The Smc5/6 complex: More than repair?

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 75, Issue , 2010, Pages 179-187

  Kegel, A ^a   Sjogren C ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; COHESIN; CONDENSIN; HYDROXYUREA; MESYLIC ACID METHYL ESTER; SINGLE STRANDED DNA; STRUCTURAL MAINTENANCE OF CHROMOSOME 5 PROTEIN; STRUCTURAL MAINTENANCE OF CHROMOSOME 6 PROTEIN; SUMO 1 PROTEIN; UNCLASSIFIED DRUG; MULTIPROTEIN COMPLEX; PROTEINS BY CELLULAR COMPONENT;

ARTICLE; CHROMOSOME CONDENSATION; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; DNA DAMAGE; DNA HELIX; DNA PROTEIN COMPLEX; DNA REPAIR; DNA SYNTHESIS; DOUBLE STRANDED DNA BREAK; GENE CONVERSION; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; IONIZING RADIATION; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SISTER CHROMATID; SUMOYLATION; TELOMERE; CHROMOSOME; CHROMOSOME STRUCTURE; DNA STRUCTURE; MEMBRANE STRUCTURE;

CELL CYCLE PROTEINS; CHROMOSOMES, FUNGAL; DNA REPAIR; MODELS, BIOLOGICAL; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 80052393142     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2010.75.047     Document Type: Article

References (80)

1. Ampatzidou E, Irmisch A, O'Connell MJ, Murray JM. 2006. Smc5/6 is required for repair at collapsed replication forks. Mol Cell Biol 26: 9387-9401.
2. Andrews EA, Palecek J, Sergeant J, Taylor E, Lehmann AR, Watts FZ. 2005. 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.
3. Arumugam P, Gruber S, Tanaka K, Haering CH, Mechtler K, Nasmyth K. 2003. ATP hydrolysis is required for cohesin's association with chromosomes. Curr Biol 13: 1941-1953.
4. Behlke-Steinert S, Touat-Todeschini L, Skoufias DA, Margolis RL. 2009. SMC5 and MMS21 are required for chromosome cohesion and mitotic progression. Cell Cycle 8: 2211-2218.
5. Boddy MN, Shanahan P, McDonald WH, Lopez-Girona A, Noguchi E, Yates IJ, Russell P. 2003. Replication checkpoint kinase Cds1 regulates recombinational repair protein Rad60. Mol Cell Biol 23: 5939-5946.
6. Branzei D, Sollier J, Liberi G, Zhao X, Maeda D, Seki M, Enomoto T, Ohta K, Foiani M. 2006. Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127: 509-522.
7. Chen YH, Choi K, Szakal B, Arenz J, Duan X, Ye H, Branzei D, Zhao X. 2009. Interplay between the Smc5/6 complex and the Mph1 helicase in recombinational repair. Proc Natl Acad Sci 106: 21252-21257.
8. Chin JK, Bashkirov VI, Heyer WD, Romesberg FE. 2006. Esc4/Rtt107 and the control of recombination during replication. DNA Repair 5: 618-628.
9. Ciosk R, Shirayama M, Shevchenko A, Tanaka T, Toth A, Nasmyth K. 2000. Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. Mol Cell 5: 243-254.
10. Cost GJ, Cozzarelli NR. 2006. Smc5p promotes faithful chromosome transmission and DNA repair in Saccharomyces cerevisiae. Genetics 172: 2185-2200.
11. Cuperus G, Shore D. 2002. Restoration of silencing in Saccharomyces cerevisiae by tethering of a novel Sir2-interacting protein, Esc8. Genetics 162: 633-645.
12. D'Ambrosio C, Schmidt CK, Katou Y, Kelly G, Itoh T, Shirahige K, Uhlmann F. 2008. Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. Genes Dev 22: 2215-2227.
13. De Piccoli G, Cortes-Ledesma F, Ira G, Torres-Rosell J, Uhle S, Farmer S, Hwang JY, 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.
14. De Piccoli G, Torres-Rosell J, Aragon L. 2009. The unnamed complex: What do we know about Smc5-Smc6? Chromosome Res 17: 251-263.
15. Dhillon N, Kamakaka RT. 2000. A histone variant, Htz1p, and a Sir1p-like protein, Esc2p, mediate silencing at HMR. Mol Cell 6: 769-780.
16. Duan X, Sarangi P, Liu X, Rangi GK, Zhao X, Ye H. 2009a. Structural and functional insights into the roles of the Mms21 subunit of the Smc5/6 complex. Mol Cell 35: 657-668.
17. Duan X, Yang Y, Chen YH, Arenz J, Rangi GK, Zhao X, Ye H. 2009b. 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.
18. Fousteri MI, Lehmann AR. 2000. A novel SMC protein complex in Schizosaccharomyces pombe contains the Rad18 DNA repair protein. EMBO J 19: 1691-1702.
19. Fujioka Y, Kimata Y, Nomaguchi K, Watanabe K, Kohno K. 2002. Identification of a novel non-structural maintenance of chromosomes (SMC) component of the SMC5/SMC6 complex involved in DNA repair. J Biol Chem 277: 21585-21591.
20. Harvey SH, Sheedy DM, Cuddihy AR, O'Connell MJ. 2004. Coordination of DNA damage responses via the Smc5/Smc6 complex. Mol Cell Biol 24: 662-674.
21. Hazbun TR, Malmström L, Anderson S, Graczyk BJ, Fox B, Riffle M, Sundin BA, Aranda JD, McDonald WH, Chiu CH, et al. 2003. Assigning function to yeast proteins by integration of technologies. Mol Cell 12: 1353-1365.
22. Hirano T. 2006. At the heart of the chromosome: SMC proteins in action. Nat Rev Mol Cell Biol 7: 311-322.
23. Hu B, Liao C, Millson SH, Mollapour M, Prodromou C, Pearl LH, Piper PW, Panaretou B. 2005. Qri2/Nse4, a component of the essential Smc5/6 DNA repair complex. Mol Microbiol 55: 1735-1750.
24. Irmisch A, Ampatzidou E, Mizuno K, O'Connell MJ, Murray JM. 2009. Smc5/6 maintains stalled replication forks in a recombination-competent conformation. EMBO J 28: 144-155.
25. Kegel A, Betts-Lindroos H, Kanno T, Jeppsson K, Ström L, Katou Y, Itoh T, Shirahige K, Sjögren C. 2011. Chromosome length influences replication-induced topological stress. Nature 471: 392-396.
26. Kim JS, Krasieva TB, LaMorte V, Taylor AM, Yokomori K. 2002. Specific recruitment of human cohesin to laser-induced DNA damage. J Biol Chem 277: 45149-45153.
27. Kimura K, Hirano T. 1997. ATP-dependent positive supercoiling of DNA by 13S condensin: A biochemical implication for chromosome condensation. Cell 90: 625-634.
28. Kozak J, West CE, White C, da Costa-Nunes JA, Angelis KJ. 2009. Rapid repair of DNA double strand breaks in Arabidopsis thaliana is dependent on proteins involved in chromosome structure maintenance. DNA Repair 8: 413-419.
29. Lee K, Nizza S, Hayes T, Bass K, Irmish A, Murray J, O'Connell M. 2007. Brc1-mediated rescue of Smc5/6 deficiency: Requirement for multiple nucleases and a novel Rad18 function. Genetics 175: 1585-1595.
30. Lehmann AR., Walicka M, Griffiths DJ, Murray JM, Watts FZ, McCready S, Carr AM. 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.
31. Lindroos HB, Strom L, Itoh T, Katou Y, Shirahige K, Sjögren C. 2006. Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways. Mol Cell 22: 755-767.
32. Mankouri HW, Ngo HP, Hickson ID. 2009. Esc2 and Sgs1 act in functionally distinct branches of the homologous recombination repair pathway in Saccharomyces cerevisiae. Mol Biol Cell 20: 1683-1694.
33. McDonald WH, Pavlova Y, Yates JR III, Boddy MN. 2003. Novel essential DNA repair proteins Nse1 and Nse2 are subunits of the fission yeast Smc5-Smc6 complex. J Biol Chem 278: 45460-45467.
34. Mengiste T, Revenkova E, Bechtold N, Paszkowski J. 1999. An SMC-like protein is required for efficient homologous recombination in Arabidopsis. EMBO J 18: 4505-4512.
35. Miyabe I, Morishita T, Hishida T, Yonei S, Shinagawa H. 2006. 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.
36. Morikawa H, Morishita T, Kawane S, Iwasaki H, Carr AM, 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.
37. Morishita T, Tsutsui Y, Iwasaki H, Shinagawa H. 2002. The Schizosaccharomyces pombe rad60 gene is essential for repairing double-strand DNA breaks spontaneously occurring during replication and induced by DNA-damaging agents. Mol Cell Biol 22: 3537-3548.
38. Nasmyth K, Haering CH. 2005. The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74: 595-648.
39. Onoda F, Takeda M, Seki M, Maeda D, Tajima J, Ui A, Yagi H, Enomoto T. 2004. SMC6 is required for MMS-induced interchromosomal and sister chromatid recombinations in Saccharomyces cerevisiae. DNA Repair 3: 429-439.
40. Outwin EA, Irmisch A, Murray JM, O'Connell MJ. 2009. Smc5-Smc6-dependent removal of cohesin from mitotic chromosomes. Mol Cell Biol 29: 4363-4375.
41. Palecek J, Vidot S, Feng M, Doherty AJ, Lehmann AR. 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.
42. Pebernard S, McDonald WH, Pavlova Y, Yates JR III, Boddy MN. 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.
43. Pebernard S, Wohlschlegel J, McDonald WH, Yates JR III, Boddy MN. 2006. The Nse5-Nse6 dimer mediates DNA repair roles of the Smc5-Smc6 complex. Mol Cell Biol 26: 1617-1630.
44. Pebernard S, Perry JJ, Tainer JA, Boddy MN. 2008a. Nse1 RINGlike domain supports functions of the Smc5-Smc6 holocomplex in genome stability. Mol Biol Cell 19: 4099-4109.
45. Pebernard S, Schaffer L, Campbell D, Head SR, Boddy MN. 2008b. Localization of Smc5/6 to centromeres and telomeres requires heterochromatin and SUMO, respectively. EMBO J 27: 3011-3023.
46. Postow L, Crisona NJ, Peter BJ, Hardy CD, Cozzarelli NR. 2001. Topological challenges to DNA replication: Conformations at the fork. Proc Natl Acad Sci 98: 8219-8226.
47. Potts PR. 2009. The yin and yang of the MMS21-SMC5/6 SUMO ligase complex in homologous recombination. DNA Repair 8: 499-506.
48. Potts PR, Yu H. 2005. Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol Cell Biol 25: 7021-7032.
49. Potts PR, Yu H. 2007. The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomerebinding proteins. Nat Struct Mol Biol 14: 581-590.
50. Potts PR, Porteus MH, Yu H. 2006. Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks. EMBO J 25: 3377-3388.
51. Prudden J, Perry JJ, Arvai AS, Tainer JA, Boddy MN. 2009. Molecular mimicry of SUMO promotes DNA repair. Nat Struct Mol Biol 16: 509-516.
52. Raffa GD, Wohlschlegel J, Yates JR III, Boddy MN. 2006. SUMObinding motifs mediate the Rad60-dependent response to replicative stress and self-association. J Biol Chem 281: 27973-27981.
53. Roberts TM, Kobor MS, Bastin-Shanower SA, Ii M, Horte SA, Gin JW, Emili A, Rine J, Brill SJ, Brown GW. 2006. Slx4 regulates DNA damage checkpoint-dependent phosphorylation of the BRCT domain protein Rtt107/Esc4. Mol Biol Cell 17: 539-548.
54. Roberts TM, Zaidi IW, Vaisica JA, Peter M, Brown GW. 2008. Regulation of rtt107 recruitment to stalled DNA replication forks by the cullin rtt101 and the rtt109 acetyltransferase. Mol Biol Cell 19: 171-180.
55. Rouse J. 2004. Esc4p, a new target of Mec1p (ATR), promotes resumption of DNA synthesis after DNA damage. EMBO J 23: 1188-1197.
56. Santa Maria SR, Gangavarapu V, Johnson RE, Prakash L, Prakash S. 2007. Requirement of Nse1, a subunit of the Smc5-Smc6 complex, for Rad52-dependent postreplication repair of UVdamaged DNA in Saccharomyces cerevisiae. Mol Cell Biol 27: 8409-8418.
57. Sergeant J, Taylor E, Palecek J, Fousteri M, Andrews EA, Sweeney S, Shinagawa H, Watts FZ, Lehmann AR. 2005. Composition and architecture of the Schizosaccharomyces pombe Rad18 (Smc5-6) complex. Mol Cell Biol 25: 172-184.
58. Sheedy DM, Dimitrova D, Rankin JK, Bass KL, Lee KM, Tapia-Alveal C, Harvey SH, Murray JM, O'Connell MJ. 2005. Brc1-mediated DNA repair and damage tolerance. Genetics 171: 457-468.
59. Sjögren C, Nasmyth K. 2001. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr Biol 11: 991-995.
60. Sollier J, Driscoll R, Castellucci F, Foiani M, Jackson SP, 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.
61. Strom L, Lindroos HB, Shirahige K, Sjögren C. 2004. Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol Cell 16: 1003-1015.
62. Strom L, Karlsson C, Lindroos HB, Wedahl S, Katou Y, Shirahige K, Sjögren C. 2007. Postreplicative formation of cohesion is required for repair and induced by a single DNA break. Science 317: 242-245.
63. Takahashi Y, Dulev S, Liu X, Hiller NJ, Zhao X, Strunnikov A. 2008. Cooperation of sumoylated chromosomal proteins in rDNA maintenance. PLoS Genet 4: e1000215.
64. Taylor EM, Moghraby JS, Lees JH, Smit B, Moens PB, Lehmann AR. 2001. Characterization of a novel human SMC heterodimer homologous to the Schizosaccharomyces pombe Rad18/Spr18 complex. Mol Biol Cell 12: 1583-1594.
65. Taylor EM, Copsey AC, Hudson JJ, Vidot S, Lehmann AR. 2008. Identification of the proteins, including MAGEG1, that make up the human SMC5-6 protein complex. Mol Cell Biol 28: 1197-1206.
66. Terret ME, Sherwood R, Rahman S, Qin J, Jallepalli PV. 2009. Cohesin acetylation speeds the replication fork. Nature 462: 231-234.
67. Torres-Rosell J, Machin F, Aragon L. 2005a. Smc5-Smc6 complex preserves nucleolar integrity in S. cerevisiae. Cell Cycle 4: 868-872.
68. Torres-Rosell J, Machin F, Farmer S, Jarmuz A, Eydmann T, Dalgaard JZ, Aragon L. 2005b. SMC5 and SMC6 genes are required for the segregation of repetitive chromosome regions. Nat Cell Biol 7: 412-419.
69. Torres-Rosell J, De Piccoli G, Cordon-Preciado V, Farmer S, Jarmuz A, Machin F, Pasero P, Lisby M, Haber JE, Aragon L. 2007a. Anaphase onset before complete DNA replication with intact checkpoint responses. Science 315: 1411-1415.
70. Torres-Rosell J, Sunjevaric I, De Piccoli G, Sacher M, Eckert-Boulet N, Reid R, Jentsch S, Rothstein R, Aragon L, Lisby M. 2007b. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat Cell Biol 9: 923-931.
71. Tsuyama T, Inou K, Seki M, Seki T, Kumata Y, Kobayashi T, Kimura K, Hanaoka F, Enomoto T, Tada S. 2006. Chromatin loading of Smc5/6 is induced by DNA replication but not by DNA double-strand breaks. Biochem Biophys Res Commun 351: 935-939.
72. Uemura T, Yanagida M. 1984. Isolation of type I and II DNA topoisomerase mutants from fission yeast: Single and double mutants show different phenotypes in cell growth and chromatin organization. EMBO J 3: 1737-1744.
73. Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber JE, Koshland D. 2004. DNA damage response pathway uses histone modification to assemble a double-strand break-specific co-hesin domain. Mol Cell 16: 991-1002.
74. Unal E, Heidinger-Pauli JM, Koshland D. 2007. DNA doublestrand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7). Science 317: 245-248.
75. Verkade HM, Bugg SJ, Lindsay HD, Carr AM, O'Connell MJ. 1999. Rad18 is required for DNA repair and checkpoint responses in fission yeast. Mol Biol Cell 10: 2905-2918.
76. Wang JC. 2002 Cellular roles of DNA topoisomerases: A molecular perspective. Nat Rev Mol Cell Biol 3: 430-440.
77. Weitzer S, Lehane C, Uhlmann F. 2003. A model for ATP hydrolysis-dependent binding of cohesin to DNA. Curr Biol 13: 1930-1940.
78. Wendt KS, Peters JM. 2009. How cohesin and CTCF cooperate in regulating gene expression. Chromosome Res 17: 201-214.
79. Yu Q, Kuzmiak H, Olsen L, Kulkarni A, Fink E, Zou Y, Bi X. 2010. Saccharomyces cerevisiae Esc2p interacts with Sir2p through a small ubiquitin-like modifier (SUMO)-binding motif and regulates transcriptionally silent chromatin in a locus-dependent manner. J Biol Chem 285: 7525-7536.
80. Zhao X, Blobel G. 2005. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc Natl Acad Sci 102: 4777-4782.