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PMID: 15309048 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Genome-wide mapping of the cohesin complex in the yeast Saccharomyces cerevisiae.

PLoS biology ·Vol. 2 ·No. 9 ·2004-09-00 ·Pages E259

Glynn EF, Megee PC, Yu HG, Mistrot C, Unal E, Koshland DE, DeRisi JL, Gerton JL

Abstract

In eukaryotic cells, cohesin holds sister chromatids together until they separate into daughter cells during mitosis. We have used chromatin immunoprecipitation coupled with microarray analysis (ChIP chip) to produce a genome-wide description of cohesin binding to meiotic and mitotic chromosomes of Saccharomyces cerevisiae. A computer program, PeakFinder, enables flexible, automated identification and annotation of cohesin binding peaks in ChIP chip data. Cohesin sites are highly conserved in meiosis and mitosis, suggesting that chromosomes share a common underlying structure during different developmental programs. These sites occur with a semiperiodic spacing of 11 kb that correlates with AT content. The number of sites correlates with chromosome size; however, binding to neighboring sites does not appear to be cooperative. We observed a very strong correlation between cohesin sites and regions between convergent transcription units. The apparent incompatibility between transcription and cohesin binding exists in both meiosis and mitosis. Further experiments reveal that transcript elongation into a cohesin-binding site removes cohesin. A negative correlation between cohesin sites and meiotic recombination sites suggests meiotic exchange is sensitive to the chromosome structure provided by cohesin. The genome-wide view of mitotic and meiotic cohesin binding provides an important framework for the exploration of cohesins and cohesion in other genomes.

MeSH Terms
Binding Sites Cell Cycle Proteins/chemistry,genetics Cells, Cultured Chromatin Immunoprecipitation Chromosomal Proteins, Non-Histone Chromosome Mapping Chromosomes, Artificial, Yeast Chromosomes, Fungal/metabolism Computational Biology DNA/metabolism Fungal Proteins/chemistry,genetics,metabolism Galactose/metabolism Genetic Techniques Genome, Fungal Meiosis Mitosis Models, Genetic Molecular Sequence Data Nocodazole/pharmacology Nuclear Proteins/chemistry,genetics Nucleic Acid Hybridization Oligonucleotide Array Sequence Analysis Polymerase Chain Reaction Promoter Regions, Genetic Protein Binding Saccharomyces cerevisiae/genetics Software Time Factors Transcription, Genetic
Chemicals
Cell Cycle Proteins Chromosomal Proteins, Non-Histone Fungal Proteins Nuclear Proteins cohesins DNA Nocodazole Galactose
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Glynn Earl F
Stowers Institute for Medical Research, Kansas City, Missouri, USA.
Megee Paul C
Yu Hong-Guo
Mistrot Cathy
Unal Elcin
Koshland Douglas E
DeRisi Joseph L
Gerton Jennifer L
Conflict of Interest

The authors have declared that no conflicts of interest exist.

References (48)
48 references, click to expand
  1. Completion of replication map of Saccharomyces cerevisiae chromosome III.
    Mol Biol Cell. 2001 Nov;12(11):3317-27 PMID: 11694569
  2. Chromosomal cohesin forms a ring.
    Cell. 2003 Mar 21;112(6):765-77 PMID: 12654244
  3. A method for the rapid sequence-independent amplification of microdissected chromosomal material.
    Genomics. 1992 Aug;13(4):1322-4 PMID: 1505965
  4. Physical and functional interactions among basic chromosome organizational features govern early steps of meiotic chiasma formation.
    Cell. 2002 Dec 13;111(6):791-802 PMID: 12526806
  5. The ctf13-30/CTF13 genomic haploinsufficiency modifier screen identifies the yeast chromatin remodeling complex RSC, which is required for the establishment of sister chromatid cohesion.
    Mol Cell Biol. 2004 Feb;24(3):1232-44 PMID: 14729968
  6. Cohesin ensures bipolar attachment of microtubules to sister centromeres and resists their precocious separation.
    Nat Cell Biol. 2000 Aug;2(8):492-9 PMID: 10934469
  7. Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes.
    Genetics. 1999 Jun;152(2):577-93 PMID: 10353901
  8. Pch2 links chromatin silencing to meiotic checkpoint control.
    Cell. 1999 Apr 30;97(3):313-24 PMID: 10319812
  9. Computational identification of cis-regulatory elements associated with groups of functionally related genes in Saccharomyces cerevisiae.
    J Mol Biol. 2000 Mar 10;296(5):1205-14 PMID: 10698627
  10. The kinetochore is an enhancer of pericentric cohesin binding.
    PLoS Biol. 2004 Sep;2(9):E260 PMID: 15309047
  11. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.
    Cell. 1999 Jul 9;98(1):91-103 PMID: 10412984
  12. A human chromosome 7 yeast artificial chromosome (YAC) resource: construction, characterization, and screening.
    Genomics. 1995 Jan 1;25(1):170-83 PMID: 7774915
  13. Transcription interferes with elements important for chromosome maintenance in Saccharomyces cerevisiae.
    Mol Cell Biol. 1988 May;8(5):2184-94 PMID: 3290652
  14. Recruitment of cohesin to heterochromatic regions by Swi6/HP1 in fission yeast.
    Nat Cell Biol. 2002 Jan;4(1):89-93 PMID: 11780129
  15. Genetic manipulation of centromere function.
    Mol Cell Biol. 1987 Jul;7(7):2397-405 PMID: 3302676
  16. Requirement of heterochromatin for cohesion at centromeres.
    Science. 2001 Dec 21;294(5551):2539-42 PMID: 11598266
  17. Disjunction of homologous chromosomes in meiosis I depends on proteolytic cleavage of the meiotic cohesin Rec8 by separin.
    Cell. 2000 Oct 27;103(3):387-98 PMID: 11081626
  18. Building a dictionary for genomes: identification of presumptive regulatory sites by statistical analysis.
    Proc Natl Acad Sci U S A. 2000 Aug 29;97(18):10096-100 PMID: 10944202
  19. The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences.
    Mol Cell. 1999 Sep;4(3):445-50 PMID: 10518226
  20. Pds1p, an inhibitor of anaphase in budding yeast, plays a critical role in the APC and checkpoint pathway(s).
    J Cell Biol. 1996 Apr;133(1):99-110 PMID: 8601617
  21. An algorithm for finding protein-DNA binding sites with applications to chromatin-immunoprecipitation microarray experiments.
    Nat Biotechnol. 2002 Aug;20(8):835-9 PMID: 12101404
  22. Evidence for nucleosome depletion at active regulatory regions genome-wide.
    Nat Genet. 2004 Aug;36(8):900-5 PMID: 15247917
  23. Global mapping of meiotic recombination hotspots and coldspots in the yeast Saccharomyces cerevisiae.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11383-90 PMID: 11027339
  24. Rules of donor preference in saccharomyces mating-type gene switching revealed by a competition assay involving two types of recombination.
    Genetics. 1997 Oct;147(2):399-407 PMID: 9335581
  25. Role for the silencing protein Dot1 in meiotic checkpoint control.
    Mol Biol Cell. 2000 Oct;11(10):3601-15 PMID: 11029058
  26. Simple Mendelian inheritance of the reiterated ribosomal DNA of yeast.
    Proc Natl Acad Sci U S A. 1977 Nov;74(11):5091-5 PMID: 337310
  27. Cohesins bind to preferential sites along yeast chromosome III, with differential regulation along arms versus the centric region.
    Cell. 1999 Jul 23;98(2):249-59 PMID: 10428036
  28. Fitting a mixture model by expectation maximization to discover motifs in biopolymers.
    Proc Int Conf Intell Syst Mol Biol. 1994;2:28-36 PMID: 7584402
  29. The anaphase inhibitor of Saccharomyces cerevisiae Pds1p is a target of the DNA damage checkpoint pathway.
    Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14361-6 PMID: 9405617
  30. Identification of cohesin association sites at centromeres and along chromosome arms.
    Cell. 1999 Sep 17;98(6):847-58 PMID: 10499801
  31. Chromosomal addresses of the cohesin component Mcd1p.
    J Cell Biol. 2000 Nov 27;151(5):1047-56 PMID: 11086006
  32. EBP2 is a member of the yeast RRB regulon, a transcriptionally coregulated set of genes that are required for ribosome and rRNA biosynthesis.
    Mol Cell Biol. 2001 Dec;21(24):8638-50 PMID: 11713296
  33. The RSC nucleosome-remodeling complex is required for Cohesin's association with chromosome arms.
    Mol Cell. 2004 Mar 12;13(5):739-50 PMID: 15023343
  34. Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins.
    Science. 2001 Dec 14;294(5550):2357-60 PMID: 11743203
  35. A chromatin remodelling complex that loads cohesin onto human chromosomes.
    Nature. 2002 Aug 29;418(6901):994-8 PMID: 12198550
  36. Cohesin Rec8 is required for reductional chromosome segregation at meiosis.
    Nature. 1999 Jul 29;400(6743):461-4 PMID: 10440376
  37. Budding yeast centromere composition and assembly as revealed by in vivo cross-linking.
    Genes Dev. 1997 Dec 15;11(24):3401-12 PMID: 9407032
  38. Cohesion between sister chromatids must be established during DNA replication.
    Curr Biol. 1998 Oct 8;8(20):1095-101 PMID: 9778527
  39. Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF.
    Nature. 2001 Jan 25;409(6819):533-8 PMID: 11206552
  40. The transcriptional program of sporulation in budding yeast.
    Science. 1998 Oct 23;282(5389):699-705 PMID: 9784122
  41. Measurement of mRNA decay rates in Saccharomyces cerevisiae.
    Methods Enzymol. 1991;194:415-23 PMID: 2005800
  42. Condensin and cohesin: more than chromosome compactor and glue.
    Nat Rev Genet. 2003 Jul;4(7):520-34 PMID: 12838344
  43. Promoter-specific binding of Rap1 revealed by genome-wide maps of protein-DNA association.
    Nat Genet. 2001 Aug;28(4):327-34 PMID: 11455386
  44. Distinct cohesin complexes organize meiotic chromosome domains.
    Science. 2003 May 16;300(5622):1152-5 PMID: 12750522
  45. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae.
    Cell. 1997 Oct 3;91(1):47-57 PMID: 9335334
  46. Molecular biology. SMC complexes--wrapped up in controversy.
    Science. 2003 May 16;300(5622):1101-2 PMID: 12750506
  47. Genomewide demarcation of RNA polymerase II transcription units revealed by physical fractionation of chromatin.
    Proc Natl Acad Sci U S A. 2003 May 27;100(11):6364-9 PMID: 12750471
  48. Time of replication of ARS elements along yeast chromosome III.
    Mol Cell Biol. 1989 Oct;9(10):4488-94 PMID: 2685553
Article Info
Journal
PLoS biology
Abbr.
PLoS Biol
ISSN
1545-7885
Published
2004-09-00
Epub
2004-00-27
Pages
E259
Language
English
Region
United States
NLM ID
101183755
PMCID
PMC490026
Subset
IM
Grants
NIGMS NIH HHS · R01 GM066213 · United States
NIGMS NIH HHS · R01 GM66213 · United States
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