Structure of Full-Length SMC and Rearrangements Required for Chromosome Organization

Molecular Cell

Volumn 67, Issue 2, 2017, Pages 334-347.e5

  Diebold Durand, Marie Laure ^a,c   Lee, Hansol ^b   Ruiz Avila, Laura B ^a   Noh, Haemin ^b   Shin, Ho Chul ^b,e   Im, Haeri ^d   Bock, Florian P ^a,c   Bürmann, Frank ^a,f   Durand, Alexandre ^a,c   Basfeld, Alrun ^a   Ham, Sihyun ^d   Basquin, Jérôme ^a   Oh, Byung Ha ^b   Gruber, Stephan ^a,c  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d Sookmyung Women's University   (South Korea)

^e Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^f MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

chromosome condensation; cohesion; condensin; DNA loop extrusion; kite; kleisin; MukB; Rad50; ScpA; ScpB; SMC

Indexed keywords

COHESIN; CYSTEINE; PROTEIN; SMC PROTEIN; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; CELL CYCLE PROTEIN; SMC PROTEIN, BACTERIA;

ARTICLE; BACILLUS SUBTILIS; CHROMOSOMAL LOCALIZATION; CHROMOSOME STRUCTURE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS LINKING; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; NONHUMAN; PROTEIN STRUCTURE; STEREOCHEMISTRY; SURFACE PROPERTY; BACTERIAL CHROMOSOME; BINDING SITE; CHEMISTRY; CHROMOSOME SEGREGATION; CONFORMATION; GENETICS; HIGH THROUGHPUT SCREENING; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION; X RAY CRYSTALLOGRAPHY;

ADENOSINE TRIPHOSPHATE; BACILLUS SUBTILIS; BACTERIAL PROTEINS; BINDING SITES; CELL CYCLE PROTEINS; CHROMOSOME SEGREGATION; CHROMOSOMES, BACTERIAL; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; HIGH-THROUGHPUT SCREENING ASSAYS; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; PROTEIN CONFORMATION; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 85021832306     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2017.06.010     Document Type: Article

References (51)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 213–221.
2. Alt, A., Dang, H.Q., Wells, O.S., Polo, L.M., Smith, M.A., McGregor, G.A., Welte, T., Lehmann, A.R., Pearl, L.H., Murray, J.M., Oliver, A.W., Specialized interfaces of Smc5/6 control hinge stability and DNA association. Nat. Commun., 8, 2017, 14011.
3. Anderson, D.E., Losada, A., Erickson, H.P., Hirano, T., Condensin and cohesin display different arm conformations with characteristic hinge angles. J. Cell Biol. 156 (2002), 419–424.
4. Arumugam, P., Gruber, S., Tanaka, K., Haering, C.H., Mechtler, K., Nasmyth, K., ATP hydrolysis is required for cohesin's association with chromosomes. Curr. Biol. 13 (2003), 1941–1953.
5. Barysz, H., Kim, J.H., Chen, Z.A., Hudson, D.F., Rappsilber, J., Gerloff, D.L., Earnshaw, W.C., Three-dimensional topology of the SMC2/SMC4 subcomplex from chicken condensin I revealed by cross-linking and molecular modelling. Open Biol., 5, 2015, 150005.
6. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998), 905–921.
7. Buheitel, J., Stemmann, O., Prophase pathway-dependent removal of cohesin from human chromosomes requires opening of the Smc3-Scc1 gate. EMBO J. 32 (2013), 666–676.
8. Bürmann, F., Shin, H.C., Basquin, J., Soh, Y.M., Giménez-Oya, V., Kim, Y.G., Oh, B.H., Gruber, S., An asymmetric SMC-kleisin bridge in prokaryotic condensin. Nat. Struct. Mol. Biol. 20 (2013), 371–379.
9. Bürmann, F., Basfeld, A., Vazquez Nunez, R., Diebold-Durand, M.L., Wilhelm, L., Gruber, S., Tuned SMC arms drive chromosomal loading of prokaryotic condensin. Mol. Cell 65 (2017), 861–872.e9.
10. Case, D.A., Babin, V., Berryman, J.T., Betz, R.M., Cai, Q., Cerutti, D.S., Cheatham, T.E., Darden, T.A., Duke, R.E., Gohlke, H., et al. AMBER 14. 2014, University of California, San Francisco.
11. Eeftens, J.M., Katan, A.J., Kschonsak, M., Hassler, M., de Wilde, L., Dief, E.M., Haering, C.H., Dekker, C., Condensin Smc2-Smc4 dimers are flexible and dynamic. Cell Rep. 14 (2016), 1813–1818.
12. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 486–501.
13. Gligoris, T.G., Scheinost, J.C., Bürmann, F., Petela, N., Chan, K.L., Uluocak, P., Beckouët, F., Gruber, S., Nasmyth, K., Löwe, J., Closing the cohesin ring: structure and function of its Smc3-kleisin interface. Science 346 (2014), 963–967.
14. Gruber, S., Errington, J., Recruitment of condensin to replication origin regions by ParB/SpoOJ promotes chromosome segregation in B. subtilis. Cell 137 (2009), 685–696.
15. Gruber, S., Arumugam, P., Katou, Y., Kuglitsch, D., Helmhart, W., Shirahige, K., Nasmyth, K., Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell 127 (2006), 523–537.
16. Gruber, S., Veening, J.W., Bach, J., Blettinger, M., Bramkamp, M., Errington, J., Interlinked sister chromosomes arise in the absence of condensin during fast replication in B. subtilis. Curr. Biol. 24 (2014), 293–298.
17. Haering, C.H., Löwe, J., Hochwagen, A., Nasmyth, K., Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9 (2002), 773–788.
18. Hirano, T., Condensin-based chromosome organization from bacteria to vertebrates. Cell 164 (2016), 847–857.
19. Hirano, M., Hirano, T., Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J. 21 (2002), 5733–5744.
20. Hirano, M., Hirano, T., Opening closed arms: long-distance activation of SMC ATPase by hinge-DNA interactions. Mol. Cell 21 (2006), 175–186.
21. Hirano, M., Anderson, D.E., Erickson, H.P., Hirano, T., Bimodal activation of SMC ATPase by intra- and inter-molecular interactions. EMBO J. 20 (2001), 3238–3250.
22. Hopfner, K.P., Invited review: architectures and mechanisms of ATP binding cassette proteins. Biopolymers 105 (2016), 492–504.
23. Huis in 't Veld, P.J., Herzog, F., Ladurner, R., Davidson, I.F., Piric, S., Kreidl, E., Bhaskara, V., Aebersold, R., Peters, J.M., Characterization of a DNA exit gate in the human cohesin ring. Science 346 (2014), 968–972.
24. Hutchison, C.A. 3rd, Chuang, R.Y., Noskov, V.N., Assad-Garcia, N., Deerinck, T.J., Ellisman, M.H., Gill, J., Kannan, K., Karas, B.J., Ma, L., et al. Design and synthesis of a minimal bacterial genome. Science, 351, 2016, aad6253.
25. Jeppsson, K., Kanno, T., Shirahige, K., Sjögren, C., The maintenance of chromosome structure: positioning and functioning of SMC complexes. Nat. Rev. Mol. Cell Biol. 15 (2014), 601–614.
26. Kabsch, W., Xds. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 125–132.
27. Kamada, K., Miyata, M., Hirano, T., Molecular basis of SMC ATPase activation: role of internal structural changes of the regulatory subcomplex ScpAB. Structure 21 (2013), 581–594.
28. Kamada, K., Su'etsugu, M., Takada, H., Miyata, M., Hirano, T., Overall shapes of the SMC-ScpAB complex are determined by balance between constraint and relaxation of its structural parts. Structure 25 (2017), 603–616.e4.
29. Lammens, A., Schele, A., Hopfner, K.P., Structural biochemistry of ATP-driven dimerization and DNA-stimulated activation of SMC ATPases. Curr. Biol. 14 (2004), 1778–1782.
30. Locher, K.P., Mechanistic diversity in ATP-binding cassette (ABC) transporters. Nat. Struct. Mol. Biol. 23 (2016), 487–493.
31. Marbouty, M., Le Gall, A., Cattoni, D.I., Cournac, A., Koh, A., Fiche, J.B., Mozziconacci, J., Murray, H., Koszul, R., Nollmann, M., Condensin- and replication-mediated bacterial chromosome folding and origin condensation revealed by Hi-C and super-resolutioni. Mol. Cell 59 (2015), 588–602.
32. Melby, T.E., Ciampaglio, C.N., Briscoe, G., Erickson, H.P., 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 (1998), 1595–1604.
33. Merkenschlager, M., Nora, E.P., CTCF and cohesin in genome folding and transcriptional gene regulation. Annu. Rev. Genomics Hum. Genet. 17 (2016), 17–43.
34. Minnen, A., Bürmann, F., Wilhelm, L., Anchimiuk, A., Diebold-Durand, M.L., Gruber, S., Control of Smc coiled coil architecture by the ATPase heads facilitates targeting to chromosomal ParB/parS and release onto flanking DNA. Cell Rep. 14 (2016), 2003–2016.
35. Park, Y.B., Hohl, M., Padjasek, M., Jeong, E., Jin, K.S., Krężel, A., Petrini, J.H., Cho, Y., Eukaryotic Rad50 functions as a rod-shaped dimer. Nat. Struct. Mol. Biol. 24 (2017), 248–257.
36. Peters, J.M., Nishiyama, T., Sister chromatid cohesion. Cold Spring Harb. Perspect. Biol., 4, 2012, 4.
37. Roversi, P., Blanc, E., Johnson, S., Lea, S.M., Tetartohedral twinning could happen to you too. Acta Crystallogr. D Biol. Crystallogr. 68 (2012), 418–424.
38. Schneider, C.A., Rasband, W.S., Eliceiri, K.W., NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9 (2012), 671–675.
39. Sheldrick, G.M., Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66 (2010), 479–485.
40. Soh, Y.M., Bürmann, F., Shin, H.C., Oda, T., Jin, K.S., Toseland, C.P., Kim, C., Lee, H., Kim, S.J., Kong, M.S., et al. Molecular basis for SMC rod formation and its dissolution upon DNA binding. Mol. Cell 57 (2015), 290–303.
41. Stigler, J., Çamdere, G.O., Koshland, D.E., Greene, E.C., Single-molecule imaging reveals a collapsed conformational state for DNA-bound cohesin. Cell Rep. 15 (2016), 988–998.
42. Studier, F.W., Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif. 41 (2005), 207–234.
43. Sullivan, N.L., Marquis, K.A., Rudner, D.Z., Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137 (2009), 697–707.
44. Waldman, V.M., Stanage, T.H., Mims, A., Norden, I.S., Oakley, M.G., Structural mapping of the coiled-coil domain of a bacterial condensin and comparative analyses across all domains of life suggest conserved features of SMC proteins. Proteins 83 (2015), 1027–1045.
45. 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. 24 (2014), 287–292.
46. Wang, X., Le, T.B., Lajoie, B.R., Dekker, J., Laub, M.T., Rudner, D.Z., Condensin promotes the juxtaposition of DNA flanking its loading site in Bacillus subtilis. Genes Dev. 29 (2015), 1661–1675.
47. Wang, X., Brandão, H.B., Le, T.B., Laub, M.T., Rudner, D.Z., Bacillus subtilis SMC complexes juxtapose chromosome arms as they travel from origin to terminus. Science 355 (2017), 524–527.
48. Weitzer, S., Lehane, C., Uhlmann, F., A model for ATP hydrolysis-dependent binding of cohesin to DNA. Curr. Biol. 13 (2003), 1930–1940.
49. Wilhelm, L., Bürmann, F., Minnen, A., Shin, H.C., Toseland, C.P., Oh, B.H., Gruber, S., SMC condensin entraps chromosomal DNA by an ATP hydrolysis dependent loading mechanism in Bacillus subtilis. eLife, 4, 2015, 4.
50. Woo, J.S., Lim, J.H., Shin, H.C., Suh, M.K., Ku, B., Lee, K.H., Joo, K., Robinson, H., Lee, J., Park, S.Y., et al. Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions. Cell 136 (2009), 85–96.
51. Zhao, S., Fernald, R.D., Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 12 (2005), 1047–1064.