Specialized interfaces of Smc5/6 control hinge stability and DNA association

Nature Communications

Volumn 8, Issue , 2017, Pages

  Alt, Aaron ^a   Dang, Hung Q ^a   Wells, Owen S ^a   Polo, Luis M ^a   Smith, Matt A ^a   McGregor, Grant A ^a   Welte, Thomas ^b   Lehmann, Alan R ^a   Pearl, Laurence H ^a   Murray, Johanne M ^a   Oliver, Antony W ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b DYNAMIC BIOSENSORS GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; CONDENSIN; DNA; SINGLE STRANDED DNA; ADENOSINE TRIPHOSPHATASE; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX; NONHISTONE PROTEIN; PROTEIN BINDING; RECOMBINANT PROTEIN; SCHIZOSACCHAROMYCES POMBE PROTEIN; SMC5 PROTEIN, HUMAN; SMC5 PROTEIN, S POMBE; SMC6 PROTEIN, HUMAN; SMC6 PROTEIN, S POMBE;

CHROMOSOME; DNA; GENETIC ANALYSIS; MOLECULAR ANALYSIS; PROTEIN; YEAST;

ARTICLE; CHROMOSOME 5; CHROMOSOME 6; CONTROLLED STUDY; FISSION YEAST; HUMAN; HUMAN CELL; MUTATION; BINDING SITE; CELL SURVIVAL; CHEMISTRY; DNA DAMAGE; DNA REPAIR; GENETICS; METABOLISM; MOLECULAR MODEL; PHENOTYPE; PHYSIOLOGY; PROTEIN DOMAIN; PROTEIN MULTIMERIZATION; SCHIZOSACCHAROMYCES; SITE DIRECTED MUTAGENESIS; TUMOR CELL LINE; X RAY CRYSTALLOGRAPHY;

EUKARYOTA; SCHIZOSACCHAROMYCETACEAE;

ADENOSINE TRIPHOSPHATASES; BINDING SITES; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; CHROMOSOMAL PROTEINS, NON-HISTONE; CRYSTALLOGRAPHY, X-RAY; DNA DAMAGE; DNA REPAIR; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HUMANS; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHENOTYPE; PROTEIN BINDING; PROTEIN DOMAINS; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS;

EID: 85011115339     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms14011     Document Type: Article

References (67)

1. Lehmann, A. R. et al. The rad18 gene of Schizosaccharomyces pombe defines a new subgroup of the SMC superfamily involved in DNA repair. Mol. Cell Biol. 15, 7067-7080 (1995).
2. Ju, L. et al. SMC6 is an essential gene in mice, but a hypomorphic mutant in the ATPase domain has a mild phenotype with a range of subtle abnormalities. DNA Repair (Amst) 12, 356-366 (2013).
3. Ampatzidou, E., Irmisch, A., O'Connell, M. J. & Murray, J.M. Smc5/6 is required for repair at collapsed replication forks. Mol. Cell Biol. 26, 9387-9401 (2006).
4. Branzei, D. et al. Ubc9-and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127, 509-522 (2006).
5. De Piccoli, G. et al. Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat. Cell Biol. 8, 1032-1034 (2006).
6. Miyabe, I., Morishita, T., Hishida, T., Yonei, S. & Shinagawa, H. 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 (2006).
7. Murray, J. M. & Carr, A. M. Smc5/6: a link between DNA repair and unidirectional replication Nat. Rev. Mol. Cell Biol. 9, 177-182 (2008).
8. Copsey, A. et al. Smc5/6 coordinates formation and resolution of joint molecules with chromosome morphology to ensure meiotic divisions. PLoS Genet. 9, e1004071 (2013).
9. Farmer, S., San-Segundo, P. A. & Aragon, L. The Smc5-Smc6 complex is required to remove chromosome junctions in meiosis. PLoS ONE 6, e20948 (2011).
10. Lilienthal, I., Kanno, T. & Sjogren, C. Inhibition of the Smc5/6 complex during meiosis perturbs joint molecule formation and resolution without significantly changing crossover or non-crossover levels. PLoS Genet. 9, e1003898 (2013).
11. Wehrkamp-Richter, S., Hyppa, R. W., Prudden, J., Smith, G. R. & Boddy, M. N. Meiotic DNA joint molecule resolution depends on Nse5-Nse6 of the Smc5-Smc6 holocomplex. Nucleic Acids Res. 40, 9633-9646 (2012).
12. Xaver, M., Huang, L., Chen, D. & Klein, F. Smc5/6-Mms21 prevents and eliminates inappropriate recombination intermediates in meiosis. PLoS Genet. 9, e1004067 (2013).
13. Outwin, E. A., Irmisch, A., Murray, J. M. & O'Connell, M. J. Smc5-Smc6-dependent removal of cohesin from mitotic chromosomes. Mol. Cell Biol. 29, 4363-4375 (2009).
14. Schleiffer, A. et al. Kleisins: a superfamily of bacterial and eukaryotic SMC protein partners. Mol. Cell 11, 571-575 (2003).
15. 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, 419-424 (2002).
16. Nasmyth, K. Cohesin: a catenase with separate entry and exit gates Nat. Cell Biol. 13, 1170-1177 (2011).
17. Peters, J. M. & Nishiyama, T. Sister chromatid cohesion. Cold Spring Harb. Perspect. Biol. 4, a011130 (2012).
18. Haering, C. H., Lowe, J., Hochwagen, A. & Nasmyth, K. Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9, 773-788 (2002).
19. Shintomi, K. & Hirano, T. How are cohesin rings opened and closed Trends Biochem. Sci. 32, 154-157 (2007).
20. Hirano, T. Condensin-based chromosome organization from bacteria to vertebrates. Cell 164, 847-857 (2016).
21. Uhlmann, F. SMC complexes: from DNA to chromosomes. Nat. Rev. Mol. Cell Biol. 17, 399-412 (2016).
22. Hazbun, T. R. et al. Assigning function to yeast proteins by integration of technologies. Mol. Cell 12, 1353-1365 (2003).
23. Sergeant, J. et al. Composition and architecture of the Schizosaccharomyces pombe Rad18 (Smc5-6) complex. Mol. Cell Biol. 25, 172-184 (2005).
24. Doyle, J. M., Gao, J., Wang, J., Yang, M. & Potts, P. R. MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Mol. Cell 39, 963-974 (2010).
25. Duan, X. et al. Structural and functional insights into the roles of the Mms21 subunit of the Smc5/6 complex. Mol. Cell 35, 657-668 (2009).
26. Andrews, E. A. et al. Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage. Mol. Cell Biol. 25, 185-196 (2005).
27. Pebernard, S., Perry, J. J., Tainer, J. A. & Boddy, M. N. Nse1 RING-like domain supports functions of the Smc5-Smc6 holocomplex in genome stability. Mol. Biol. Cell 19, 4099-4109 (2008).
28. Zhao, X. & Blobel, G. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl Acad. Sci. USA 102, 4777-4782 (2005).
29. Raschle, M. et al. DNA repair. Proteomics reveals dynamic assembly of repair complexes during bypass of DNA cross-links. Science 348, 1253671 (2015).
30. Griese, J. J., Witte, G. & Hopfner, K. P. Structure and DNA binding activity of the mouse condensin hinge domain highlight common and diverse features of SMC proteins. Nucleic Acids Res. 38, 3454-3465 (2010).
31. Kurze, A. et al. A positively charged channel within the Smc1/Smc3 hinge required for sister chromatid cohesion. EMBO J 30, 364-378 (2011).
32. Griese, J. J. & Hopfner, K. P. Structure and DNA-binding activity of the Pyrococcus furiosus SMC protein hinge domain. Proteins 79, 558-568 (2011).
33. Mishra, A. et al. Both interaction surfaces within cohesin's hinge domain are essential for its stable chromosomal association. Curr. Biol. 20, 279-289 (2010).
34. Watson, A. T., Garcia, V., Bone, N., Carr, A. M. & Armstrong, J. Gene tagging and gene replacement using recombinase-mediated cassette exchange in Schizosaccharomyces pombe. Gene 407, 63-74 (2008).
35. Hirano, M., Anderson, D. E., Erickson, H. P. & Hirano, T. Bimodal activation of SMC ATPase by intra-and inter-molecular interactions. EMBO J 20, 3238-3250 (2001).
36. Hirano, M. & Hirano, T. Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J 21, 5733-5744 (2002).
37. Nasim, A. & Smith, B. P. Genetic control of radiation sensitivity in Schizosaccharomyces pombe. Genetics 79, 573-582 (1975).
38. Fousteri, M. I. & Lehmann, A. R. A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein. EMBO J 19, 1691-1702 (2000).
39. Chiu, A., Revenkova, E. & Jessberger, R. DNA interaction and dimerization of eukaryotic SMC hinge domains. J. Biol. Chem. 279, 26233-26242 (2004).
40. Roy, M. A. & D'Amours, D. DNA-binding properties of Smc6, a core component of the Smc5-6 DNA repair complex. Biochem. Biophys. Res. Commun. 416, 80-85 (2011).
41. Roy, M. A., Siddiqui, N. & D'Amours, D. Dynamic and selective DNA-binding activity of Smc5, a core component of the Smc5-Smc6 complex. Cell Cycle 10, 690-700 (2011).
42. Li, Y., Schoeffler, A. J., Berger, J. M. & Oakley, M. G. The crystal structure of the hinge domain of the Escherichia coli structural maintenance of chromosomes protein MukB. J. Mol. Biol. 395, 11-19 (2010).
43. Soh, Y. M. et al. Molecular basis for SMC rod formation and its dissolution upon DNA binding. Mol. Cell 57, 290-303 (2015).
44. Schneidman-Duhovny, D., Hammel, M. & Sali, A. FoXS: a web server for rapid computation and fitting of SAXS profiles. Nucleic Acids Res. 38, W540-W544 (2010).
45. Putnam, C. D., Hammel, M., Hura, G. L. & Tainer, J. A. X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q. Rev. Biophys 40, 191-285 (2007).
46. Forster, S., Apostol, L. & Bras, W. Scatter: software for the analysis of nano-and mesoscale small-angle scattering. J. Appl. Crystallogr. 43, 639-646 (2010).
47. Cobbe, N. & Heck, M. M. The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol. Biol. Evol. 21, 332-347 (2004).
48. Buheitel, J. & Stemmann, O. Prophase pathway-dependent removal of cohesin from human chromosomes requires opening of the Smc3-Scc1 gate. EMBO J 32, 666-676 (2013).
49. Gruber, S. et al. Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell 127, 523-537 (2006).
50. Irmisch, A., Ampatzidou, E., Mizuno, K. i., O'Connell, M. J. & Murray, J. M. Smc5/6 maintains stalled replication forks in a recombination-competent conformation. EMBO J 28, 144-155 (2009).
51. Hirano, M. & Hirano, T. Opening closed arms: long-distance activation of SMC ATPase by hinge-DNA interactions. Mol. Cell 21, 175-186 (2006).
52. Kelley, L. A. & Sternberg, M. J. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371 (2009).
53. Kabsch, W. XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
54. Evans, P. R. & Murshudov, G. N. How good are my data and what is the resolution Acta Crystallogr. D Biol. Crystallogr. 69, 1204-1214 (2013).
55. Winn, M. D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
56. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
57. Terwilliger, T. SOLVE and RESOLVE: automated structure solution, density modification and model building. J. Synchrotron. Radiat. 11, 49-52 (2004).
58. Terwilliger, T. C. et al. Iterative model building, structure refinement and density modification with the PHENIX AutoBuild wizard. Acta Crystallogr. D Biol. Crystallogr. 64, 61-69 (2008).
59. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008).
60. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004).
61. Bricogne, G. et al. BUSTER version 2.10.2 (Global Phasing Ltd., 2011).
62. Moreno, S., Klar, A. & Nurse, P. Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823 (1991).
63. Taylor, E. M. et al. Characterization of a novel human SMC heterodimer homologous to the Schizosaccharomyces pombe Rad18/Spr18 complex. Mol. Biol. Cell 12, 1583-1594 (2001).
64. De Maria Antolinos, A. et al. ISPyB for BioSAXS, the gateway to user autonomy in solution scattering experiments. Acta Crystallogr. D Biol. Crystallogr. 71, 76-85 (2015).
65. Petoukhov, M. V. et al. New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr. 45, 342-350 (2012).
66. Franke, D. & Svergun, D. I. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342-346 (2009).
67. Langer, A. et al. Protein sizing and conformation analysis with an electroswitchable DNA chip. Biophys. J. 104, 194a-194a (2013).