The SMC complexes, DNA and chromosome topology: right or knot?

References

• Adachi Y, Luke M, Laemmli UK. 1991. Chromosome assembly in vitro: Topoisomerase II is required for condensation. Cell 64:137–148.
   PubMed Web of Science ®Google Scholar
• Ampatzidou E, Irmisch A, O’Connell MJ, Murray JM. 2006. Smc5/6 is required for repair at collapsed replication forks. Mol Cell Biol 26:9387–9401.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Baxter J, Sen N, Martínez VL, De Carandini ME, Schvartzman JB, Diffley JF, Aragón L. 2011. Positive supercoiling of mitotic DNA drives decatenation by topoisomerase II in eukaryotes. Science 331:1328–1332.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Bermejo R, Capra T, Gonzalez-Huici V, Fachinetti D, Cocito A, Natoli G, Katou Y, Mori H, Kurokawa K, Shirahige K, Foiani M. 2009. Genome-organizing factors Top2 and Hmo1 prevent chromosome fragility at sites of S phase transcription. Cell 138:870–884.
   PubMed Web of Science ®Google Scholar
• Bermúdez I, García-Martínez J, Pérez-Ortín JE, Roca J. 2010. A method for genome-wide analysis of DNA helical tension by means of psoralen-DNA photobinding. Nucleic Acids Res 38:e182.
   PubMed Web of Science ®Google Scholar
• Bhat MA, Philp AV, Glover DM, Bellen HJ. 1996. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II. Cell 87:1103–1114.
   PubMed Web of Science ®Google Scholar
• Branzei D, Sollier J, Liberi G, Zhao X, Maeda D, Seki M, Enomoto T, Ohta K, Foiani M. 2006. Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127:509–522.
   PubMed Web of Science ®Google Scholar
• Britton RA, Lin DC, Grossman AD. 1998. Characterization of a prokaryotic SMC protein involved in chromosome partitioning. Genes Dev 12:1254–1259.
   PubMed Web of Science ®Google Scholar
• Buongiorno-Nardelli M, Micheli G, Carri MT, Marilley M. 1982. A relationship between replicon size and supercoiled loop domains in the eukaryotic genome. Nature 298:100–102.
   PubMed Web of Science ®Google Scholar
• Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH. 2011. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144:732–744.
   PubMed Web of Science ®Google Scholar
• Coelho PA, Queiroz-Machado J, Sunkel CE. 2003. Condensin-dependent localisation of topoisomerase II to an axial chromosomal structure is required for sister chromatid resolution during mitosis. J Cell Sci 116:4763–4776.
   PubMed Web of Science ®Google Scholar
• Courbet S, Gay S, Arnoult N, Wronka G, Anglana M, Brison O, Debatisse M. 2008. Replication fork movement sets chromatin loop size and origin choice in mammalian cells. Nature 455:557–560.
   PubMed Web of Science ®Google Scholar
• Cui Y, Petrushenko ZM, Rybenkov VV. 2008. MukB acts as a macromolecular clamp in DNA condensation. Nat Struct Mol Biol 15:411–418.
   PubMed Web of Science ®Google Scholar
• D’Ambrosio C, Kelly G, Shirahige K, Uhlmann F. 2008a. Condensin-dependent rDNA decatenation introduces a temporal pattern to chromosome segregation. Curr Biol 18:1084–1089.
   PubMed Web of Science ®Google Scholar
• D’Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, Shirahige K, Uhlmann F. 2008b. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22:2215–2227.
   PubMed Web of Science ®Google Scholar
• Davies HG, Small JV. 1968. Structural units in chromatin and their orientation on membranes. Nature 217:1122–1125.
   PubMed Web of Science ®Google Scholar
• Duncan IW. 2002. Transvection effects in Drosophila. Annu Rev Genet 36:521–556.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Earnshaw WC, Heck MM. 1985. Localization of topoisomerase II in mitotic chromosomes. J Cell Biol 100:1716–1725.
   PubMed Web of Science ®Google Scholar
• Edgar BA, Orr-Weaver TL. 2001. Endoreplication cell cycles: More for less. Cell 105:297–306.
   PubMed Web of Science ®Google Scholar
• Elcock LS, Bridger JM. 2010. Exploring the relationship between interphase gene positioning, transcriptional regulation and the nuclear matrix. Biochem Soc Trans 38:263–267.
   PubMed Web of Science ®Google Scholar
• Fennell-Fezzie R, Gradia SD, Akey D, Berger JM. 2005. The MukF subunit of Escherichia coli condensin: Architecture and functional relationship to kleisins. EMBO J 24:1921–1930.
   PubMed Web of Science ®Google Scholar
• Finch JT, Lutter LC, Rhodes D, Brown RS, Rushton B, Levitt M, Klug A. 1977. Structure of nucleosome core particles of chromatin. Nature 269:29–36.
   PubMed Web of Science ®Google Scholar
• Fousteri MI, Lehmann AR. 2000. A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein. EMBO J 19:1691–1702.
   PubMed Web of Science ®Google Scholar
• Freeman L, Aragon-Alcaide L, Strunnikov A. 2000. The condensin complex governs chromosome condensation and mitotic transmission of rDNA. J Cell Biol 149:811–824.
   PubMedGoogle Scholar
• Fujioka Y, Kimata Y, Nomaguchi K, Watanabe K, Kohno K. 2002. Identification of a novel non-structural maintenance of chromosomes (SMC) component of the SMC5-SMC6 complex involved in DNA repair. J Biol Chem 277:21585–21591.
   PubMed Web of Science ®Google Scholar
• Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH, Chew EG, Huang PY, Welboren WJ, Han Y, Ooi HS, Ariyaratne PN, Vega VB, Luo Y, Tan PY, Choy PY, Wansa KD, Zhao B, Lim KS, Leow SC, Yow JS, Joseph R, Li H, Desai KV, Thomsen JS, Lee YK, Karuturi RK, Herve T, Bourque G, Stunnenberg HG, Ruan X, Cacheux-Rataboul V, Sung WK, Liu ET, Wei CL, Cheung E, Ruan Y. 2009. An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 462:58–64.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Guacci V, Koshland D, Strunnikov A. 1997. A direct link between sister chromatid cohesion and chromosome condensation revealed through the analysis of MCD1 in S. cerevisiae. Cell 91:47–57.
   PubMed Web of Science ®Google Scholar
• Guillou E, Ibarra A, Coulon V, Casado-Vela J, Rico D, Casal I, Schwob E, Losada A, Méndez J. 2010. Cohesin organizes chromatin loops at DNA replication factories. Genes Dev 24:2812–2822.
   PubMed Web of Science ®Google Scholar
• Hadjur S, Williams LM, Ryan NK, Cobb BS, Sexton T, Fraser P, Fisher AG, Merkenschlager M. 2009. Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus. Nature 460:410–413.
   PubMed Web of Science ®Google Scholar
• Haering CH, Löwe J, Hochwagen A, Nasmyth K. 2002. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol Cell 9:773–788.
   PubMed Web of Science ®Google Scholar
• Haeusler RA, Pratt-Hyatt M, Good PD, Gipson TA, Engelke DR. 2008. Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. Genes Dev 22:2204–2214.
   PubMed Web of Science ®Google Scholar
• Hartl TA, Smith HF, Bosco G. 2008. Chromosome alignment and transvection are antagonized by condensin II. Science 322:1384–1387.
   PubMed Web of Science ®Google Scholar
• Hayama R, Marians KJ. 2010. Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli. Proc Natl Acad Sci USA 107:18826–18831.
   PubMed Web of Science ®Google Scholar
• Hazbun TR, Malmström L, Anderson S, Graczyk BJ, Fox B, Riffle M, Sundin BA, Aranda JD, McDonald WH, Chiu CH, Snydsman BE, Bradley P, Muller EG, Fields S, Baker D, Yates JR 3rd, Davis TN. 2003. Assigning function to yeast proteins by integration of technologies. Mol Cell 12:1353–1365.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hirano M, Hirano T. 1998. ATP-dependent aggregation of single-stranded DNA by a bacterial SMC homodimer. EMBO J 17:7139–7148.
   PubMed Web of Science ®Google Scholar
• Hirano M, Hirano T. 2002. Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J 21:5733–5744.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Hirano T, Mitchison TJ. 1993. Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus egg extracts. J Cell Biol 120:601–612.
   PubMed Web of Science ®Google Scholar
• Hirano T, Mitchison TJ. 1994. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79:449–458.
   PubMed Web of Science ®Google Scholar
• Holm C, Stearns T, Botstein D. 1989. DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage. Mol Cell Biol 9:159–168.
   PubMed Web of Science ®Google Scholar
• Hu B, Liao C, Millson SH, Mollapour M, Prodromou C, Pearl LH, Piper PW, Panaretou B. 2005. Qri2/Nse4, a component of the essential Smc5/6 DNA repair complex. Mol Microbiol 55:1735–1750.
   PubMed Web of Science ®Google Scholar
• Jackson DA, Pombo A. 1998. Replicon clusters are stable units of chromosome structure: Evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J Cell Biol 140:1285–1295.
   PubMed Web of Science ®Google Scholar
• Joshi RS, Piña B, Roca J. 2010. Positional dependence of transcriptional inhibition by DNA torsional stress in yeast chromosomes. EMBO J 29:740–748.
   PubMed Web of Science ®Google Scholar
• Kadauke S, Blobel GA. 2009. Chromatin loops in gene regulation. Biochim Biophys Acta 1789:17–25.
   PubMed Web of Science ®Google Scholar
• Kato J, Nishimura Y, Imamura R, Niki H, Hiraga S, Suzuki H. 1990. New topoisomerase essential for chromosome segregation in E. coli. Cell 63:393–404.
   PubMed Web of Science ®Google Scholar
• Kegel A, Betts-Lindroos H, Kanno T, Jeppsson K, Ström L, Katou Y, Itoh T, Shirahige K, Sjögren C. 2011. Chromosome length influences replication-induced topological stress. Nature 471:392–396.
   Google Scholar
• Kimura K, Hirano M, Kobayashi R, Hirano T. 1998. Phosphorylation and activation of 13S condensin by Cdc2 in vitro. Science 282:487–490.
   PubMed Web of Science ®Google Scholar
• Kimura K, Hirano T. 1997. ATP-dependent positive supercoiling of DNA by 13S condensin: A biochemical implication for chromosome condensation. Cell 90:625–634.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Kireeva N, Lakonishok M, Kireev I, Hirano T, Belmont AS. 2004. Visualization of early chromosome condensation: A hierarchical folding, axial glue model of chromosome structure. J Cell Biol 166:775–785.
   PubMed Web of Science ®Google Scholar
• Kitamura E, Blow JJ, Tanaka TU. 2006. Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories. Cell 125:1297–1308.
   PubMed Web of Science ®Google Scholar
• Kornberg RD. 1974. Chromatin structure: A repeating unit of histones and DNA. Science 184:868–871.
   PubMed Web of Science ®Google Scholar
• Laemmli UK, Cheng SM, Adolph KW, Paulson JR, Brown JA, Baumbach WR. 1978. Metaphase chromosome structure: The role of nonhistone proteins. Cold Spring Harb Symp Quant Biol 42 Pt 1:351–360.
   PubMedGoogle Scholar
• Larionov VL, Karpova TS, Kouprina NY, Jouravleva GA. 1985. A mutant of Saccharomyces cerevisiae with impaired maintenance of centromeric plasmids. Curr Genet 10:15–20.
   PubMed Web of Science ®Google Scholar
• Lehmann AR, Walicka M, Griffiths DJ, Murray JM, Watts FZ, McCready S, Carr AM. 1995. The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair. Mol Cell Biol 15:7067–7080.
   PubMed Web of Science ®Google Scholar
• Lemaitre JM, Danis E, Pasero P, Vassetzky Y, Méchali M. 2005. Mitotic remodeling of the replicon and chromosome structure. Cell 123:787–801.
   PubMed Web of Science ®Google Scholar
• Lewis CD, Laemmli UK. 1982. Higher order metaphase chromosome structure: Evidence for metalloprotein interactions. Cell 29:171–181.
   PubMed Web of Science ®Google Scholar
• Li Y, Stewart NK, Berger AJ, Vos S, Schoeffler AJ, Berger JM, Chait BT, Oakley MG. 2010. Escherichia coli condensin MukB stimulates topoisomerase IV activity by a direct physical interaction. Proc Natl Acad Sci USA 107:18832–18837.
   PubMed Web of Science ®Google Scholar
• Lindow JC, Britton RA, Grossman AD. 2002. Structural maintenance of chromosomes protein of Bacillus subtilis affects supercoiling in vivo. J Bacteriol 184:5317–5322.
   PubMed Web of Science ®Google Scholar
• Lindroos HB, Ström L, Itoh T, Katou Y, Shirahige K, Sjögren C. 2006. Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways. Mol Cell 22:755–767.
   PubMed Web of Science ®Google Scholar
• Losada A, Hirano M, Hirano T. 1998. Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. Genes Dev 12:1986–1997.
   PubMed Web of Science ®Google Scholar
• Losada A, Hirano T. 2001. Intermolecular DNA interactions stimulated by the cohesin complex in vitro: Implications for sister chromatid cohesion. Curr Biol 11:268–272.
   PubMed Web of Science ®Google Scholar
• Maeshima K, Laemmli UK. 2003. A two-step scaffolding model for mitotic chromosome assembly. Dev Cell 4:467–480.
   PubMed Web of Science ®Google Scholar
• Mankouri HW, Hickson ID. 2007. The RecQ helicase-topoisomerase III-Rmi1 complex: A DNA structure-specific ‘dissolvasome’? Trends Biochem Sci 32:538–546.
   PubMed Web of Science ®Google Scholar
• Mankouri HW, Ngo HP, Hickson ID. 2009. Esc2 and Sgs1 act in functionally distinct branches of the homologous recombination repair pathway in Saccharomyces cerevisiae. Mol Biol Cell 20:1683–1694.
   PubMed Web of Science ®Google Scholar
• Marsden MP, Laemmli UK. 1979. Metaphase chromosome structure: Evidence for a radial loop model. Cell 17:849–858.
   PubMed Web of Science ®Google Scholar
• Mascarenhas J, Soppa J, Strunnikov AV, Graumann PL. 2002. Cell cycle-dependent localization of two novel prokaryotic chromosome segregation and condensation proteins in Bacillus subtilis that interact with SMC protein. EMBO J 21:3108–3118.
   PubMed Web of Science ®Google Scholar
• McDonald WH, Pavlova Y, Yates JR 3rd, Boddy MN. 2003. Novel essential DNA repair proteins Nse1 and Nse2 are subunits of the fission yeast Smc5-Smc6 complex. J Biol Chem 278:45460–45467.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Michaelis C, Ciosk R, Nasmyth K. 1997. Cohesins: Chromosomal proteins that prevent premature separation of sister chromatids. Cell 91:35–45.
   PubMed Web of Science ®Google Scholar
• Mika S, Rost B. 2005. NMPdb: Database of Nuclear Matrix Proteins. Nucleic Acids Res 33:D160–D163.
   PubMed Web of Science ®Google Scholar
• Mirkin SM. 2001. DNA topology: Fundamentals. In Encyclopedia of Life Sciences (London, Nature Publishing Group).
   Google Scholar
• Miyabe I, Morishita T, Hishida T, Yonei S, Shinagawa H. 2006. Rhp51-dependent recombination intermediates that do not generate checkpoint signal are accumulated in Schizosaccharomyces pombe rad60 and smc5/6 mutants after release from replication arrest. Mol Cell Biol 26:343–353.
   PubMed Web of Science ®Google Scholar
• Morikawa H, Morishita T, Kawane S, Iwasaki H, Carr AM, Shinagawa H. 2004. Rad62 protein functionally and physically associates with the smc5/smc6 protein complex and is required for chromosome integrity and recombination repair in fission yeast. Mol Cell Biol 24:9401–9413.
   PubMed Web of Science ®Google Scholar
• Moriya S, Tsujikawa E, Hassan AK, Asai K, Kodama T, Ogasawara N. 1998. A Bacillus subtilis gene-encoding protein homologous to eukaryotic SMC motor protein is necessary for chromosome partition. Mol Microbiol 29:179–187.
   PubMed Web of Science ®Google Scholar
• Nasim A, Smith BP. 1975. Genetic control of radiation sensitivity in Schizosaccharomyces pombe. Genetics 79:573–582.
   PubMed Web of Science ®Google Scholar
• Nativio R, Wendt KS, Ito Y, Huddleston JE, Uribe-Lewis S, Woodfine K, Krueger C, Reik W, Peters JM, Murrell A. 2009. Cohesin is required for higher-order chromatin conformation at the imprinted IGF2-H19 locus. PLoS Genet 5:e1000739.
   PubMed Web of Science ®Google Scholar
• Niki H, Imamura R, Kitaoka M, Yamanaka K, Ogura T, Hiraga S. 1992. E.coli MukB protein involved in chromosome partition forms a homodimer with a rod-and-hinge structure having DNA binding and ATP/GTP binding activities. EMBO J 11:5101–5109.
   PubMed Web of Science ®Google Scholar
• Niki H, Jaffé A, Imamura R, Ogura T, Hiraga S. 1991. The new gene mukB codes for a 177 kd protein with coiled-coil domains involved in chromosome partitioning of E. coli. EMBO J 10:183–193.
   PubMed Web of Science ®Google Scholar
• Onn I, Aono N, Hirano M, Hirano T. 2007. Reconstitution and subunit geometry of human condensin complexes. EMBO J 26:1024–1034.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ortiz-Lombardía M, González A, Eritja R, Aymamí J, Azorín F, Coll M. 1999. Crystal structure of a DNA Holliday junction. Nat Struct Biol 6:913–917.
   PubMedGoogle Scholar
• Palecek J, Vidot S, Feng M, Doherty AJ, Lehmann AR. 2006. The Smc5-Smc6 DNA repair complex. bridging of the Smc5-Smc6 heads by the KLEISIN, Nse4, and non-Kleisin subunits. J Biol Chem 281:36952–36959.
   PubMed Web of Science ®Google Scholar
• Parelho V, Hadjur S, Spivakov M, Leleu M, Sauer S, Gregson HC, Jarmuz A, Canzonetta C, Webster Z, Nesterova T, Cobb BS, Yokomori K, Dillon N, Aragon L, Fisher AG, Merkenschlager M. 2008. Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132:422–433.
   PubMed Web of Science ®Google Scholar
• Pebernard S, McDonald WH, Pavlova Y, Yates JR 3rd, Boddy MN. 2004. Nse1, Nse2, and a novel subunit of the Smc5-Smc6 complex, Nse3, play a crucial role in meiosis. Mol Biol Cell 15:4866–4876.
   PubMed Web of Science ®Google Scholar
• Pebernard S, Wohlschlegel J, McDonald WH, Yates JR 3rd, Boddy MN. 2006. The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6 complex. Mol Cell Biol 26:1617–1630.
   PubMed Web of Science ®Google Scholar
• Petrushenko ZM, Cui Y, She W, Rybenkov VV. 2010. Mechanics of DNA bridging by bacterial condensin MukBEF in vitro and in singulo. EMBO J 29:1126–1135.
   PubMed Web of Science ®Google Scholar
• Petrushenko ZM, Lai CH, Rai R, Rybenkov VV. 2006a. DNA reshaping by MukB. Right-handed knotting, left-handed supercoiling. J Biol Chem 281:4606–4615.
   PubMed Web of Science ®Google Scholar
• Petrushenko ZM, Lai CH, Rybenkov VV. 2006b. Antagonistic interactions of kleisins and DNA with bacterial Condensin MukB. J Biol Chem 281:34208–34217.
   PubMed Web of Science ®Google Scholar
• Petrushenko ZM, She W, Rybenkov VV. 2011. A new family of bacterial condensins. Mol Microbiol 81:881–896.
   PubMed Web of Science ®Google Scholar
• Phillips JE, Corces VG. 2009. CTCF: Master weaver of the genome. Cell 137:1194–1211.
   PubMed Web of Science ®Google Scholar
• Poirier MG, Marko JF. 2002. Mitotic chromosomes are chromatin networks without a mechanically contiguous protein scaffold. Proc Natl Acad Sci USA 99:15393–15397.
   PubMed Web of Science ®Google Scholar
• Postow L, Crisona NJ, Peter BJ, Hardy CD, Cozzarelli NR. 2001. Topological challenges to DNA replication: Conformations at the fork. Proc Natl Acad Sci USA 98:8219–8226.
   PubMed Web of Science ®Google Scholar
• Prakash L, Prakash S. 1977a. Isolation and characterization of MMS-sensitive mutants of Saccharomyces cerevisiae. Genetics 86:33–55.
   PubMed Web of Science ®Google Scholar
• Prakash S, Prakash L. 1977b. Increased spontaneous mitotic segregation in MMS-sensitive mutants of Saccharomyces cerevisiae. Genetics 87:229–236.
   PubMed Web of Science ®Google Scholar
• Ris H, Kubai DF. 1970. Chromosome structure. Annu Rev Genet 4:263–294.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Saka Y, Sutani T, Yamashita Y, Saitoh S, Takeuchi M, Nakaseko Y, Yanagida M. 1994. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO J 13:4938–4952.
   PubMed Web of Science ®Google Scholar
• Sawitzke JA, Austin S. 2000. Suppression of chromosome segregation defects of Escherichia coli muk mutants by mutations in topoisomerase I. Proc Natl Acad Sci USA 97:1671–1676.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A, Brown GD, Carroll JS, Flicek P, Odom DT. 2010. A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 20:578–588.
   PubMed Web of Science ®Google Scholar
• Schmiesing JA, Gregson HC, Zhou S, Yokomori K. 2000. A human condensin complex containing hCAP-C-hCAP-E and CNAP1, a homolog of Xenopus XCAP-D2, colocalizes with phosphorylated histone H3 during the early stage of mitotic chromosome condensation. Mol Cell Biol 20:6996–7006.
   PubMed Web of Science ®Google Scholar
• Sivolob A, Prunell A. 2003. Linker histone-dependent organization and dynamics of nucleosome entry/exit DNAs. J Mol Biol 331:1025–1040.
   PubMed Web of Science ®Google Scholar
• Sollier J, Driscoll R, Castellucci F, Foiani M, Jackson SP, Branzei D. 2009. The Saccharomyces cerevisiae Esc2 and Smc5-6 proteins promote sister chromatid junction-mediated intra-S repair. Mol Biol Cell 20:1671–1682.
   PubMed Web of Science ®Google Scholar
• Soppa J, Kobayashi K, Noirot-Gros MF, Oesterhelt D, Ehrlich SD, Dervyn E, Ogasawara N, Moriya S. 2002. Discovery of two novel families of proteins that are proposed to interact with prokaryotic SMC proteins, and characterization of the Bacillus subtilis family members ScpA and ScpB. Mol Microbiol 45:59–71.
   PubMed Web of Science ®Google Scholar
• Stray JE, Crisona NJ, Belotserkovskii BP, Lindsley JE, Cozzarelli NR. 2005. The Saccharomyces cerevisiae Smc2/4 condensin compacts DNA into (+) chiral structures without net supercoiling. J Biol Chem 280:34723–34734.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Strick TR, Kawaguchi T, Hirano T. 2004. Real-time detection of single-molecule DNA compaction by condensin I. Curr Biol 14:874–880.
   PubMed Web of Science ®Google Scholar
• Ström L, Lindroos HB, Shirahige K, Sjögren C. 2004. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16:1003–1015.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Strunnikov AV, Larionov VL, Koshland D. 1993. SMC1: An essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous protein family. J Cell Biol 123:1635–1648.
   PubMed Web of Science ®Google Scholar
• Sutani T, Yuasa T, Tomonaga T, Dohmae N, Takio K, Yanagida M. 1999. Fission yeast condensin complex: Essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. Genes Dev 13:2271–2283.
   PubMed Web of Science ®Google Scholar
• Tadesse S, Mascarenhas J, Kösters B, Hasilik A, Graumann PL. 2005. Genetic interaction of the SMC complex with topoisomerase IV in Bacillus subtilis. Microbiology (Reading, Engl) 151:3729–3737.
   PubMed Web of Science ®Google Scholar
• Tavormina PA, Côme MG, Hudson JR, Mo YY, Beck WT, Gorbsky GJ. 2002. Rapid exchange of mammalian topoisomerase II alpha at kinetochores and chromosome arms in mitosis. J Cell Biol 158:23–29.
   PubMed Web of Science ®Google Scholar
• Taylor EM, Copsey AC, Hudson JJ, Vidot S, Lehmann AR. 2008. Identification of the proteins, including MAGEG1, that make up the human SMC5-6 protein complex. Mol Cell Biol 28:1197–1206.
   PubMedGoogle Scholar
• Taylor EM, Moghraby JS, Lees JH, Smit B, Moens PB, Lehmann AR. 2001. Characterization of a novel human SMC heterodimer homologous to the Schizosaccharomyces pombe Rad18/Spr18 complex. Mol Biol Cell 12:1583–1594.
   PubMed Web of Science ®Google Scholar
• Thompson M, Haeusler RA, Good PD, Engelke DR. 2003. Nucleolar clustering of dispersed tRNA genes. Science 302:1399–1401.
   PubMed Web of Science ®Google Scholar
• Torres-Rosell J, De Piccoli G, Cordon-Preciado V, Farmer S, Jarmuz A, Machin F, Pasero P, Lisby M, Haber JE, Aragón L. 2007b. Anaphase onset before complete DNA replication with intact checkpoint responses. Science 315:1411–1415.
   PubMed Web of Science ®Google Scholar
• Torres-Rosell J, Machín F, Farmer S, Jarmuz A, Eydmann T, Dalgaard JZ, Aragón L. 2005. SMC5 and SMC6 genes are required for the segregation of repetitive chromosome regions. Nat Cell Biol 7:412–419.
   PubMed Web of Science ®Google Scholar
• Torres-Rosell J, Sunjevaric I, De Piccoli G, Sacher M, Eckert-Boulet N, Reid R, Jentsch S, Rothstein R, Aragón L, Lisby M. 2007a. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat Cell Biol 9:923–931.
   PubMed Web of Science ®Google Scholar
• Tóth A, Ciosk R, Uhlmann F, Galova M, Schleiffer A, Nasmyth K. 1999. Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev 13:320–333.
   PubMed Web of Science ®Google Scholar
• Tsutsui KM, Sano K, Tsutsui K. 2005. Dynamic view of the nuclear matrix. Acta Med Okayama 59:113–120.
   Google Scholar
• Uemura T, Ohkura H, Adachi Y, Morino K, Shiozaki K, Yanagida M. 1987. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50:917–925.
   PubMed Web of Science ®Google Scholar
• Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber JE, Koshland D. 2004. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell 16:991–1002.
   PubMed Web of Science ®Google Scholar
• Verkade HM, Bugg SJ, Lindsay HD, Carr AM, O’Connell MJ. 1999. Rad18 is required for DNA repair and checkpoint responses in fission yeast. Mol Biol Cell 10:2905–2918.
   PubMed Web of Science ®Google Scholar
• Vogelstein B, Pardoll DM, Coffey DS. 1980. Supercoiled loops and eucaryotic DNA replicaton. Cell 22:79–85.
   PubMed Web of Science ®Google Scholar
• Wang JC. 2002. Cellular roles of DNA topoisomerases: A molecular perspective. Nat Rev Mol Cell Biol 3:430–440.
   PubMed Web of Science ®Google Scholar
• Wang L, Haeusler RA, Good PD, Thompson M, Nagar S, Engelke DR. 2005. Silencing near tRNA genes requires nucleolar localization. J Biol Chem 280:8637–8639.
   PubMed Web of Science ®Google Scholar
• Weitao T, Dasgupta S, Nordström K. 2000a. Role of the mukB gene in chromosome and plasmid partition in Escherichia coli. Mol Microbiol 38:392–400.
   PubMed Web of Science ®Google Scholar
• Weitao T, Nordström K, Dasgupta S. 2000b. Escherichia coli cell cycle control genes affect chromosome superhelicity. EMBO Rep 1:494–499.
   PubMed Web of Science ®Google Scholar
• Weitzer S, Lehane C, Uhlmann F. 2003. A model for ATP hydrolysis-dependent binding of cohesin to DNA. Curr Biol 13:1930–1940.
   PubMed Web of Science ®Google Scholar
• Wendt KS, Peters JM. 2009. How cohesin and CTCF cooperate in regulating gene expression. Chromosome Res 17:201–214.
   PubMed Web of Science ®Google Scholar
• Wendt KS, Yoshida K, Itoh T, Bando M, Koch B, Schirghuber E, Tsutsumi S, Nagae G, Ishihara K, Mishiro T, Yahata K, Imamoto F, Aburatani H, Nakao M, Imamoto N, Maeshima K, Shirahige K, Peters JM. 2008. Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451:796–801.
   PubMed Web of Science ®Google Scholar
• Witz G, Stasiak A. 2010. DNA supercoiling and its role in DNA decatenation and unknotting. Nucleic Acids Res 38:2119–2133.
   PubMed Web of Science ®Google Scholar
• Woo JS, Lim JH, Shin HC, Suh MK, Ku B, Lee KH, Joo K, Robinson H, Lee J, Park SY, Ha NC, Oh BH. 2009. Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions. Cell 136:85–96.
   Google Scholar
• Woodcock CL, Ghosh RP. 2010. Chromatin higher-order structure and dynamics. Cold Spring Harb Perspect Biol 2:a000596.
   PubMed Web of Science ®Google Scholar
• Yamanaka K, Ogura T, Niki H, Hiraga S. 1996. Identification of two new genes, mukE and mukF, involved in chromosome partitioning in Escherichia coli. Mol Gen Genet 250:241–251.
   PubMedGoogle Scholar
• Yamazoe M, Onogi T, Sunako Y, Niki H, Yamanaka K, Ichimura T, Hiraga S. 1999. Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J 18:5873–5884.
   PubMed Web of Science ®Google Scholar