5oqn Citations

Structural Basis for a Safety-Belt Mechanism That Anchors Condensin to Chromosomes.

OpenAccess logo Cell 171 588-600.e24 (2017)
Related entries: 5oqo, 5oqp, 5oqq, 5oqr

Cited: 74 times
EuropePMC logo PMID: 28988770

Abstract

Condensin protein complexes coordinate the formation of mitotic chromosomes and thereby ensure the successful segregation of replicated genomes. Insights into how condensin complexes bind to chromosomes and alter their topology are essential for understanding the molecular principles behind the large-scale chromatin rearrangements that take place during cell divisions. Here, we identify a direct DNA-binding site in the eukaryotic condensin complex, which is formed by its Ycg1Cnd3 HEAT-repeat and Brn1Cnd2 kleisin subunits. DNA co-crystal structures reveal a conserved, positively charged groove that accommodates the DNA double helix. A peptide loop of the kleisin subunit encircles the bound DNA and, like a safety belt, prevents its dissociation. Firm closure of the kleisin loop around DNA is essential for the association of condensin complexes with chromosomes and their DNA-stimulated ATPase activity. Our data suggest a sophisticated molecular basis for anchoring condensin complexes to chromosomes that enables the formation of large-sized chromatin loops.

Articles - 5oqn mentioned but not cited (3)

  1. Structural Basis for a Safety-Belt Mechanism That Anchors Condensin to Chromosomes. Kschonsak M, Merkel F, Bisht S, Metz J, Rybin V, Hassler M, Haering CH. Cell 171 588-600.e24 (2017)
  2. Structural basis of HEAT-kleisin interactions in the human condensin I subcomplex. Hara K, Kinoshita K, Migita T, Murakami K, Shimizu K, Takeuchi K, Hirano T, Hashimoto H. EMBO Rep 20 e47183 (2019)
  3. Modeling of DNA binding to the condensin hinge domain using molecular dynamics simulations guided by atomic force microscopy. Koide H, Kodera N, Bisht S, Takada S, Terakawa T. PLoS Comput Biol 17 e1009265 (2021)


Reviews citing this publication (15)

  1. Genome folding through loop extrusion by SMC complexes. Davidson IF, Peters JM. Nat Rev Mol Cell Biol 22 445-464 (2021)
  2. Towards a Unified Model of SMC Complex Function. Hassler M, Shaltiel IA, Haering CH. Curr Biol 28 R1266-R1281 (2018)
  3. Condensins and cohesins - one of these things is not like the other! Skibbens RV. J Cell Sci 132 jcs220491 (2019)
  4. SMC5/6: Multifunctional Player in Replication. Palecek JJ. Genes (Basel) 10 E7 (2018)
  5. Molecular Genetics of Microcephaly Primary Hereditary: An Overview. Siskos N, Stylianopoulou E, Skavdis G, Grigoriou ME. Brain Sci 11 581 (2021)
  6. The regulation of chromosome segregation via centromere loops. Lawrimore J, Bloom K. Crit Rev Biochem Mol Biol 54 352-370 (2019)
  7. Shaping of the 3D genome by the ATPase machine cohesin. Kim Y, Yu H. Exp Mol Med 52 1891-1897 (2020)
  8. Genome-in-a-Box: Building a Chromosome from the Bottom Up. Birnie A, Dekker C. ACS Nano 15 111-124 (2021)
  9. Condensin complexes: understanding loop extrusion one conformational change at a time. Cutts EE, Vannini A. Biochem Soc Trans 48 2089-2100 (2020)
  10. Structural insights into DNA loop extrusion by SMC protein complexes. Datta S, Lecomte L, Haering CH. Curr Opin Struct Biol 65 102-109 (2020)
  11. Rec8 Cohesin: A Structural Platform for Shaping the Meiotic Chromosomes. Sakuno T, Hiraoka Y. Genes (Basel) 13 200 (2022)
  12. Structural Biology of the HEAT-Like Repeat Family of DNA Glycosylases. Shi R, Shen XX, Rokas A, Eichman BF. Bioessays 40 e1800133 (2018)
  13. Are SMC Complexes Loop Extruding Factors? Linking Theory With Fact. Baxter J, Oliver AW, Schalbetter SA. Bioessays 41 e1800182 (2019)
  14. A mini-review of the role of condensin in human nervous system diseases. Pang D, Yu S, Yang X. Front Mol Neurosci 15 889796 (2022)
  15. Structural biology of SMC complexes across the tree of life. Bürmann F, Löwe J. Curr Opin Struct Biol 80 102598 (2023)

Articles citing this publication (56)

  1. Real-time imaging of DNA loop extrusion by condensin. Ganji M, Shaltiel IA, Bisht S, Kim E, Kalichava A, Haering CH, Dekker C. Science 360 102-105 (2018)
  2. The structural basis for cohesin-CTCF-anchored loops. Li Y, Haarhuis JHI, Sedeño Cacciatore Á, Oldenkamp R, van Ruiten MS, Willems L, Teunissen H, Muir KW, de Wit E, Rowland BD, Panne D. Nature 578 472-476 (2020)
  3. Emerging Evidence of Chromosome Folding by Loop Extrusion. Fudenberg G, Abdennur N, Imakaev M, Goloborodko A, Mirny LA. Cold Spring Harb Symp Quant Biol 82 45-55 (2017)
  4. Scc2 Is a Potent Activator of Cohesin's ATPase that Promotes Loading by Binding Scc1 without Pds5. Petela NJ, Gligoris TG, Metson J, Lee BG, Voulgaris M, Hu B, Kikuchi S, Chapard C, Chen W, Rajendra E, Srinivisan M, Yu H, Löwe J, Nasmyth KA. Mol Cell 70 1134-1148.e7 (2018)
  5. A quantitative map of human Condensins provides new insights into mitotic chromosome architecture. Walther N, Hossain MJ, Politi AZ, Koch B, Kueblbeck M, Ødegård-Fougner Ø, Lampe M, Ellenberg J. J Cell Biol 217 2309-2328 (2018)
  6. The Cohesin Ring Uses Its Hinge to Organize DNA Using Non-topological as well as Topological Mechanisms. Srinivasan M, Scheinost JC, Petela NJ, Gligoris TG, Wissler M, Ogushi S, Collier JE, Voulgaris M, Kurze A, Chan KL, Hu B, Costanzo V, Nasmyth KA. Cell 173 1508-1519.e18 (2018)
  7. Bridging-induced phase separation induced by cohesin SMC protein complexes. Ryu JK, Bouchoux C, Liu HW, Kim E, Minamino M, de Groot R, Katan AJ, Bonato A, Marenduzzo D, Michieletto D, Uhlmann F, Dekker C. Sci Adv 7 eabe5905 (2021)
  8. Human Condensin I and II Drive Extensive ATP-Dependent Compaction of Nucleosome-Bound DNA. Kong M, Cutts EE, Pan D, Beuron F, Kaliyappan T, Xue C, Morris EP, Musacchio A, Vannini A, Greene EC. Mol Cell 79 99-114.e9 (2020)
  9. Chromosome organization by one-sided and two-sided loop extrusion. Banigan EJ, van den Berg AA, Brandão HB, Marko JF, Mirny LA. Elife 9 e53558 (2020)
  10. Cryo-EM structures of holo condensin reveal a subunit flip-flop mechanism. Lee BG, Merkel F, Allegretti M, Hassler M, Cawood C, Lecomte L, O'Reilly FJ, Sinn LR, Gutierrez-Escribano P, Kschonsak M, Bravo S, Nakane T, Rappsilber J, Aragon L, Beck M, Löwe J, Haering CH. Nat Struct Mol Biol 27 743-751 (2020)
  11. DNA-segment-capture model for loop extrusion by structural maintenance of chromosome (SMC) protein complexes. Marko JF, De Los Rios P, Barducci A, Gruber S. Nucleic Acids Res 47 6956-6972 (2019)
  12. Real-time detection of condensin-driven DNA compaction reveals a multistep binding mechanism. Eeftens JM, Bisht S, Kerssemakers J, Kschonsak M, Haering CH, Dekker C. EMBO J 36 3448-3457 (2017)
  13. In Vivo Evidence for ATPase-Dependent DNA Translocation by the Bacillus subtilis SMC Condensin Complex. Wang X, Hughes AC, Brandão HB, Walker B, Lierz C, Cochran JC, Oakley MG, Kruse AC, Rudner DZ. Mol Cell 71 841-847.e5 (2018)
  14. Transport of DNA within cohesin involves clamping on top of engaged heads by Scc2 and entrapment within the ring by Scc3. Collier JE, Lee BG, Roig MB, Yatskevich S, Petela NJ, Metson J, Voulgaris M, Gonzalez Llamazares A, Löwe J, Nasmyth KA. Elife 9 e59560 (2020)
  15. Structural Basis of an Asymmetric Condensin ATPase Cycle. Hassler M, Shaltiel IA, Kschonsak M, Simon B, Merkel F, Thärichen L, Bailey HJ, Macošek J, Bravo S, Metz J, Hennig J, Haering CH. Mol Cell 74 1175-1188.e9 (2019)
  16. Structural basis for Scc3-dependent cohesin recruitment to chromatin. Li Y, Muir KW, Bowler MW, Metz J, Haering CH, Panne D. Elife 7 e38356 (2018)
  17. The condensin holocomplex cycles dynamically between open and collapsed states. Ryu JK, Katan AJ, van der Sluis EO, Wisse T, de Groot R, Haering CH, Dekker C. Nat Struct Mol Biol 27 1134-1141 (2020)
  18. Sister DNA Entrapment between Juxtaposed Smc Heads and Kleisin of the Cohesin Complex. Chapard C, Jones R, van Oepen T, Scheinost JC, Nasmyth K. Mol Cell 75 224-237.e5 (2019)
  19. OnTAD: hierarchical domain structure reveals the divergence of activity among TADs and boundaries. An L, Yang T, Yang J, Nuebler J, Xiang G, Hardison RC, Li Q, Zhang Y. Genome Biol 20 282 (2019)
  20. Transient DNA Occupancy of the SMC Interarm Space in Prokaryotic Condensin. Vazquez Nunez R, Ruiz Avila LB, Gruber S. Mol Cell 75 209-223.e6 (2019)
  21. SUMO is a pervasive regulator of meiosis. Bhagwat NR, Owens SN, Ito M, Boinapalli JV, Poa P, Ditzel A, Kopparapu S, Mahalawat M, Davies OR, Collins SR, Johnson JR, Krogan NJ, Hunter N. Elife 10 e57720 (2021)
  22. Distinct Roles for Condensin's Two ATPase Sites in Chromosome Condensation. Elbatsh AMO, Kim E, Eeftens JM, Raaijmakers JA, van der Weide RH, García-Nieto A, Bravo S, Ganji M, Uit de Bos J, Teunissen H, Medema RH, de Wit E, Haering CH, Dekker C, Rowland BD. Mol Cell 76 724-737.e5 (2019)
  23. Nse5/6 inhibits the Smc5/6 ATPase and modulates DNA substrate binding. Taschner M, Basquin J, Steigenberger B, Schäfer IB, Soh YM, Basquin C, Lorentzen E, Räschle M, Scheltema RA, Gruber S. EMBO J 40 e107807 (2021)
  24. Cohesin Causes Replicative DNA Damage by Trapping DNA Topological Stress. Minchell NE, Keszthelyi A, Baxter J. Mol Cell 78 739-751.e8 (2020)
  25. Plasmodium Condensin Core Subunits SMC2/SMC4 Mediate Atypical Mitosis and Are Essential for Parasite Proliferation and Transmission. Pandey R, Abel S, Boucher M, Wall RJ, Zeeshan M, Rea E, Freville A, Lu XM, Brady D, Daniel E, Stanway RR, Wheatley S, Batugedara G, Hollin T, Bottrill AR, Gupta D, Holder AA, Le Roch KG, Tewari R. Cell Rep 30 1883-1897.e6 (2020)
  26. Condensin controls cellular RNA levels through the accurate segregation of chromosomes instead of directly regulating transcription. Hocquet C, Robellet X, Modolo L, Sun XM, Burny C, Cuylen-Haering S, Toselli E, Clauder-Münster S, Steinmetz L, Haering CH, Marguerat S, Bernard P. Elife 7 e38517 (2018)
  27. Arabidopsis NSE4 Proteins Act in Somatic Nuclei and Meiosis to Ensure Plant Viability and Fertility. Zelkowski M, Zelkowska K, Conrad U, Hesse S, Lermontova I, Marzec M, Meister A, Houben A, Schubert V. Front Plant Sci 10 774 (2019)
  28. Condensin extrudes DNA loops in steps up to hundreds of base pairs that are generated by ATP binding events. Ryu JK, Rah SH, Janissen R, Kerssemakers JWJ, Bonato A, Michieletto D, Dekker C. Nucleic Acids Res 50 820-832 (2022)
  29. Intermediate step of cohesin's ATPase cycle allows cohesin to entrap DNA. Çamdere GÖ, Carlborg KK, Koshland D. Proc Natl Acad Sci U S A 115 9732-9737 (2018)
  30. DNA tension-modulated translocation and loop extrusion by SMC complexes revealed by molecular dynamics simulations. Nomidis SK, Carlon E, Gruber S, Marko JF. Nucleic Acids Res 50 4974-4987 (2022)
  31. Clamping of DNA shuts the condensin neck gate. Lee BG, Rhodes J, Löwe J. Proc Natl Acad Sci U S A 119 e2120006119 (2022)
  32. Cancer-associated mutations in the condensin II subunit CAPH2 cause genomic instability through telomere dysfunction and anaphase chromosome bridges. Weyburne E, Bosco G. J Cell Physiol 236 3579-3598 (2021)
  33. Non-SMC condensin I complex subunit H mediates mature chromosome condensation and DNA damage in pancreatic cancer cells. Kim JH, Youn Y, Kim KT, Jang G, Hwang JH. Sci Rep 9 17889 (2019)
  34. Structure Basis for Shaping the Nse4 Protein by the Nse1 and Nse3 Dimer within the Smc5/6 Complex. Jo A, Li S, Shin JW, Zhao X, Cho Y. J Mol Biol 433 166910 (2021)
  35. Suppressor screening reveals common kleisin-hinge interaction in condensin and cohesin, but different modes of regulation. Xu X, Yanagida M. Proc Natl Acad Sci U S A 116 10889-10898 (2019)
  36. Condensin I subunit Cap-G is essential for proper gene expression during the maturation of post-mitotic neurons. Hassan A, Araguas Rodriguez P, Heidmann SK, Walmsley EL, Aughey GN, Southall TD. Elife 9 e55159 (2020)
  37. A loop extrusion-independent mechanism contributes to condensin I-mediated chromosome shaping. Kinoshita K, Tsubota Y, Tane S, Aizawa Y, Sakata R, Takeuchi K, Shintomi K, Nishiyama T, Hirano T. J Cell Biol 221 e202109016 (2022)
  38. Braiding topology and the energy landscape of chromosome organization proteins. Krepel D, Davtyan A, Schafer NP, Wolynes PG, Onuchic JN. Proc Natl Acad Sci U S A 117 1468-1477 (2020)
  39. The interplay between asymmetric and symmetric DNA loop extrusion. Banigan EJ, Mirny LA. Elife 9 e63528 (2020)
  40. Binding of an X-Specific Condensin Correlates with a Reduction in Active Histone Modifications at Gene Regulatory Elements. Street LA, Morao AK, Winterkorn LH, Jiao CY, Albritton SE, Sadic M, Kramer M, Ercan S. Genetics 212 729-742 (2019)
  41. 14-3-3 Protein Bmh1 triggers short-range compaction of mitotic chromosomes by recruiting sirtuin deacetylase Hst2. Jain N, Janning P, Neumann H. J Biol Chem 296 100078 (2021)
  42. A Role for Caenorhabditis elegans COMPASS in Germline Chromatin Organization. Herbette M, Robert V, Bailly A, Gely L, Feil R, Llères D, Palladino F. Cells 9 E2049 (2020)
  43. Knockdown of Dinoflagellate Condensin CcSMC4 Subunit Leads to S-Phase Impediment and Decompaction of Liquid Crystalline Chromosomes. Yan THK, Wu Z, Kwok ACM, Wong JTY. Microorganisms 8 E565 (2020)
  44. Solution structure and flexibility of the condensin HEAT-repeat subunit Ycg1. Manalastas-Cantos K, Kschonsak M, Haering CH, Svergun DI. J Biol Chem 294 13822-13829 (2019)
  45. A specialized condensin complex participates in somatic nuclear maturation in Tetrahymena thermophila. Howard-Till R, Tian M, Loidl J. Mol Biol Cell 30 1326-1338 (2019)
  46. Molecular dissection of condensin II-mediated chromosome assembly using in vitro assays. Yoshida MM, Kinoshita K, Aizawa Y, Tane S, Yamashita D, Shintomi K, Hirano T. Elife 11 e78984 (2022)
  47. Three-dimensional loop extrusion. Bonato A, Michieletto D. Biophys J 120 5544-5552 (2021)
  48. Condensin pinches a short negatively supercoiled DNA loop during each round of ATP usage. Martínez-García B, Dyson S, Segura J, Ayats A, Cutts EE, Gutierrez-Escribano P, Aragón L, Roca J. EMBO J 42 e111913 (2023)
  49. Control of mitotic chromosome condensation by the fission yeast transcription factor Zas1. Schiklenk C, Petrova B, Kschonsak M, Hassler M, Klein C, Gibson TJ, Haering CH. J Cell Biol 217 2383-2401 (2018)
  50. Rec8 Cohesin-mediated Axis-loop chromatin architecture is required for meiotic recombination. Sakuno T, Tashiro S, Tanizawa H, Iwasaki O, Ding DQ, Haraguchi T, Noma KI, Hiraoka Y. Nucleic Acids Res 50 3799-3816 (2022)
  51. The histone H4 lysine 20 demethylase DPY-21 regulates the dynamics of condensin DC binding. Breimann L, Morao AK, Kim J, Sebastian Jimenez D, Maryn N, Bikkasani K, Carrozza MJ, Albritton SE, Kramer M, Street LA, Cerimi K, Schumann VF, Bahry E, Preibisch S, Woehler A, Ercan S. J Cell Sci 135 jcs258818 (2022)
  52. Condensin positioning at telomeres by shelterin proteins drives sister-telomere disjunction in anaphase. Colin L, Reyes C, Berthezene J, Maestroni L, Modolo L, Toselli E, Chanard N, Schaak S, Cuvier O, Gachet Y, Coulon S, Bernard P, Tournier S. Elife 12 RP89812 (2023)
  53. Cell cycle-specific loading of condensin I is regulated by the N-terminal tail of its kleisin subunit. Tane S, Shintomi K, Kinoshita K, Tsubota Y, Yoshida MM, Nishiyama T, Hirano T. Elife 11 e84694 (2022)
  54. Chromatin Dynamics During Entry to Quiescence and Compromised Functionality in Cancer Cells. Dobbs OG, Coverley D. Results Probl Cell Differ 70 279-294 (2022)
  55. Direct imaging of intracellular RNA, DNA, and liquid-liquid phase separated membraneless organelles with Raman microspectroscopy. Samuel AZ, Sugiyama K, Ando M, Takeyama H. Commun Biol 5 1383 (2022)
  56. Ycs4 Subunit of Saccharomyces cerevisiae Condensin Binds DNA and Modulates the Enzyme Turnover. Sarkar R, Petrushenko ZM, Dawson DS, Rybenkov VV. Biochemistry 60 3385-3397 (2021)