title: RNA pol II transcript abundance controls condensin accumulation at mitotically up-regulated and heat-shock-inducible genes in fission yeast.
abstract: Condensin plays fundamental roles in chromosome dynamics. In this study, we determined the binding sites of condensin on fission yeast (Schizosaccharomyces pombe) chromosomes at the level of nucleotide sequences using chromatin immunoprecipitation (ChIP) and ChIP sequencing (ChIP-seq). We found that condensin binds to RNA polymerase I-, II- and III-transcribed genes during both mitosis and interphase, and we focused on pol II constitutive and inducible genes. Accumulation sites for condensin are distinct from those of cohesin and DNA topoisomerase II. Using cell cycle stage and heat-shock-inducible genes, we show that pol II-mediated transcripts cause condensin accumulation. First, condensin's enrichment on mitotically activated genes was abolished by deleting the sep1(+) gene that encodes an M-phase-specific forkhead transcription factor. Second, by raising the temperature, condensin accumulation was rapidly induced at heat-shock protein genes in interphase and even during mid-mitosis. In interphase, condensin accumulates preferentially during the postreplicative phase. Pol II-mediated transcription was neither repressed nor activated by condensin, as levels of transcripts per se did not change when mutant condensin failed to associate with chromosomal DNA. However, massive chromosome missegregation occurred, suggesting that abundant pol II transcription may require active condensin before proper chromosome segregation.
authors.affiliation: G0 Cell Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Okinawa, 904-0495, Japan.
authors.forename: Norihiko
authors.initials: N
authors.lastname: Nakazawa
authors.affiliation: G0 Cell Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Okinawa, 904-0495, Japan.
authors.forename: Kenichi
authors.initials: K
authors.lastname: Sajiki
authors.affiliation: G0 Cell Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Okinawa, 904-0495, Japan.
authors.forename: Xingya
authors.initials: X
authors.lastname: Xu
authors.affiliation: G0 Cell Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Okinawa, 904-0495, Japan.
authors.forename: Alejandro
authors.initials: A
authors.lastname: Villar-Briones
authors.affiliation: G0 Cell Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Okinawa, 904-0495, Japan.
authors.forename: Orie
authors.initials: O
authors.lastname: Arakawa
authors.affiliation: G0 Cell Unit, Okinawa Institute of Science and Technology Graduate University, Onna-son, Okinawa, 904-0495, Japan.
authors.forename: Mitsuhiro
authors.initials: M
authors.lastname: Yanagida
mesh_terms: D000251:Adenosine Triphosphatases / Q000378:metabolism*; D047369:Chromatin Immunoprecipitation; D020090:Chromosome Segregation; D004268:DNA-Binding Proteins / Q000378:metabolism*; D051858:Forkhead Transcription Factors / Q000378:metabolism; D059565:G2 Phase Cell Cycle Checkpoints; D006360:Heat-Shock Proteins / Q000235:genetics*; D008938:Mitosis; D008969:Molecular Sequence Data; D046912:Multiprotein Complexes / Q000378:metabolism*; D012319:RNA Polymerase II / Q000378:metabolism*; D012333:RNA, Messenger / Q000378:metabolism*; D012568:Schizosaccharomyces / Q000166:cytology / Q000201:enzymology / Q000235:genetics / Q000378:metabolism*; D029702:Schizosaccharomyces pombe Proteins / Q000378:metabolism; D015854:Up-Regulation
chemical_list: D004268:DNA-Binding Proteins; D051858:Forkhead Transcription Factors; D006360:Heat-Shock Proteins; D046912:Multiprotein Complexes; D012333:RNA, Messenger; D029702:Schizosaccharomyces pombe Proteins; C108312:condensin complexes; C090209:cut14 protein, S pombe; C121803:sep1 protein, S pombe; D012319:RNA Polymerase II; D000251:Adenosine Triphosphatases
references.citation: Curr Biol. 2002 Mar 19;12(6):508-13
references.pmid: 11909539
references.citation: Annu Rev Cell Dev Biol. 1996;12:305-33
references.pmid: 8970729
references.citation: J Cell Sci. 2011 Jun 1;124(Pt 11):1795-807
references.pmid: 21540296
references.citation: Mol Cell Biol. 2005 Aug;25(16):7216-25
references.pmid: 16055730
references.citation: J Cell Biol. 2008 Mar 24;180(6):1115-31
references.pmid: 18362178
references.citation: Mol Biol Cell. 2003 Jan;14(1):214-29
references.pmid: 12529438
references.citation: Stem Cell Reports. 2013;1(5):371-8
references.pmid: 24286025
references.citation: PLoS Genet. 2013;9(3):e1003371
references.pmid: 23516381
references.citation: EMBO J. 2010 Jul 7;29(13):2126-34
references.pmid: 20526281
references.citation: Genes Dev. 2008 Aug 15;22(16):2215-27
references.pmid: 18708580
references.citation: Nucleic Acids Res. 1982 May 11;10(9):2851-64
references.pmid: 6285312
references.citation: J Cell Biol. 1994 Oct;127(2):303-18
references.pmid: 7929577
references.citation: Genome Biol. 2013;14(10):R112
references.pmid: 24125077
references.citation: Trends Cell Biol. 2011 Sep;21(9):552-9
references.pmid: 21763138
references.citation: Genome Biol. 2009;10(5):R52
references.pmid: 19454013
references.citation: Genes Dev. 2000 Nov 1;14(21):2757-70
references.pmid: 11069892
references.citation: J Cell Sci. 2004 Nov 1;117(Pt 23):5623-32
references.pmid: 15509866
references.citation: Nature. 2011 Jun 23;474(7352):477-83
references.pmid: 21633354
references.citation: Nat Genet. 2004 Aug;36(8):809-17
references.pmid: 15195092
references.citation: Chromosome Res. 2009;17(2):131-44
references.pmid: 19308696
references.citation: Nat Rev Mol Cell Biol. 2009 Jul;10(7):489-96
references.pmid: 19491928
references.citation: Nature. 1997 Aug 21;388(6644):798-801
references.pmid: 9285594
references.citation: J Cell Biol. 1992 Dec;119(5):1023-36
references.pmid: 1332977
references.citation: Ann N Y Acad Sci. 1960 Oct 7;90:409-21
references.pmid: 13775619
references.citation: J Biol Chem. 1995 Mar 31;270(13):7703-11
references.pmid: 7706319
references.citation: J Biol Chem. 2011 Jul 1;286(26):23600-7
references.pmid: 21531710
references.citation: Biochem Biophys Res Commun. 1999 Sep 24;263(2):465-74
references.pmid: 10491317
references.citation: Mol Cell Biol. 2012 Oct;32(19):4035-43
references.pmid: 22851695
references.citation: Methods. 2009 Jul;48(3):240-8
references.pmid: 19275939
references.citation: Cell. 1997 Oct 3;91(1):35-45
references.pmid: 9335333
references.citation: Mol Cell. 2009 May 14;34(4):416-26
references.pmid: 19481522
references.citation: J Cell Sci. 2009 May 1;122(Pt 9):1418-29
references.pmid: 19366728
references.citation: J Cell Biol. 1993 Dec;123(6 Pt 2):1635-48
references.pmid: 8276886
references.citation: Mol Biol Cell. 2010 Jan 15;21(2):254-65
references.pmid: 19910488
references.citation: Cell. 1994 Nov 4;79(3):449-58
references.pmid: 7954811
references.citation: Nature. 2002 May 9;417(6885):197-202
references.pmid: 12000964
references.citation: Cell. 1984 Dec;39(2 Pt 1):349-58
references.pmid: 6094012
references.citation: Bioinformatics. 2009 Oct 15;25(20):2730-1
references.pmid: 19654113
references.citation: Cell. 2003 Oct 3;115(1):109-21
references.pmid: 14532007
references.citation: Cell Cycle. 2008 Mar 15;7(6):765-76
references.pmid: 18239448
references.citation: Nat Commun. 2013;4:2537
references.pmid: 24088984
references.citation: Cell. 2014 Oct 23;159(3):572-83
references.pmid: 25417108
references.citation: Nature. 2009 Mar 12;458(7235):219-22
references.pmid: 19158678
references.citation: Proc Natl Acad Sci U S A. 1977 Nov;74(11):4937-41
references.pmid: 270727
references.citation: Curr Genet. 1984 Feb;8(2):93-7
references.pmid: 24177582
references.citation: Nat Genet. 2014 Oct;46(10):1147-51
references.pmid: 25173104
references.citation: Open Biol. 2011 Dec;1(4):110023
references.pmid: 22645654
references.citation: Genes Dev. 1999 Sep 1;13(17):2271-83
references.pmid: 10485849
references.citation: Nat Rev Genet. 2010 Jun;11(6):391-404
references.pmid: 20442714
references.citation: Genes Dev. 2012 Aug 1;26(15):1659-78
references.pmid: 22855829
references.citation: Yeast. 2006 Feb;23(3):173-83
references.pmid: 16498704
references.citation: EMBO J. 1994 Oct 17;13(20):4938-52
references.pmid: 7957061
references.citation: EMBO J. 1995 Dec 15;14(24):6193-208
references.pmid: 8557039
references.citation: Mol Cell. 2012 Nov 30;48(4):532-46
references.pmid: 23084836
references.citation: Nat Rev Genet. 2012 Oct;13(10):720-31
references.pmid: 22986266
references.citation: EMBO J. 2003 Jun 2;22(11):2764-75
references.pmid: 12773391
references.citation: Genes Dev. 1995 Mar 1;9(5):587-99
references.pmid: 7698648
references.citation: Curr Biol. 1998 Sep 10;8(18):1031-4
references.pmid: 9740803