CPF-Associated Phosphatase Activity Opposes Condensin-Mediated Chromosome Condensation

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Failure to properly condense chromosomes prior to their segregation in mitosis can lead to genome instability. The evolutionary-conserved condensin complex is key to the condensation process but the molecular mechanisms underlying its localization pattern on chromosomes remain unclear. Previous observations showed that the localization of condensin is intimately linked to regions of high transcription, although, somewhat paradoxically, its association with chromatin is disrupted by a processive polymerase activity. Here we identify several RNA processing factors as negative regulators of condensin in fission yeast. Two of these factors associate with PP1 phosphatase as an independent entity within the Cleavage and Polyadenylation Factor (CPF), a complex key for 3′ end RNA processing. Lack of this module induces only minor and context-dependent effects on gene expression. Our data suggest that this module helps maintaining the proper level of phosphatase activity within the CPF and thereby opposes the function of condensin in mitotic chromosome condensation.

Vyšlo v časopise: CPF-Associated Phosphatase Activity Opposes Condensin-Mediated Chromosome Condensation. PLoS Genet 10(6): e32767. doi:10.1371/journal.pgen.1004415
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004415

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Zdroje

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

2. TadaK, SusumuH, SakunoT, WatanabeY (2011) Condensin association with histone H2A shapes mitotic chromosomes. Nature 474 : 477–483.

3. 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.

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

5. TanakaA, TanizawaH, SriswasdiS, IwasakiO, ChatterjeeAG, et al. (2012) Epigenetic regulation of condensin-mediated genome organization during the cell cycle and upon DNA damage through histone H3 lysine 56 acetylation. Mol Cell 48 : 532–546.

6. IwasakiO, TanakaA, TanizawaH, GrewalSI, NomaK (2010) Centromeric localization of dispersed Pol III genes in fission yeast. Mol Biol Cell 21 : 254–265.

7. PekJW, KaiT (2011) A role for vasa in regulating mitotic chromosome condensation in Drosophila. Curr Biol 21 : 39–44.

8. PekJW, KaiT (2011) DEAD-box RNA helicase Belle/DDX3 and the RNA interference pathway promote mitotic chromosome segregation. Proc Natl Acad Sci U S A 108 : 12007–12012.

9. SchubertT, PuschMC, DiermeierS, BenesV, KremmerE, et al. (2012) Df31 protein and snoRNAs maintain accessible higher-order structures of chromatin. Mol Cell 48 : 434–444.

10. 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.

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

12. XingH, VanderfordNL, SargeKD (2008) The TBP-PP2A mitotic complex bookmarks genes by preventing condensin action. Nat Cell Biol 10 : 1318–1323.

13. ParsonsGG, SpencerCA (1997) Mitotic repression of RNA polymerase II transcription is accompanied by release of transcription elongation complexes. Mol Cell Biol 17 : 5791–5802.

14. LoomisRJ, NaoeY, ParkerJB, SavicV, BozovskyMR, et al. (2009) Chromatin binding of SRp20 and ASF/SF2 and dissociation from mitotic chromosomes is modulated by histone H3 serine 10 phosphorylation. Mol Cell 33 : 450–461.

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

16. 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.

17. KimM, KroganNJ, VasiljevaL, RandoOJ, NedeaE, et al. (2004) The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II. Nature 432 : 517–522.

18. SugiyamaT, Sugioka-SugiyamaR, HadaK, NiwaR (2012) Rhn1, a nuclear protein, is required for suppression of meiotic mRNAs in mitotically dividing fission yeast. PLoS One 7: e42962.

19. LemayJF, D'AmoursA, LemieuxC, LacknerDH, St-SauveurVG, et al. (2010) The nuclear poly(A)-binding protein interacts with the exosome to promote synthesis of noncoding small nucleolar RNAs. Mol Cell 37 : 34–45.

20. 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.

21. PetrovaB, DehlerS, KruitwagenT, HericheJK, MiuraK, et al. (2013) Quantitative analysis of chromosome condensation in fission yeast. Mol Cell Biol 33 : 984–998.

22. KimHS, VanoosthuyseV, FillinghamJ, RoguevA, WattS, et al. (2009) An acetylated form of histone H2A.Z regulates chromosome architecture in Schizosaccharomyces pombe. Nat Struct Mol Biol 16 : 1286–1293.

23. RoguevA, ShevchenkoA, SchaftD, ThomasH, StewartAF (2004) A comparative analysis of an orthologous proteomic environment in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Mol Cell Proteomics 3 : 125–132.

24. WangSW, AsakawaK, WinTZ, TodaT, NorburyCJ (2005) Inactivation of the pre-mRNA cleavage and polyadenylation factor Pfs2 in fission yeast causes lethal cell cycle defects. Mol Cell Biol 25 : 2288–2296.

25. NedeaE, HeX, KimM, PootoolalJ, ZhongG, et al. (2003) Organization and function of APT, a subcomplex of the yeast cleavage and polyadenylation factor involved in the formation of mRNA and small nucleolar RNA 3′-ends. J Biol Chem 278 : 33000–33010.

26. NedeaE, NalbantD, XiaD, TheoharisNT, SuterB, et al. (2008) The Glc7 phosphatase subunit of the cleavage and polyadenylation factor is essential for transcription termination on snoRNA genes. Mol Cell 29 : 577–587.

27. LeeJH, YouJ, DobrotaE, SkalnikDG (2010) Identification and characterization of a novel human PP1 phosphatase complex. J Biol Chem 285 : 24466–24476.

28. HendrickxA, BeullensM, CeulemansH, Den AbtT, Van EyndeA, et al. (2009) Docking motif-guided mapping of the interactome of protein phosphatase-1. Chem Biol 16 : 365–371.

29. MeadowsJC, ShepperdLA, VanoosthuyseV, LancasterTC, SochajAM, et al. (2011) Spindle checkpoint silencing requires association of PP1 to both Spc7 and kinesin-8 motors. Dev Cell 20 : 739–750.

30. BeauregardPB, GuerinR, TurcotteC, LindquistS, RokeachLA (2009) A nucleolar protein allows viability in the absence of the essential ER-residing molecular chaperone calnexin. J Cell Sci 122 : 1342–1351.

31. HsuJY, SunZW, LiX, ReubenM, TatchellK, et al. (2000) Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes. Cell 102 : 279–291.

32. 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.

33. TodaT, UmesonoK, HirataA, YanagidaM (1983) Cold-sensitive nuclear division arrest mutants of the fission yeast Schizosaccharomyces pombe. J Mol Biol 168 : 251–270.

34. KimHS, KimSH, ParkHY, LeeJ, YoonJH, et al. (2013) Functional interplay between Aurora B kinase and Ssu72 phosphatase regulates sister chromatid cohesion. Nat Commun 4 : 2631.

35. ShiY, Di GiammartinoDC, TaylorD, SarkeshikA, RiceWJ, et al. (2009) Molecular architecture of the human pre-mRNA 3′ processing complex. Mol Cell 33 : 365–376.

36. Alvarez-TabaresI, GrallertA, OrtizJM, HaganIM (2007) Schizosaccharomyces pombe protein phosphatase 1 in mitosis, endocytosis and a partnership with Wsh3/Tea4 to control polarised growth. J Cell Sci 120 : 3589–3601.

37. LandsverkHB, KirkhusM, BollenM, KuntzigerT, CollasP (2005) PNUTS enhances in vitro chromosome decondensation in a PP1-dependent manner. Biochem J 390 : 709–717.

38. WlotzkaW, KudlaG, GrannemanS, TollerveyD (2011) The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J 30 : 1790–1803.

39. KimH, EricksonB, LuoW, SewardD, GraberJH, et al. (2010) Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat Struct Mol Biol 17 : 1279–1286.

40. VagnarelliP, HudsonDF, RibeiroSA, Trinkle-MulcahyL, SpenceJM, et al. (2006) Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat Cell Biol 8 : 1133–1142.

41. KrishnamurthyS, HeX, Reyes-ReyesM, MooreC, HampseyM (2004) Ssu72 Is an RNA polymerase II CTD phosphatase. Mol Cell 14 : 387–394.

42. WashingtonK, AmmosovaT, BeullensM, JerebtsovaM, KumarA, et al. (2002) Protein phosphatase-1 dephosphorylates the C-terminal domain of RNA polymerase-II. J Biol Chem 277 : 40442–40448.

43. CiurciuA, DuncalfL, JonchereV, LansdaleN, VasievaO, et al. (2013) PNUTS/PP1 Regulates RNAPII-Mediated Gene Expression and Is Necessary for Developmental Growth. PLoS Genet 9: e1003885.

44. Reyes-ReyesM, HampseyM (2007) Role for the Ssu72 C-terminal domain phosphatase in RNA polymerase II transcription elongation. Mol Cell Biol 27 : 926–936.

45. Reyes-TurcuFE, ZhangK, ZofallM, ChenE, GrewalSI (2011) Defects in RNA quality control factors reveal RNAi-independent nucleation of heterochromatin. Nat Struct Mol Biol 18 : 1132–1138.

46. RobelletX, FauqueL, LegrosP, MollereauE, JanczarskiS, et al. (2014) A genetic screen for functional partners of condensin in fission yeast. G3 (Bethesda) 4 : 373–381.

47. Luke-GlaserS, RoyM, LarsenB, Le BihanT, MetalnikovP, et al. (2007) CIF-1, a shared subunit of the COP9/signalosome and eukaryotic initiation factor 3 complexes, regulates MEL-26 levels in the Caenorhabditis elegans embryo. Mol Cell Biol 27 : 4526–4540.

48. Le BihanT, GrimaR, MartinS, ForsterT, Le BihanY (2010) Quantitative analysis of low-abundance peptides in HeLa cell cytoplasm by targeted liquid chromatography/mass spectrometry and stable isotope dilution: emphasising the distinction between peptide detection and peptide identification. Rapid Commun Mass Spectrom 24 : 1093–1104.

49. CoxJ, MaticI, HilgerM, NagarajN, SelbachM, et al. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc 4 : 698–705.

50. WilhelmBT, MargueratS, WattS, SchubertF, WoodV, et al. (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453 : 1239–1243.

51. BernardP, DrogatJ, DheurS, GenierS, JaverzatJP (2010) Splicing factor Spf30 assists exosome-mediated gene silencing in fission yeast. Mol Cell Biol 30 : 1145–1157.

52. BolstadBM, IrizarryRA, AstrandM, SpeedTP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19 : 185–193.

53. IrizarryRA, HobbsB, CollinF, Beazer-BarclayYD, AntonellisKJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4 : 249–264.