Two modes of binding of DinI to RecA filament provide a new insight into the regulation of sos response by DinI protein

Journal of Molecular Biology

Volumn 408, Issue 5, 2011, Pages 815-824

  Galkin, Vitold E ^a   Britt, Rachel L ^b   Bane, Lukas B ^b   Yu, Xiong ^a   Cox, Michael M ^b   Egelman, Edward H ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

bacterial SOS response; DinI; homologous recombination; LexA cleavage; RecA filament

Indexed keywords

BACTERIAL PROTEIN; DINI PROTEIN; RECA PROTEIN; SOS PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ESCHERICHIA COLI; MICROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

BACTERIA (MICROORGANISMS);

EID: 79955476626     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.03.046     Document Type: Article

References (45)

1. Kowalczykowski S.C., and Eggleston A.K. Homologous pairing and DNA strand-exchange proteins Annu. Rev. Biochem. 63 1994 991 1043 (Pubitemid 24218654)
2. Little J.W., and Mount D.W. The SOS regulatory system of Escherichia coli Cell 29 1982 11 22 (Pubitemid 12027667)
3. Smith K.C., and Wang T.C. recA-dependent DNA repair processes BioEssays 10 1989 12 16
4. Story R.M., and Steitz T.A. Structure of the recA protein-ADP complex Nature 355 1992 374 376
5. Datta S., Prabu M.M., Vaze M.B., Ganesh N., Chandra N.R., Muniyappa K., and Vijayan M. Crystal structures of Mycobacterium tuberculosis RecA and its complex with ADP-AlF(4): implications for decreased ATPase activity and molecular aggregation Nucleic Acids Res. 28 2000 4964 4973 (Pubitemid 32014267)
6. Xing X., and Bell C.E. Crystal structures of Escherichia coli RecA in complex with MgADP and MnAMP-PNP Biochemistry 43 2004 16142 16152 (Pubitemid 40041027)
7. Xing X., and Bell C.E. Crystal structures of Escherichia coli RecA in a compressed helical filament J. Mol. Biol. 342 2004 1471 1485 (Pubitemid 39208673)
8. Datta S., Krishna R., Ganesh N., Chandra N.R., Muniyappa K., and Vijayan M. Crystal structures of Mycobacterium smegmatis RecA and its nucleotide complexes J. Bacteriol. 185 2003 4280 4284 (Pubitemid 36835270)
9. Krishna R., Manjunath G.P., Kumar P., Surolia A., Chandra N.R., Muniyappa K., and Vijayan M. Crystallographic identification of an ordered C-terminal domain and a second nucleotide-binding site in RecA: new insights into allostery Nucleic Acids Res. 34 2006 2186 2195 (Pubitemid 43985657)
10. Roca A.I., and Cox M.M. RecA protein: structure, function, and role in recombinational DNA repair Prog. Nucleic Acid Res. Mol. Biol. 56 1997 129 223
11. Fernandez de Henestrosa A.R., Ogi T., Aoyagi S., Chafin D., Hayes J.J., Ohmori H., and Woodgate R. Identification of additional genes belonging to the LexA regulon in Escherichia coli Mol. Microbiol. 35 2000 1560 1572 (Pubitemid 30175530)
12. Little J.W. Autodigestion of lexA and phage repressors Proc. Natl Acad. Sci. USA 81 1984 1375 1379
13. VanLoock M.S., Yu X., Yang S., Galkin V.E., Huang H., and Rajan S.S. Complexes of RecA with LexA and RecX differentiate between active and inactive RecA nucleoprotein filaments J. Mol. Biol. 333 2003 345 354 (Pubitemid 37188577)
14. Kowalczykowski S.C., Clow J., and Krupp R.A. Properties of the duplex DNA-dependent ATPase activity of Escherichia coli RecA protein and its role in branch migration Proc. Natl Acad. Sci. USA 84 1987 3127 3131 (Pubitemid 17085357)
15. Lusetti S.L., Shaw J.J., and Cox M.M. Magnesium ion-dependent activation of the RecA protein involves the C terminus J. Biol. Chem. 278 2003 16381 16388 (Pubitemid 36799765)
16. Tateishi S., Horii T., Ogawa T., and Ogawa H. C-terminal truncated Escherichia coli RecA protein RecA5327 has enhanced binding affinities to single- and double-stranded DNAs J. Mol. Biol. 223 1992 115 129
17. Eggler A.L., Lusetti S.L., and Cox M.M. The C terminus of the Escherichia coli RecA protein modulates the DNA binding competition with single-stranded DNA-binding protein J. Biol. Chem. 278 2003 16389 16396 (Pubitemid 36799766)
18. Chen Z., Yang H., and Pavletich N.P. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures Nature 453 2008 489 494 (Pubitemid 351733325)
19. Sano Y. Role of the recA-related gene adjacent to the recA gene in Pseudomonas aeruginosa J. Bacteriol. 175 1993 2451 2454 (Pubitemid 23123523)
20. Vierling S., Weber T., Wohlleben W., and Muth G. Transcriptional and mutational analyses of the Streptomyces lividans recX gene and its interference with RecA activity J. Bacteriol. 182 2000 4005 4011 (Pubitemid 30436562)
21. Stohl E.A., Brockman J.P., Burkle K.L., Morimatsu K., Kowalczykowski S.C., and Seifert H.S. Escherichia coli RecX inhibits RecA recombinase and coprotease activities in vitro and in vivo J. Biol. Chem. 278 2003 2278 2285 (Pubitemid 36801297)
22. Drees J.C., Lusetti S.L., Chitteni-Pattu S., Inman R.B., and Cox M.M. A RecA filament capping mechanism for RecX protein Mol. Cell 15 2004 789 798 (Pubitemid 39194908)
23. Drees J.C., Lusetti S.L., and Cox M.M. Inhibition of RecA protein by the Escherichia coli RecX protein: modulation by the RecA C terminus and filament functional state J. Biol. Chem. 279 2004 52991 52997 (Pubitemid 40051797)
24. Lewis L.K., Harlow G.R., Gregg-Jolly L.A., and Mount D.W. Identification of high affinity binding sites for LexA which define new DNA damage-inducible genes in Escherichia coli J. Mol. Biol. 241 1994 507 523 (Pubitemid 24269326)
25. Yasuda T., Nagata T., and Ohmori H. Multicopy suppressors of the cold-sensitive phenotype of the pcsA68 (dinD68) mutation in Escherichia coli J. Bacteriol. 178 1996 3854 3859 (Pubitemid 26227202)
26. Yasuda T., Morimatsu K., Kato R., Usukura J., Takahashi M., and Ohmori H. Physical interactions between DinI and RecA nucleoprotein filament for the regulation of SOS mutagenesis EMBO J. 20 2001 1192 1202 (Pubitemid 32186809)
27. Voloshin O.N., Ramirez B.E., Bax A., and Camerini-Otero R.D. A model for the abrogation of the SOS response by an SOS protein: a negatively charged helix in DinI mimics DNA in its interaction with RecA Genes Dev. 15 2001 415 427 (Pubitemid 32187003)
28. Lusetti S.L., Voloshin O.N., Inman R.B., Camerini-Otero R.D., and Cox M.M. The DinI protein stabilizes RecA protein filaments J. Biol. Chem. 279 2004 30037 30046 (Pubitemid 38937924)
29. Craig N.L., and Roberts J.W. Function of nucleotide triphosphate and polynucleotide in E. coli RecA protein-directed cleavage of phage lambda repressor J. Biol. Chem. 256 1981 8039 8044 (Pubitemid 12229841)
30. Campbell M.J., and Davis R.W. On the in vivo function of the RecA ATPase J. Mol. Biol. 286 1999 437 445 (Pubitemid 29090161)
31. VanLoock M.S., Yu X., Yang S., Lai A.L., Low C., Campbell M.J., and Egelman E.H. ATP-mediated conformational changes in the RecA filament Structure (Cambridge) 11 2003 187 196 (Pubitemid 36183643)
32. Yu X., and Egelman E.H. Removal of the RecA C-terminus results in a conformational change in the RecA-DNA filament J. Struct. Biol. 106 1991 243 254
33. Weinstock G.M., McEntee K., and Lehman I.R. Hydrolysis of nucleoside triphosphates catalyzed by the recA protein of Escherichia coli. Steady state kinetic analysis of ATP hydrolysis J. Biol. Chem. 256 1981 8845 8849 (Pubitemid 12229900)
34. De Zutter J.K., and Knight K.L. The hRad51 and RecA proteins show significant differences in cooperative binding to single-stranded DNA J. Mol. Biol. 293 1999 769 780 (Pubitemid 29527665)
35. Egelman E.H. Problems in fitting high resolution structures into electron microscopic reconstructions HFSP J. 2 2008 324 331
36. Ramirez B.E., Voloshin O.N., Camerini-Otero R.D., and Bax A. Solution structure of DinI provides insight into its mode of RecA inactivation Protein Sci. 9 2000 2161 2169 (Pubitemid 32104152)
37. Wang Y., and Adzuma K. Differential proximity probing of two DNA binding sites in the Escherichia coli recA protein using photo-cross-linking methods Biochemistry 35 1996 3563 3571 (Pubitemid 26092575)
38. Malkov V.A., and Camerini-Otero R.D. Photocross-links between single-stranded DNA and Escherichia coli RecA protein map to loops L1 (amino acid residues 157-164) and L2 (amino acid residues 195-209) J. Biol. Chem. 270 1995 30230 30233 (Pubitemid 26001701)
39. Wang L., Voloshin O.N., Stasiak A., and Camerini-Otero R.D. Homologous DNA pairing domain peptides of RecA protein: intrinsic propensity to form beta-structures and filaments J. Mol. Biol. 277 1998 1 11 (Pubitemid 28151879)
40. Ragone S., Maman J.D., Furnham N., and Pellegrini L. Structural basis for inhibition of homologous recombination by the RecX protein EMBO J. 27 2008 2259 2269
41. Lindsley J.E., and Cox M.M. Assembly and disassembly of RecA protein filaments occur at opposite filament ends. Relationship to DNA strand exchange J. Biol. Chem. 265 1990 9043 9054
42. Morrical S.W., Lee J., and Cox M.M. Continuous association of Escherichia coli single-stranded DNA binding protein with stable complexes of recA protein and single-stranded DNA Biochemistry 25 1986 1482 1494 (Pubitemid 16013918)
43. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., and Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields J. Struct. Biol. 116 1996 190 199 (Pubitemid 26093143)
44. Egelman E.H. A robust algorithm for the reconstruction of helical filaments using single-particle methods Ultramicroscopy 85 2000 225 234
45. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612