Conformational Adaptability of Redβ during DNA Annealing and Implications for Its Structural Relationship with Rad52

Journal of Molecular Biology

Volumn 391, Issue 3, 2009, Pages 586-598

  Erler, Axel ^a   Wegmann, Susanne ^a   Elie Caille, Celine ^a,b   Bradshaw, Charles Richard ^c   Maresca, Marcello ^a   Seidel, Ralf ^a   Habermann, Bianca ^c,d   Muller, Daniel J ^a   Stewart, A Francis ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b FEMTO ST INSTITUTE   (France)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^d Scionics Computer Innovation GmbH   (Germany)

Author keywords

atomic force microscopy; DNA annealing; homologous recombination; phage lambda; recombineering

Indexed keywords

DNA; MONOMER; RAD52 PROTEIN; SINGLE STRANDED DNA;

AMINO ACID SEQUENCE; ARTICLE; ATOMIC FORCE MICROSCOPY; BACTERIOPHAGE LAMBDA; BASE PAIRING; COLIPHAGE; COMPLEX FORMATION; CONTROLLED STUDY; DNA PROTEIN COMPLEX; GENE DISRUPTION; HOMOLOGOUS RECOMBINATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN QUATERNARY STRUCTURE; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; BINDING SITE; CHEMISTRY; GENETIC RECOMBINATION; METABOLISM; ULTRASTRUCTURE;

ENTEROBACTERIA PHAGE LAMBDA; EUKARYOTA;

BASE PAIRING; BINDING SITES; DNA, SINGLE-STRANDED; MICROSCOPY, ATOMIC FORCE; PROTEIN STRUCTURE, QUATERNARY; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC;

EID: 67651164996     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.06.030     Document Type: Article

References (58)

1. Cox M.M., Goodman M.F., Kreuzer K.N., Sherratt D.J., Sandler S.J., and Marians K.J. The importance of repairing stalled replication forks. Nature 404 (2000) 37-41
2. McGlynn P., and Lloyd R.G. Recombinational repair and restart of damaged replication forks. Nat. Rev., Mol. Cell. Biol. 3 (2002) 859-870
3. van den Bosch M., Lohman P.H., and Pastink A. DNA double-strand break repair by homologous recombination. Biol. Chem. 383 (2002) 873-892
4. Wyman C., and Kanaar R. Homologous recombination: down to the wire. Curr. Biol. 14 (2004) R629-R631
5. Kuzminov A. Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol. Mol. Biol. Rev. 63 (1999) 751-813
6. Lin Z., Kong H., Nei M., and Ma H. Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer. Proc. Natl Acad. Sci. USA 103 (2006) 10328-10333
7. Cox M.M. Motoring along with the bacterial RecA protein. Nat. Rev., Mol. Cell. Biol. 8 (2007) 127-138
8. Iyer L.M., Koonin E.V., and Aravind L. Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52. BMC Genomics 3 (2002) 8
9. Muyrers J.P., Zhang Y., Buchholz F., and Stewart A.F. RecE/RecT and Redalpha/Redbeta initiate double-stranded break repair by specifically interacting with their respective partners. Genes Dev. 14 (2000) 1971-1982
10. Kolodner R., Hall S.D., and Luisi-DeLuca C. Homologous pairing proteins encoded by the Escherichia coli recE and recT genes. Mol. Microbiol. 11 (1994) 23-30
11. Court D.L., Sawitzke J.A., and Thomason L.C. Genetic engineering using homologous recombination. Annu. Rev. Genet. 36 (2002) 361-388
12. Poteete A.R. Involvement of DNA replication in phage lambda Red-mediated homologous recombination. Mol. Microbiol. 68 (2008) 66-74
13. Zhang Y., Buchholz F., Muyrers J.P., and Stewart A.F. A new logic for DNA engineering using recombination in Escherichia coli. Nat. Genet. 20 (1998) 123-128
14. Copeland N.G., Jenkins N.A., and Court D.L. Recombineering: a powerful new tool for mouse functional genomics. Nat. Rev., Genet. 2 (2001) 769-779
15. Zhang Y., Muyrers J.P., Testa G., and Stewart A.F. DNA cloning by homologous recombination in Escherichia coli. Nat. Biotechnol. 18 (2000) 1314-1317
16. Muyrers J.P., Zhang Y., Testa G., and Stewart A.F. Rapid modification of bacterial artificial chromosomes by ET-recombination. Nucleic Acids Res. 27 (1999) 1555-1557
17. Karakousis G., Ye N., Li Z., Chiu S.K., Reddy G., and Radding C.M. The beta protein of phage lambda binds preferentially to an intermediate in DNA renaturation. J. Mol. Biol. 276 (1998) 721-731
18. Mythili E., Kumar K.A., and Muniyappa K. Characterization of the DNA-binding domain of beta protein, a component of phage lambda red-pathway, by UV catalyzed cross-linking. Gene 182 (1996) 81-87
19. Passy S.I., Yu X., Li Z., Radding C.M., and Egelman E.H. Rings and filaments of beta protein from bacteriophage lambda suggest a superfamily of recombination proteins. Proc. Natl Acad. Sci. USA 96 (1999) 4279-4284
20. Kagawa W., Kurumizaka H., Ishitani R., Fukai S., Nureki O., Shibata T., and Yokoyama S. Crystal structure of the homologous-pairing domain from the human Rad52 recombinase in the undecameric form. Mol. Cell 10 (2002) 359-371
21. Singleton M.R., Wentzell L.M., Liu Y., West S.C., and Wigley D.B. Structure of the single-strand annealing domain of human RAD52 protein. Proc. Natl Acad. Sci. USA 99 (2002) 13492-13497
22. Stasiak A.Z., Larquet E., Stasiak A., Müller S., Engel A., Van Dyck E., et al. The human Rad52 protein exists as a heptameric ring. Curr. Biol. 10 (2000) 337-340
23. Van Dyck E., Stasiak A.Z., Stasiak A., and West S.C. Visualization of recombination intermediates produced by RAD52-mediated single-strand annealing. EMBO Rep. 2 (2001) 905-909
24. Ploquin M., Bransi A., Paquet E.R., Stasiak A., Yu X., Cieslinska A.M., et al. Functional and structural basis for a bacteriophage homolog of human RAD52. Curr. Biol. 18 (2008) 1142-1146
25. Thresher R.J., Makhov A.M., Hall S.D., Kolodner R., and Griffith J.D. Electron microscopic visualization of RecT protein and its complexes with DNA. J. Mol. Biol. 254 (1995) 364-371
26. Poteete A.R., Sauer R.T., and Hendrix R.W. Domain structure and quaternary organization of the bacteriophage P22 Erf protein. J. Mol. Biol. 171 (1983) 401-418
27. Kagawa W., Kurumizaka H., Ikawa S., Yokoyama S., and Shibata T. Homologous pairing promoted by the human Rad52 protein. J. Biol. Chem. 276 (2001) 35201-35208
28. Mortensen U.H., Bendixen C., Sunjevaric I., and Rothstein R. DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl Acad. Sci. USA 93 (1996) 10729-10734
29. Binnig G., Quate C.F., and Gerber C. Atomic force microscope. Phys. Rev. Lett. 56 (1986) 930-933
30. Shao Z., and Zhang Y. Biological cryo atomic force microscopy: a brief review. Ultramicroscopy 66 (1996) 141-152
31. Muller D.J., Sapra K.T., Scheuring S., Kedrov A., Frederix P.L., Fotiadis D., and Engel A. Single-molecule studies of membrane proteins. Curr. Opin. Struct. Biol. 16 (2006) 489-495
32. Lyubchenko Y.L. DNA structure and dynamics: an atomic force microscopy study. Cell Biochem. Biophys. 41 (2004) 75-98
33. Hansma H.G. Surface biology of DNA by atomic force microscopy. Annu. Rev. Phys. Chem. 52 (2001) 71-92
34. Engel A., and Muller D.J. Observing single biomolecules at work with the atomic force microscope. Nat. Struct. Biol. 7 (2000) 715-718
35. Wu Z., Xing X., Bohl C.E., Wisler J.W., Dalton J.T., and Bell C.E. Domain structure and DNA binding regions of beta protein from bacteriophage lambda. J. Biol. Chem. 281 (2006) 25205-25214
36. Fischer H., Polikarpov I., and Craievich A.F. Average protein density is a molecular-weight-dependent function. Protein Sci. 13 (2004) 2825-2828
37. McIlwraith M.J., and West S.C. DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair. Mol. Cell 29 (2008) 510-516
38. Kmiec E., and Holloman W.K. Beta protein of bacteriophage lambda promotes renaturation of DNA. J. Biol. Chem. 256 (1981) 12636-12639
39. Muniyappa K., and Radding C.M. The homologous recombination system of phage lambda. Pairing activities of beta protein. J. Biol. Chem. 261 (1986) 7472-7478
40. Howard J. Mechanics of Motor Proteins and the Cytoskeleton (2001), Sinauer Associates, Inc., Sutherland, MA 163
41. Li Z., Karakousis G., Chiu S.K., Reddy G., and Radding C.M. The beta protein of phage lambda promotes strand exchange. J. Mol. Biol. 276 (1998) 733-744
42. Stasiak A., Di Capua E., and Koller T. Elongation of duplex DNA by recA protein. J. Mol. Biol. 151 (1981) 557-564
43. Ellis H.M., Yu D., DiTizio T., and Court D.L. High efficiency mutagenesis, repair, and engineering of chromosomal DNA using single-stranded oligonucleotides. Proc. Natl Acad. Sci. USA 98 (2001) 6742-6746
44. Storici F., Lewis L.K., and Resnick M.A. In vivo site-directed mutagenesis using oligonucleotides. Nat. Biotechnol. 19 (2001) 773-776
45. Zhang Y., Muyrers J.P., Rientjes J., and Stewart A.F. Phage annealing proteins promote oligonucleotide-directed mutagenesis in Escherichia coli and mouse ES cells. BMC Mol. Biol. 4 (2003) 1
46. Rothenberg E., Grimme J.M., Spies M., and Ha T. Human Rad52-mediated homology search and annealing occurs by continuous interactions between overlapping nucleoprotein complexes. Proc. Natl Acad. Sci. USA 105 (2008) 20274-20279
47. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
48. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., et al. Clustal W and Clustal X version 2.0. Bioinformatics 23 (2007) 2947-2948
49. Kim D., Xu D., Guo J.T., Ellrott K., and Xu Y. PROSPECT II: protein structure prediction program for genome-scale applications. Protein Eng. 16 (2003) 641-650
50. Murzin A.G., Brenner S.E., Hubbard T., and Chothia C. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247 (1995) 536-540
51. Bradshaw C.R., Surendranath V., and Habermann B. ProFAT: a web-based tool for the functional annotation of protein sequences. BMC Bioinformatics 7 (2006) 466
52. Wang J., Sarov M., Rientjes J., Fu J., Hollak H., Kranz H., et al. An improved recombineering approach by adding RecA to lambda Red recombination. Mol. Biotechnol. 32 (2006) 43-53
53. Heymann J.B., Moller C., and Muller D.J. Sampling effects influence heights measured with atomic force microscopy. J. Microsc. 207 (2002) 43-51
54. Saxton W.O., Pitt T.J., and Horner M. Digital image processing: the semper system. Ultramicroscopy 4 (1979) 343-353
55. Saxton W.O., and Baumeister W. The correlation averaging of a regularly arranged bacterial cell envelope protein. J. Microsc. 127 (1982) 127-138
56. Saxton W.O., Baumeister W., and Hahn M. Three-dimensional reconstruction of imperfect two-dimensional crystals. Ultramicroscopy 13 (1984) 57-70
57. Wiggins P.A., van der Heijden T., Moreno-Herrero F., Spakowitz A., Phillips R., Widom J., et al. High flexibility of DNA on short length scales probed by atomic force microscopy. Nat. Nanotechnol. 1 (2006) 137-141
58. Moreno-Herrero F., Seidel R., Johnson S.M., Fire A., and Dekker N.H. Structural analysis of hyperperiodic DNA from Caenorhabditis elegans. Nucleic Acids Res. 34 (2006) 3057-3066