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PMID: 19454013 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Conserved features of cohesin binding along fission yeast chromosomes.

Genome biology ·Vol. 10 ·No. 5 ·2009-00-00 ·Pages R52

Schmidt CK, Brookes N, Uhlmann F

Abstract

Cohesin holds sister chromatids together to enable their accurate segregation in mitosis. How, and where, cohesin binds to chromosomes are still poorly understood, and recent genome-wide surveys have revealed an apparent disparity between its chromosomal association patterns in different organisms. Here, we present the high-resolution analysis of cohesin localization along fission yeast chromosomes. This reveals that several determinants, thought specific for different organisms, come together to shape the overall distribution. Cohesin is detected at chromosomal loading sites, characterized by the cohesin loader Mis4/Ssl3, in regions of strong transcriptional activity. Cohesin also responds to transcription by downstream translocation and accumulation at convergent transcriptional terminators surrounding the loading sites. As cells enter mitosis, a fraction of cohesin leaves chromosomes in a cleavage-independent reaction, while a substantial pool of cohesin dissociates when it is cleaved at anaphase onset. We furthermore observe that centromeric cohesin spreads out onto chromosome arms during mitosis, dependent on Aurora B kinase activity, emphasizing the plasticity of cohesin behavior. Our findings suggest that features that were thought to differentiate cohesin between organisms collectively define the overall behavior of fission yeast cohesin. Apparent differences between organisms might reflect an emphasis on different aspects, rather than different principles, of cohesin action.

MeSH Terms
Cell Cycle Proteins/analysis,metabolism Centromere/chemistry,metabolism Chromatin Immunoprecipitation Chromosomal Proteins, Non-Histone/analysis,metabolism Chromosomes, Fungal/chemistry,metabolism Prophase Schizosaccharomyces/chemistry,cytology,genetics,metabolism Schizosaccharomyces pombe Proteins/analysis,metabolism
Chemicals
Cell Cycle Proteins Chromosomal Proteins, Non-Histone MIS4 protein, S pombe Schizosaccharomyces pombe Proteins Swi6 protein, S pombe cohesins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Schmidt Christine K
Chromosome Segregation Laboratory, Cancer Research UK London Research Institute, Lincoln's Inn Fields, London WC2A 3PX, UK. schmidtck@mail.nih.gov
Brookes Neil
Uhlmann Frank
References (57)
57 references, click to expand
  1. Sister chromatid cohesion: a simple concept with a complex reality.
    Annu Rev Cell Dev Biol. 2008;24:105-29 PMID: 18616427
  2. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation.
    Nature. 2005 Dec 22;438(7071):1116-22 PMID: 16222246
  3. Chromatin insulators.
    Annu Rev Genet. 2006;40:107-38 PMID: 16953792
  4. Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase.
    Genes Dev. 2000 Nov 1;14(21):2757-70 PMID: 11069892
  5. Displacement and re-accumulation of centromeric cohesin during transient pre-anaphase centromere splitting.
    Chromosoma. 2007 Dec;116(6):531-44 PMID: 17763979
  6. Establishment and maintenance of sister chromatid cohesion in fission yeast by a unique mechanism.
    EMBO J. 2001 Oct 15;20(20):5779-90 PMID: 11598020
  7. Meiotic cohesins modulate chromosome compaction during meiotic prophase in fission yeast.
    J Cell Biol. 2006 Aug 14;174(4):499-508 PMID: 16893973
  8. Cohesin complex promotes transcriptional termination between convergent genes in S. pombe.
    Cell. 2008 Mar 21;132(6):983-95 PMID: 18358811
  9. Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4.
    Genes Dev. 1999 Sep 1;13(17):2271-83 PMID: 10485849
  10. Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes.
    Genes Dev. 2008 Aug 15;22(16):2204-14 PMID: 18708579
  11. Cohesins functionally associate with CTCF on mammalian chromosome arms.
    Cell. 2008 Feb 8;132(3):422-33 PMID: 18237772
  12. Drosophila nipped-B protein supports sister chromatid cohesion and opposes the stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene.
    Mol Cell Biol. 2004 Apr;24(8):3100-11 PMID: 15060134
  13. Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe.
    Yeast. 1998 Jul;14(10):943-51 PMID: 9717240
  14. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe.
    Methods Enzymol. 1991;194:795-823 PMID: 2005825
  15. S. pombe aurora kinase/survivin is required for chromosome condensation and the spindle checkpoint attachment response.
    Curr Biol. 2003 Apr 1;13(7):590-7 PMID: 12676091
  16. Two distinct pathways remove mammalian cohesin from chromosome arms in prophase and from centromeres in anaphase.
    Cell. 2000 Oct 27;103(3):399-410 PMID: 11081627
  17. The structure and function of SMC and kleisin complexes.
    Annu Rev Biochem. 2005;74:595-648 PMID: 15952899
  18. Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons.
    Dev Cell. 2008 Feb;14(2):239-51 PMID: 18267092
  19. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex.
    Nature. 2003 Aug 28;424(6952):1078-83 PMID: 12944972
  20. Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways.
    Mol Cell. 2006 Jun 23;22(6):755-767 PMID: 16793545
  21. Recruitment of Xenopus Scc2 and cohesin to chromatin requires the pre-replication complex.
    Nat Cell Biol. 2004 Oct;6(10):991-6 PMID: 15448702
  22. A network of multiple regulatory layers shapes gene expression in fission yeast.
    Mol Cell. 2007 Apr 13;26(1):145-55 PMID: 17434133
  23. Efficient PCR-based gene disruption in Saccharomyces strains using intergenic primers.
    Yeast. 2002 Mar 15;19(4):319-28 PMID: 11870855
  24. Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae.
    PLoS Biol. 2004 Sep;2(9):E259 PMID: 15309048
  25. New drug-resistant cassettes for gene disruption and epitope tagging in Schizosaccharomyces pombe.
    Yeast. 2005 May;22(7):583-91 PMID: 15942936
  26. Scc2 couples replication licensing to sister chromatid cohesion in Xenopus egg extracts.
    Curr Biol. 2004 Sep 7;14(17):1598-603 PMID: 15341749
  27. Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome.
    Chromosoma. 2008 Feb;117(1):89-102 PMID: 17965872
  28. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis.
    Nature. 1989 Nov 2;342(6245):39-45 PMID: 2682257
  29. Genetic control of the cell division cycle in the fission yeast Schizosaccharomyces pombe.
    Mol Gen Genet. 1976 Jul 23;146(2):167-78 PMID: 958201
  30. A screen for cohesion mutants uncovers Ssl3, the fission yeast counterpart of the cohesin loading factor Scc4.
    Curr Biol. 2006 May 9;16(9):875-81 PMID: 16682348
  31. Cell cycle control of centromeric repeat transcription and heterochromatin assembly.
    Nature. 2008 Feb 7;451(7179):734-7 PMID: 18216783
  32. Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion.
    Science. 2008 Jul 25;321(5888):563-6 PMID: 18653893
  33. Roles of the sister chromatid cohesion apparatus in gene expression, development, and human syndromes.
    Chromosoma. 2007 Feb;116(1):1-13 PMID: 16819604
  34. The cohesin ring concatenates sister DNA molecules.
    Nature. 2008 Jul 17;454(7202):297-301 PMID: 18596691
  35. Aurora controls sister kinetochore mono-orientation and homolog bi-orientation in meiosis-I.
    EMBO J. 2007 Oct 31;26(21):4475-86 PMID: 17932486
  36. Degradation of a cohesin subunit by the N-end rule pathway is essential for chromosome stability.
    Nature. 2001 Apr 19;410(6831):955-9 PMID: 11309624
  37. The Suv39h-HP1 histone methylation pathway is dispensable for enrichment and protection of cohesin at centromeres in mammalian cells.
    Chromosoma. 2008 Apr;117(2):199-210 PMID: 18075750
  38. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae.
    Genes Dev. 1999 Mar 15;13(6):698-708 PMID: 10090726
  39. Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1.
    Nature. 1999 Jul 1;400(6739):37-42 PMID: 10403247
  40. Cold-sensitive nuclear division arrest mutants of the fission yeast Schizosaccharomyces pombe.
    J Mol Biol. 1983 Aug 5;168(2):251-70 PMID: 6887244
  41. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast.
    Nat Cell Biol. 2002 Jan;4(1):89-93 PMID: 11780129
  42. The nuclear rim protein Amo1 is required for proper microtubule cytoskeleton organisation in fission yeast.
    J Cell Sci. 2005 Apr 15;118(Pt 8):1705-14 PMID: 15797925
  43. Cell-cycle regulation of cohesin stability along fission yeast chromosomes.
    EMBO J. 2008 Jan 9;27(1):111-21 PMID: 18079700
  44. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin.
    Nature. 2005 Dec 22;438(7071):1176-80 PMID: 16222244
  45. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae.
    Curr Biol. 2001 Jun 26;11(12):991-5 PMID: 11448778
  46. Requirement of heterochromatin for cohesion at centromeres.
    Science. 2001 Dec 21;294(5551):2539-42 PMID: 11598266
  47. Identification and characterization of SA/Scc3p subunits in the Xenopus and human cohesin complexes.
    J Cell Biol. 2000 Aug 7;150(3):405-16 PMID: 10931856
  48. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes.
    Genes Dev. 2008 Aug 15;22(16):2215-27 PMID: 18708580
  49. Cohesin relocation from sites of chromosomal loading to places of convergent transcription.
    Nature. 2004 Jul 29;430(6999):573-8 PMID: 15229615
  50. Human Scc4 is required for cohesin binding to chromatin, sister-chromatid cohesion, and mitotic progression.
    Curr Biol. 2006 May 9;16(9):863-74 PMID: 16682347
  51. Cohesin mediates transcriptional insulation by CCCTC-binding factor.
    Nature. 2008 Feb 14;451(7180):796-801 PMID: 18235444
  52. The rad21 gene product of Schizosaccharomyces pombe is a nuclear, cell cycle-regulated phosphoprotein.
    J Biol Chem. 1995 Mar 31;270(13):7703-11 PMID: 7706319
  53. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins.
    Mol Cell. 2000 Feb;5(2):243-54 PMID: 10882066
  54. A molecular determinant for the establishment of sister chromatid cohesion.
    Science. 2008 Jul 25;321(5888):566-9 PMID: 18653894
  55. Dicer is essential for formation of the heterochromatin structure in vertebrate cells.
    Nat Cell Biol. 2004 Aug;6(8):784-91 PMID: 15247924
  56. Cleavage of cohesin by the CD clan protease separin triggers anaphase in yeast.
    Cell. 2000 Oct 27;103(3):375-86 PMID: 11081625
  57. Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1.
    Nature. 2004 Dec 23;432(7020):1058-61 PMID: 15616569
Article Info
Journal
Genome biology
Abbr.
Genome Biol
ISSN
1474-760X
DOI
10.1186/gb-2009-10-5-r52
Email
schmidtck@mail.nih.gov
Published
2009-00-00
Epub
2009-00-19
Pages
R52
Language
English
Region
England
NLM ID
100960660
PMCID
PMC2718518
Subset
IM
Grants
Cancer Research UK · United Kingdom
External Links
PubMed source DOI: 10.1186/gb-2009-10-5-r52 PMC Full Text View journal details
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