Condensin: Architect of mitotic chromosomes

Springer Science and Business Media LLC - Tập 17 - Trang 131-144 - 2009
Damien F. Hudson1,2, Kathryn M. Marshall3, William C. Earnshaw4
1Murdoch Children’s Research Institute, Royal Children’s Hospital, Melbourne, Australia
2Department of Paediatrics, University of Melbourne, Royal Children’s Hospital, Melbourne, Australia
3Department of Surgery, University of Melbourne, Austin Health, Heidelberg, Australia
4Wellcome Trust Centre for Cell Biology, Institute of Cell and Molecular Biology, University of Edinburgh, Edinburgh, UK

Tóm tắt

Condensin is a highly conserved pentameric complex consisting of two structural maintenance of chromosome (SMC) ATPase subunits and three auxiliary components. While initially regarded as a key driver of mitotic chromosome condensation, condensin is increasingly viewed as having a more subtle influence on chromosome architecture. The two condensin complexes are required to direct the correct folding and organization of chromosomes prior to anaphase and for keeping the chromosomes compact as they separate to the poles. This ancient complex is essential in mitosis and meiosis and has additional roles in gene regulation and DNA repair. The wide variety of biochemical and genetic tools available are gradually unravelling the numerous roles condensin plays during the cell cycle and shedding light on its mechanism of action.

Tài liệu tham khảo

Adams RR, Maiato H, Earnshaw WC, Carmena M (2001) 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 153:865–880 Adolph KW, Cheng SM, Laemmli UK (1977) Role of nonhistone proteins in metaphase chromosome structure. Cell 12:805–816 Anderson DE, Losada A, Erickson HP, Hirano T (2002) Condensin and cohesin display different arm conformations with characteristic hinge angles. J Cell Biol 156:419–424 Arumugam P, Gruber S, Tanaka K, Haering CH, Mechtler K, Nasmyth K (2003) ATP hydrolysis is required for cohesin's association with chromosomes. Curr Biol 13:1941–1953 Arumugam P, Nishino T, Haering CH, Gruber S, Nasmyth K (2006) Cohesin's ATPase activity is stimulated by the C-terminal Winged-Helix domain of its kleisin subunit. Curr Biol 16:1998–2008 Bazett-Jones DP, Kimura K, Hirano T (2002) Efficient supercoiling of DNA by a single condensin complex as revealed by electron spectroscopic imaging. Mol Cell 9:1183–1190 Belmont AS (2006) Mitotic chromosome structure and condensation. Curr Opin Cell Biol 18:632–638 Chuang PT, Albertson DG, Meyer BJ (1994) DPY-27: a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell 79:459–474 Cobbe N, Heck MM (2004) The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol Biol Evol 21:332–347 Csankovszki G, Collete K, Spahl K (2009) Three distinct condensin complexes control C. elegans chromosome dynamics. Curr Biol 19:9–19 D’Ambrosio C, Schmidt CK, Katou Y et al (2008) Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22:2215–2227 Earnshaw WC, Laemmli UK (1983) Architecture of metaphase chromosomes and chromosome scaffolds. J Cell Biol 96:84–93 Earnshaw WC, Halligan B, Cooke CA, Heck MM, Liu LF (1985) Topoisomerase II is a structural component of mitotic chromosome scaffolds. J Cell Biol 100:1706–1715 Eide T, Carlson C, Taskén KA, Hirano T, Taskén K, Collas P (2002) Distinct but overlapping domains of AKAP95 are implicated in chromosome condensation and condensin targeting. EMBO Rep 3:426–432 Ercan S, Lieb L (2009) Regulation of transcription by a condensin-like complex to achieve dosage compensation. Chromosome Res (this issue) Gasser SM, Laroche T, Falquet J, Boy de la Tour E, Laemmli UK (1986) Metaphase chromosome structure. Involvement of topoisomerase II. J Mol Biol 188:613–629 Gerlich D, Hirota T, Koch B, Peters JM, Ellenberg J (2006) Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr Biol 16:333–344 Giet R, Glover DM (2001) Drosophila aurora B kinase is required for histone H3 phosphorylation and condensin recruitment during chromosome condensation and to organize the central spindle during cytokinesis. J Cell Biol 152:669–682 Graumann P, Knust T (2009) Dynamics and function of the SMC/MukB complex in bacteria. Chromosome Res Gruber S, Haering CH, Nasmyth K (2003) Chromosomal cohesin forms a ring. Cell 112:765–777 Gruber S, Arumugam P, Katou Y et al (2006) Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell 127:523–537 Haering CH, Löwe J, Hochwagen A, Nasmyth K (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9:773–788 Haering CH, Schoffnegger D, Nishino T, Helmhart W, Nasmyth K, Löwe J (2004) Structure and stability of cohesin’s Smc1-kleisin interaction. Mol Cell 15:951–964 Haering CH, Farcas AM, Arumugam P, Metson J, Nasmyth K (2008) The cohesin ring concatenates sister DNA molecules. Nature 454:297–301 Hagstrom KA, Holmes VF, Cozzarelli NR, Meyer BJ (2002) C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev 16:729–742 Hirano T (2005) Condensins: organizing and segregating the genome. Curr Biol 15:R265–R275 Hirano T (2006) At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 7:311–322 Hirano M, Hirano T (2006) Opening closed arms: long-distance activation of SMC ATPase by hinge-DNA interaction. Mol Cell 21:175–186 Hirano T, Mitchison TJ (1994) A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79:449–458 Hirano T, Funahashi SI, Uemura T, Yanagida M (1986) Isolation and characterization of Schizosaccharomyces pombe cut mutants that block nuclear division but not cytokinesis. EMBO J 5:2973–2979 Hirano T, Kobayashi R, Hirano M (1997) Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 89:511–521 Hirano M, Anderson DE, Erickson HP, Hirano T (2001) Bimodal activation of SMC ATPase by intra- and inter-molecular interactions. EMBO J 20:3238–3250 Hirota T, Gerlich D, Koch B, Ellenberg J, Peters JM (2004) Distinct functions of condensin I and II in mitotic chromosome assembly. J Cell Sci 117:6435–6445 Hopfner KP, Karcher A, Craig L, Woo TT, Carney JP, Tainer JA (2001) Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell 105:473–485 Hudson DF, Vagnarelli P, Gassmann R, Earnshaw WC (2003) Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. Dev Cell 5:323–336 Hudson DF, Ohta S, Freisinger T et al (2008) Molecular and genetic analysis of condensin function in vertebrate cells. Mol Biol Cell 19:3070–3079 Kaitna S, Pasierbek P, Jantsch M, Loidl J, Glotzer M (2002) The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous chromosomes during meiosis. Curr Biol 12:798–812 Kimura K, Hirano T (2000) Dual roles of the 11S regulatory subcomplex in condensin functions. Proc Natl Acad Sci USA 97:11972–11977 Kimura K, Rybenkov VV, Crisona NJ, Hirano T, Cozzarelli NR (1999) 13S condensin actively reconfigures DNA by introducing global positive writhe: implications for chromosome condensation. Cell 98:239–248 Koshland D, Strunnikov A (1996) Mitotic chromosome condensation. Annu Rev Cell Dev Biol 12:305–333 Laemmli UK, Käs E, Poljak L, Adachi Y (1992) Scaffold-associated regions: cis-acting determinants of chromatin structural loops and functional domains. Curr Opin Genet Dev 2:275–285 Lavoie BD, Hogan E, Koshland D (2004) In vivo requirements for rDNA chromosome condensation reveal two cell-cycle-regulated pathways for mitotic chromosome folding. Genes Dev 18:76–87 Lewis CD, Laemmli UK (1982) Higher order metaphase chromosome structure: evidence for metalloprotein interactions. Cell 29:171–181 Lipp JJ, Hirota T, Poser I, Peters JM (2007) Aurora B controls the association of condensin I but not condensin II with mitotic chromosomes. J Cell Sci 120:1245–1255 Longworth MS, Herr A, Ji JY, Dyson NJ (2008) RBF1 promotes chromatin condensation through a conserved interaction with the condensin II protein dCAP-D3. Genes Dev 22:1011–1024 Maeshima K, Laemmli UK (2003) A two-step scaffolding model for mitotic chromosome assembly. Dev Cell 4:467–480 Melby TE, Ciampaglio CN, Briscoe G, Erickson HP (1998) The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J Cell Biol 142:1595–1604 Murnion ME, Adams RR, Callister DM, Allis CD, Earnshaw WC, Swedlow JR (2001) Chromatin-associated protein phosphatase 1 regulates aurora-B and histone H3 phosphorylation. J Biol Chem 276:26656–26665 Nakazawa N, Nakamura T, Kokubu A, Ebe M, Nagao K, Yanagida M (2008) Dissection of the essential steps for condensin accumulation at kinetochores and rDNAs during fission yeast mitosis. J Cell Biol 180:1115–1131 Nasmyth K, Haering CH (2005) The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74:595–648 Oliveira RA, Coelho PA, Sunkel CE (2005) The condensin I subunit Barren/CAP-H is essential for the structural integrity of centromeric heterochromatin during mitosis. Mol Cell Biol 25:8971–8984 Onn I, Aono N, Hirano M, Hirano T (2007) Reconstitution and subunit geometry of human condensin complexes. EMBO J 26:1024–1034 Ono T, Losada A, Hirano M, Myers MP, Neuwald AF, Hirano T (2003) Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115:109–121 Ono T, Fang Y, Spector DL, Hirano T (2004) Spatial and temporal regulation of condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 15:3296–3308 Parelho V, Hadjur S, Spivakov M et al (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422–433 Paulson JR, Laemmli UK (1977) The structure of histone-depleted metaphase chromosomes. Cell 12:817–828 Poirier MG, Marko JF (2002) Mitotic chromosomes are chromatin networks without a mechanically contiguous protein scaffold. Proc Natl Acad Sci USA 99:15393–15397 Ribeiro S, Gatlin JC, Dong Y et al (2008) Condensin regulates the stiffness of vertebrates centromeres. Submitted Saitoh N, Goldberg IG, Wood ER, Earnshaw WC (1994) ScII: an abundant chromosome scaffold protein is a member of a family of putative ATPases with an unusual predicted tertiary structure. J Cell Biol 127:303–318 Saitoh N, Goldberg I, Earnshaw WC (1995) The SMC proteins and the coming of age of the chromosome scaffold hypothesis. Bioessays 17:759–766 Schleiffer A, Kaitna S, Maurer-Stroh S, Glotzer M, Nasmyth K, Eisenhaber F (2003) Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol Cell 11:571–575 Stray JE, Lindsley JE (2003) Biochemical analysis of the yeast condensin Smc2/4 complex: an ATPase that promotes knotting of circular DNA. J Biol Chem 278:26238–26248 Strunnikov AV, Hogan E, Koshland D (1995) SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation, defines a subgroup within the SMC family. Genes Dev 9:587–599 Surcel A, Koshland D, Ma H, Simpson RT (2008) Cohesin interaction with centromeric minichromosomes shows a multi-complex rod-shaped structure. PLoS ONE 3:e2453 Takemoto A, Kimura K, Yokoyama S, Hanaoka F (2004) Cell cycle-dependent phosphorylation, nuclear localization, and activation of human condensin. J Biol Chem 279:4551–4559 Takemoto A, Kimura K, Yanagisawa J, Yokoyama S, Hanaoka F (2006) Negative regulation of condensin I by CK2-mediated phosphorylation. EMBO J 25:5339–5348 Trinkle-Mulcahy L, Andersen J, Lam YW, Moorhead G, Mann M, Lamond AI (2006) Repo-Man recruits PP1 gamma to chromatin and is essential for cell viability. J Cell Biol 172:679–692 Vagnarelli P, Hudson DF, Ribeiro SA et al (2006) Condensin and Repo-Man-PP1 co-operate in the regulation of chromosome architecture during mitosis. Nat Cell Biol 8:1133–1142 Volkov A, Mascarenhas J, Andrei-Selmer C, Ulrich HD, Graumann PL (2003) A prokaryotic condensin/cohesin-like complex can actively compact chromosomes from a single position on the nucleoid and binds to DNA as a ring-like structure. Mol Cell Biol 23:5638–5650 Wang BD, Eyre D, Basrai M, Lichten M, Strunnikov A (2005) Condensin binding at distinct and specific chromosomal sites in the Saccharomyces cerevisiae genome. Mol Cell Biol 25:7216–7225 Weitzer S, Lehane C, Uhlmann F (2003) A model for ATP hydrolysis-dependent binding of cohesin to DNA. Curr Biol 13:1930–1940 Wendt KS, Yoshida K, Itoh T et al (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796–801 Yeong FM, Hombauer H, Wendt KS et al (2003) Identification of a subunit of a novel Kleisin-beta/SMC complex as a potential substrate of protein phosphatase 2A. Curr Biol 13:2058–2064 Yoshimura SH, Hizume K, Murakami A, Sutani T, Takeyasu K, Yanagida M (2002) Condensin architecture and interaction with DNA: regulatory non-SMC subunits bind to the head of SMC heterodimer. Curr Biol 12:508–513