A Topology-Centric View on Mitotic Chromosome Architecture
Abstract
1. Introduction
2. Topoisomerase II and Sister Chromatid Resolution
3. Topoisomerase II and Chromosome Compaction
4. Topoisomerase II and Biophysical Properties of Chromosomes
5. Regulation of Topoisomerase II Activity: Guidance by the Structural Maintenance of Chromosomes (SMC) Complexes
5.1. The Directionality Problem
5.2. Bacterial SMCs
5.3. SMC5/6
5.4. Cohesin—The Resolution Blocker
5.5. Condensin—The Guiding Complex
6. Concluding Remarks
Acknowledgments
Author Contributions
Conflicts of Interest
Abbreviations
SMC | Structural maintenance of chromosomes |
UBF | Ultra-fine bridges |
BLM | Bloom syndrome protein |
PICH | Polo-like kinase 1-interacting checkpoint helicase |
References
- Goto, T.; Wang, J.C. Yeast DNA topoisomerase II. An ATP-dependent type II topoisomerase that catalyzes the catenation, decatenation, unknotting, and relaxation of double-stranded DNA rings. J. Biol. Chem. 1982, 257, 5866–5872. [Google Scholar] [PubMed]
- Hsieh, T.; Brutlag, D. ATP-dependent DNA topoisomerase from D. melanogaster reversibly catenates duplex DNA rings. Cell 1980, 21, 115–125. [Google Scholar] [CrossRef]
- Bauer, D.L.V.; Marie, R.; Rasmussen, K.H.; Kristensen, A.; Mir, K.U. DNA catenation maintains structure of human metaphase chromosomes. Nucleic Acids Res. 2012, 40, 11428–11434. [Google Scholar] [CrossRef] [PubMed]
- Pommier, Y.; Sun, Y.; Huang, S.N.; Nitiss, J.L. Roles of eukaryotic topoisomerases in transcription, replication and genomic stability. Nat. Rev. Mol. Cell Biol. 2016, 17, 703–721. [Google Scholar] [CrossRef] [PubMed]
- Uemura, T.; Ohkura, H.; Adachi, Y.; Morino, K.; Shiozaki, K.; Yanagida, M. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 1987, 50, 917–925. [Google Scholar] [CrossRef]
- Clarke, D.J.; Johnson, R.T.; Downes, C.S. Topoisomerase II inhibition prevents anaphase chromatid segregation in mammalian cells independently of the generation of DNA strand breaks. J. Cell Sci. 1993, 105, 563–569. [Google Scholar] [PubMed]
- Oliveira, R.A.; Hamilton, R.S.; Pauli, A.; Davis, I.; Nasmyth, K. Cohesin cleavage and Cdk inhibition trigger formation of daughter nuclei. Nat. Cell Biol. 2010, 12, 185–192. [Google Scholar] [CrossRef] [PubMed]
- Coelho, P.A.; Queiroz-Machado, J.; Carmo, A.M.; Moutinho-Pereira, S.; Maiato, H.; Sunkel, C.E. Dual Role of Topoisomerase II in Centromere Resolution and Aurora B Activity. PLoS Biol. 2008, 6, e207. [Google Scholar] [CrossRef] [PubMed]
- Charbin, A.; Bouchoux, C.; Uhlmann, F. Condensin aids sister chromatid decatenation by topoisomerase II. Nucleic Acids Res. 2014, 42, 340–348. [Google Scholar] [CrossRef] [PubMed]
- Downes, C.S.; Clarke, D.J.; Mullinger, A.M.; Gimenez-Abian, J.F.; Creighton, A.M.; Johnson, R.T. A topoisomerase II-dependent G2 cycle checkpoint in mammalian cells. Nature 1994, 372, 467–470. [Google Scholar] [CrossRef] [PubMed]
- Giménez-Abián, J.F.; Clarke, D.J.; Devlin, J.; Giménez-Abián, M.I.; De la Torre, C.; Johnson, R.T.; Mullinger, A.M.; Downes, C.S. Premitotic chromosome individualization in mammalian cells depends on topoisomerase II activity. Chromosoma 2000, 109, 235–244. [Google Scholar] [CrossRef] [PubMed]
- Clarke, D.J.; Giménez-Abián, J.F. Checkpoints controlling mitosis. BioEssays 2000, 22, 351–363. [Google Scholar] [CrossRef]
- Furniss, K.L.; Tsai, H.-J.; Byl, J.A.W.; Lane, A.B.; Vas, A.C.; Hsu, W.-S.; Osheroff, N.; Clarke, D.J. Direct Monitoring of the Strand Passage Reaction of DNA Topoisomerase II Triggers Checkpoint Activation. PLoS Genet. 2013, 9, e1003832. [Google Scholar] [CrossRef] [PubMed]
- Bower, J.J.; Karaca, G.F.; Zhou, Y.; Simpson, D.A.; Cordeiro-Stone, M.; Kaufmann, W.K. Topoisomerase IIα maintains genomic stability through decatenation G(2) checkpoint signaling. Oncogene 2010, 29, 4787–4799. [Google Scholar] [CrossRef] [PubMed]
- Nagasaka, K.; Hossain, M.J.; Roberti, M.J.; Ellenberg, J.; Hirota, T. Sister chromatid resolution is an intrinsic part of chromosome organization in prophase. Nat. Cell Biol. 2016, 18, 692–699. [Google Scholar] [CrossRef] [PubMed]
- Liang, Z.; Zickler, D.; Prentiss, M.; Chang, F.S.; Witz, G.; Maeshima, K.; Kleckner, N. Chromosomes Progress to Metaphase in Multiple Discrete Steps via Global Compaction/Expansion Cycles. Cell 2015, 161, 1124–1137. [Google Scholar] [CrossRef] [PubMed]
- Koshland, D.; Hartwell, L.H. The structure of sister minichromosome DNA before anaphase in Saccharomyces cerevisiae. Science 1987, 238, 1713–1716. [Google Scholar] [CrossRef] [PubMed]
- Baxter, J.; Sen, N.; Martinez, V.L.; De Carandini, M.E.M.; Schvartzman, J.B.; Diffley, J.F.X.; Aragon, L. Positive Supercoiling of Mitotic DNA Drives Decatenation by Topoisomerase II in Eukaryotes. Science 2011, 331, 1328–1332. [Google Scholar] [CrossRef] [PubMed]
- Sen, N.; Leonard, J.; Torres, R.; Garcia-Luis, J.; Palou-Marin, G.; Aragón, L. Physical Proximity of Sister Chromatids Promotes Top2-Dependent Intertwining. Mol. Cell 2016, 64, 134–147. [Google Scholar] [CrossRef] [PubMed]
- Piskadlo, E.; Tavares, A.; Oliveira, R.A. Metaphase chromosome structure is dynamically maintained by condensin I-directed DNA (de)catenation. Elife 2017, 6, e26120. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Nielsen, C.F.; Yao, Q.; Hickson, I.D. The origins and processing of ultra fine anaphase DNA bridges. Curr. Opin. Genet. Dev. 2014, 26, 1–5. [Google Scholar] [CrossRef] [PubMed]
- Chan, K.; North, P.S.; Hickson, I.D. BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J. 2007, 26, 3397–3409. [Google Scholar] [CrossRef] [PubMed]
- Baumann, C.; Körner, R.; Hofmann, K.; Nigg, E.A. PICH, a Centromere-Associated SNF2 Family ATPase, Is Regulated by Plk1 and Required for the Spindle Checkpoint. Cell 2007, 128, 101–114. [Google Scholar] [CrossRef] [PubMed]
- Chan, K.L.; Palmai-Pallag, T.; Ying, S.; Hickson, I.D. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 2009, 11, 753–760. [Google Scholar] [CrossRef] [PubMed]
- Naim, V.; Rosselli, F. The FANC pathway and BLM collaborate during mitosis to prevent micro-nucleation and chromosome abnormalities. Nat. Cell Biol. 2009, 11, 761–768. [Google Scholar] [CrossRef] [PubMed]
- Ishikawa, F. Portrait of replication stress viewed from telomeres. Cancer Sci. 2013, 104, 790–794. [Google Scholar] [CrossRef] [PubMed]
- Barefield, C.; Karlseder, J. The BLM helicase contributes to telomere maintenance through processing of late-replicating intermediate structures. Nucleic Acids Res. 2012, 40, 7358–7367. [Google Scholar] [CrossRef] [PubMed]
- Debatisse, M.; Le Tallec, B.; Letessier, A.; Dutrillaux, B.; Brison, O. Common fragile sites: Mechanisms of instability revisited. Trends Genet. 2012, 28, 22–32. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.H.-C.; Mayer, B.; Stemmann, O.; Nigg, E.A. Centromere DNA decatenation depends on cohesin removal and is required for mammalian cell division. J. Cell Sci. 2010, 123, 806–813. [Google Scholar] [CrossRef] [PubMed]
- Sumner, A.T. The distribution of topoisomerase II on mammalian chromosomes. Chromosom. Res. 1996, 4, 5–14. [Google Scholar] [CrossRef]
- Díaz-Martínez, L.A.; Giménez-Abián, J.F.; Azuma, Y.; Guacci, V.; Giménez-Martín, G.; Lanier, L.M.; Clarke, D.J. PIASγ Is Required for Faithful Chromosome Segregation in Human Cells. PLoS ONE 2006, 1, e53. [Google Scholar] [CrossRef] [PubMed]
- Nielsen, C.F.; Huttner, D.; Bizard, A.H.; Hirano, S.; Li, T.-N.; Palmai-Pallag, T.; Bjerregaard, V.A.; Liu, Y.; Nigg, E.A.; Wang, L.H.-C.; et al. PICH promotes sister chromatid disjunction and co-operates with topoisomerase II in mitosis. Nat. Commun. 2015, 6, 8962. [Google Scholar] [CrossRef] [PubMed]
- Kschonsak, M.; Haering, C.H. Shaping mitotic chromosomes: From classical concepts to molecular mechanisms. Bioessays 2015, 37, 755–766. [Google Scholar] [CrossRef] [PubMed]
- Piskadlo, E.; Oliveira, R.A. Novel insights into mitotic chromosome condensation. F1000Res. 2016, 5. [Google Scholar] [CrossRef] [PubMed]
- Paulson, J.R.; Laemmli, U.K. The structure of histone-depleted metaphase chromosomes. Cell 1977, 12, 817–828. [Google Scholar] [CrossRef]
- Adolph, K.W.; Cheng, S.M.; Laemmli, U.K. Role of nonhistone proteins in metaphase chromosome structure. Cell 1977, 12, 805–816. [Google Scholar] [CrossRef]
- Earnshaw, W.C. Architecture of metaphase chromosomes and chromosome scaffolds. J. Cell Biol. 1983, 96, 84–93. [Google Scholar] [CrossRef] [PubMed]
- Gasser, S.M.; Laroche, T.; Falquet, J.; Boy de la Tour, E.; Laemmli, U.K. Metaphase chromosome structure. J. Mol. Biol. 1986, 188, 613–629. [Google Scholar] [CrossRef]
- Earnshaw, W.C. Topoisomerase II is a structural component of mitotic chromosome scaffolds. J. Cell Biol. 1985, 100, 1706–1715. [Google Scholar] [CrossRef] [PubMed]
- Belmont, A.S. Mitotic chromosome scaffold structure: New approaches to an old controversy. Proc. Natl. Acad. Sci. USA 2002, 99, 15855–15857. [Google Scholar] [CrossRef] [PubMed]
- Christensen, M.O. Dynamics of human {DNA} topoisomerases {IIalpha} and {IIbeta} in living cells. J. Cell Biol. 2002, 157, 31–44. [Google Scholar] [CrossRef] [PubMed]
- 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. 2006, 16, 333–344. [Google Scholar] [CrossRef] [PubMed]
- Oliveira, R.A.; Heidmann, S.; Sunkel, C.E. Condensin I binds chromatin early in prophase and displays a highly dynamic association with Drosophila mitotic chromosomes. Chromosoma 2007, 116, 259–274. [Google Scholar] [CrossRef] [PubMed]
- Tavormina, P.A.; Côme, M.-G.; Hudson, J.R.; Mo, Y.-Y.; Beck, W.T.; Gorbsky, G.J. Rapid exchange of mammalian topoisomerase IIα at kinetochores and chromosome arms in mitosis. J. Cell Biol. 2002, 158, 23–29. [Google Scholar] [CrossRef] [PubMed]
- Buchenau, P.; Saumweber, H.; Arndt-Jovin, D.J. Consequences of topoisomerase II inhibition in early embryogenesis of Drosophila revealed by in vivo confocal laser scanning microscopy. J. Cell Sci. 1993, 104, 1175–1185. [Google Scholar] [PubMed]
- Andoh, T.; Sato, M.; Narita, T.; Ishida, R. Role of DNA topoisomerase II in chromosome dynamics in mammalian cells. Biotechnol. Appl. Biochem. 1993, 18, 165–174. [Google Scholar] [CrossRef] [PubMed]
- Gorbsky, G.J. Cell cycle progression and chromosome segregation in mammalian cells cultured in the presence of the topoisomerase II inhibitors ICRF-187 [(+)-1,2-bis(3,5-dioxopiperazinyl-1-yl)propane; ADR-529] and ICRF-159 (Razoxane). Cancer Res. 1994, 54, 1042–1048. [Google Scholar] [PubMed]
- Roca, J.; Ishida, R.; Berger, J.M.; Andoh, T.; Wang, J.C. Antitumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp. Proc. Natl. Acad. Sci. USA 1994, 91, 1781–1785. [Google Scholar] [CrossRef] [PubMed]
- Anderson, H.; Roberge, M. Topoisomerase II inhibitors affect entry into mitosis and chromosome condensation in BHK cells. Cell Growth Differ. 1996, 7, 83–90. [Google Scholar] [PubMed]
- Tanabe, K.; Ikegami, Y.; Ishida, R.; Andoh, T. Inhibition of Topoisomerase II by Antitumor Agents Bis(2,6-dioxopiperazine) Derivatives. Cancer Res. 1991, 51, 4903–4908. [Google Scholar] [PubMed]
- Chen, G.L.; Yang, L.; Rowe, T.C.; Halligan, B.D.; Tewey, K.M.; Liu, L.F. Nonintercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J. Biol. Chem. 1984, 259, 13560–13566. [Google Scholar] [PubMed]
- Fasulo, B.; Koyama, C.; Yu, K.R.; Homola, E.M.; Hsieh, T.S.; Campbell, S.D.; Sullivan, W. Chk1 and Wee1 kinases coordinate DNA replication, chromosome condensation, and anaphase entry. Mol. Biol. Cell 2012, 23, 1047–1057. [Google Scholar] [CrossRef] [PubMed]
- 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. 2002, 156, 805–815. [Google Scholar] [CrossRef] [PubMed]
- Vas, A.C.J.; Andrews, C.A.; Kirkland Matesky, K.; Clarke, D.J. In Vivo Analysis of Chromosome Condensation in Saccharomyces cerevisiae. Mol. Biol. Cell 2007, 18, 557–568. [Google Scholar] [CrossRef] [PubMed]
- Petrova, B.; Dehler, S.; Kruitwagen, T.; Hériché, J.-K.; Miura, K.; Haering, C.H. Quantitative analysis of chromosome condensation in fission yeast. Mol. Cell. Biol. 2013, 33, 984–998. [Google Scholar] [CrossRef] [PubMed]
- Ladouceur, A.-M.; Ranjan, R.; Smith, L.; Fadero, T.; Heppert, J.; Goldstein, B.; Maddox, A.S.; Maddox, P.S. CENP-A and topoisomerase-II antagonistically affect chromosome length. J. Cell Biol. 2017. [Google Scholar] [CrossRef] [PubMed]
- Mengoli, V.; Bucciarelli, E.; Lattao, R.; Piergentili, R.; Gatti, M.; Bonaccorsi, S. The Analysis of Mutant Alleles of Different Strength Reveals Multiple Functions of Topoisomerase 2 in Regulation of Drosophila Chromosome Structure. PLoS Genet. 2014, 10, e1004739. [Google Scholar] [CrossRef] [PubMed]
- Somma, M.P.; Ceprani, F.; Bucciarelli, E.; Naim, V.; De Arcangelis, V.; Piergentili, R.; Palena, A.; Ciapponi, L.; Giansanti, M.G.; Pellacani, C.; et al. Identification of Drosophila Mitotic Genes by Combining Co-Expression Analysis and RNA Interference. PLoS Genet. 2008, 4, e1000126. [Google Scholar] [CrossRef] [PubMed]
- Chang, C.-J.; Goulding, S.; Earnshaw, W.C.; Carmena, M. RNAi analysis reveals an unexpected role for topoisomerase II in chromosome arm congression to a metaphase plate. J. Cell Sci. 2003, 116, 4715–4726. [Google Scholar] [CrossRef] [PubMed]
- Samejima, K.; Samejima, I.; Vagnarelli, P.; Ogawa, H.; Vargiu, G.; Kelly, D.A.; de Lima Alves, F.; Kerr, A.; Green, L.C.; Hudson, D.F.; et al. Mitotic chromosomes are compacted laterally by KIF4 and condensin and axially by topoisomerase IIα. J. Cell Biol. 2012, 199, 755–770. [Google Scholar] [CrossRef] [PubMed]
- Johnson, M.; Phua, H.H.; Bennett, S.C.; Spence, J.M.; Farr, C.J. Studying vertebrate topoisomerase 2 function using a conditional knockdown system in DT40 cells. Nucleic Acids Res. 2009, 37, e98. [Google Scholar] [CrossRef] [PubMed]
- Sakaguchi, A.; Kikuchi, A. Functional compatibility between isoform α and β of type II DNA topoisomerase. J. Cell Sci. 2004, 117, 1047–1054. [Google Scholar] [CrossRef] [PubMed]
- Gonzalez, R.E.; Lim, C.-U.; Cole, K.; Bianchini, C.H.; Schools, G.P.; Davis, B.E.; Wada, I.; Roninson, I.B.; Broude, E. V Effects of conditional depletion of topoisomerase II on cell cycle progression in mammalian cells. Cell Cycle 2011, 10, 3505–3514. [Google Scholar] [CrossRef] [PubMed]
- Carpenter, A.J.; Porter, A.C.G. Construction, Characterization, and Complementation of a Conditional-Lethal DNA Topoisomerase IIα Mutant Human Cell Line. Mol. Biol. Cell 2004, 15, 5700–5711. [Google Scholar] [CrossRef] [PubMed]
- Green, L.C.; Kalitsis, P.; Chang, T.M.; Cipetic, M.; Kim, J.H.; Marshall, O.; Turnbull, L.; Whitchurch, C.B.; Vagnarelli, P.; Samejima, K.; et al. Contrasting roles of condensin I and condensin II in mitotic chromosome formation. J. Cell Sci. 2012, 125, 1591–1604. [Google Scholar] [CrossRef] [PubMed]
- Farr, C.J.; Antoniou-Kourounioti, M.; Mimmack, M.L.; Volkov, A.; Porter, A.C.G. The α isoform of topoisomerase II is required for hypercompaction of mitotic chromosomes in human cells. Nucleic Acids Res. 2014, 42, 4414–4426. [Google Scholar] [CrossRef] [PubMed]
- Adachi, Y.; Luke, M.; Laemmli, U.K. Chromosome assembly in vitro: Topoisomerase II is required for condensation. Cell 1991, 64, 137–148. [Google Scholar] [CrossRef]
- Hirano, T.; Mitchison, J.T. Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus egg extracts. J. Cell Biol. 1993, 120, 601–612. [Google Scholar] [CrossRef] [PubMed]
- Shintomi, K.; Takahashi, T.S.; Hirano, T. Reconstitution of mitotic chromatids with a minimum set of purified factors. Nat. Cell Biol. 2015, 17, 1014–1023. [Google Scholar] [CrossRef] [PubMed]
- Deming, P.B.; Cistulli, C.A.; Zhao, H.; Graves, P.R.; Piwnica-Worms, H.; Paules, R.S.; Downes, C.S.; Kaufmann, W.K. The human decatenation checkpoint. Proc. Natl. Acad. Sci. USA 2001, 98, 12044–12049. [Google Scholar] [CrossRef] [PubMed]
- Roberge, M.; Th’ng, J.; Hamaguchi, J.; Bradbury, E.M. The topoisomerase II inhibitor VM-26 induces marked changes in histone H1 kinase activity, histones H1 and H3 phosphorylation, and chromosome condensation in G2 phase and mitotic BHK cells. J. Cell Biol. 1990, 111, 1753–1762. [Google Scholar] [CrossRef] [PubMed]
- Andreassen, P.R.; Lacroix, F.B.; Margolis, R.L. Chromosomes with Two Intact Axial Cores Are Induced by G(2 )Checkpoint Override: Evidence That DNA Decatenation Is not Required to Template the Chromosome Structure. J. Cell Biol. 1997, 136, 29–43. [Google Scholar] [CrossRef] [PubMed]
- Clarke, J.D.; Azuma, Y. Non-Catalytic Roles of the Topoisomerase IIα C-Terminal Domain. Int. J. Mol. Sci. 2017, 18. [Google Scholar] [CrossRef] [PubMed]
- Christensen, M.O.; Larsen, M.K.; Barthelmes, H.U.; Hock, R.; Andersen, C.L.; Kjeldsen, E.; Knudsen, B.R.; Westergaard, O.; Boege, F.; Mielke, C. Dynamics of human DNA topoisomerases IIalpha and IIbeta in living cells. J. Cell Biol. 2002, 157, 31–44. [Google Scholar] [CrossRef] [PubMed]
- Long, B.H. Mechanisms of action of teniposide (VM-26) and comparison with etoposide (VP-16). Semin. Oncol. 1992, 19, 3–19. [Google Scholar] [CrossRef] [PubMed]
- Kawamura, R.; Pope, L.H.; Christensen, M.O.; Sun, M.; Terekhova, K.; Boege, F.; Mielke, C.; Andersen, A.H.; Marko, J.F. Mitotic chromosomes are constrained by topoisomerase II–sensitive DNA entanglements. J. Cell Biol. 2010, 188, 653–663. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.F.; Liu, C.-C.; Alberts, B.M. Type II DNA topoisomerases: Enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell 1980, 19, 697–707. [Google Scholar] [CrossRef]
- Hsieh, T. Knotting of the circular duplex DNA by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem. 1983, 258, 8413–8420. [Google Scholar] [PubMed]
- Roca, J.; Berger, J.M.; Wang, J.C. On the simultaneous binding of eukaryotic DNA topoisomerase II to a pair of double-stranded DNA helices. J. Biol. Chem. 1993, 268, 14250–14255. [Google Scholar] [PubMed]
- Valdés, A.; Segura, J.; Dyson, S.; Martínez-García, B.; Roca, J. DNA knots occur in intracellular chromatin. Nucleic Acids Res. 2017. [Google Scholar] [CrossRef] [PubMed]
- Maresca, T.J.; Salmon, E.D. Welcome to a new kind of tension: Translating kinetochore mechanics into a wait-anaphase signal. J. Cell Sci. 2010, 123, 825–835. [Google Scholar] [CrossRef] [PubMed]
- Khodjakov, A.; Pines, J. Centromere tension: A divisive issue. Nat. Cell Biol. 2010, 12, 919–923. [Google Scholar] [CrossRef] [PubMed]
- Andrews, C.A.; Vas, A.C.; Meier, B.; Giménez-Abián, J.F.; Díaz-Martínez, L.A.; Green, J.; Erickson, S.L.; VanderWaal, K.E.; Hsu, W.-S.; Clarke, D.J. A mitotic topoisomerase II checkpoint in budding yeast is required for genome stability but acts independently of Pds1/securin. Genes Dev. 2006, 20, 1162–1174. [Google Scholar] [CrossRef] [PubMed]
- Skoufias, D.A.; Lacroix, F.B.; Andreassen, P.R.; Wilson, L.; Margolis, R.L. Inhibition of DNA Decatenation, but Not DNA Damage, Arrests Cells at Metaphase. Mol. Cell 2004, 15, 977–990. [Google Scholar] [CrossRef] [PubMed]
- Mikhailov, A.; Shinohara, M.; Rieder, C.L. Topoisomerase II and histone deacetylase inhibitors delay the G2/M transition by triggering the p38 MAPK checkpoint pathway. J. Cell Biol. 2004, 166, 517–526. [Google Scholar] [CrossRef] [PubMed]
- Clarke, D.J.; Vas, A.C.; Andrews, C.A.; Díaz-Martínez, L.A.; Gimenez-Abian, J.F. Topoisomerase II Checkpoints: Universal Mechanisms that Regulate Mitosis. Cell Cycle 2006, 5, 1925–1928. [Google Scholar] [CrossRef] [PubMed]
- Warsi, T.H.; Navarro, M.S.; Bachant, J. DNA Topoisomerase II Is a Determinant of the Tensile Properties of Yeast Centromeric Chromatin and the Tension Checkpoint. Mol. Biol. Cell 2008, 19, 4421–4433. [Google Scholar] [CrossRef] [PubMed]
- Corbett, A.H.; Fernald, A.W.; Osheroff, N. Protein kinase C modulates the catalytic activity of topoisomerase II by enhancing the rate of ATP hydrolysis: Evidence for a common mechanism of regulation by phosphorylation. Biochemistry 1993, 32, 2090–2097. [Google Scholar] [CrossRef] [PubMed]
- Chikamori, K.; Grabowski, D.R.; Kinter, M.; Willard, B.B.; Yadav, S.; Aebersold, R.H.; Bukowski, R.M.; Hickson, I.D.; Andersen, A.H.; Ganapathi, R.; et al. Phosphorylation of Serine 1106 in the Catalytic Domain of Topoisomerase IIα Regulates Enzymatic Activity and Drug Sensitivity. J. Biol. Chem. 2003, 278, 12696–12702. [Google Scholar] [CrossRef] [PubMed]
- Ryu, H.; Furuta, M.; Kirkpatrick, D.; Gygi, S.P.; Azuma, Y. PIASy-dependent SUMOylation regulates DNA topoisomerase IIα activity. J. Cell Biol. 2010, 191, 783–794. [Google Scholar] [CrossRef] [PubMed]
- Azuma, Y.; Arnaoutov, A.; Anan, T.; Dasso, M. PIASy mediates SUMO-2 conjugation of Topoisomerase-II on mitotic chromosomes. EMBO J. 2005, 24, 2172–2182. [Google Scholar] [CrossRef] [PubMed]
- Agostinho, M.; Santos, V.; Ferreira, F.; Costa, R.; Cardoso, J.; Pinheiro, I.; Rino, J.; Jaffray, E.; Hay, R.T.; Ferreira, J. Conjugation of Human Topoisomerase 2α with Small Ubiquitin-like Modifiers 2/3 in Response to Topoisomerase Inhibitors: Cell Cycle Stage and Chromosome Domain Specificity. Cancer Res. 2008, 68, 2409–2418. [Google Scholar] [CrossRef] [PubMed]
- Dawlaty, M.M.; Malureanu, L.; Jeganathan, K.B.; Kao, E.; Sustmann, C.; Tahk, S.; Shuai, K.; Grosschedl, R.; van Deursen, J.M. Resolution of Sister Centromeres Requires RanBP2-Mediated SUMOylation of Topoisomerase IIα. Cell 2008, 133, 103–115. [Google Scholar] [CrossRef] [PubMed]
- Takahashi, Y.; Yong-Gonzalez, V.; Kikuchi, Y.; Strunnikov, A. SIZ1/SIZ2 Control of Chromosome Transmission Fidelity Is Mediated by the Sumoylation of Topoisomerase II. Genetics 2006, 172, 783–794. [Google Scholar] [CrossRef] [PubMed]
- Liu, Z.; Deibler, R.W.; Chan, H.S.; Zechiedrich, L. The why and how of DNA unlinking. Nucleic Acids Res. 2009, 37, 661–671. [Google Scholar] [CrossRef] [PubMed]
- Rybenkov, V.V.; Ullsperger, C.; Vologodskii, A.V.; Cozzarelli, N.R. Simplification of DNA Topology Below Equilibrium Values by Type II Topoisomerases. Science 1997, 277, 690–693. [Google Scholar] [CrossRef] [PubMed]
- Hirano, T. At the heart of the chromosome: SMC proteins in action. Nat. Rev. Mol. Cell Biol. 2006, 7, 311–322. [Google Scholar] [CrossRef] [PubMed]
- Uhlmann, F. SMC complexes: From DNA to chromosomes. Nat. Rev. Mol. Cell Biol. 2016, 17, 399–412. [Google Scholar] [CrossRef] [PubMed]
- Rybenkov, V.V.; Herrera, V.; Petrushenko, Z.M.; Zhao, H. MukBEF, a chromosomal organizer. J. Mol. Microbiol. Biotechnol. 2014, 24, 371–383. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Stewart, N.K.; Berger, A.J.; Vos, S.; Schoeffler, A.J.; Berger, J.M.; Chait, B.T.; Oakley, M.G. Escherichia coli condensin MukB stimulates topoisomerase IV activity by a direct physical interaction. Proc. Natl. Acad. Sci. USA 2010, 107, 18832–18837. [Google Scholar] [CrossRef] [PubMed]
- Hayama, R.; Marians, K.J. Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli. Proc. Natl. Acad. Sci. USA 2010, 107, 18826–18831. [Google Scholar] [CrossRef] [PubMed]
- Hayama, R.; Bahng, S.; Karasu, M.E.; Marians, K.J. The MukB-ParC Interaction Affects the Intramolecular, Not Intermolecular, Activities of Topoisomerase IV. J. Biol. Chem. 2013, 288, 7653–7661. [Google Scholar] [CrossRef] [PubMed]
- Nicolas, E.; Upton, A.L.; Uphoff, S.; Henry, O.; Badrinarayanan, A.; Sherratt, D. The SMC Complex MukBEF Recruits Topoisomerase IV to the Origin of Replication Region in Live Escherichia coli. mBio 2014, 5. [Google Scholar] [CrossRef] [PubMed]
- Zawadzki, P.; Stracy, M.; Ginda, K.; Zawadzka, K.; Lesterlin, C.; Kapanidis, A.N.; Sherratt, D.J. The Localization and Action of Topoisomerase IV in Escherichia coli Chromosome Segregation Is Coordinated by the SMC Complex, MukBEF. Cell Rep. 2015, 13, 2587–2596. [Google Scholar] [CrossRef] [PubMed]
- Kumar, R.; Nurse, P.; Bahng, S.; Lee, C.M.; Marians, K.J. The MukB–topoisomerase IV interaction is required for proper chromosome compaction. J. Biol. Chem. 2017, 292, 16921–16932. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Tang, O.W.; Riley, E.P.; Rudner, D.Z. The SMC Condensin Complex Is Required for Origin Segregation in Bacillus subtilis. Curr. Biol. 2014, 24, 287–292. [Google Scholar] [CrossRef] [PubMed]
- Tadesse, S.; Mascarenhas, J.; Kösters, B.; Hasilik, A.; Graumann, P.L. Genetic interaction of the SMC complex with topoisomerase IV in Bacillus subtilis. Microbiology 2005, 151, 3729–3737. [Google Scholar] [CrossRef] [PubMed]
- Jeppsson, K.; Kanno, T.; Shirahige, K.; Sjogren, C. The maintenance of chromosome structure: Positioning and functioning of SMC complexes. Nat. Rev. Mol. Cell Biol. 2014, 15, 601–614. [Google Scholar] [CrossRef] [PubMed]
- Kanno, T.; Berta, D.G.; Sjögren, C. The Smc5/6 Complex Is an ATP-Dependent Intermolecular DNA Linker. Cell Rep. 2015, 12, 1471–1482. [Google Scholar] [CrossRef] [PubMed]
- Jeppsson, K.; Carlborg, K.K.; Nakato, R.; Berta, D.G.; Lilienthal, I.; Kanno, T.; Lindqvist, A.; Brink, M.C.; Dantuma, N.P.; Katou, Y.; et al. The Chromosomal Association of the Smc5/6 Complex Depends on Cohesion and Predicts the Level of Sister Chromatid Entanglement. PLoS Genet. 2014, 10, e1004680. [Google Scholar] [CrossRef] [PubMed]
- Verver, D.E.; Zheng, Y.; Speijer, D.; Hoebe, R.; Dekker, H.L.; Repping, S.; Stap, J.; Hamer, G. Non-SMC Element 2 (NSMCE2) of the SMC5/6 Complex Helps to Resolve Topological Stress. Int. J. Mol. Sci. 2016, 17, 1782. [Google Scholar] [CrossRef] [PubMed]
- Gallego-Paez, L.M.; Tanaka, H.; Bando, M.; Takahashi, M.; Nozaki, N.; Nakato, R.; Shirahige, K.; Hirota, T. Smc5/6-mediated regulation of replication progression contributes to chromosome assembly during mitosis in human cells. Mol. Biol. Cell 2014, 25, 302–317. [Google Scholar] [CrossRef] [PubMed]
- Pryzhkova, M.V.; Jordan, P.W. Conditional mutation of Smc5 in mouse embryonic stem cells perturbs condensin localization and mitotic progression. J. Cell Sci. 2016, 129, 1619–1634. [Google Scholar] [CrossRef] [PubMed]
- Gómez, R.; Jordan, P.W.; Viera, A.; Alsheimer, M.; Fukuda, T.; Jessberger, R.; Llano, E.; Pendás, A.M.; Handel, M.A.; Suja, J.A. Dynamic localization of SMC5/6 complex proteins during mammalian meiosis and mitosis suggests functions in distinct chromosome processes. J. Cell Sci. 2013, 126, 4239–4252. [Google Scholar] [CrossRef] [PubMed]
- Mirkovic, M.; Oliveira, R.A. Centromeric Cohesin: Molecular Glue and Much More. In Centromeres and Kinetochores; Black, B.E., Ed.; Springer International Publishing: Cham, Switzerland, 2017; pp. 485–513. ISBN 978-3-319-58592-5. [Google Scholar]
- Litwin, I.; Wysocki, R. New insights into cohesin loading. Curr. Genet. 2017. [Google Scholar] [CrossRef] [PubMed]
- Haarhuis, J.H.I.; Elbatsh, A.M.O.; Rowland, B.D. Cohesin and Its Regulation: On the Logic of X-Shaped Chromosomes. Dev. Cell 2014, 31, 7–18. [Google Scholar] [CrossRef] [PubMed]
- Farcas, A.-M.; Uluocak, P.; Helmhart, W.; Nasmyth, K. Cohesin’s Concatenation of Sister DNAs Maintains Their Intertwining. Mol. Cell 2011, 44, 97–107. [Google Scholar] [CrossRef] [PubMed]
- Gómez, R.; Viera, A.; Berenguer, I.; Llano, E.; Pendás, A.M.; Barbero, J.L.; Kikuchi, A.; Suja, J.A. Cohesin removal precedes topoisomerase IIα-dependent decatenation at centromeres in male mammalian meiosis II. Chromosoma 2014, 123, 129–146. [Google Scholar] [CrossRef] [PubMed]
- Tedeschi, A.; Wutz, G.; Huet, S.; Jaritz, M.; Wuensche, A.; Schirghuber, E.; Davidson, I.F.; Tang, W.; Cisneros, D.A.; Bhaskara, V.; et al. Wapl is an essential regulator of chromatin structure and chromosome segregation. Nature 2013, 501, 564–568. [Google Scholar] [CrossRef] [PubMed]
- Haarhuis, J.H.I.; Elbatsh, A.M.O.; van den Broek, B.; Camps, D.; Erkan, H.; Jalink, K.; Medema, R.H.; Rowland, B.D. WAPL-Mediated Removal of Cohesin Protects against Segregation Errors and Aneuploidy. Curr. Biol. 2013, 23, 2071–2077. [Google Scholar] [CrossRef] [PubMed]
- Oliveira, R.A.; Kotadia, S.; Tavares, A.; Mirkovic, M.; Bowlin, K.; Eichinger, C.S.; Nasmyth, K.; Sullivan, W. Centromere-Independent Accumulation of Cohesin at Ectopic Heterochromatin Sites Induces Chromosome Stretching during Anaphase. PLoS Biol. 2014, 12, e1001962. [Google Scholar] [CrossRef] [PubMed]
- Murray, A.W.; Szostak, J.W. Chromosome Segregation in Mitosis and Meiosis. Annu. Rev. Cell Biol. 1985, 1, 289–315. [Google Scholar] [CrossRef] [PubMed]
- Uhlmann, F.; Wernic, D.; Poupart, M.-A.; Koonin, E.V.; Nasmyth, K. Cleavage of Cohesin by the CD Clan Protease Separin Triggers Anaphase in Yeast. Cell 2000, 103, 375–386. [Google Scholar] [CrossRef]
- Díaz-Martínez, L.A.; Giménez-Abián, J.F.; Clarke, D.J. Chromosome cohesion–Rings, knots, orcs and fellowship. J. Cell Sci. 2008, 121, 2107–2114. [Google Scholar] [CrossRef] [PubMed]
- Toyoda, Y.; Yanagida, M. Coordinated Requirements of Human Topo II and Cohesin for Metaphase Centromere Alignment under Mad2-dependent Spindle Checkpoint Surveillance. Mol. Biol. Cell 2006, 17, 2287–2302. [Google Scholar] [CrossRef] [PubMed]
- Vagnarelli, P.; Morrison, C.; Dodson, H.; Sonoda, E.; Takeda, S.; Earnshaw, W.C. Analysis of Scc1-deficient cells defines a key metaphase role of vertebrate cohesin in linking sister kinetochores. EMBO Rep. 2004, 5, 167–171. [Google Scholar] [CrossRef] [PubMed]
- Dewar, H.; Tanaka, K.; Nasmyth, K.; Tanaka, T.U. Tension between two kinetochores suffices for their bi-orientation on the mitotic spindle. Nature 2004, 428, 93–97. [Google Scholar] [CrossRef] [PubMed]
- Hirano, T. Condensin-Based Chromosome Organization from Bacteria to Vertebrates. Cell 2016, 164, 847–857. [Google Scholar] [CrossRef] [PubMed]
- Hirano, T.; Mitchison, T.J. A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 1994, 79, 449–458. [Google Scholar] [CrossRef]
- Hirano, T.; Kobayashi, R.; Hirano, M. Condensins, Chromosome Condensation Protein Complexes Containing XCAP-C, XCAP-E and a Xenopus Homolog of the Drosophila Barren Protein. Cell 1997, 89, 511–521. [Google Scholar] [CrossRef]
- Oliveira, R.A.; Coelho, P.A.; Sunkel, C.E. The Condensin I Subunit Barren/CAP-H Is Essential for the Structural Integrity of Centromeric Heterochromatin during Mitosis. Mol. Cell. Biol. 2005, 25, 8971–8984. [Google Scholar] [CrossRef] [PubMed]
- Ribeiro, S.A.; Gatlin, J.C.; Dong, Y.; Joglekar, A.; Cameron, L.; Hudson, D.F.; Farr, C.J.; Mcewen, B.F.; Salmon, E.D.; Earnshaw, W.C.; et al. Condensin Regulates the Stiffness of Vertebrate Centromeres. Mol. Biol. Cell 2009, 20, 2371–2380. [Google Scholar] [CrossRef] [PubMed]
- Hudson, D.F.; Vagnarelli, P.; Gassmann, R.; Earnshaw, W.C. Condensin Is Required for Nonhistone Protein Assembly and Structural Integrity of Vertebrate Mitotic Chromosomes. Dev. Cell 2003, 5, 323–336. [Google Scholar] [CrossRef]
- Bhat, M.A.; Philp, A.V.; Glover, D.M.; Bellen, H.J. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with Topoisomerase II. Cell 1996, 87, 1103–1114. [Google Scholar] [CrossRef]
- Steffensen, S.; Coelho, P.A.; Cobbe, N.; Vass, S.; Costa, M.; Hassan, B.; Prokopenko, S.N.; Bellen, H.; Heck, M.M.S.; Sunkel, C.E. A role for Drosophila SMC4 in the resolution of sister chromatids in mitosis. Curr. Biol. 2001, 11, 295–307. [Google Scholar] [CrossRef]
- Hagstrom, K.A. C. elegans condensin promotes mitotic chromosome architecture centromere organization, and sister chromatid segregation during mitosis and meiosis. Genes Dev. 2002, 16, 729–742. [Google Scholar] [CrossRef] [PubMed]
- Coelho, P.A.; Queiroz-Machado, J.; Sunkel, C.E. Condensin-dependent localisation of topoisomerase II to an axial chromosomal structure is required for sister chromatid resolution during mitosis. J. Cell Sci. 2003, 116, 4763–4776. [Google Scholar] [CrossRef] [PubMed]
- Cuvier, O.; Hirano, T. A role of topoisomerase II in linking DNA replication to chromosome condensation. J. Cell Biol. 2003, 160, 645–655. [Google Scholar] [CrossRef] [PubMed]
- Baxter, J.; Aragón, L. A model for chromosome condensation based on the interplay between condensin and topoisomerase II. Trends Genet. 2012, 28, 110–117. [Google Scholar] [CrossRef] [PubMed]
- Kimura, K.; Hirano, T. ATP-Dependent Positive Supercoiling of DNA by 13S Condensin: A Biochemical Implication for Chromosome Condensation. Cell 1997, 90, 625–634. [Google Scholar] [CrossRef]
- Kimura, K.; Hirano, T. Dual roles of the 11S regulatory subcomplex in condensin functions. Proc. Natl. Acad. Sci. USA 2000, 97, 11972–11977. [Google Scholar] [CrossRef] [PubMed]
- Kimura, K.; Cuvier, O.; Hirano, T. Chromosome Condensation by a Human Condensin Complex in Xenopus Egg Extracts. J. Biol. Chem. 2001, 276, 5417–5420. [Google Scholar] [CrossRef] [PubMed]
- Eeftens, J.M.; Bisht, S.; Kschonsak, M.; Haering, C.H.; Dekker, C. Real-time detection of condensin-driven DNA compaction reveals a multistep binding mechanism. EMBO J. 2017, 36, 3269–3405. [Google Scholar] [CrossRef] [PubMed]
- Nasmyth, K. Disseminating the Genome: Joining, Resolving, and Separating Sister Chromatids During Mitosis and Meiosis. Annu. Rev. Genet. 2001, 35, 673–745. [Google Scholar] [CrossRef] [PubMed]
- Alipour, E.; Marko, J.F. Self-organization of domain structures by DNA-loop-extruding enzymes. Nucleic Acids Res. 2012, 40, 11202–11212. [Google Scholar] [CrossRef] [PubMed]
- Goloborodko, A.; Imakaev, M.V.; Marko, J.F.; Mirny, L. Compaction and segregation of sister chromatids via active loop extrusion. Elife 2016, 5, e14864. [Google Scholar] [CrossRef] [PubMed]
- Terakawa, T.; Bisht, S.; Eeftens, J.M.; Dekker, C.; Haering, C.H.; Greene, E.C. The condensin complex is a mechanochemical motor that translocates along DNA. Science 2017. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Brandão, H.B.; Le, T.B.K.; Laub, M.T.; Rudner, D.Z. Bacillus subtilis SMC complexes juxtapose chromosome arms as they travel from origin to terminus. Science 2017, 355, 524–527. [Google Scholar] [CrossRef] [PubMed]
- Diebold-Durand, M.-L.; Lee, H.; Ruiz Avila, L.B.; Noh, H.; Shin, H.-C.; Im, H.; Bock, F.P.; Bürmann, F.; Durand, A.; Basfeld, A.; et al. Structure of Full-Length SMC and Rearrangements Required for Chromosome Organization. Mol. Cell 2017, 67, 334.e5–347.e5. [Google Scholar] [CrossRef] [PubMed]
- Shintomi, K.; Hirano, T. The relative ratio of condensin I to II determines chromosome shapes. Genes Dev. 2011, 25, 1464–1469. [Google Scholar] [CrossRef] [PubMed]
- Elbatsh, A.M.O.; Raaijmakers, J.A.; van der Weide, R.H.; uit de Bos, J.; Teunissen, H.; Bravo, S.; Medema, R.H.; de Wit, E.; Haering, C.H.; Rowland, B.D. Condensin’s ATPase Machinery Drives and Dampens Mitotic Chromosome Condensation. bioRxiv 2017. [Google Scholar] [CrossRef]
- Houlard, M.; Godwin, J.; Metson, J.; Lee, J.; Hirano, T.; Nasmyth, K. Condensin confers the longitudinal rigidity of chromosomes. Nat. Cell Biol. 2015, 17, 771–781. [Google Scholar] [CrossRef] [PubMed]
- Mazia, D. Mitosis and the physiology of cell division. Cell. Biochem. Physiol. Morphol. 1961, 77–412. [Google Scholar] [CrossRef]
© 2017 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Piskadlo, E.; Oliveira, R.A. A Topology-Centric View on Mitotic Chromosome Architecture. Int. J. Mol. Sci. 2017, 18, 2751. https://doi.org/10.3390/ijms18122751
Piskadlo E, Oliveira RA. A Topology-Centric View on Mitotic Chromosome Architecture. International Journal of Molecular Sciences. 2017; 18(12):2751. https://doi.org/10.3390/ijms18122751
Chicago/Turabian StylePiskadlo, Ewa, and Raquel A. Oliveira. 2017. "A Topology-Centric View on Mitotic Chromosome Architecture" International Journal of Molecular Sciences 18, no. 12: 2751. https://doi.org/10.3390/ijms18122751
APA StylePiskadlo, E., & Oliveira, R. A. (2017). A Topology-Centric View on Mitotic Chromosome Architecture. International Journal of Molecular Sciences, 18(12), 2751. https://doi.org/10.3390/ijms18122751