Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.


Logo for

Science 317 (5835): 242-245

Copyright © 2007 by the American Association for the Advancement of Science

Postreplicative Formation of Cohesion Is Required for Repair and Induced by a Single DNA Break

Lena Ström,1 Charlotte Karlsson,1 Hanna Betts Lindroos,1 Sara Wedahl,1 Yuki Katou,2 Katsuhiko Shirahige,2 Camilla Sjögren1*

Abstract: Sister-chromatid cohesion, established during replication by the protein complex cohesin, is essential for both chromosome segregation and double-strand break (DSB) repair. Normally, cohesion formation is strictly limited to the S phase of the cell cycle, but DSBs can trigger cohesion also after DNA replication has been completed. The function of this damage-induced cohesion remains unknown. In this investigation, we show that damage-induced cohesion is essential for repair in postreplicative cells in yeast. Furthermore, it is established genome-wide after induction of a single DSB, and it is controlled by the DNA damage response and cohesin-regulating factors. We thus define a cohesion establishment pathway that is independent of DNA duplication and acts together with cohesion formed during replication in sister chromatid–based DSB repair.

1 Department of Cell and Molecular Biology, Karolinska Institute, 171 77 Stockholm, Sweden.
2 Gene Research Centre, Tokyo Institute of Technology, 4259 Nagatsuta, Midori-ku, 226-8501 Yokohama, Japan.

* To whom correspondence should be addressed. E-mail: camilla.sjogren{at}

The cohesin acetyltransferase Eco1 coordinates rDNA replication and transcription.
S. Lu, K. K. Lee, B. Harris, B. Xiong, T. Bose, A. Saraf, G. Hattem, L. Florens, C. Seidel, and J. L. Gerton (2014)
   Abstract »    Full Text »    PDF »
Distinct Functions of Human Cohesin-SA1 and Cohesin-SA2 in Double-Strand Break Repair.
X. Kong, A. R. Ball Jr., H. X. Pham, W. Zeng, H.-Y. Chen, J. A. Schmiesing, J.-S. Kim, M. Berns, and K. Yokomori (2014)
Mol. Cell. Biol. 34, 685-698
   Abstract »    Full Text »    PDF »
The Sister Chromatid Cohesion Pathway Suppresses Multiple Chromosome Gain and Chromosome Amplification.
S. Covo, C. M. Puccia, J. L. Argueso, D. A. Gordenin, and M. A. Resnick (2014)
Genetics 196, 373-384
   Abstract »    Full Text »    PDF »
Chromosome Segregation in Budding Yeast: Sister Chromatid Cohesion and Related Mechanisms.
A. L. Marston (2014)
Genetics 196, 31-63
   Abstract »    Full Text »    PDF »
Stress-induced Condensation of Bacterial Genomes Results in Re-pairing of Sister Chromosomes: IMPLICATIONS FOR DOUBLE STRAND DNA BREAK REPAIR.
N. Shechter, L. Zaltzman, A. Weiner, V. Brumfeld, E. Shimoni, Y. Fridmann-Sirkis, and A. Minsky (2013)
J. Biol. Chem. 288, 25659-25667
   Abstract »    Full Text »    PDF »
Cohesin codes - interpreting chromatin architecture and the many facets of cohesin function.
S. Rudra and R. V. Skibbens (2013)
J. Cell Sci. 126, 31-41
   Abstract »    Full Text »    PDF »
Sister Chromatid Cohesion.
J.-M. Peters and T. Nishiyama (2012)
Cold Spring Harb Perspect Biol 4, a011130
   Abstract »    Full Text »    PDF »
Radiation-induced double-strand breaks require ATM but not Artemis for homologous recombination during S-phase.
S. Kocher, T. Rieckmann, G. Rohaly, W. Y. Mansour, E. Dikomey, I. Dornreiter, and J. Dahm-Daphi (2012)
Nucleic Acids Res. 40, 8336-8347
   Abstract »    Full Text »    PDF »
Scc1 sumoylation by Mms21 promotes sister chromatid recombination through counteracting Wapl.
N. Wu, X. Kong, Z. Ji, W. Zeng, P. R. Potts, K. Yokomori, and H. Yu (2012)
Genes & Dev. 26, 1473-1485
   Abstract »    Full Text »    PDF »
Acetylation of the SUN protein Mps3 by Eco1 regulates its function in nuclear organization.
S. Ghosh, J. M. Gardner, C. J. Smoyer, J. M. Friederichs, J. R. Unruh, B. D. Slaughter, R. Alexander, R. D. Chisholm, K. K. Lee, J. L. Workman, et al. (2012)
Mol. Biol. Cell 23, 2546-2559
   Abstract »    Full Text »    PDF »
Cohesin-independent segregation of sister chromatids in budding yeast.
V. Guacci and D. Koshland (2012)
Mol. Biol. Cell 23, 729-739
   Abstract »    Full Text »    PDF »
Gene Regulation by Cohesin in Cancer: Is the Ring an Unexpected Party to Proliferation?.
J. M. Rhodes, M. McEwan, and J. A. Horsfield (2011)
Mol. Cancer Res. 9, 1587-1607
   Abstract »    Full Text »    PDF »
Calpain-1 Cleaves Rad21 To Promote Sister Chromatid Separation.
A. K. Panigrahi, N. Zhang, Q. Mao, and D. Pati (2011)
Mol. Cell. Biol. 31, 4335-4347
   Abstract »    Full Text »    PDF »
RSC Facilitates Rad59-Dependent Homologous Recombination between Sister Chromatids by Promoting Cohesin Loading at DNA Double-Strand Breaks.
J.-H. Oum, C. Seong, Y. Kwon, J.-H. Ji, A. Sid, S. Ramakrishnan, G. Ira, A. Malkova, P. Sung, S. E. Lee, et al. (2011)
Mol. Cell. Biol. 31, 3924-3937
   Abstract »    Full Text »    PDF »
Psm3 Acetylation on Conserved Lysine Residues Is Dispensable for Viability in Fission Yeast but Contributes to Eso1-Mediated Sister Chromatid Cohesion by Antagonizing Wpl1.
A. Feytout, S. Vaur, S. Genier, S. Vazquez, and J.-P. Javerzat (2011)
Mol. Cell. Biol. 31, 1771-1786
   Abstract »    Full Text »    PDF »
The Smc5/6 Complex: More Than Repair?.
A. Kegel and C. Sjogren (2011)
Cold Spring Harb Symp Quant Biol
   Abstract »    PDF »
Roles of Vertebrate Smc5 in Sister Chromatid Cohesion and Homologous Recombinational Repair.
A. K. Stephan, M. Kliszczak, H. Dodson, C. Cooley, and C. G. Morrison (2011)
Mol. Cell. Biol. 31, 1369-1381
   Abstract »    Full Text »    PDF »
A new meiosis-specific cohesin complex implicated in the cohesin code for homologous pairing.
K.-i. Ishiguro, J. Kim, S. Fujiyama-Nakamura, S. Kato, and Y. Watanabe (2011)
EMBO Rep. 12, 267-275
   Abstract »    Full Text »    PDF »
The splicing-factor related protein SFPQ/PSF interacts with RAD51D and is necessary for homology-directed repair and sister chromatid cohesion.
C. Rajesh, D. K. Baker, A. J. Pierce, and D. L. Pittman (2011)
Nucleic Acids Res. 39, 132-145
   Abstract »    Full Text »    PDF »
Rec8-containing cohesin maintains bivalents without turnover during the growing phase of mouse oocytes.
K. Tachibana-Konwalski, J. Godwin, L. van der Weyden, L. Champion, N. R. Kudo, D. J. Adams, and K. Nasmyth (2010)
Genes & Dev. 24, 2505-2516
   Abstract »    Full Text »    PDF »
The hsSsu72 phosphatase is a cohesin-binding protein that regulates the resolution of sister chromatid arm cohesion.
H.-S. Kim, K.-H. Baek, G.-H. Ha, J.-C. Lee, Y.-N. Kim, J. Lee, H.-Y. Park, N. R. Lee, H. Lee, Y. Cho, et al. (2010)
EMBO J. 29, 3544-3557
   Abstract »    Full Text »    PDF »
Genome-wide Reinforcement of Cohesin Binding at Pre-existing Cohesin Sites in Response to Ionizing Radiation in Human Cells.
B.-J. Kim, Y. Li, J. Zhang, Y. Xi, Y. Li, T. Yang, S. Y. Jung, X. Pan, R. Chen, W. Li, et al. (2010)
J. Biol. Chem. 285, 22784-22792
   Abstract »    Full Text »    PDF »
Mek1 Suppression of Meiotic Double-Strand Break Repair Is Specific to Sister Chromatids, Chromosome Autonomous and Independent of Rec8 Cohesin Complexes.
T. L. Callender and N. M. Hollingsworth (2010)
Genetics 185, 771-782
   Abstract »    Full Text »    PDF »
Structure and DNA binding activity of the mouse condensin hinge domain highlight common and diverse features of SMC proteins.
J. J. Griese, G. Witte, and K.-P. Hopfner (2010)
Nucleic Acids Res. 38, 3454-3465
   Abstract »    Full Text »    PDF »
The human intra-S checkpoint response to UVC-induced DNA damage.
W. K. Kaufmann (2010)
Carcinogenesis 31, 751-765
   Abstract »    Full Text »    PDF »
Drf1-dependent Kinase Interacts with Claspin through a Conserved Protein Motif.
D. A. Gold and W. G. Dunphy (2010)
J. Biol. Chem. 285, 12638-12646
   Abstract »    Full Text »    PDF »
Cohesinopathies, gene expression, and chromatin organization.
T. Bose and J. L. Gerton (2010)
J. Cell Biol. 189, 201-210
   Abstract »    Full Text »    PDF »
Mechanics of DNA bridging by bacterial condensin MukBEF in vitro and in singulo.
Z. M. Petrushenko, Y. Cui, W. She, and V. V. Rybenkov (2010)
EMBO J. 29, 1126-1135
   Abstract »    Full Text »    PDF »
Human Timeless and Tipin stabilize replication forks and facilitate sister-chromatid cohesion.
A. R. Leman, C. Noguchi, C. Y. Lee, and E. Noguchi (2010)
J. Cell Sci. 123, 660-670
   Abstract »    Full Text »    PDF »
Yeast cohesin complex embraces 2 micron plasmid sisters in a tri-linked catenane complex.
S. K. Ghosh, C.-C. Huang, S. Hajra, and M. Jayaram (2010)
Nucleic Acids Res. 38, 570-584
   Abstract »    Full Text »    PDF »
Cohesin promotes the repair of ionizing radiation-induced DNA double-strand breaks in replicated chromatin.
C. Bauerschmidt, C. Arrichiello, S. Burdak-Rothkamm, M. Woodcock, M. A. Hill, D. L. Stevens, and K. Rothkamm (2010)
Nucleic Acids Res. 38, 477-487
   Abstract »    Full Text »    PDF »
Increased sister chromatid cohesion and DNA damage response factor localization at an enzyme-induced DNA double-strand break in vertebrate cells.
H. Dodson and C. G. Morrison (2009)
Nucleic Acids Res. 37, 6054-6063
   Abstract »    Full Text »    PDF »
The Scc2/Scc4 cohesin loader determines the distribution of cohesin on budding yeast chromosomes.
I. Kogut, J. Wang, V. Guacci, R. K. Mistry, and P. C. Megee (2009)
Genes & Dev. 23, 2345-2357
   Abstract »    Full Text »    PDF »
A matter of choice: the establishment of sister chromatid cohesion.
F. Uhlmann (2009)
EMBO Rep. 10, 1095-1102
   Abstract »    Full Text »    PDF »
The cohesin complex is required for the DNA damage-induced G2/M checkpoint in mammalian cells.
E. Watrin and J.-M. Peters (2009)
EMBO J. 28, 2625-2635
   Abstract »    Full Text »    PDF »
The STRUCTURAL MAINTENANCE OF CHROMOSOMES 5/6 Complex Promotes Sister Chromatid Alignment and Homologous Recombination after DNA Damage in Arabidopsis thaliana.
K. Watanabe, M. Pacher, S. Dukowic, V. Schubert, H. Puchta, and I. Schubert (2009)
PLANT CELL 21, 2688-2699
   Abstract »    Full Text »    PDF »
Smc5-Smc6-Dependent Removal of Cohesin from Mitotic Chromosomes.
E. A. Outwin, A. Irmisch, J. M. Murray, and M. J. O'Connell (2009)
Mol. Cell. Biol. 29, 4363-4375
   Abstract »    Full Text »    PDF »
Screen for DNA-damage-responsive histone modifications identifies H3K9Ac and H3K56Ac in human cells.
J. V. Tjeertes, K. M. Miller, and S. P. Jackson (2009)
EMBO J. 28, 1878-1889
   Abstract »    Full Text »    PDF »
The Dot1 Histone Methyltransferase and the Rad9 Checkpoint Adaptor Contribute to Cohesin-Dependent Double-Strand Break Repair by Sister Chromatid Recombination in Saccharomyces cerevisiae.
F. Conde, E. Refolio, V. Cordon-Preciado, F. Cortes-Ledesma, L. Aragon, A. Aguilera, and P. A. San-Segundo (2009)
Genetics 182, 437-446
   Abstract »    Full Text »    PDF »
Cornelia de Lange syndrome mutations in SMC1A or SMC3 affect binding to DNA.
E. Revenkova, M. L. Focarelli, L. Susani, M. Paulis, M. T. Bassi, L. Mannini, A. Frattini, D. Delia, I. Krantz, P. Vezzoni, et al. (2009)
Hum. Mol. Genet. 18, 418-427
   Abstract »    Full Text »    PDF »
The Evolution of Meiosis From Mitosis.
A. S. Wilkins and R. Holliday (2009)
Genetics 181, 3-12
   Full Text »    PDF »
Localization of Smc5/6 to centromeres and telomeres requires heterochromatin and SUMO, respectively.
S. Pebernard, L. Schaffer, D. Campbell, S. R. Head, and M. N. Boddy (2008)
EMBO J. 27, 3011-3023
   Abstract »    Full Text »    PDF »
The cohesin complex and its roles in chromosome biology.
J.-M. Peters, A. Tedeschi, and J. Schmitz (2008)
Genes & Dev. 22, 3089-3114
   Abstract »    Full Text »    PDF »
Sister Chromatid Cohesion Role for CDC28-CDK in Saccharomyces cerevisiae.
A. Brands and R. V. Skibbens (2008)
Genetics 180, 7-16
   Abstract »    Full Text »    PDF »
Eco1-Dependent Cohesin Acetylation During Establishment of Sister Chromatid Cohesion.
T. R. Ben-Shahar, S. Heeger, C. Lehane, P. East, H. Flynn, M. Skehel, and F. Uhlmann (2008)
Science 321, 563-566
   Abstract »    Full Text »    PDF »
A Molecular Determinant for the Establishment of Sister Chromatid Cohesion.
E. Unal, J. M. Heidinger-Pauli, W. Kim, V. Guacci, I. Onn, S. P. Gygi, and D. E. Koshland (2008)
Science 321, 566-569
   Abstract »    Full Text »    PDF »
The molecular mechanism underlying Roberts syndrome involves loss of ESCO2 acetyltransferase activity.
M. Gordillo, H. Vega, A. H. Trainer, F. Hou, N. Sakai, R. Luque, H. Kayserili, S. Basaran, F. Skovby, R. C. M. Hennekam, et al. (2008)
Hum. Mol. Genet. 17, 2172-2180
   Abstract »    Full Text »    PDF »
Chromosome cohesion - rings, knots, orcs and fellowship.
L. A. Diaz-Martinez, J. F. Gimenez-Abian, and D. J. Clarke (2008)
J. Cell Sci. 121, 2107-2114
   Abstract »    Full Text »    PDF »
Cell-cycle regulation of cohesin stability along fission yeast chromosomes.
P. Bernard, C. K. Schmidt, S. Vaur, S. Dheur, J. Drogat, S. Genier, K. Ekwall, F. Uhlmann, and J.-P. Javerzat (2008)
EMBO J. 27, 111-121
   Abstract »    Full Text »    PDF »
MOLECULAR BIOLOGY: How and When the Genome Sticks Together.
E. Watrin and J.-M. Peters (2007)
Science 317, 209-210
   Abstract »    Full Text »    PDF »
DNA Double-Strand Breaks Trigger Genome-Wide Sister-Chromatid Cohesion Through Eco1 (Ctf7).
E. Unal, J. M. Heidinger-Pauli, and D. Koshland (2007)
Science 317, 245-248
   Abstract »    Full Text »    PDF »

To Advertise     Find Products

Science Signaling. ISSN 1937-9145 (online), 1945-0877 (print). Pre-2008: Science's STKE. ISSN 1525-8882