Calorimetric Analysis of Binding of two Consecutive DNA Strands to RecA Protein Illuminates Mechanism for Recognition Of Homology

Journal of Molecular Biology

Volumn 365, Issue 3, 2007, Pages 603-611

  Takahashi, Masayuki ^a,b   Maraboeuf, Fabrice ^a   Morimatsu, Katsumi ^c   Selmane, Tassadite ^a   Fleury, Fabrice ^b   Norden, Bengt ^c  

^a CNRS   (France)

^b UNIVERSITÉ DE NANTES   (France)

^c CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

DNA binding; homologous recombination; isothermal titration calorimetry; RecA protein; thermodynamics

Indexed keywords

ADENOSINE 5' O (3 THIOTRIPHOSPHATE); ADENOSINE TRIPHOSPHATE; BUFFER; COMPLEMENTARY DNA; RECA PROTEIN;

ARTICLE; BASE PAIRING; BINDING AFFINITY; BINDING KINETICS; CIRCULAR DICHROISM; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DNA BINDING MOTIF; DNA CONFORMATION; DNA PROTEIN COMPLEX; DNA STRAND; DNA STRUCTURE; ENTHALPY; HOMOLOGOUS RECOMBINATION; ISOTHERMAL TITRATION CALORIMETRY; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DNA BINDING; PROTON TRANSPORT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRUCTURE ACTIVITY RELATION; TEMPERATURE DEPENDENCE; THERMODYNAMICS;

EID: 33845599600     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.10.042     Document Type: Article

References (48)

1. Lusetti S.L., and Cox M.M. The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annu. Rev. Biochem. 71 (2002) 71-100
2. Volodin A.A., Voloshin O.N., and Camerini-Otero R.D. Homologous recombination and RecA protein: towards a new generation of tools for genome manipulations. Trends. Biotechnol. 23 (2005) 97-102
3. Little J.W., Edmiston S.H., Pacelli L.Z., and Mount D.W. Cleavage of the Escherichia coli lexA protein by the recA protease. Proc. Natl Acad. Sci. USA 77 (1980) 3225-3229
4. Shibata T., DasGupta C., Cunningham R.P., and Radding C.M. Purified Escherichia coli RecA protein catalyzes homologous pairing of superhelical DNA and single-stranded fragments. Proc. Natl Acad. Sci. USA 76 (1979) 1638-1642
5. McEntee K., Weinstock G.M., and Lehman I.R. Initiation of general recombination catalyzed in vitro by the recA protein of Escherichia coli. Proc. Natl Acad. Sci. USA 76 (1979) 2615-2618
6. Stasiak A., DiCapua E., and Koller Th. Elongation of duplex DNA by recA protein. J. Mol. Biol. 151 (1981) 557-564
7. Takahashi M. Analysis of DNA-RecA protein interactions involving the protein self-association reaction. J. Biol. Chem. 264 (1989) 288-295
8. Bazemore L.R., Takahahsi M., and Radding C.M. Kinetic analysis of pairing and strand exchange catalyzed by RecA: detection by fluorescence energy transfer. J. Biol. Chem. 272 (1997) 14672-14682
9. Bazemore L.R., Folta-Stogniew E., Takahashi M., and Radding C.M. RecA tests homology at both pairing and strand exchange. Proc. Natl Acad. Sci. USA 94 (1997) 11863-11868
10. Ogawa T., Yu X., Shinohara A., and Egelman E. Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259 (1993) 1896-1899
11. Benson F.E., Stasiak A., and West S.C. Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J. 13 (1994) 5764-5771
12. Ellouze C., Kim H.-K., Maeshima K., Tuite E., Morimatsu K., Horii T., et al. Nucleotide cofactor dependent structural change of Xenopus Rad51 protein filament detected by small-angle neutron scattering measurements in solution. Biochemistry 36 (1997) 13524-13529
13. Wittung P., Nordén B., Kim S.-K., and Takahashi M. Interactions between DNA molecules bound to RecA filament: effects of base complementarity. J. Biol. Chem. 269 (1994) 5799-5803
14. Takahashi M., Kubista M., and Nordén B. Binding stoichiometry and structure of RecA-DNA complexes studied by flow linear dichroism and fluorescence spectroscopy: evidence for multiple heterogeneous DNA coordination. J. Mol. Biol. 205 (1989) 137-147
15. Chabbert M., Lami H., and Takahashi M. Cofactor induced orientation of the DNA bases in single-stranded DNA, complexed with RecA protein: a fluorescence anisotropy and time-decay study. J. Biol. Chem. 266 (1991) 5395-5400
16. Nordén B., Wittung-Stafshede P., Ellouze C., Kim H.-K., Mortensen K., and Takahashi M. Base orientation of second DNA in the RecA-DNA filaments: analysis by combination of linear dichroism and small-angle neutron scattering in flow oriented solution. J. Biol. Chem. 273 (1998) 15682-15686
17. Nishinaka T., Ito Y., Kurumizaka H., Terada T., Yokoyama S., and Shibata T. An extended DNA structure through deoxyribose-base stacking induced by RecA protein. Proc. Natl Acad. Sci. USA 94 (1997) 6623-6628
18. Nishinaka T., Shinohara A., Ito Y., Yokoyama S., and Shibata T. Base pair switching by interconversion of sugar puckers in DNA extended by proteins of RecA-family: a model for homology search in homologous genetic recombination. Proc. Natl Acad. Sci. USA 95 (1998) 11071-11076
19. Prévost C., and Takahashi M. Geometry of the DNA strands within the RecA nucleofilament: role in homologous recombination. Quart. Rev. Biophys. 36 (2004) 1-25
20. Freire E., Mayorga O.L., and Straume M. Isothermal titration. Anal. Chem. 62 (1990) 950A-959A
21. Fisher H.F., and Singh N. Calorimetric methods for interpreting protein-ligand interactions. Methods Enzymol. 259 (1995) 194-221
22. Wittung P., Ellouze C., Maraboeuf F., Nordén B., and Takahashi M. Thermochemical and kinetic evidence of nucelobase dependent RecA-DNA interactions. Eur. J. Biochem. 245 (1997) 715-719
23. Spolar R.S., and Record Jr. M.T. Coupling of local folding to site-specific binding of proteins to DNA. Science 263 (1994) 777-785
24. Leder L., Berger C., Bornhauser S., Wendt H., Ackermann F., Jelesarov I., and Bosshard H.R. Spectroscopic, calorimetric, and kinetic demonstration of conformational adaptation in peptide-antibody recognition. Biochemistry 34 (1995) 16509-16518
25. 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
26. 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
27. Morimatsu K., and Horii T. The DNA binding-site of the RecA protein: photochemical cross-linking of Tyr103 to single-stranded DNA. Eur. J. Biochem. 228 (1995) 772-778
28. Takahashi M., Maraboeuf F., and Nordén B. Locations of functional domains in the RecA protein: overlap of domains and regulation of activities. Eur. J. Biochem. 242 (1996) 20-28
29. Wang L., Voloshin O.N., Stasiak A., 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
30. Muller B., Koller T., and Stasiak A. Characterization of the DNA binding activity of stable RecA-DNA complexes. J. Mol. Biol. 212 (1990) 97-112
31. Menetski J.P., Bear D.G., and Kowalczykowski S.C. Stable DNA heteroduplex formation catalyzed by the Escherichia coli RecA protein in the absence of ATP hydrolysis. Proc. Natl Acad. Sci. USA 87 (1990) 21-25
32. Datta K., and LiCata V.J. Thermodynamics of the binding of Thermus aquqticus DNA polymerase to primed-template DNA. Nucl. Acids Res. 31 (2003) 5590-5597
33. Wittung P., Nordén B., and Takahashi M. Secondary structure of RecA in solution: effects of cofactor, DNA and ionic conditions. Eur. J. Biochem. 228 (1995) 149-154
34. Tracy R.B., and Kowalczykowski S.C. In vitro selection of preferred DNA pairing sequences by the Escherichia coli RecA protein. Genes Develop. 10 (1996) 1890-1903
35. Bar-Ziv R., and Libchaber A. Effects of DNA sequence and structure on binding of RecA to single-stranded DNA. Proc. Natl Acad. Sci. USA 98 (2001) 9068-9073
36. Ts'o P.O., Rapaport S.A., and Bollum F.J. A comparative study of polydeoxyribonucleotides and polyribonucleotides by optical rotatory dispersion. Biochemistry 5 (1966) 4153-4170
37. Ferrari M.E., and Lohman T.M. Apparent heat capacity change accompanying a non-specific protein-DNA interaction. Escherichia coli SSB tetramer binding to oligodeoxyadenylate. Biochemistry 33 (1994) 12896-12910
38. Chabbert M., Cazenave C., and Hélène C. Kinetic studies of recA protein binding to a fluorescent single-stranded polynucleotide. Biochemistry 26 (1987) 2218-2225
39. Morrical S.W., and Cox M.M. Light scattering studies of the recA protein of Escherichia coli: relationship between free recA filaments and the recA-ssDNA complex. Biochemistry 24 (1985) 760-767
40. + reductase and the role of water at the complex interface. Biochemistry 33 (1994) 13321-13328
41. Morimatsu M., and Takahashi M. Structural analysis of RecA protein-DNA complexes by fluorescence-detected linear dichroism: Absence of structural change of filament for pairing of complementary DNA strands. Anal. Biochem. 358 (2006) 192-198
42. Fulconi R., Dutreix M., and Viovy J.L. Numerical investigation of sequence dependence in homologous recognition: evidence for homology traps. Biophys. J. 88 (2005) 3770-3779
43. Ellouze C., Takahashi M., Wittung P., Mortensen K., Schnarr M., and Nordén B. Evidence for elongation of helical pitch of the RecA filament upon ATP and ADP binding using small-angle neutron scattering. Eur. J. Biochem. 233 (1995) 579-583
44. 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 11 (2003) 187-196
45. Jonsson M., Jacobsson U., Takahashi M., and Nordén B. Orientation of large DNA during free solution electrophoresis studied by linear dichroism. J. Chem. Soc. Faraday Trans. 89 (1993) 2791-2798
46. Conway A.B., Lynch T.W., Zhang Y., Fortin G.S., Fung C.W., Symington L.S., and Rice P.A. Crystal structure of a Rad51 filament. Nature Struct. Biol. 11 (2004) 791-796
47. Simonson T., Kubista M., Sjöback R., Ryberg H., and Takahashi M. Properties of RecA-oligonucleotide complexes. J. Mol. Recogn. 7 (1994) 199-206
48. Takahashi M., and Hagmar P. Use of ion exchange chromatography for the study of RecA-DNA interactions. FEBS Letters 279 (1991) 270-272