Complexes of RecA with LexA and RecX differentiate between active and inactive RecA nucleoprotein filaments

Journal of Molecular Biology

Volumn 333, Issue 2, 2003, Pages 345-354

  VanLoock, Margaret S ^a   Yu, Xiong ^a   Yang, Shixin ^a   Galkin, Vitold E ^a   Huang, Hao ^a   Rajan, Shyamala S ^b   Anderson, Wayne F ^b   Stohl, Elizabeth A ^b   Seifert, H Steven ^b   Egelman, Edward H ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Electron microscopy; Helical polymers; Image analysis; Recombination

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; LEXA PROTEIN; NUCLEOPROTEIN; NUCLEOTIDE; PROTEIN RECX; PROTEIN SUBUNIT; RECA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL; INHIBITION KINETICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN STABILITY; SEQUENCE ANALYSIS; STOICHIOMETRY;

BACTERIA (MICROORGANISMS);

EID: 0141757508     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.08.053     Document Type: Article

References (62)

1. Bianco P.R., Tracy R.B., Kowalczykowski S.C. DNA strand exchange proteins: a biochemical and physical comparison. Front Biosci. 3:1998;D570-D603.
2. Dunderdale H.J., West S.C. Recombination genes and proteins. Curr. Opin. Genet. Dev. 4:1994;221-228.
3. Roca A.I., Cox M.M. RecA protein: structure, function, and role in recombinational DNA repair. Prog. Nucl. Acid. Res. Mol. Biol. 56:1997;129-223.
4. Story R.M., Weber I.T., Steitz T.A. The structure of the E. coli recA protein monomer and polymer. Nature. 355:1992;318-325.
5. Datta S., Ganesh N., Chandra N.R., Muniyappa K., Vijayan M. Structural studies on MtRecA-nucleotide complexes: insights into DNA and nucleotide binding and the structural signature of NTP recognition. Proteins: Struct. Funct. Genet. 50:2003;474-485.
6. Yu X., Egelman E.H. Structural data suggest that the active and inactive forms of the RecA filament are not simply interconvertible. J. Mol. Biol. 227:1992;334-346.
7. Yu X., Shibata T., Egelman E.H. Identification of a defined epitope on the surface of the active RecA-DNA filament using a monoclonal antibody and three-dimensional reconstruction. J. Mol. Biol. 283:1998;985-992.
8. VanLoock M.S., Yu X., Yang S., Lai A.L., Low C., Campbell M.J., Egelman E.H. ATP-mediated conformational changes in the RecA filament. Structure. 11:2003;187-196.
9. Egelman E.H., Stasiak A. Electron microscopy of RecA-DNA complexes: two different states, their functional significance and relation to the solved crystal structure. Micron. 24:1993;309-324.
10. Pellegrini L., Yu D.S., Lo T., Anand S., Lee M.-Y., Blundell T.L., Venkitaraman. Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature. 420:2002;287-293.
11. Morimatsu K., Takahashi M., Norden B. Arrangement of RecA protein in its active filament determined by polarized-light spectroscopy. Proc. Natl Acad. Sci. USA. 99:2002;11688-11693.
12. Singleton M.R., Sawaya M.R., Ellenberger T., Wigley D.B. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell. 101:2000;589-600.
13. Yu X., Jacobs S.A., West S.C., Ogawa T., Egelman E.H. Domain structure and dynamics in the helical filaments formed by RecA and Rad51 on DNA. Proc. Natl Acad. Sci. USA. 98:2001;8419-8424.
14. Yu X., Egelman E.H. The LexA repressor binds within the deep helical groove of the activated RecA filament. J. Mol. Biol. 231:1993;29-40.
15. Courcelle J., Khodursky A., Peter B., Brown P.O., Hanawalt P.C. Comparative gene expression profiles following UV exposure in wild-type and SOS-deficient Escherichia coli. Genetics. 158:2001;41-64.
16. Lin L.L., Little J.W. Autodigestion and RecA-dependent cleavage of Ind-mutant LexA proteins. J. Mol. Biol. 210:1989;439-452.
17. Sassanfar M., Roberts J.W. Nature of the SOS-inducing signal in Escherichia coli. The involvement of DNA replication. J. Mol. Biol. 212:1990;79-96.
18. Venkatesh R., Ganesh N., Guhan N., Reddy M.S., Chandrasekhar T., Muniyappa K. RecX protein abrogates ATP hydrolysis and strand exchange promoted by RecA: insights into negative regulation of homologous recombination. Proc. Natl Acad. Sci. USA. 99:2002;12091-12096.
19. Papavinasasundaram K.G., et al. Mycobacterial recA is cotranscribed with a potential regulatory gene called recX. Mol. Microbiol. 24:1997;141-153.
20. Vierling S., Weber T., Wohlleben W., Muth G. Transcriptional and mutational analyses of the Streptomyces lividans recX gene and its interference with RecA activity. J. Bacteriol. 182:2000;4005-4011.
21. Stohl E.A., Seifert H.S. The recX gene potentiates homologous recombination in Neisseria gonorrhoeae. Mol. Microbiol. 40:2001;1301-1310.
22. Pages V., Koffel-Schwartz N., Fuchs R.P. recX, a new SOS gene that is co-transcribed with the recA gene in Escherichia coli. DNA Repair (Amst). 2:2003;273-284.
23. Stohl E.A., Brockman J.P., Burkle K.L., Morimatsu K., Kowalczykowski S.C., Seifert H.S. Escherichia coli RecX inhibits RecA recombinase and coprotease activities in vitro and in vivo. J. Biol. Chem. 278:2003;2278-2285.
24. Chang C.F., Rankert D.A., Jeng T.W., Morgan D.G., Schmid M.F., Chiu W. Cryo electron microscopy of unstained, unfixed RecA-cssDNA complexes. J. Ultrastruct. Mol. Struct. Res. 100:1988;166-172.
25. Frank E.G., Cheng N., Do C.C., Cerritelli M.E., Bruck I., Goodman M.F., et al. Visualization of two binding sites for the Escherichia coli UmuD'(2)C complex (DNA pol V) on RecA-ssDNA filaments. J. Mol. Biol. 297:2000;585-597.
26. DeRosier D.J., Klug A. Reconstruction of three-dimensional structures from electron micrographs. Nature. 217:1968;130-134.
27. Egelman E.H. A robust algorithm for the reconstruction of helical filaments using single-particle methods. Ultramicroscopy. 85:2000;225-234.
28. Yang S., VanLoock M.S., Yu X., Egelman E.H. Comparison of bacteriophage T4 UvsX and human Rad51 filaments suggests that RecA-like polymers may have evolved independently. J. Mol. Biol. 312:2001;999-1009.
29. Yang S., Yu X., Seitz E.M., Kowalczykowski S.C., Egelman E.H. Archaeal RadA protein binds DNA as both helical filaments and octameric rings. J. Mol. Biol. 314:2001;1077-1085.
30. Galkin V.E., Orlova A., Lukoyanova N., Wriggers W., Egelman E.H. Actin depolymerizing factor stabilizes an existing state of F-actin and can change the tilt of F-actin subunits. J. Cell Biol. 153:2001;75-86.
31. Orlova A., Galkin V.E., VanLoock M.S., Kim E., Shvetsov A., Reisler E.H., Egelman E.H., et al. Probing the structure of f-actin: cross-links constrain atomic models and modify actin dynamics. J. Mol. Biol. 312:2001;95-106.
32. Lukoyanova N., VanLoock M.S., Orlova A., Galkin V.E., Wang K., Egelman E.H. Each actin subunit has three nebulin-binding sites: implications for steric blocking. Curr. Biol. 12:2002;383-388.
33. Galkin V.E., VanLoock M.S., Orlova A., Egelman E.H. A new internal mode in F-actin helps explain the remarkable evolutionary conservation of actin's sequence and structure. Curr. Biol. 12:2002;570-575.
34. Galkin V.E., Orlova A., VanLoock M.S., Rybakova I.N., Ervast J.M., Egelman E.H. The utrophin actin-binding domain binds F-actin in two different modes: implications for the spectrin superfamily of proteins. J. Cell Biol. 157:2002;243-251.
35. Galkin V.E., Orlova A., VanLoock M.S., Zhou D., Galain E., Egelman E.H. The bacterial protein SipA polymerizes G-actin and mimics muscle nebulin. Nature Struct. Biol. 9:2002;518-521.
36. Mu X.Q., Egelman E.H., Bullitt E. Structure and function of Hib pili from Haemophilus influenzae type b. J. Bacteriol. 278:2002;17103-17107.
37. Cordes F.S., Komoriya K., Larquet E., Yang S., Egelman E.H., Blocker A., et al. Helical structure of the needle of the type III secretion system of Shigella flexneri. J. Biol. Chem. 278:2003;17103-17107.
38. Dutreix M., Moreau P.L., Bailone A., Galibert F., Battista J.R., Walker G.C., Devoret R. New recA mutations that dissociate the various RecA protein activities in Escherichia coli provide evidence for an additional role for RecA protein in UV mutagenesis. J. Bacteriol. 171:1989;2415-2423.
39. Ogawa H., Ogawa T. General recombination: functions and structure of RecA protein. Advan. Biophys. 21:1986;135-148.
40. Konola J.T., Guzzo A., Gow J.B., Walker G.C., Knight K.L. Differential cleavage of LexA and UmuD mediated by recA Pro67 mutants: implications for common LexA and UmuD binding sites on RecA. J. Mol. Biol. 276:1998;405-415.
41. Nastri H.G., Guzzo A., Lange C.S., Walker G.C., Knight K.L. Mutational analysis of the RecA protein L1 region identifies this area as a probable part of the co-protease substrate binding site. Mol. Microbiol. 25:1997;967-978.
42. Slilaty S.N., Little J.W. Lysine-156 and serine-119 are required for LexA repressor cleavage: a possible mechanism. Proc. Natl Acad. Sci. USA. 84:1987;3987-3991.
43. Lusetti S.L., Wood E.A., Fleming C.D., Modica M.J., Korth J., Abbott L., et al. C-terminal deletions of the E. coli RecA protein: characterization of in vivo and in vitro effects. J. Biol. Chem. 278:2003;16372-16380.
44. Eggler A.L., Lusetti S.L., Cox M.M. The C-terminus of the E. coli RecA protein modulates the DNA binding competition with SSB. J. Biol. Chem. 278:2003;16389-16396.
45. Lusetti S.L., Shaw J.J., Cox M.M. Magnesium ion-dependent activation of the RecA protein involves the C-terminus. J. Biol. Chem. 278:2003;16381-16388.
46. Yu X., 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.
47. Galkin V.E., Orlova A., Lukoyanova N., VanLoock M.S., Haag P., Bullard B., Egelman E.H. The location of ubiquitin in Lethocerus arthrin. J. Mol. Biol. 325:2003;623-628.
48. Stasiak A., Egelman E.H. Structure and function of RecA-DNA complexes. Experientia. 50:1994;192-203.
49. Egelman E.H., Yu X. The location of DNA in RecA-DNA helical filaments. Science. 245:1989;404-407.
50. Smith B.T., Walker G.C. Mutagenesis and more: umuDC and the Escherichia coli SOS response. Genetics. 148:1998;1599-1610.
51. Pham P., Seitz E.M., Saveliev S., Shen X., Woodgate R., Cox M.M., Goodman M.F. Two distinct modes of RecA action are required for DNA polymerase V-catalyzed translesion synthesis. Proc. Natl Acad. Sci. USA. 99:2002;11061-11066.
52. Gudas L.J., Pardee A.B. DNA synthesis inhibition and the induction of protein X in Escherichia coli. J. Mol. Biol. 101:1976;459-477.
53. Yu X., Angov E., Camerini-Otero R.D., Egelman E.H. Structural polymorphism of the RecA protein from the thermophilic bacterium Thermus aquaticus. Biophys. J. 69:1995;2728-2738.
54. Yu X., Egelman E.H. The RecA hexamer is a structural homologue of ring helicases. Nature Struct. Biol. 4:1997;101-104.
55. Passy S.I., Yu X., Li Z., Radding C.M., Masson J.Y., West S.C., Egelman E.H. Human Dmc1 protein binds DNA as an octameric ring. Proc. Natl Acad. Sci. USA. 96:1999;10684-10688.
56. Egelman E.H., Francis N., DeRosier D.J. F-actin is a helix with a random variable twist. Nature. 298:1982;131-135.
57. McGough A., Pope B., Chiu W., Weeds A. Cofilin changes the twist of F-actin: implications for actin filament dynamics and cellular function. J. Cell Biol. 138:1997;771-781.
58. Bird L.E., Subramanya H.S., Wigley D.B. Helicases: a unifying structural theme? Curr. Opin. Struct. Biol. 8:1998;14-18.
59. Sawaya M.R., Guo S., Tabor S., Richardson C.C., Ellenberger T. Crystal structure of the helicase domain from the replicative helicase-primase of bacteriophage T7. Cell. 99:1999;167-177.
60. Yamashita I., Hasegawa K., Suzuki H., Vonderviszt F., Mimori-Kiyosue Y., Namba K. Structure and switching of bacterial flagellar filaments studied by X-ray fiber diffraction. Nature Struct. Biol. 5:1998;125-132.
61. Samatey F.A., Imada K., Nagashima S., Vonderviszt F., Kumasaka T., Yamamoto M., Namba K. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature. 410:2001;331-337.
62. Yu X., Egelman E.H. Direct visualization of dynamics and cooperative conformational changes within RecA filaments that appear to be associated with the hydrolysis of Adenosine-5′-O-(thiotriphosphate). J. Mol. Biol. 225:1992;193-216.