD, Shah PK, Kheradpour P, Morrison C a, et al. (2010) A comprehensive map of insulator elements for the Drosophila genome. PLoS Genet 6: e1000814. doi: 10.1371/journal.pgen.1000814 20084099
24. Kasinathan S, Orsi GA, Zentner GE, Ahmad K, Henikoff S, (2014) High-resolution mapping of transcription factor binding sites on native chromatin. Nat Methods 11: 203–209. doi: 10.1038/nmeth.2766 24336359
25. Hendrix D a, Hong J-W, Zeitlinger J, Rokhsar DS, Levine MS, (2008) Promoter elements associated with RNA Pol II stalling in the Drosophila embryo. Proc Natl Acad Sci U S A 105: 7762–7767. doi: 10.1073/pnas.0802406105 18505835
26. Kwak H, Fuda NJ, Core LJ, Lis JT, (2013) Precise Maps of RNA Polymerase Reveal How Promoters Direct Initiation and Pausing. Science (80-) 339: 950–953.
27. Wang YV, Tang H, Gilmour DS, (2005) Identification In Vivo of Different Rate-Limiting Steps Associated with Transcriptional Activators in the Presence and Absence of a GAGA Element. Mol Cell Biol 25: 3543–3552. 15831460
28. Lee H, Kraus KW, Wolfner MF, Lis JT, (1992) DNA sequence requirements for generating paused polymerase at the start of hsp70. Genes Dev 6: 284–295. 1737619
29. Adkins NL, Hagerman TA, Georgel P, (2006) GAGA protein: a multi-faceted transcription factor. Biochem cell Biol 84: 559–567. 16936828
30. Tsukiyama T, Becker PB, Wu C, (1994) ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature 367: 525–532. 8107823
31. Tsukiyama T, Wu C, (1995) Purification and Properties of an ATP-Dependent Nucleosome Remodeling Factor. Cell 83: 1011–1020. 8521501
32. Okada M, Hirose S, (1998) Chromatin remodeling mediated by Drosophila GAGA factor and ISWI activates fushi tarazu gene transcription in vitro. Mol Cell Biol 18: 2455–2461. 9566866
33. Nakayama T, Nishioka K, Dong Y-X, Shimojima T, Hirose S, (2007) Drosophila GAGA factor directs histone H3.3 replacement that prevents the heterochromatin spreading. Genes Dev 21: 552–561. 17344416
34. Core LJ, Waterfall JJ, Lis JT, (2008) Nascent RNA Sequencing Reveals Widespread Pausing and Divergent Initiation at Human Promoters. Science (80-) 322: 1845–1848.
35. Chopra VS, Hendrix D a, Core LJ, Tsui C, Lis JT, et al. (2011) The Polycomb Group Mutant esc Leads to Augmented Levels of Paused Pol II in the Drosophila Embryo. Mol Cell 42: 837–844. doi: 10.1016/j.molcel.2011.05.009 21700228
36. Larschan E, Bishop EP, Kharchenko P V, Core L, Lis JT, et al. (2011) X chromosome dosage compensation via enhanced transcriptional elongation in Drosophila. Nature 471: 115–118. doi: 10.1038/nature09757 21368835
37. Core LJ, Waterfall JJ, Gilchrist DA, Fargo DC, Kwak H, et al. (2012) Defining the status of RNA polymerase at promoters. Cell Rep 2: 1025–1035. doi: 10.1016/j.celrep.2012.08.034 23062713
38. Muse GW, Gilchrist D a, Nechaev S, Shah R, Parker JS, et al. (2007) RNA polymerase is poised for activation across the genome. Nat Genet 39: 1507–1511. 17994021
39. Robinson MD, McCarthy DJ, Smyth GK, (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140. doi: 10.1093/bioinformatics/btp616 19910308
40. Jonkers I, Kwak H, Lis JT, (2014) Genome-wide dynamics of Pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons. Elife 3: e02407. doi: 10.7554/eLife.02407 24843027
41. Henriques T, Gilchrist DA, Nechaev S, Bern M, Muse GW, et al. (2013) Stable pausing by RNA polymerase II provides an opportunity to target and integrate regulatory signals. Mol Cell 52: 517–528. doi: 10.1016/j.molcel.2013.10.001 24184211
42. Kharchenko P V, Alekseyenko AA, Schwartz YB, Minoda A, Riddle NC, et al. (2011) Comprehensive analysis of the chromatin landscape in Drosophila melanogaster. Nature 471: 480–485. doi: 10.1038/nature09725 21179089
43. Mathelier A, Zhao X, Zhang AW, Parcy F, Worsley-Hunt R, et al. (2014) JASPAR 2014: an extensively expanded and updated open-access database of transcription factor binding profiles. Nucleic Acids Res 42: D142–D147. doi: 10.1093/nar/gkt997 24194598
44. Liang J, Lacroix L, Gamot A, Cuddapah S, Queille S, et al. (2014) Chromatin immunoprecipitation indirect peaks highlight long-range interactions of insulator proteins and Pol II pausing. Mol Cell 53: 672–681. doi: 10.1016/j.molcel.2013.12.029 24486021
45. Li J, Gilmour DS (2013) Distinct mechanisms of transcriptional pausing orchestrated by GAGA factor and M1BP, a novel transcription factor. EMBO J.
46. Sexton T, Yaffe E, Kenigsberg E, Bantignies F, Leblanc B, et al. (2012) Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148: 458–472. doi: 10.1016/j.cell.2012.01.010 22265598
47. Xiao H, Sandaltzopoulos R, Wang H-M, Hamiche A, Ranallo R, et al. (2001) Dual Functions of Largest NURF Subunit NURF301 in Nucleosome Sliding and Transcription Factor Interactions. Mol Cell 8: 531–543. 11583616
48. Gilchrist D a, Dos Santos G, Fargo DC, Xie B, Gao Y, et al. (2010) Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation. Cell 143: 540–551. doi: 10.1016/j.cell.2010.10.004 21074046
49. Core LJ, Lis JT, (2008) Transcription regulation through promoter-proximal pausing of RNA polymerase II. Science 319: 1791–1792. doi: 10.1126/science.1150843 18369138
50. Danko CG, Hah N, Luo X, Martins AL, Core L, et al. (2013) Signaling pathways differentially affect RNA polymerase II initiation, pausing, and elongation rate in cells. Mol Cell 50: 212–222. doi: 10.1016/j.molcel.2013.02.015 23523369
51. Wada T, Takagi T, Yamaguchi Y, Ferdous a, Imai T, et al. (1998) DSIF, a novel transcription elongation factor that regulates RNA polymerase II processivity, is composed of human Spt4 and Spt5 homologs. Genes Dev 12: 343–356. 9450929
52. Yamaguchi Y, Inukai N, Narita T, Wada T, Handa H, (2002) Evidence that Negative Elongation Factor Represses Transcription Elongation through Binding to a DRB Sensitivity-Inducing Factor/RNA Polymerase II Complex and RNA. Mol Cell Biol 22: 2918–2927. 11940650
53. Krumm A, Hickey LB, Groudine M, (1995) Promoter-proximal pausing of RNA polymerase II defines a general rate-limiting step after transcription initiation. Genes Dev 9: 559–572. 7698646
54. Blau J, Xiao H, McCracken S, O’Hare P, Greenblatt J, et al. (1996) Three functional classes of transcriptional activation domain. Mol Cell Biol 16: 2044–2055. 8628270
55. Chopra VS, Srinivasan A, Kumar RP, Mishra K, Basquin D, et al. (2008) Transcriptional activation by GAGA factor is through its direct interaction with dmTAF3. Dev Biol 317: 660–670. doi: 10.1016/j.ydbio.2008.02.008 18367161
56. Li J, Liu Y, Rhee HS, Ghosh SKB, Bai L, et al. (2013) Kinetic competition between elongation rate and binding of NELF controls promoter-proximal pausing. Mol Cell 50: 711–722. doi: 10.1016/j.molcel.2013.05.016 23746353
57. Fuda NJ, Buckley MS, Wei W, Core LJ, Waters CT, et al. (2012) Fcp1 dephosphorylation of the RNA polymerase II C-terminal domain is required for efficient transcription of heat shock genes. Mol Cell Biol 32: 3428–3437. doi: 10.1128/MCB.00247-12 22733996
58. O’Brien T, Wilkins RC, Giardina C, Lis JT, (1995) Distribution of GAGA protein on Drosophila genes in vivo. Genes Dev 9: 1098–1110. 7744251
59. Boehm AK, Saunders A, Werner J, Lis JT, (2003) Transcription Factor and Polymerase Recruitment, Modification, and Movement on dhsp70 In Vivo in the Minutes following Heat Shock. Mol Cell Biol 23: 7628–7637. 14560008
60. Guertin MJ, Lis JT, (2010) Chromatin landscape dictates HSF binding to target DNA elements. PLoS Genet 6.
61. Ingolia NT, Ghaemmaghami S, Newman JRS, Weissman JS, (2009) Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324: 218–223. doi: 10.1126/science.1168978 19213877
62. Salmon-Divon M, Dvinge H, Tammoja K, Bertone P, (2010) PeakAnalyzer: genome-wide annotation of chromatin binding and modification loci. BMC Bioinformatics 11: 415. doi: 10.1186/1471-2105-11-415 20691053
63. Grant CE, Bailey TL, Noble WS, (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27: 1017–1018. doi: 10.1093/bioinformatics/btr064 21330290