RNA Processing Factors Swd2.2 and Sen1 Antagonize RNA Pol III-Dependent Transcription and the Localization of Condensin at Pol III Genes

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Failure to condense chromosomes prior to anaphase onset can lead to genome instability. The evolutionary-conserved condensin complex drives chromosome condensation, probably by changing the topology of chromatin around its binding sites. Condensin localizes to regions of high transcription, suggesting that some transcription-associated feature(s) direct its association with chromatin. Here we considered that transcription-dependent DNA:RNA hybrids or topological stress could be involved in recruiting condensin. Our data show that condensin is indeed enriched at regions accumulating DNA:RNA hybrids but that they are not involved in its recruitment. Rather, we identify a mutant combination where increased transcription by RNA Pol III is associated locally with stronger topological stress. Strikingly the localization of condensin is dramatically enhanced at the same loci and we show that topological stress contributes to this enhanced association. Our data strengthen the idea that transcription creates the environment necessary to recruit condensin in mitosis.

Vyšlo v časopise: RNA Processing Factors Swd2.2 and Sen1 Antagonize RNA Pol III-Dependent Transcription and the Localization of Condensin at Pol III Genes. PLoS Genet 10(11): e32767. doi:10.1371/journal.pgen.1004794
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004794

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Zdroje

1. HiranoT, MitchisonTJ (1994) A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79: 449–458.

2. KimuraK, HiranoT (1997) ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell 90: 625–634.

3. St-PierreJ, DouziechM, BazileF, PascariuM, BonneilE, et al. (2009) Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. Mol Cell 34: 416–426.

4. PiazzaI, HaeringCH, RutkowskaA (2013) Condensin: crafting the chromosome landscape. Chromosoma 122: 175–190.

5. D'AmbrosioC, SchmidtCK, KatouY, KellyG, ItohT, et al. (2008) Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22: 2215–2227.

6. KimJH, ZhangT, WongNC, DavidsonN, MaksimovicJ, et al. (2013) Condensin I associates with structural and gene regulatory regions in vertebrate chromosomes. Nat Commun 4: 2537.

7. GruberS, ErringtonJ (2009) Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137: 685–696.

8. KranzAL, JiaoCY, WinterkornLH, AlbrittonSE, KramerM, et al. (2013) Genome-wide analysis of condensin binding in Caenorhabditis elegans. Genome Biol 14: R112.

9. Clemente-BlancoA, SenN, Mayan-SantosM, SacristanMP, GrahamB, et al. (2011) Cdc14 phosphatase promotes segregation of telomeres through repression of RNA polymerase II transcription. Nat Cell Biol 13: 1450–1456.

10. Clemente-BlancoA, Mayan-SantosM, SchneiderDA, MachinF, JarmuzA, et al. (2009) Cdc14 inhibits transcription by RNA polymerase I during anaphase. Nature 458: 219–222.

11. AguileraA, Garcia-MuseT (2012) R loops: from transcription byproducts to threats to genome stability. Mol Cell 46: 115–124.

12. PiazzaI, RutkowskaA, OriA, WalczakM, MetzJ, et al. (2014) Association of condensin with chromosomes depends on DNA binding by its HEAT-repeat subunits. Nat Struct Mol Biol 21: 560–568.

13. GrieseJJ, WitteG, HopfnerKP (2010) Structure and DNA binding activity of the mouse condensin hinge domain highlight common and diverse features of SMC proteins. Nucleic Acids Res 38: 3454–3465.

14. Castellano-PozoM, Santos-PereiraJM, RondonAG, BarrosoS, AndujarE, et al. (2013) R loops are linked to histone h3 s10 phosphorylation and chromatin condensation. Mol Cell 52: 583–590.

15. AkaiY, KurokawaY, NakazawaN, Tonami-MurakamiY, SuzukiY, et al. (2011) Opposing role of condensin hinge against replication protein A in mitosis and interphase through promoting DNA annealing. Open Biol 1: 110023.

16. GinnoPA, LottPL, ChristensenHC, KorfI, ChedinF (2012) R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol Cell 45: 814–825.

17. TsaoYP, WuHY, LiuLF (1989) Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell 56: 111–118.

18. NaughtonC, AvlonitisN, CorlessS, PrendergastJG, MatiIK, et al. (2013) Transcription forms and remodels supercoiling domains unfolding large-scale chromatin structures. Nat Struct Mol Biol 20: 387–395.

19. TevesSS, HenikoffS (2014) Transcription-generated torsional stress destabilizes nucleosomes. Nat Struct Mol Biol 21: 88–94.

20. KouzineF, GuptaA, BaranelloL, WojtowiczD, Ben-AissaK, et al. (2013) Transcription-dependent dynamic supercoiling is a short-range genomic force. Nat Struct Mol Biol 20: 396–403.

21. KimuraK, RybenkovVV, CrisonaNJ, HiranoT, CozzarelliNR (1999) 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 98: 239–248.

22. VanoosthuyseV, LegrosP, van der SarSJA, YvertG, TodaK, et al. (2014) CPF-associated phosphatase activity opposes condensin-mediated chromosome condensation. PLoS Genet 10: e1004415.

23. SakaY, SutaniT, YamashitaY, SaitohS, TakeuchiM, et al. (1994) Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO J 13: 4938–4952.

24. RichardP, ManleyJL (2009) Transcription termination by nuclear RNA polymerases. Genes Dev 23: 1247–1269.

25. KimHD, ChoeJ, SeoYS (1999) The sen1(+) gene of Schizosaccharomyces pombe, a homologue of budding yeast SEN1, encodes an RNA and DNA helicase. Biochemistry 38: 14697–14710.

26. PorruaO, LibriD (2013) A bacterial-like mechanism for transcription termination by the Sen1p helicase in budding yeast. Nat Struct Mol Biol 20: 884–891.

27. SchrammL, HernandezN (2002) Recruitment of RNA polymerase III to its target promoters. Genes Dev 16: 2593–2620.

28. ChanYA, AristizabalMJ, LuPY, LuoZ, HamzaA, et al. (2014) Genome-Wide Profiling of Yeast DNA:RNA Hybrid Prone Sites with DRIP-Chip. PLoS Genet 10: e1004288.

29. WuH, LimaWF, CrookeST (2001) Investigating the structure of human RNase H1 by site-directed mutagenesis. J Biol Chem 276: 23547–23553.

30. El HageA, FrenchSL, BeyerAL, TollerveyD (2010) Loss of Topoisomerase I leads to R-loop-mediated transcriptional blocks during ribosomal RNA synthesis. Genes Dev 24: 1546–1558.

31. PhillipsDD, GarbocziDN, SinghK, HuZ, LepplaSH, et al. (2013) The sub-nanomolar binding of DNA-RNA hybrids by the single-chain Fv fragment of antibody S9.6. J Mol Recognit 26: 376–381.

32. LemieuxC, BachandF (2009) Cotranscriptional recruitment of the nuclear poly(A)-binding protein Pab2 to nascent transcripts and association with translating mRNPs. Nucleic Acids Res 37: 3418–3430.

33. UemuraT, OhkuraH, AdachiY, MorinoK, ShiozakiK, et al. (1987) DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50: 917–925.

34. LeTB, ImakaevMV, MirnyLA, LaubMT (2013) High-resolution mapping of the spatial organization of a bacterial chromosome. Science 342: 731–734.

35. Hamperl S, Cimprich KA (2014) The contribution of co-transcriptional RNA:DNA hybrid structures to DNA damage and genome instability. DNA Repair (Amst).

36. GinnoPA, LimYW, LottPL, KorfI, ChedinF (2013) GC skew at the 5′ and 3′ ends of human genes links R-loop formation to epigenetic regulation and transcription termination. Genome Res 23: 1590–1600.

37. WilkinsBJ, RallNA, OstwalY, KruitwagenT, Hiragami-HamadaK, et al. (2014) A cascade of histone modifications induces chromatin condensation in mitosis. Science 343: 77–80.

38. StirlingPC, ChanYA, MinakerSW, AristizabalMJ, BarrettI, et al. (2012) R-loop-mediated genome instability in mRNA cleavage and polyadenylation mutants. Genes Dev 26: 163–175.

39. MischoHE, Gomez-GonzalezB, GrzechnikP, RondonAG, WeiW, et al. (2011) Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol Cell 41: 21–32.

40. Nguyen NT, Saguez C, Conesa C, Lefebvre O, Acker J (2014) Identification of proteins associated with RNA polymerase III using a modified tandem chromatin affinity purification. Gene. E-pub ahead of print. doi:10.1016/j.gene.2014.07.070

41. DroletM (2006) Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol Microbiol 59: 723–730.