CPF-Associated Phosphatase Activity Opposes Condensin-Mediated Chromosome Condensation

PLoS Genetics

Volumn 10, Issue 6, 2014, Pages

  Vanoosthuyse, Vincent ^a,b   Legros, Pénélope ^a   van der Sar, Sjaak J A ^b   Yvert, Gaël ^a   Toda, Kenji ^c   Le Bihan, Thierry ^d   Watanabe, Yoshinori ^c   Hardwick, Kevin ^b   Bernard, Pascal ^a  

^a UNIVERSITÉ DE LYON   (France)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; CND2 PROTEIN; CONDENSIN; DNA DIRECTED RNA POLYMERASE III; FUNGAL PROTEIN; HISTONE H2AZ; PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 1; PPN1 PROTEIN; RNA POLYMERASE II; SSU72 PROTEIN; SWD2 2 PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ACID ANHYDRIDE HYDROLASE; ADENOSINE TRIPHOSPHATASE; CELL CYCLE PROTEIN; CHROMATIN; DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE GAMMA; HISTONE; HISTONE LYSINE METHYLTRANSFERASE; MULTIPROTEIN COMPLEX; PHOSPHOPROTEIN PHOSPHATASE; PPN1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SSU72 PROTEIN, S CEREVISIAE; SWD2 PROTEIN, S CEREVISIAE;

ARTICLE; CHROMATIN; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; HISTONE ACETYLATION; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA PROCESSING; RNA TRANSCRIPTION; SCHIZOSACCHAROMYCES; TRANSCRIPTION ELONGATION; TRANSCRIPTION TERMINATION; ACETYLATION; GENETICS; METABOLISM; PHOSPHORYLATION; SACCHAROMYCES CEREVISIAE;

ACETYLATION; ACID ANHYDRIDE HYDROLASES; ADENOSINE TRIPHOSPHATASES; CELL CYCLE PROTEINS; CHROMATIN; DNA POLYMERASE III; DNA-BINDING PROTEINS; HISTONE-LYSINE N-METHYLTRANSFERASE; HISTONES; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; MULTIPROTEIN COMPLEXES; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHORYLATION; PROTEIN PHOSPHATASE 1; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSCRIPTION TERMINATION, GENETIC;

EID: 84903481077     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004415     Document Type: Article

References (53)

1. Piazza I, Haering CH, Rutkowska A, (2013) Condensin: crafting the chromosome landscape. Chromosoma 122: 175-190.
2. Tada K, Susumu H, Sakuno T, Watanabe Y, (2011) Condensin association with histone H2A shapes mitotic chromosomes. Nature 474: 477-483.
3. D'Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, et al. (2008) Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22: 2215-2227.
4. Kim JH, Zhang T, Wong NC, Davidson N, Maksimovic J, et al. (2013) Condensin I associates with structural and gene regulatory regions in vertebrate chromosomes. Nat Commun 4: 2537.
5. Tanaka A, Tanizawa H, Sriswasdi S, Iwasaki O, Chatterjee AG, 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. Iwasaki O, Tanaka A, Tanizawa H, Grewal SI, Noma K, (2010) Centromeric localization of dispersed Pol III genes in fission yeast. Mol Biol Cell 21: 254-265.
7. Pek JW, Kai T, (2011) A role for vasa in regulating mitotic chromosome condensation in Drosophila. Curr Biol 21: 39-44.
8. Pek JW, Kai T, (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. Schubert T, Pusch MC, Diermeier S, Benes V, Kremmer E, et al. (2012) Df31 protein and snoRNAs maintain accessible higher-order structures of chromatin. Mol Cell 48: 434-444.
10. Clemente-Blanco A, Sen N, Mayan-Santos M, Sacristan MP, Graham B, et al. (2011) Cdc14 phosphatase promotes segregation of telomeres through repression of RNA polymerase II transcription. Nat Cell Biol 13: 1450-1456.
11. Clemente-Blanco A, Mayan-Santos M, Schneider DA, Machin F, Jarmuz A, et al. (2009) Cdc14 inhibits transcription by RNA polymerase I during anaphase. Nature 458: 219-222.
12. Xing H, Vanderford NL, Sarge KD, (2008) The TBP-PP2A mitotic complex bookmarks genes by preventing condensin action. Nat Cell Biol 10: 1318-1323.
13. Parsons GG, Spencer CA, (1997) Mitotic repression of RNA polymerase II transcription is accompanied by release of transcription elongation complexes. Mol Cell Biol 17: 5791-5802.
14. Loomis RJ, Naoe Y, Parker JB, Savic V, Bozovsky MR, 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. Richard P, Manley JL, (2009) Transcription termination by nuclear RNA polymerases. Genes Dev 23: 1247-1269.
16. Saka Y, Sutani T, Yamashita Y, Saitoh S, Takeuchi M, 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. Kim M, Krogan NJ, Vasiljeva L, Rando OJ, Nedea E, et al. (2004) The yeast Rat1 exonuclease promotes transcription termination by RNA polymerase II. Nature 432: 517-522.
18. Sugiyama T, Sugioka-Sugiyama R, Hada K, Niwa R, (2012) Rhn1, a nuclear protein, is required for suppression of meiotic mRNAs in mitotically dividing fission yeast. PLoS One 7: e42962.
19. Lemay JF, D'Amours A, Lemieux C, Lackner DH, St-Sauveur VG, 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. Uemura T, Ohkura H, Adachi Y, Morino K, Shiozaki K, et al. (1987) DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50: 917-925.
21. Petrova B, Dehler S, Kruitwagen T, Heriche JK, Miura K, et al. (2013) Quantitative analysis of chromosome condensation in fission yeast. Mol Cell Biol 33: 984-998.
22. Kim HS, Vanoosthuyse V, Fillingham J, Roguev A, Watt S, et al. (2009) An acetylated form of histone H2A.Z regulates chromosome architecture in Schizosaccharomyces pombe. Nat Struct Mol Biol 16: 1286-1293.
23. Roguev A, Shevchenko A, Schaft D, Thomas H, Stewart AF, (2004) A comparative analysis of an orthologous proteomic environment in the yeasts Saccharomyces cerevisiae and Schizosaccharomyces pombe. Mol Cell Proteomics 3: 125-132.
24. Wang SW, Asakawa K, Win TZ, Toda T, Norbury CJ, (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. Nedea E, He X, Kim M, Pootoolal J, Zhong G, 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. Nedea E, Nalbant D, Xia D, Theoharis NT, Suter B, 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. Lee JH, You J, Dobrota E, Skalnik DG, (2010) Identification and characterization of a novel human PP1 phosphatase complex. J Biol Chem 285: 24466-24476.
28. Hendrickx A, Beullens M, Ceulemans H, Den Abt T, Van Eynde A, et al. (2009) Docking motif-guided mapping of the interactome of protein phosphatase-1. Chem Biol 16: 365-371.
29. Meadows JC, Shepperd LA, Vanoosthuyse V, Lancaster TC, Sochaj AM, et al. (2011) Spindle checkpoint silencing requires association of PP1 to both Spc7 and kinesin-8 motors. Dev Cell 20: 739-750.
30. Beauregard PB, Guerin R, Turcotte C, Lindquist S, Rokeach LA, (2009) A nucleolar protein allows viability in the absence of the essential ER-residing molecular chaperone calnexin. J Cell Sci 122: 1342-1351.
31. Hsu JY, Sun ZW, Li X, Reuben M, Tatchell K, 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-Pozo M, Santos-Pereira JM, Rondon AG, Barroso S, Andujar E, et al. (2013) R loops are linked to histone H3 S10 phosphorylation and chromatin condensation. Mol Cell 52: 583-590.
33. Toda T, Umesono K, Hirata A, Yanagida M, (1983) Cold-sensitive nuclear division arrest mutants of the fission yeast Schizosaccharomyces pombe. J Mol Biol 168: 251-270.
34. Kim HS, Kim SH, Park HY, Lee J, Yoon JH, et al. (2013) Functional interplay between Aurora B kinase and Ssu72 phosphatase regulates sister chromatid cohesion. Nat Commun 4: 2631.
35. Shi Y, Di Giammartino DC, Taylor D, Sarkeshik A, Rice WJ, et al. (2009) Molecular architecture of the human pre-mRNA 3′ processing complex. Mol Cell 33: 365-376.
36. Alvarez-Tabares I, Grallert A, Ortiz JM, Hagan IM, (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. Landsverk HB, Kirkhus M, Bollen M, Kuntziger T, Collas P, (2005) PNUTS enhances in vitro chromosome decondensation in a PP1-dependent manner. Biochem J 390: 709-717.
38. Wlotzka W, Kudla G, Granneman S, Tollervey D, (2011) The nuclear RNA polymerase II surveillance system targets polymerase III transcripts. EMBO J 30: 1790-1803.
39. Kim H, Erickson B, Luo W, Seward D, Graber JH, et al. (2010) Gene-specific RNA polymerase II phosphorylation and the CTD code. Nat Struct Mol Biol 17: 1279-1286.
40. Vagnarelli P, Hudson DF, Ribeiro SA, Trinkle-Mulcahy L, Spence JM, 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. Krishnamurthy S, He X, Reyes-Reyes M, Moore C, Hampsey M, (2004) Ssu72 Is an RNA polymerase II CTD phosphatase. Mol Cell 14: 387-394.
42. Washington K, Ammosova T, Beullens M, Jerebtsova M, Kumar A, et al. (2002) Protein phosphatase-1 dephosphorylates the C-terminal domain of RNA polymerase-II. J Biol Chem 277: 40442-40448.
43. Ciurciu A, Duncalf L, Jonchere V, Lansdale N, Vasieva O, et al. (2013) PNUTS/PP1 Regulates RNAPII-Mediated Gene Expression and Is Necessary for Developmental Growth. PLoS Genet 9: e1003885.
44. Reyes-Reyes M, Hampsey M, (2007) Role for the Ssu72 C-terminal domain phosphatase in RNA polymerase II transcription elongation. Mol Cell Biol 27: 926-936.
45. Reyes-Turcu FE, Zhang K, Zofall M, Chen E, Grewal SI, (2011) Defects in RNA quality control factors reveal RNAi-independent nucleation of heterochromatin. Nat Struct Mol Biol 18: 1132-1138.
46. Robellet X, Fauque L, Legros P, Mollereau E, Janczarski S, et al. (2014) A genetic screen for functional partners of condensin in fission yeast. G3 (Bethesda) 4: 373-381.
47. Luke-Glaser S, Roy M, Larsen B, Le Bihan T, Metalnikov P, 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 Bihan T, Grima R, Martin S, Forster T, Le Bihan Y, (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. Cox J, Matic I, Hilger M, Nagaraj N, Selbach M, et al. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat Protoc 4: 698-705.
50. Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, et al. (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453: 1239-1243.
51. Bernard P, Drogat J, Dheur S, Genier S, Javerzat JP, (2010) Splicing factor Spf30 assists exosome-mediated gene silencing in fission yeast. Mol Cell Biol 30: 1145-1157.
52. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
53. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.