Structural analysis of shu proteins reveals a DNA binding role essential for resisting damage

Journal of Biological Chemistry

Volumn 287, Issue 24, 2012, Pages 20231-20239

  Tao, Yuyong ^a,b   Li, Xu ^a,b   Liu, Yiwei ^a,b   Ruan, Jianbin ^a,b   Qi, Shali ^a,b   Niu, Liwen ^a,b   Teng, Maikun ^a,b  

^a UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ATPASE CORE DOMAIN; DNA BINDING; DNA BINDING ACTIVITY; DNA DAMAGES; GENOMIC STABILITY; HETERODIMERS; HOMOLOGOUS RECOMBINATION; HYDROPHOBIC CORE; NUCLEOPROTEIN FILAMENTS; STRUCTURAL INFORMATION; STRUCTURE-BASED;

BINDING SITES; NUCLEIC ACIDS; PROTEINS;

COMPLEXATION;

ADENOSINE TRIPHOSPHATASE; FUNGAL PROTEIN; HETERODIMER; NUCLEOPROTEIN; PROTEIN CSM2; PROTEIN PSY3; RAD51 PROTEIN; THIOMESYLIC ACID METHYL ESTER; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA DAMAGE; DNA REPAIR; HYDROPHOBICITY; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; SACCHAROMYCES CEREVISIAE; STRUCTURAL HOMOLOGY; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

CRYSTALLOGRAPHY, X-RAY; DNA, FUNGAL; DNA-BINDING PROTEINS; HUMANS; MULTIPROTEIN COMPLEXES; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84862006681     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.334698     Document Type: Article

References (32)

1. Jackson, S. P., and Bartek, J. (2009) The DNA-damage response in human biology and disease. Nature 461, 1071-1078
2. Ciccia, A., and Elledge, S. J. (2010) The DNA damage response. Making it safe to play with knives. Mol. Cell 40, 179-204
3. Broomfield, S., Hryciw, T., and Xiao, W. (2001) DNA postreplication repair and mutagenesis in Saccharomyces cerevisiae. Mutat. Res. 486, 167-184 (Pubitemid 32675329)
4. Barbour, L., and Xiao, W. (2003) Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability. A yeast model. Mutat. Res. 532, 137-155 (Pubitemid 37487851)
5. Hoege, C., Pfander, B., Moldovan, G. L., Pyrowolakis, G., and Jentsch, S. (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135-141 (Pubitemid 35025438)
6. Hofmann, R. M., and Pickart, C. M. (1999) Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96, 645-653 (Pubitemid 29122807)
7. Brusky, J., Zhu, Y., and Xiao, W. (2000) UBC13, a DNA-damage-inducible gene, is a member of the error-free postreplication repair pathway in Saccharomyces cerevisiae. Curr. Genet. 37, 168-174 (Pubitemid 30198928)
8. Ulrich, H. D., and Jentsch, S. (2000) Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J. 19, 3388-3397 (Pubitemid 30428216)
9. Ball, L. G., Zhang, K., Cobb, J. A., Boone, C., and Xiao, W. (2009) The yeast Shu complex couples error-free post-replication repair to homologous recombination. Mol. Microbiol. 73, 89-102
10. Shor, E., Weinstein, J., and Rothstein, R. (2005) A genetic screen for top3 suppressors in Saccharomyces cerevisiae identifies SHU1, SHU2, PSY3, and CSM2. Four genes involved in error-free DNA repair. Genetics 169, 1275-1289 (Pubitemid 40547442)
11. Mankouri, H. W., Ngo, H. P., and Hickson, I. D. (2007) Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1-Rmi1-Top3. Mol. Biol. Cell 18, 4062-4073 (Pubitemid 47519496)
12. Wu, L., and Hickson, I. D. (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870-874 (Pubitemid 38056876)
13. Krejci, L., Van Komen, S., Li, Y., Villemain, J., Reddy, M. S., Klein, H., Ellenberger, T., and Sung, P. (2003) DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423, 305-309 (Pubitemid 40852702)
14. Veaute, X., Jeusset, J., Soustelle, C., Kowalczykowski, S. C., Le Cam, E., and Fabre, F. (2003) The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423, 309-312 (Pubitemid 40852703)
15. German, J. (1993) Bloom syndrome. A Mendelian prototype of somatic mutational disease. Medicine 72, 393-406
16. Bernstein, K. A., Reid, R. J., Sunjevaric, I., Demuth, K., Burgess, R. C., and Rothstein, R. (2011) The Shu complex, which contains Rad51 paralogues, promotes DNA repair through inhibition of the Srs2 anti-recombinase. Mol. Biol. Cell 22, 1599-1607
17. Martín, V., Chahwan, C., Gao, H., Blais, V., Wohlschlegel, J., Yates, J. R., 3rd, McGowan, C. H., and Russell, P. (2006) Sws1 is a conserved regulator of homologous recombination in eukaryotic cells. EMBO J. 25, 2564-2574 (Pubitemid 44012238)
18. Otwinowski, Z., and Minor, W. (1997) Processing of x-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
19. Collaborative Computational Project No. 4 (1994) The CCP4 suite. Programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
20. Terwilliger, T. C., and Berendzen, J. (1999) Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55, 849-861 (Pubitemid 29194533)
21. Terwilliger, T. C. (2003) Automated main chain model building by template matching and iterative fragment extension. Acta Crystallogr. D Biol. Crystallogr. 59, 38-44
22. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
23. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
24. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
25. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, W. B., 3rd, Snoeyink, J., Richardson, J. S., and Richardson, D. C. (2007) MolProbity. All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
26. Pellegrini, L., Yu, D. S., Lo, T., Anand, S., Lee, M., Blundell, T. L., and Venkitaraman, A. R. (2002) Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature 420, 287-293 (Pubitemid 35398178)
27. Shin, D. S., Pellegrini, L., Daniels, D. S., Yelent, B., Craig, L., Bates, D., Yu, D. S., Shivji, M. K., Hitomi, C., Arvai, A. S., Volkmann, N., Tsuruta, H., Blundell, T. L., Venkitaraman, A. R., and Tainer, J. A. (2003) Full-length archaeal Rad51 structure and mutants. Mechanisms for RAD51 assembly and control by BRCA2. EMBO J. 22, 4566-4576 (Pubitemid 37087209)
28. Story, R. M., Weber, I. T., and Steitz, T. A. (1992) The structure of the E. coli recA protein monomer and polymer. Nature 355, 318-325
29. Conway, A. B., Lynch, T. W., Zhang, Y., Fortin, G. S., Fung, C. W., Symington, L. S., and Rice, P. A. (2004) Crystal structure of a Rad51 filament. Nat. Struct Mol. Biol. 11, 791-796 (Pubitemid 39014506)
30. Chen, Z., Yang, H., and Pavletich, N. P. (2008) Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453, 489-494 (Pubitemid 351733325)
31. Kinebuchi, T., Kagawa, W., Enomoto, R., Tanaka, K., Miyagawa, K., Shibata, T., Kurumizaka, H., and Yokoyama, S. (2004) Structural basis for octameric ring formation and DNA interaction of the human homologous-pairing protein Dmc1. Mol. Cell 14, 363-374 (Pubitemid 38591407)
32. Liu, J., Renault, L., Veaute, X., Fabre, F., Stahlberg, H., and Heyer, W. D. (2011) Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 479, 245-248