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.
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 bythe protein complex cohesin, is essential for both chromosomesegregation and double-strand break (DSB) repair. Normally,cohesion formation is strictly limited to the S phase of thecell cycle, but DSBs can trigger cohesion also after DNA replicationhas been completed. The function of this damage-induced cohesionremains unknown. In this investigation, we show that damage-inducedcohesion is essential for repair in postreplicative cells inyeast. Furthermore, it is established genome-wide after inductionof a single DSB, and it is controlled by the DNA damage responseand cohesin-regulating factors. We thus define a cohesion establishmentpathway that is independent of DNA duplication and acts togetherwith cohesion formed during replication in sister chromatidbasedDSB 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}ki.se
The editors suggest the following Related Resources on Science sites:
In Science Magazine
PERSPECTIVES
Erwan Watrin and Jan-Michael Peters (13 July 2007) Science317 (5835), 209.
[DOI: 10.1126/science.1146072] |Summary »|Full Text »|PDF »
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.
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 »
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 »
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.
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.
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 »
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 »
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 »
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.
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 »
MOLECULAR BIOLOGY: How and When the Genome Sticks Together.