SUMOylation of the α-kleisin subunit of cohesin is required for DNA damage-induced cohesion

Current Biology

Volumn 22, Issue 17, 2012, Pages 1564-1575

  McAleenan, Alexandra ^a   Cordon Preciado, Violeta ^a   Clemente Blanco, Andres ^a   Liu, I Chun ^a   Sen, Nicholas ^a   Leonard, Joanne ^a   Jarmuz, Adam ^a   Aragón, Luis ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CYCLE PROTEIN; COHESIN; MCD1 PROTEIN, S CEREVISIAE; NONHISTONE PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CHROMATID; CHROMOSOME SEGREGATION; DNA DAMAGE; DOUBLE STRANDED DNA BREAK; GENETICS; METABOLISM; PHYSIOLOGY; SACCHAROMYCES CEREVISIAE; SUMOYLATION;

CELL CYCLE PROTEINS; CHROMATIDS; CHROMOSOMAL PROTEINS, NON-HISTONE; CHROMOSOME SEGREGATION; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUMOYLATION;

EID: 84866148011     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2012.06.045     Document Type: Article

References (38)

1. I. Onn, J.M. Heidinger-Pauli, V. Guacci, E. Unal, and D.E. Koshland Sister chromatid cohesion: a simple concept with a complex reality Annu. Rev. Cell Dev. Biol. 24 2008 105 129
2. K. Nasmyth Segregating sister genomes: the molecular biology of chromosome separation Science 297 2002 559 565 (Pubitemid 34815333)
3. F. Uhlmann, and K. Nasmyth Cohesion between sister chromatids must be established during DNA replication Curr. Biol. 8 1998 1095 1101 (Pubitemid 28501371)
4. F. Uhlmann, F. Lottspeich, and K. Nasmyth Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1 Nature 400 1999 37 42 (Pubitemid 29315102)
5. F. Cortés-Ledesma, and A. Aguilera Double-strand breaks arising by replication through a nick are repaired by cohesin-dependent sister-chromatid exchange EMBO Rep. 7 2006 919 926 (Pubitemid 44523972)
6. E. Unal, A. Arbel-Eden, U. Sattler, R. Shroff, M. Lichten, J.E. Haber, and D. Koshland DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain Mol. Cell 16 2004 991 1002 (Pubitemid 40018408)
7. L. Ström, H.B. Lindroos, K. Shirahige, and C. Sjögren Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair Mol. Cell 16 2004 1003 1015 (Pubitemid 40018409)
8. L. Ström, C. Karlsson, H.B. Lindroos, S. Wedahl, Y. Katou, K. Shirahige, and C. Sjögren Postreplicative formation of cohesion is required for repair and induced by a single DNA break Science 317 2007 242 245 (Pubitemid 47076199)
9. E. Unal, J.M. Heidinger-Pauli, and D. Koshland DNA double-strand breaks trigger genome-wide sister-chromatid cohesion through Eco1 (Ctf7) Science 317 2007 245 248 (Pubitemid 47076200)
10. J.S. Kim, T.B. Krasieva, V. LaMorte, A.M. Taylor, and K. Yokomori Specific recruitment of human cohesin to laser-induced DNA damage J. Biol. Chem. 277 2002 45149 45153 (Pubitemid 36159117)
11. S. Bekker-Jensen, C. Lukas, R. Kitagawa, F. Melander, M.B. Kastan, J. Bartek, and J. Lukas Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks J. Cell Biol. 173 2006 195 206
12. P.R. Potts, M.H. Porteus, and H. Yu Human SMC5/6 complex promotes sister chromatid homologous recombination by recruiting the SMC1/3 cohesin complex to double-strand breaks EMBO J. 25 2006 3377 3388 (Pubitemid 44141795)
13. J.M. Heidinger-Pauli, E. Unal, V. Guacci, and D. Koshland The kleisin subunit of cohesin dictates damage-induced cohesion Mol. Cell 31 2008 47 56 (Pubitemid 351905925)
14. J.M. Heidinger-Pauli, E. Unal, and D. Koshland Distinct targets of the Eco1 acetyltransferase modulate cohesion in S phase and in response to DNA damage Mol. Cell 34 2009 311 321
15. B.D. Rowland, M.B. Roig, T. Nishino, A. Kurze, P. Uluocak, A. Mishra, F. Beckouët, P. Underwood, J. Metson, and R. Imre Building sister chromatid cohesion: smc3 acetylation counteracts an antiestablishment activity Mol. Cell 33 2009 763 774
16. T. Rolef Ben-Shahar, S. Heeger, C. Lehane, P. East, H. Flynn, M. Skehel, and F. Uhlmann Eco1-dependent cohesin acetylation during establishment of sister chromatid cohesion Science 321 2008 563 566
17. E. Unal, J.M. Heidinger-Pauli, W. Kim, V. Guacci, I. Onn, S.P. Gygi, and D.E. Koshland A molecular determinant for the establishment of sister chromatid cohesion Science 321 2008 566 569
18. W. Zhou, J.J. Ryan, and H. Zhou Global analyses of sumoylated proteins in Saccharomyces cerevisiae. Induction of protein sumoylation by cellular stresses J. Biol. Chem. 279 2004 32262 32268 (Pubitemid 39014675)
19. V.G. Panse, U. Hardeland, T. Werner, B. Kuster, and E. Hurt A proteome-wide approach identifies sumoylated substrate proteins in yeast J. Biol. Chem. 279 2004 41346 41351 (Pubitemid 39313573)
20. J.A. Wohlschlegel, E.S. Johnson, S.I. Reed, and J.R. Yates 3rd Global analysis of protein sumoylation in Saccharomyces cerevisiae J. Biol. Chem. 279 2004 45662 45668 (Pubitemid 39491554)
21. C. Denison, A.D. Rudner, S.A. Gerber, C.E. Bakalarski, D. Moazed, and S.P. Gygi A proteomic strategy for gaining insights into protein sumoylation in yeast Mol. Cell. Proteomics 4 2005 246 254 (Pubitemid 40439768)
22. J.T. Hannich, A. Lewis, M.B. Kroetz, S.J. Li, H. Heide, A. Emili, and M. Hochstrasser Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae J. Biol. Chem. 280 2005 4102 4110 (Pubitemid 40288574)
23. Y. Takahashi, S. Dulev, X. Liu, N.J. Hiller, X. Zhao, and A. Strunnikov Cooperation of sumoylated chromosomal proteins in rDNA maintenance PLoS Genet. 4 2008 e1000215
24. X. Zhao, and G. Blobel A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization Proc. Natl. Acad. Sci. USA 102 2005 4777 4782 (Pubitemid 40471530)
25. E.A. Andrews, J. Palecek, J. Sergeant, E. Taylor, A.R. Lehmann, and F.Z. Watts Nse2, a component of the Smc5-6 complex, is a SUMO ligase required for the response to DNA damage Mol. Cell. Biol. 25 2005 185 196 (Pubitemid 40039810)
26. G. De Piccoli, F. Cortes-Ledesma, G. Ira, J. Torres-Rosell, S. Uhle, S. Farmer, J.Y. Hwang, F. Machin, A. Ceschia, and A. McAleenan Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination Nat. Cell Biol. 8 2006 1032 1034 (Pubitemid 44314736)
27. H.B. Lindroos, L. Ström, T. Itoh, Y. Katou, K. Shirahige, and C. Sjögren Chromosomal association of the Smc5/6 complex reveals that it functions in differently regulated pathways Mol. Cell 22 2006 755 767
28. C.A. Cremona, P. Sarangi, Y. Yang, L.E. Hang, S. Rahman, and X. Zhao Extensive DNA damage-induced sumoylation contributes to replication and repair and acts in addition to the mec1 checkpoint Mol. Cell 45 2012 422 432
29. F. Pâques, and J.E. Haber Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae Microbiol. Mol. Biol. Rev. 63 1999 349 404 (Pubitemid 29264976)
30. J.A. Tercero, M.P. Longhese, and J.F. Diffley A central role for DNA replication forks in checkpoint activation and response Mol. Cell 11 2003 1323 1336 (Pubitemid 36645150)
31. J.E. Haber Uses and abuses of HO endonuclease Methods Enzymol. 350 2002 141 164 (Pubitemid 34619489)
32. P.R. Potts, and H. Yu Human MMS21/NSE2 is a SUMO ligase required for DNA repair Mol. Cell. Biol. 25 2005 7021 7032 (Pubitemid 41105901)
33. G.R. Bylebyl, I. Belichenko, and E.S. Johnson The SUMO isopeptidase Ulp2 prevents accumulation of SUMO chains in yeast J. Biol. Chem. 278 2003 44113 44120 (Pubitemid 37377153)
34. S. Almedawar, N. Colomina, M. Bermúdez-López, I. Pociño-Merino, and J. Torres-Rosell A SUMO-dependent step during establishment of sister chromatid cohesion Curr. Bio. 2012 10.1016/j.cub.2012. 06.046 Published online July 5, 2012
35. T. Tanaka, M.P. Cosma, K. Wirth, and K. Nasmyth Identification of cohesin association sites at centromeres and along chromosome arms Cell 98 1999 847 858 (Pubitemid 29446901)
36. C. Hoege, B. Pfander, G.L. Moldovan, G. Pyrowolakis, and S. Jentsch RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO Nature 419 2002 135 141 (Pubitemid 35025438)
37. M. Sacher, B. Pfander, C. Hoege, and S. Jentsch Control of Rad52 recombination activity by double-strand break-induced SUMO modification Nat. Cell Biol. 8 2006 1284 1290 (Pubitemid 44660594)
38. M.A. Roy, N. Siddiqui, and D. D'Amours Dynamic and selective DNA-binding activity of Smc5, a core component of the Smc5-Smc6 complex Cell Cycle 10 2011 690 700