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PMID: 17268547 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Reconstitution and subunit geometry of human condensin complexes.

The EMBO journal ·Vol. 26 ·No. 4 ·2007-02-21 ·Pages 1024-34

Onn I, Aono N, Hirano M, Hirano T

Abstract

Vertebrate cells possess two different condensin complexes, known as condensin I and condensin II, that play a fundamental role in chromosome assembly and segregation during mitosis. Each complex contains a pair of structural maintenance of chromosomes (SMC) ATPases, a kleisin subunit and two HEAT-repeat subunits. Here we use recombinant human condensin subunits to determine their geometry within each complex. We show that both condensin I and condensin II have a pseudo-symmetrical structure, in which the N-terminal half of kleisin links the first HEAT subunit to SMC2, whereas its C-terminal half links the second HEAT subunit to SMC4. No direct interactions are detectable between the SMC dimer and the HEAT subunits, indicating that the kleisin subunit acts as the linchpin in holocomplex assembly. ATP has little, if any, effects on the assembly and integrity of condensin. Cleavage pattern of SMC2 by limited proteolysis is changed upon its binding to ATP or DNA. Our results shed new light on the architecture and dynamics of this highly elaborate machinery designed for chromosome assembly.

MeSH Terms
Adenosine Triphosphatases/chemistry,genetics Amino Acid Sequence Animals Carrier Proteins/metabolism Cell Cycle Proteins Cell Extracts/genetics Chromosome Segregation/genetics DNA-Binding Proteins/chemistry,genetics Genetic Complementation Test Humans Mitosis/genetics Models, Molecular Molecular Sequence Data Multiprotein Complexes/chemistry,genetics Nuclear Proteins/metabolism Ovum/chemistry Protein Conformation Protein Subunits/chemistry,metabolism Xenopus
Chemicals
Carrier Proteins Cell Cycle Proteins Cell Extracts DNA-Binding Proteins Multiprotein Complexes Nuclear Proteins Protein Subunits SMC2 protein, human condensin complexes Adenosine Triphosphatases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Onn Itay
Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11724, USA.
Aono Nobuki
Hirano Michiko
Hirano Tatsuya
References (39)
39 references, click to expand
  1. Positive and negative regulation of SMC-DNA interactions by ATP and accessory proteins.
    EMBO J. 2004 Jul 7;23(13):2664-73 PMID: 15175656
  2. At the heart of the chromosome: SMC proteins in action.
    Nat Rev Mol Cell Biol. 2006 May;7(5):311-22 PMID: 16633335
  3. Structural biochemistry of ATP-driven dimerization and DNA-stimulated activation of SMC ATPases.
    Curr Biol. 2004 Oct 5;14(19):1778-82 PMID: 15458651
  4. ScII: an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure.
    J Cell Biol. 1994 Oct;127(2):303-18 PMID: 7929577
  5. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro.
    Cell. 1994 Nov 4;79(3):449-58 PMID: 7954811
  6. 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
  7. 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
  8. 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
  9. DNA renaturation activity of the SMC complex implicated in chromosome condensation.
    Nature. 1997 Aug 21;388(6644):798-801 PMID: 9285594
  10. HEAT repeats associated with condensins, cohesins, and other complexes involved in chromosome-related functions.
    Genome Res. 2000 Oct;10(10):1445-52 PMID: 11042144
  11. 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
  12. Chromosome condensation by a human condensin complex in Xenopus egg extracts.
    J Biol Chem. 2001 Feb 23;276(8):5417-20 PMID: 11136719
  13. Bimodal activation of SMC ATPase by intra- and inter-molecular interactions.
    EMBO J. 2001 Jun 15;20(12):3238-50 PMID: 11406600
  14. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi.
    Nature. 2001 Nov 22;414(6862):450-3 PMID: 11719806
  15. Condensin and cohesin display different arm conformations with characteristic hinge angles.
    J Cell Biol. 2002 Feb 4;156(3):419-24 PMID: 11815634
  16. Molecular architecture of SMC proteins and the yeast cohesin complex.
    Mol Cell. 2002 Apr;9(4):773-88 PMID: 11983169
  17. Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA.
    EMBO J. 2002 Nov 1;21(21):5733-44 PMID: 12411491
  18. Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners.
    Mol Cell. 2003 Mar;11(3):571-5 PMID: 12667442
  19. Condensin but not cohesin SMC heterodimer induces DNA reannealing through protein-protein assembly.
    EMBO J. 2003 Jun 2;22(11):2764-75 PMID: 12773391
  20. Biochemical analysis of the yeast condensin Smc2/4 complex: an ATPase that promotes knotting of circular DNA.
    J Biol Chem. 2003 Jul 11;278(28):26238-48 PMID: 12719426
  21. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells.
    Cell. 2003 Oct 3;115(1):109-21 PMID: 14532007
  22. Condensin and biological role of chromosome condensation.
    Prog Cell Cycle Res. 2003;5:361-7 PMID: 14593730
  23. A model for ATP hydrolysis-dependent binding of cohesin to DNA.
    Curr Biol. 2003 Nov 11;13(22):1930-40 PMID: 14614818
  24. ATP hydrolysis is required for cohesin's association with chromosomes.
    Curr Biol. 2003 Nov 11;13(22):1941-53 PMID: 14614819
  25. Identification of a subunit of a novel Kleisin-beta/SMC complex as a potential substrate of protein phosphatase 2A.
    Curr Biol. 2003 Dec 2;13(23):2058-64 PMID: 14653995
  26. The evolution of SMC proteins: phylogenetic analysis and structural implications.
    Mol Biol Evol. 2004 Feb;21(2):332-47 PMID: 14660695
  27. Real-time detection of single-molecule DNA compaction by condensin I.
    Curr Biol. 2004 May 25;14(10):874-80 PMID: 15186743
  28. ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation.
    Cell. 1997 Aug 22;90(4):625-34 PMID: 9288743
  29. The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge.
    J Cell Biol. 1998 Sep 21;142(6):1595-604 PMID: 9744887
  30. ATP-dependent aggregation of single-stranded DNA by a bacterial SMC homodimer.
    EMBO J. 1998 Dec 1;17(23):7139-48 PMID: 9843517
  31. 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
  32. Condensins: organizing and segregating the genome.
    Curr Biol. 2005 Apr 12;15(7):R265-75 PMID: 15823530
  33. Functional contribution of Pds5 to cohesin-mediated cohesion in human cells and Xenopus egg extracts.
    J Cell Sci. 2005 May 15;118(Pt 10):2133-41 PMID: 15855230
  34. Drosophila CAP-D2 is required for condensin complex stability and resolution of sister chromatids.
    J Cell Sci. 2005 Jun 1;118(Pt 11):2529-43 PMID: 15923665
  35. The MukF subunit of Escherichia coli condensin: architecture and functional relationship to kleisins.
    EMBO J. 2005 Jun 1;24(11):1921-30 PMID: 15902272
  36. Dynamic molecular linkers of the genome: the first decade of SMC proteins.
    Genes Dev. 2005 Jun 1;19(11):1269-87 PMID: 15937217
  37. The structure and function of SMC and kleisin complexes.
    Annu Rev Biochem. 2005;74:595-648 PMID: 15952899
  38. Opening closed arms: long-distance activation of SMC ATPase by hinge-DNA interactions.
    Mol Cell. 2006 Jan 20;21(2):175-86 PMID: 16427008
  39. Structure and stability of cohesin's Smc1-kleisin interaction.
    Mol Cell. 2004 Sep 24;15(6):951-64 PMID: 15383284
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2007-02-21
Epub
2007-00-01
Pages
1024-34
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1852836
Subset
IM
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