Association of condensin with chromosomes depends on DNA binding by its HEAT-repeat subunits

Nature Structural and Molecular Biology

Volumn 21, Issue 6, 2014, Pages 560-568

  Piazza, Ilaria ^a   Rutkowska, Anna ^a   Ori, Alessandro ^a   Walczak, Marta ^a,b   Metz, Jutta ^a   Pelechano, Vicent ^a   Beck, Martin ^a   Haering, Christian H ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b MAX F PERUTZ LABORATORIES   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CONDENSIN; DOUBLE STRANDED DNA;

ANISOTROPY; ARTICLE; BINDING KINETICS; CHROMOSOME; CONTROLLED STUDY; ENZYME ACTIVITY; HEAT REPEAT SUBUNIT; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

ADENOSINE TRIPHOSPHATASES; BINDING SITES; CHROMOSOMES; DNA; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, PROTEIN;

EID: 84901982905     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2831     Document Type: Article

References (57)

1. Hirano, T. Condensins: universal organizers of chromosomes with diverse functions. Genes Dev. 26, 1659-1678 (2012).
2. Piazza, I., Haering, C.H. & Rutkowska, A. Condensin: crafting the chromosome landscape. Chromosoma 122, 175-190 (2013).
3. Aragón, L., Martinez-Perez, E. & Merkenschlager, M. Condensin, cohesin and the control of chromatin states. Curr. Opin. Genet. Dev. 23, 204-211 (2013).
4. Wood, A.J., Severson, A.F. & Meyer, B.J. Condensin and cohesin complexity: the expanding repertoire of functions. Nat. Rev. Genet. 11, 391-404 (2010).
5. Anderson, D.E., Losada, A., Erickson, H.P. & Hirano, T. Condensin and cohesin display different arm conformations with characteristic hinge angles. J. Cell Biol. 156, 419-424 (2002). (Pubitemid 34839891)
6. Schleiffer, A. et al. Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol. Cell 11, 571-575 (2003). (Pubitemid 36385114)
7. Onn, I., Aono, N., Hirano, M. & Hirano, T. Reconstitution and subunit geometry of human condensin complexes. EMBO J. 26, 1024-1034 (2007).
8. Neuwald, A.F. & Hirano, T. HEAT repeats associated with condensins, cohesins, and other complexes involved in chromosome-related functions. Genome Res. 10, 1445-1452 (2000).
9. Ono, T., Fang, Y., Spector, D.L. & Hirano, T. Spatial and temporal regulation of condensins I and II in mitotic chromosome assembly in human cells. Mol. Biol. Cell 15, 3296-3308 (2004). (Pubitemid 38850124)
10. Kimura, K. & Hirano, T. ATP-dependent positive supercoiling of DNA by 13S condensin: a biochemical implication for chromosome condensation. Cell 90, 625-634 (1997). (Pubitemid 27357955)
11. Kimura, K., Rybenkov, V.V., Crisona, N.J., Hirano, T. & Cozzarelli, N.R. 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 98, 239-248 (1999). (Pubitemid 29355127)
12. Kimura, K. & Hirano, T. Dual roles of the 11S regulatory subcomplex in condensin functions. Proc. Natl. Acad. Sci. USA 97, 11972-11977 (2000).
13. Stray, J.E. & Lindsley, J.E. Biochemical analysis of the yeast condensin Smc2/4 complex: an ATPase that promotes knotting of circular DNA. J. Biol. Chem. 278, 26238-26248 (2003). (Pubitemid 36835393)
14. Stray, J.E., Crisona, N.J., Belotserkovskii, B.P., Lindsley, J.E. & Cozzarelli, N.R. The Saccharomyces cerevisiae Smc2/4 condensin compacts DNA into (+) chiral structures without net supercoiling. J. Biol. Chem. 280, 34723-34734 (2005). (Pubitemid 41504605)
15. Sakai, A., Hizume, K., Sutani, T., Takeyasu, K. & Yanagida, M. Condensin but not cohesin SMC heterodimer induces DNA reannealing through protein-protein assembly. EMBO J. 22, 2764-2775 (2003). (Pubitemid 36712372)
16. Cuylen, S., Metz, J. & Haering, C.H. Condensin structures chromosomal DNA through topological links. Nat. Struct. Mol. Biol. 18, 894-901 (2011).
17. Haering, C.H., Farcas, A.-M., Arumugam, P., Metson, J. & Nasmyth, K. The cohesin ring concatenates sister DNA molecules. Nature 454, 297-301 (2008).
18. Tada, K., Susumu, H., Sakuno, T. & Watanabe, Y. Condensin association with histone H2A shapes mitotic chromosomes. Nature 474, 477-483 (2011).
19. Liu, W. et al. PHF8 mediates histone H4 lysine 20 demethylation events involved in cell cycle progression. Nature 466, 508-512 (2010).
20. Gajiwala, K.S. & Burley, S.K. Winged helix proteins. Curr. Opin. Struct. Biol. 10, 110-116 (2000). (Pubitemid 30099335)
21. Bürmann, F. et al. An asymmetric SMC-kleisin bridge in prokaryotic condensin. Nat. Struct. Mol. Biol. 20, 371-379 (2013).
22. Haering, C.H. et al. Structure and stability of cohesin's Smc1-kleisin interaction. Mol. Cell 15, 951-964 (2004). (Pubitemid 39277991)
23. Woo, J.-S. et al. Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions. Cell 136, 85-96 (2009).
24. Yoshimura, S.H. et al. Condensin architecture and interaction with DNA: regulatory non-SMC subunits bind to the head of SMC heterodimer. Curr. Biol. 12, 508-513 (2002). (Pubitemid 34248900)
25. Griese, J.J., Witte, G. & Hopfner, K.-P. Structure and DNA binding activity of the mouse condensin hinge domain highlight common and diverse features of SMC proteins. Nucleic Acids Res. 38, 3454-3465 (2010).
26. Lowary, P.T. & Widom, J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19-42 (1998). (Pubitemid 28085408)
27. Mavrich, T.N. et al. A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome. Genome Res. 18, 1073-1083 (2008). (Pubitemid 351931158)
28. Albert, I. et al. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 446, 572-576 (2007). (Pubitemid 46514724)
29. Amlacher, S. et al. Insight into structure and assembly of the nuclear pore complex by utilizing the genome of a eukaryotic thermophile. Cell 146, 277-289 (2011).
30. Leitner, A. et al. Probing native protein structures by chemical cross-linking, mass spectrometry, and bioinformatics. Mol. Cell. Proteomics 9, 1634-1649 (2010).
31. Leitner, A. et al. Expanding the chemical cross-linking toolbox by the use of multiple proteases and enrichment by size exclusion chromatography. Mol. Cell Proteomics 11, M111.014126 (2012).
32. Lavoie, B.D., Hogan, E. & Koshland, D. In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin. J. Cell Biol. 156, 805-815 (2002). (Pubitemid 34839864)
33. Cuylen, S., Metz, J., Hruby, A. & Haering, C.H. Entrapment of chromosomes by condensin rings prevents their breakage during cytokinesis. Dev. Cell 27, 469-478 (2013).
34. Neumann, B. et al. Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464, 721-727 (2010).
35. Arumugam, P. et al. ATP hydrolysis is required for cohesin's association with chromosomes. Curr. Biol. 13, 1941-1953 (2003). (Pubitemid 37425203)
36. Weitzer, S., Lehane, C. & Uhlmann, F. A model for ATP hydrolysis-dependent binding of cohesin to DNA. Curr. Biol. 13, 1930-1940 (2003). (Pubitemid 37425202)
37. Arumugam, P., Nishino, T., Haering, C.H., Gruber, S. & Nasmyth, K. Cohesin's ATPase activity is stimulated by the C-terminal winged-helix domain of its kleisin subunit. Curr. Biol. 16, 1998-2008 (2006). (Pubitemid 44573822)
38. Akai, Y. et al. Opposing role of condensin hinge against replication protein A in mitosis and interphase through promoting DNA annealing. Open Biol. 1, 110023 (2011).
39. Rubinson, E.H., Gowda, A.S.P., Spratt, T.E., Gold, B. & Eichman, B.F. An unprecedented nucleic acid capture mechanism for excision of DNA damage. Nature 468, 406-411 (2010).
40. Ouspenski, I.I., Cabello, O.A. & Brinkley, B.R. Chromosome condensation factor Brn1p is required for chromatid separation in mitosis. Mol. Biol. Cell 11, 1305-1313 (2000). (Pubitemid 30211031)
41. Ivanov, D. & Nasmyth, K. A topological interaction between cohesin rings and a circular minichromosome. Cell 122, 849-860 (2005). (Pubitemid 41345203)
42. Gruber, S. et al. Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell 127, 523-537 (2006). (Pubitemid 44647422)
43. Hudson, D.F. et al. Molecular and genetic analysis of condensin function in vertebrate cells. Mol. Biol. Cell 19, 3070-3079 (2008).
44. Murayama, Y. & Uhlmann, F. Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature 505, 367-371 (2014).
45. Fitzgerald, D.J. et al. Protein complex expression by using multigene baculoviral vectors. Nat. Methods 3, 1021-1032 (2006). (Pubitemid 44782702)
46. Luger, K., Rechsteiner, T.J. & Richmond, T.J. Preparation of nucleosome core particle from recombinant histones. Methods Enzymol. 304, 3-19 (1999). (Pubitemid 29268874)
47. Saravanan, M. et al. Interactions between the nucleosome histone core and Arp8 in the INO80 chromatin remodeling complex. Proc. Natl. Acad. Sci. USA 109, 20883-20888 (2012).
48. Xu, H., Zhang, L. & Freitas, M.A. Identification and characterization of disulfide bonds in proteins and peptides from tandem MS data by use of the MassMatrix MS/MS search engine. J. Proteome Res. 7, 138-144 (2008). (Pubitemid 351171125)
49. Rinner, O. et al. Identification of cross-linked peptides from large sequence databases. Nat. Methods 5, 315-318 (2008). (Pubitemid 351455158)
50. Walzthoeni, T. et al. False discovery rate estimation for cross-linked peptides identified by mass spectrometry. Nat. Methods 9, 901-903 (2012).
51. Notredame, C., Higgins, D.G. & Heringa, J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217 (2000).
52. Kelley, L.A. & Sternberg, M.J.E. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371 (2009).
53. Thompson, J.D., Higgins, D.G. & Gibson, T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680 (1994). (Pubitemid 24354800)
54. Langmead, B. & Salzberg, S.L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359 (2012).
55. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
56. Gerlich, D., Hirota, T., Koch, B., Peters, J.-M. & Ellenberg, J. Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr. Biol. 16, 333-344 (2006). (Pubitemid 43259343)
57. Carpenter, A.E. et al. CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 7, R100 (2006).