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PMID: 11864994 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin.

The Journal of cell biology ·Vol. 156 ·No. 5 ·2002-03-04 ·Pages 805-15

Lavoie BD, Hogan E, Koshland D

Abstract

The machinery mediating chromosome condensation is poorly understood. To begin to dissect the in vivo function(s) of individual components, we monitored mitotic chromosome structure in mutants of condensin, cohesin, histone H3, and topoisomerase II (topo II). In budding yeast, both condensation establishment and maintenance require all of the condensin subunits, but not topo II activity or phospho-histone H3. Structural maintenance of chromosome (SMC) protein 2, as well as each of the three non-SMC proteins (Ycg1p, Ycs4p, and Brn1p), was required for chromatin binding of the condensin complex in vivo. Using reversible condensin alleles, we show that chromosome condensation does not involve an irreversible modification of condensin or chromosomes. Finally, we provide the first evidence of a mechanistic link between condensin and cohesin function. A model discussing the functional interplay between cohesin and condensin is presented.

MeSH Terms
Adenosine Triphosphatases/genetics,metabolism Carrier Proteins/genetics,metabolism Cell Cycle Proteins Cell Survival/genetics Chromosomal Proteins, Non-Histone Chromosome Segregation/physiology DNA Topoisomerases, Type II/genetics,metabolism DNA-Binding Proteins/genetics,metabolism Fungal Proteins Histones/genetics,metabolism Mitosis/genetics,physiology Multiprotein Complexes Mutation/genetics Nuclear Proteins/genetics,metabolism Saccharomyces cerevisiae/genetics,metabolism Saccharomyces cerevisiae Proteins
Chemicals
Carrier Proteins Cell Cycle Proteins Chromosomal Proteins, Non-Histone DNA-Binding Proteins Fungal Proteins Histones Multiprotein Complexes Nuclear Proteins SMC2 protein, S cerevisiae Saccharomyces cerevisiae Proteins cohesins condensin complexes Adenosine Triphosphatases DNA Topoisomerases, Type II
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Lavoie Brigitte D
Department of Medical Genetics and Microbiology, University of Toronto, Toronto, ON M5S 1A8, Canada. brigitte.lavoie@utoronto.ca
Hogan Eileen
Koshland Douglas
References (52)
52 references, click to expand
  1. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids.
    Cell. 1997 Oct 3;91(1):35-45 PMID: 9335333
  2. DNA renaturation activity of the SMC complex implicated in chromosome condensation.
    Nature. 1997 Aug 21;388(6644):798-801 PMID: 9285594
  3. MIX-1: an essential component of the C. elegans mitotic machinery executes X chromosome dosage compensation.
    Cell. 1998 Jan 23;92(2):265-77 PMID: 9458050
  4. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion.
    Genes Dev. 1998 Jul 1;12(13):1986-97 PMID: 9649503
  5. Entry into mitosis in vertebrate somatic cells is guarded by a chromosome damage checkpoint that reverses the cell cycle when triggered during early but not late prophase.
    J Cell Biol. 1998 Aug 24;142(4):1013-22 PMID: 9722613
  6. Phosphorylation and activation of 13S condensin by Cdc2 in vitro.
    Science. 1998 Oct 16;282(5388):487-90 PMID: 9774278
  7. Facilitation of chromatin dynamics by SARs.
    Curr Opin Genet Dev. 1998 Oct;8(5):519-25 PMID: 9794825
  8. pEg7, a new Xenopus protein required for mitotic chromosome condensation in egg extracts.
    J Cell Biol. 1998 Dec 14;143(6):1437-46 PMID: 9852142
  9. Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication.
    Genes Dev. 1999 Feb 1;13(3):320-33 PMID: 9990856
  10. The boundaries of the silenced HMR domain in Saccharomyces cerevisiae.
    Genes Dev. 1999 Mar 15;13(6):698-708 PMID: 10090726
  11. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation.
    Cell. 1999 Apr 2;97(1):99-109 PMID: 10199406
  12. 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
  13. Identification of a novel phosphorylation site on histone H3 coupled with mitotic chromosome condensation.
    J Biol Chem. 1999 Sep 3;274(36):25543-9 PMID: 10464286
  14. 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
  15. Identification of cohesin association sites at centromeres and along chromosome arms.
    Cell. 1999 Sep 17;98(6):847-58 PMID: 10499801
  16. The centromeric sister chromatid cohesion site directs Mcd1p binding to adjacent sequences.
    Mol Cell. 1999 Sep;4(3):445-50 PMID: 10518226
  17. The condensin complex governs chromosome condensation and mitotic transmission of rDNA.
    J Cell Biol. 2000 May 15;149(4):811-24 PMID: 10811823
  18. Splitting the chromosome: cutting the ties that bind sister chromatids.
    Science. 2000 May 26;288(5470):1379-85 PMID: 10827941
  19. 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
  20. Mitotic phosphorylation of histone H3 is governed by Ipl1/aurora kinase and Glc7/PP1 phosphatase in budding yeast and nematodes.
    Cell. 2000 Aug 4;102(3):279-91 PMID: 10975519
  21. Chromosome cohesion, condensation, and separation.
    Annu Rev Biochem. 2000;69:115-44 PMID: 10966455
  22. Microtubule disassembly delays the G2-M transition in vertebrates.
    Curr Biol. 2000 Sep 7;10(17):1067-70 PMID: 10996076
  23. Dual roles of the 11S regulatory subcomplex in condensin functions.
    Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):11972-7 PMID: 11027308
  24. Pds5p is an essential chromosomal protein required for both sister chromatid cohesion and condensation in Saccharomyces cerevisiae.
    J Cell Biol. 2000 Oct 30;151(3):613-26 PMID: 11062262
  25. Holding your own: establishing sister chromatid cohesion.
    Genome Res. 2000 Nov;10(11):1664-71 PMID: 11076851
  26. 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
  27. Chromosomal addresses of the cohesin component Mcd1p.
    J Cell Biol. 2000 Nov 27;151(5):1047-56 PMID: 11086006
  28. Chromosome condensation by a human condensin complex in Xenopus egg extracts.
    J Biol Chem. 2001 Feb 23;276(8):5417-20 PMID: 11136719
  29. A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis.
    Curr Biol. 2001 Mar 6;11(5):295-307 PMID: 11267866
  30. Saccharomyces cerevisiae CTF18 and CTF4 are required for sister chromatid cohesion.
    Mol Cell Biol. 2001 May;21(9):3144-58 PMID: 11287619
  31. Essential roles of Drosophila inner centromere protein (INCENP) and aurora B in histone H3 phosphorylation, metaphase chromosome alignment, kinetochore disjunction, and chromosome segregation.
    J Cell Biol. 2001 May 14;153(4):865-80 PMID: 11352945
  32. Genes involved in sister chromatid separation and segregation in the budding yeast Saccharomyces cerevisiae.
    Genetics. 2001 Oct;159(2):453-70 PMID: 11606525
  33. Scc1/Rad21/Mcd1 is required for sister chromatid cohesion and kinetochore function in vertebrate cells.
    Dev Cell. 2001 Dec;1(6):759-70 PMID: 11740938
  34. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe.
    Cell. 1987 Sep 11;50(6):917-25 PMID: 3040264
  35. The structure of sister minichromosome DNA before anaphase in Saccharomyces cerevisiae.
    Science. 1987 Dec 18;238(4834):1713-6 PMID: 3317838
  36. DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage.
    Mol Cell Biol. 1989 Jan;9(1):159-68 PMID: 2538717
  37. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites.
    Gene. 1988 Dec 30;74(2):527-34 PMID: 3073106
  38. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae.
    Genetics. 1989 May;122(1):19-27 PMID: 2659436
  39. Chromosome assembly in vitro: topoisomerase II is required for condensation.
    Cell. 1991 Jan 11;64(1):137-48 PMID: 1846085
  40. Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus egg extracts.
    J Cell Biol. 1993 Feb;120(3):601-12 PMID: 8381118
  41. Chromosome condensation and sister chromatid pairing in budding yeast.
    J Cell Biol. 1994 May;125(3):517-30 PMID: 8175878
  42. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis.
    EMBO J. 1994 Oct 17;13(20):4938-52 PMID: 7957061
  43. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family.
    Genes Dev. 1995 Mar 1;9(5):587-99 PMID: 7698648
  44. Mitotic chromosome condensation in the rDNA requires TRF4 and DNA topoisomerase I in Saccharomyces cerevisiae.
    Genes Dev. 1996 Oct 15;10(20):2564-76 PMID: 8895658
  45. Mitotic chromosome condensation requires Brn1p, the yeast homologue of Barren.
    Mol Biol Cell. 2000 Apr;11(4):1293-304 PMID: 10749930
  46. Chromosome condensation factor Brn1p is required for chromatid separation in mitosis.
    Mol Biol Cell. 2000 Apr;11(4):1305-13 PMID: 10749931
  47. Sister chromatid cohesion: the beginning of a long and beautiful relationship.
    Curr Opin Cell Biol. 2000 Jun;12(3):297-301 PMID: 10801457
  48. Review: SMCs in the world of chromosome biology- from prokaryotes to higher eukaryotes.
    J Struct Biol. 2000 Apr;129(2-3):123-43 PMID: 10806064
  49. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II.
    Cell. 1996 Dec 13;87(6):1103-14 PMID: 8978614
  50. Chromosomes with two intact axial cores are induced by G2 checkpoint override: evidence that DNA decatenation is not required to template the chromosome structure.
    J Cell Biol. 1997 Jan 13;136(1):29-43 PMID: 9008701
  51. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein.
    Cell. 1997 May 16;89(4):511-21 PMID: 9160743
  52. 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
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2002-03-04
Epub
2002-00-25
Pages
805-15
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2173308
Subset
IM
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