Chromatin association of the SMC5/6 complex is dependent on binding of its NSE3 subunit to DNA

Nucleic Acids Research

Volumn 44, Issue 3, 2016, Pages 1064-1079

  Zabrady, Katerina ^a   Adamus, Marek ^a   Vondrova, Lucie ^a   Liao, Chunyan ^b   Skoupilova, Hana ^a   Novakova, Marketa ^a,c   Jurcisinova, Lenka ^a   Alt, Aaron ^b   Oliver, Antony W ^b   Lehmann, Alan R ^b   Palecek, Jan J ^a  

^a MASARYK UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF SUSSEX   (United Kingdom)

^c UNIVERSITY OF VETERINARY AND PHARMACEUTICAL SCIENCES   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; MEMBRANE PROTEIN; PROTEIN NSE1; PROTEIN NSE3; PROTEIN NSE4; STRUCTURAL MAINTENANCE OF CHROMOSOME 5; STRUCTURAL MAINTENANCE OF CHROMOSOME 6; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CHROMATIN; DNA; NSE3 PROTEIN, S POMBE; NUCLEAR PROTEIN; PROTEIN BINDING; SCHIZOSACCHAROMYCES POMBE PROTEIN;

ARTICLE; BINDING AFFINITY; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA BINDING; DNA REPLICATION; GENOME; HYDROLYSIS; MOLECULAR CLONING; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN PURIFICATION; SCHIZOSACCHAROMYCES POMBE; SITE DIRECTED MUTAGENESIS; AMINO ACID SEQUENCE; CHEMISTRY; GENETIC RECOMBINATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; SCHIZOSACCHAROMYCES; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; CELL CYCLE PROTEINS; CHROMATIN; DNA; DNA REPLICATION; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN BINDING; RECOMBINATION, GENETIC; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84964765934     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv1021     Document Type: Article

References (56)

1. Losada, A. and Hirano, T. (2005) Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev., 19, 1269-1287.
2. Carter, S.D. and Sjögren, C. (2012) The SMC complexes, DNA and chromosome topology: right or knot? Crit. Rev. Biochem. Mol. Biol., 47, 1-16.
3. Lehmann, A.R. (2005) The role of SMC proteins in the responses to DNA damage. DNA Repair, 4, 309-314.
4. Wu, N. and Yu, H. (2012) The Smc complexes in DNA damage response. Cell Biosci., 2, 5.
5. Lehmann, A.R.,Walicka, M., Griffiths, D.J., Murray, J.M., Watts, F.Z., McCready, S. and Carr, A.M. (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.
6. Ju, L., Wing, J., Taylor, E., Brandt, R., Slijepcevic, P., Horsch, M., Rathkolb, B., Rácz, I., Becker, L., Hans, W. et al. (2013) 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, 12, 356-366.
7. Irmisch, A., Ampatzidou, E.,Mizuno, K., O'Connell, M.J. and Murray, J.M. (2009) Smc5/6 maintains stalled replication forks in a recombination-competent conformation. EMBO J., 28, 144-155.
8. Kegel, A. and Sjögren, C. (2010) The Smc5/6 Complex:More Than Repair? Cold Spring Harb. Symp. Quant. Biol., 75, 179-187.
9. Murray, J.M. and Carr, A.M. (2008) Smc5/6: a link between DNA repair and unidirectional replication? Nat. Rev. Mol. Cell Biol., 9, 177-182.
10. De Piccoli, G., Cortes-Ledesma, F., Ira, G., Torres-Rosell, J., Uhle, S., Farmer, S., Hwang, J.-Y., Machin, F., Ceschia, A., McAleenan, A. et al. (2006) Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat. Cell Biol., 8, 1032-1034.
11. Sollier, J., Driscoll, R., Castellucci, F., Foiani, M., Jackson, S.P. and 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.
12. Copsey, A., Tang, S., Jordan, P.W., Blitzblau, H.G., Newcombe, S., Chan, A.C.-H., Newnham, L., Li, Z., Gray, S., Herbert, A.D. et al. (2013) Smc5/6 coordinates formation and resolution of joint molecules with chromosome morphology to ensure meiotic divisions. PLoS Genet., 9, e1004071.
13. Xaver, M., Huang, L., Chen, D. and Klein, F. (2013) Smc5/6-Mms21 Prevents and Eliminates Inappropriate Recombination Intermediates in Meiosis. PLoS Genet., 9, e1004067.
14. McAleenan, A., Cordon-Preciado, V., Clemente-Blanco, A., Liu, I.-C., Sen, N., Leonard, J., Jarmuz, A. and Aragón, L. (2012) SUMOylation of the α-kleisin subunit of cohesin is required for DNA damage-induced cohesion. Curr. Biol., 22, 1564-1575.
15. Outwin, E.A., Irmisch, A., Murray, J.M. and O'Connell, M.J. (2009) Smc5-Smc6-Dependent Removal of Cohesin from Mitotic Chromosomes. Mol. Cell. Biol., 29, 4363-4375.
16. Gallego-Paez, L.M., Tanaka, H., Bando, M., Takahashi, M., Nozaki, N., Nakato, R., Shirahige, K. and Hirota, T. (2014) Smc5/6-mediated regulation of replication progression contributes to chromosome assembly during mitosis in human cells. Mol. Biol. Cell, 25, 302-317.
17. Potts, P.R. and Yu, H. (2007) The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat. Struct. Mol. Biol., 14, 581-590.
18. Cuylen, S., Metz, J. and Haering, C.H. (2011) Condensin structures chromosomal DNA through topological links. Nat. Struct. Mol. Biol., 18, 894-901.
19. Ivanov, D. and Nasmyth, K. (2005) A Topological Interaction between Cohesin Rings and a Circular Minichromosome. Cell, 122, 849-860.
20. Arumugam, P., Gruber, S., Tanaka, K., Haering, C.H., Mechtler, K. and Nasmyth, K. (2003) ATP Hydrolysis Is Required for Cohesin's Association with Chromosomes. Curr. Biol., 13, 1941-1953.
21. Gruber, S., Arumugam, P., Katou, Y., Kuglitsch, D., Helmhart, W., Shirahige, K. and Nasmyth, K. (2006) Evidence that Loading of Cohesin Onto Chromosomes Involves Opening of Its SMC Hinge. Cell, 127, 523-537.
22. Weitzer, S., Lehane, C. and Uhlmann, F. (2003) A Model for ATP Hydrolysis-Dependent Binding of Cohesin to DNA. Curr. Biol., 13, 1930-1940.
23. Murayama, Y. and Uhlmann, F. (2014) Biochemical reconstitution of topological DNA binding by the cohesin ring. Nature, 505, 367-371.
24. Piazza, I., Rutkowska, A., Ori, A., Walczak, M., Metz, J., Pelechano, V., Beck, M. and Haering, C.H. (2014) Association of condensin with chromosomes depends on DNA binding by its HEAT-repeat subunits. Nat. Struct. Mol. Biol., 21, 560-568.
25. Griese, J.J., Witte, G. and Hopfner, K.-P. (2010) 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.
26. Roy, M.-A. and D'Amours, D. (2011) DNA-binding properties of Smc6, a core component of the Smc5-6 DNA repair complex. Biochem. Biophys. Res. Commun., 416, 80-85.
27. Roy, M.-A., Siddiqui, N. and D'Amours, D. (2011) Dynamic and selective DNA-binding activity of Smc5, a core component of the Smc5-Smc6 complex. Cell Cycle, 10, 690-700.
28. Fousteri, M.I. and Lehmann, A.R. (2000) A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein. EMBO J., 19, 1691-1702.
29. Palecek, J., Vidot, S., Feng, M., Doherty, A.J. and Lehmann, A.R. (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.
30. Duan, X., Yang, Y., Chen, Y.-H., Arenz, J., Rangi, G.K., Zhao, X. and Ye, H. (2009) Architecture of the Smc5/6 Complex of Saccharomyces cerevisiae Reveals a Unique Interaction between the Nse5-6 Subcomplex and the Hinge Regions of Smc5 and Smc6. J. Biol. Chem., 284, 8507-8515.
31. Sergeant, J., Taylor, E., Palecek, J., Fousteri, M., Andrews, E.A., Sweeney, S., Shinagawa, H., Watts, F.Z. and Lehmann, A.R. (2005) Composition and Architecture of the Schizosaccharomyces pombe Rad18 (Smc5-6) Complex. Mol. Cell. Biol., 25, 172-184.
32. Hudson, J.J.R., Bednarova, K., Kozakova, L., Liao, C., Guerineau, M., Colnaghi, R., Vidot, S., Marek, J., Bathula, S.R., Lehmann, A.R. et al. (2011) Interactions between the Nse3 and Nse4 Components of the SMC5-6 Complex Identify Evolutionarily Conserved Interactions between MAGE and EID Families. PLoS ONE, 6, e17270.
33. Doyle, J.M., Gao, J., Wang, J., Yang, M. and Potts, P.R. (2010) MAGE-RING Protein Complexes Comprise a Family of E3 Ubiquitin Ligases. Mol. Cell, 39, 963-974.
34. Roy, A., Kucukural, A. and Zhang, Y. (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc., 5, 725-738.
35. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr., 60, 2126-2132.
36. de Vries, S.J., van Dijk, M. and Bonvin, A.M.J.J. (2010) The HADDOCK web server for data-driven biomolecular docking. Nat. Protoc., 5, 883-897.
37. Wassenaar, T.A., van Dijk, M., Loureiro-Ferreira, N., van der Schot, G., de Vries, S.J., Schmitz, C., van der Zwan, J., Boelens, R., Giachetti, A., Ferella, L. et al. (2012) WeNMR: Structural Biology on the Grid. J. Grid Comput., 10, 743-767.
38. Studier, F.W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr. Purif., 41, 207-234.
39. Moreno, S., Klar, A. and Nurse, P. (1991) Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol., 194, 795-823.
40. Morikawa, H., Morishita, T., Kawane, S., Iwasaki, H., Carr, A.M. and 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.
41. Watson, A.T., Werler, P. and Carr, A.M. (2011) Regulation of gene expression at the fission yeast Schizosaccharomyces pombe urg1 locus. Gene, 484, 75-85.
42. Pebernard, S., Schaffer, L., Campbell, D., Head, S.R. and Boddy, M.N. (2008) Localization of Smc5/6 to centromeres and telomeres requires heterochromatin and SUMO, respectively. EMBO J., 27, 3011-3023.
43. Guerineau, M., Kriz, Z., Kozakova, L., Bednarova, K., Janos, P. and Palecek, J. (2012) Analysis of the Nse3/MAGE-binding domain of the Nse4/EID family proteins. PloS One, 7, e35813.
44. Kozakova, L., Vondrova, L., Stejskal, K., Charalabous, P., Kolesar, P., Lehmann, A.R., Uldrijan, S., Sanderson, C.M., Zdrahal, Z. and Palecek, J.J. (2015) The melanoma-associated antigen 1 (MAGEA1) protein stimulates the E3 ubiquitin-ligase activity of TRIM31 within a TRIM31-MAGEA1-NSE4 complex. Cell Cycle, 14, 920-930.
45. Palecek, J.J. and Gruber, S.(2015) Kite proteins: A superfamily of SMC/kleisin partners conserved across bacteria, archaea and eukaryotes. Structure, in press.
46. Gajiwala, K.S. and Burley, S.K. (2000) Winged helix proteins. Curr. Opin. Struct. Biol., 10, 110-116.
47. Harami, G.M., Gyimesi, M. and Kovács, M. (2013) From keys to bulldozers: expanding roles for winged helix domains in nucleic-acid-binding proteins. Trends Biochem. Sci., 38, 364-371.
48. Ke, C., Humeniuk, M., S-Gracz, H. and Marszalek, P.E. (2007) Direct Measurements of Base Stacking Interactions in DNA by Single-Molecule Atomic-Force Spectroscopy. Phys. Rev. Lett., 99, 018302.
49. Cost, G.J. and Cozzarelli, N.R. (2006) Smc5p promotes faithful chromosome transmission and DNA repair in Saccharomyces cerevisiae. Genetics, 172, 2185-2200.
50. Stephan, A.K., Kliszczak, M., Dodson, H., Cooley, C. and Morrison, C.G. (2011) Roles of vertebrate Smc5 in sister chromatid cohesion and homologous recombinational repair. Mol. Cell. Biol., 31, 1369-1381.
51. Pebernard, S.,Wohlschlegel, J., McDonald, W.H., Yates, J.R. and Boddy, M.N. (2006) The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6 complex. Mol. Cell. Biol., 26, 1617-1630.
52. Bass, K.L., Murray, J.M. and O'Connell, M.J. (2012) Brc1-dependent recovery from replication stress. J. Cell Sci., 125, 2753-2764.
53. McDonald, W.H., Pavlova, Y., Yates, J.R. and Boddy, M.N. (2003) Novel essential DNA repair proteins Nse1 and Nse2 are subunits of the fission yeast Smc5-Smc6 complex. J. Biol. Chem., 278, 45460-45467.
54. Pebernard, S.,McDonald, W.H., Pavlova, Y., Yates, J.R. and Boddy, M.N. (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.
55. Verkade, H.M., Bugg, S.J., Lindsay, H.D., Carr, A.M. and O'Connell, M.J. (1999) Rad18 is required for DNA repair and checkpoint responses in fission yeast. Mol. Biol. Cell, 10, 2905-2918.
56. Lammens, A., Schele, A. and Hopfner, K.-P. (2004) Structural biochemistry of ATP-driven dimerization and DNA-stimulated activation of SMC ATPases. Curr. Biol., 14, 1778-1782.