Structure and interactions of RecA: plasticity revealed by molecular dynamics simulations

References

• Arif, S. M., Geethanandan, K., Mishra, P., Surolia, A., Varshney, U., & Vijayan, M. (2015). Structural plasticity in Mycobacterium tuberculosis uracil-DNA glycosylase (MtUng) and its functional implications. Acta Crystallographica Section D – Biological Crystallography, 71, 1514–1527. doi:10.1107/S1399004715009311
   PubMedGoogle Scholar
• Arif, S. M., & Vijayan, M. (2012). Structural diversity based on variability in quaternary association. A case study involving eubacterial and related SSBs. Methods in Molecular Biology, 922, 23–35. doi:10.1007/978-1-62703-032-8_2
   PubMedGoogle Scholar
• Arora, A., Chandra, N. R., Das, A., Gopal, B., Mande, S. C., Prakash, B., … Vijayan, M. (2011). Structural biology of Mycobacterium tuberculosis proteins: The Indian efforts. Tuberculosis, 91, 456–468. doi:10.1016/j.tube.2011.03.004
   PubMed Web of Science ®Google Scholar
• Chandran, A. V., Prabu, J. R., Nautiyal, A., Patil, K. N., Muniyappa, K., & Vijayan, M. (2015). Structural studies on Mycobacterium tuberculosis RecA: Molecular plasticity and interspecies variability. Journal of Biosciences, 40, 13–30. doi:10.1007/s12038-014-9497-x
   PubMed Web of Science ®Google Scholar
• Chandran, A. V., & Vijayan, M. (2013). Allosteric movements in eubacterial RecA. Biophysical Reviews, 5, 249–258.10.1007/s12551-012-0097-4
   PubMedGoogle Scholar
• Chetnani, B., Kumar, P., Surolia, A., & Vijayan, M. (2010). M. tuberculosis pantothenate kinase: Dual substrate specificity and unusual changes in ligand locations. Journal of Molecular Biology, 400, 171–185. doi:10.1016/j.jmb.2010.04.064
   PubMed Web of Science ®Google Scholar
• Cohen, G. H. (1997). ALIGN: A program to superimpose protein coordinates, accounting for insertions and deletions. Journal of Applied Crystallography, 30, 1160–1161.10.1107/S0021889897006729
   Web of Science ®Google Scholar
• Cox, M. M. (1994). Why does RecA protein hydrolyse ATP? Trends in Biochemical Sciences, 19, 217–222. doi:10.1016/0968-0004(94)90025-6
   PubMed Web of Science ®Google Scholar
• Cox, M. M. (2003). The bacterial RecA protein as a motor protein. Annual Review of Microbiology, 57, 551–577. doi:10.1146/annurev.micro.57.030502.090953
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle Mesh Ewald: An N⋅log(N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98, 10089–10092. doi:10.1063/1.464397
   Web of Science ®Google Scholar
• Datta, S., Ganesh, N., Chandra, N. R., Muniyappa, K., & Vijayan, M. (2003). Structural studies on MtRecA-nucleotide complexes: Insights into DNA and nucleotide binding and the structural signature of NTP recognition. Proteins: Structure, Function, and Bioinformatics, 50, 474–485. doi:10.1002/prot.10315
   PubMed Web of Science ®Google Scholar
• Datta, S., Krishna, R., Ganesh, N., Chandra, N. R., Muniyappa, K., & Vijayan, M. (2003). Crystal structures of Mycobacterium smegmatis RecA and its nucleotide complexes. Journal of Bacteriology, 185, 4280–4284.10.1128/JB.185.14.4280-4284.2003
   PubMed Web of Science ®Google Scholar
• Datta, S., Prabu, M. M., Vaze, M. B., Ganesh, N., Chandra, N. R., Muniyappa, K., & Vijayan, M. (2000). Crystal structures of Mycobacterium tuberculosis RecA and its complex with ADP-AlF4: Implications for decreased ATPase activity and molecular aggregation. Nucleic Acids Research, 28, 4964–4973.10.1093/nar/28.24.4964
   PubMed Web of Science ®Google Scholar
• DeLano, W. L. (2002). The PyMOL molecular graphics system. San Carlos, CA: DeLano Scientific LLC.
   Google Scholar
• Dutreix, M., Moreau, P. L., Bailone, A., Galibert, F., Battista, J. R., Walker, G. C., & Devoret, R. (1989). 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. Journal of Bacteriology, 171, 2415–2423.10.1128/jb.171.5.2415-2423.1989
   PubMed Web of Science ®Google Scholar
• Egelman, E. H. (1993). What do X-ray crystallographic and electron microscopic structural studies of the RecA protein tell us about recombination? Current Opinion in Structural Biology, 3, 189–197. doi:10.1016/S0959-440x(05)80151-4
   Web of Science ®Google Scholar
• Egelman, E. H., & Stasiak, A. (1993). Electron microscopy of RecA-DNA complexes: Two different states, their functional significance and relation to the solved crystal structure. Micron, 24, 309–324. doi:10.1016/0968-4328(93)90056-7
   Web of Science ®Google Scholar
• Emsley, P., Lohkamp, B., Scott, W. G., & Cowtan, K. (2010). Features and development of Coot. Acta Crystallographica Section D – Biological Crystallography, 66(Pt 4), 486–501. doi:10.1107/S0907444910007493
   PubMed Web of Science ®Google Scholar
• Flory, J., Tsang, S. S., & Muniyappa, K. (1984). Isolation and visualization of active presynaptic filaments of recA protein and single-stranded DNA. Proceedings of the National Academy of Sciences, 81, 7026–7030. doi:10.1073/pnas.81.22.7026
   PubMed Web of Science ®Google Scholar
• Goyal, A., Verma, P., Anandhakrishnan, M., Gokhale, R. S., & Sankaranarayanan, R. (2012). Molecular basis of the functional divergence of fatty acyl-AMP ligase biosynthetic enzymes of mycobacterium tuberculosis. Journal of Molecular Biology, 416, 221–238. doi:10.1016/j.jmb.2011.12.031
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J., & Fraaije, J. G. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18, 1463–1472.10.1002/(ISSN)1096-987X
   Web of Science ®Google Scholar
• Hess, B., Kutzner, C., van der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4, 435–447. doi:10.1021/ct700301q
   PubMed Web of Science ®Google Scholar
• Hoover, W. G. (1985). Canonical dynamics: Equilibrium phase-space distributions. Physical Review A, 31, 1695.10.1103/PhysRevA.31.1695
   PubMed Web of Science ®Google Scholar
• Hörtnagel, K., Voloshin, O. N., Kinal, H. H., Ma, N., Schaffer-Judge, C., & Camerini-Otero, R. D. (1999). Saturation mutagenesis of the E. coli RecA loop L2 homologous DNA pairing region reveals residues essential for recombination and recombinational repair. Journal of Molecular Biology, 286, 1097–1106. doi:10.1006/jmbi.1998.2515
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics, 79, 926–935. doi:10.1063/1.445869
   Web of Science ®Google Scholar
• Jorgensen, W. L., & Tirado-Rives, J. (1988). The OPLS [optimized potentials for liquid simulations] potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin. Journal of the American Chemical Society, 110, 1657–1666.10.1021/ja00214a001
   PubMed Web of Science ®Google Scholar
• Kowalczykowski, S. C., Dixon, D. A., Eggleston, A. K., Lauder, S. D., & Rehrauer, W. M. (1994). Biochemistry of homologous recombination in Escherichia coli. Microbiological Reviews, 58, 401–465.
   PubMedGoogle Scholar
• Krishna, R., Manjunath, G. P., Kumar, P., Surolia, A., Chandra, N. R., Muniyappa, K., & Vijayan, M. (2006). Crystallographic identification of an ordered C-terminal domain and a second nucleotide-binding site in RecA: New insights into allostery. Nucleic Acids Research, 34, 2186–2195. doi:10.1093/nar/gkl107
   PubMed Web of Science ®Google Scholar
• Krishna, R., Prabu, J. R., Manjunath, G. P., Datta, S., Chandra, N. R., Muniyappa, K., & Vijayan, M. (2007). Snapshots of RecA protein involving movement of the C-domain and different conformations of the DNA-binding loops: Crystallographic and comparative analysis of 11 structures of Mycobacterium smegmatis RecA. Journal of Molecular Biology, 367, 1130–1144. doi:10.1016/j.jmb.2007.01.058
   PubMed Web of Science ®Google Scholar
• Kukshal, V., Khanam, T., Chopra, D., Singh, N., Sanyal, S., & Ramachandran, R. (2012). M. tuberculosis sliding beta-clamp does not interact directly with the NAD+-dependent DNA ligase. PLoS ONE, 7, e35702. doi:10.1371/journal.pone.0035702
   PubMed Web of Science ®Google Scholar
• Kumar, P., & Bansal, M. (2012). HELANAL-Plus: A web server for analysis of helix geometry in protein structures. Journal of Biomolecular Structure and Dynamics, 30, 773–783.10.1080/07391102.2012.689705
   PubMed Web of Science ®Google Scholar
• Little, J. W. (1991). Mechanism of specific LexA cleavage: Autodigestion and the role of RecA coprotease. Biochimie, 73, 411–421.10.1016/0300-9084(91)90108-D
   PubMed Web of Science ®Google Scholar
• Logan, K. M., & Knight, K. L. (1993). Mutagenesis of the P-loop motif in the ATP binding site of the RecA protein from Escherichia coli. Journal of Molecular Biology, 232, 1048–1059. doi:10.1006/jmbi.1993.1459
   PubMed Web of Science ®Google Scholar
• Lusetti, S. L., & Cox, M. M. (2002). The bacterial RecA protein and the recombinational DNA repair of stalled replication forks. Annual Review of Biochemistry, 71, 71–100. doi:10.1146/annurev.biochem.71.083101.133940
   PubMed Web of Science ®Google Scholar
• Murillo, A. C., Li, H. Y., Alber, T., Baker, E. N., Berger, J. M., Cherney, L. T., … Sacchettini, J. C. (2007). High throughput crystallography of TB drug targets. Infectious Disorders – Drug Targets, 7, 127–139.10.2174/187152607781001853
   PubMedGoogle Scholar
• Nayak, S., Hildebrand, E. L., & Bryant, F. R. (2001). ADP-dependent DNA strand exchange by the mutant [P67G/E68A] RecA protein. Journal of Biological Chemistry, 276, 14933–14938. doi:10.1074/jbc.M100470200
   PubMed Web of Science ®Google Scholar
• Nosé, S. (1984). A unified formulation of the constant temperature molecular dynamics methods. The Journal of Chemical Physics, 81, 511–519.10.1063/1.447334
   Web of Science ®Google Scholar
• Ogawa, T., Shinohara, A., Nabetani, A., Ikeya, T., Yu, X., Egelman, E. H., & Ogawa, H. (1993). RecA-like recombination proteins in eukaryotes: Functions and structures of RAD51 genes. Cold Spring Harbor Symposia on Quantitative Biology, 58, 567–576.10.1101/SQB.1993.058.01.063
   PubMedGoogle Scholar
• Ogawa, T., Yu, X., Shinohara, A., & Egelman, E. H. (1993). Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science, 259, 1896–1899.10.1126/science.8456314
   PubMed Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52, 7182–7190.10.1063/1.328693
   Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera – A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25, 1605–1612.10.1002/(ISSN)1096-987X
   PubMed Web of Science ®Google Scholar
• Phulera, S., & Mande, S. C. (2013). The crystal structure of Mycobacterium tuberculosis NrdH at 0.87 Å suggests a possible mode of its activity. Biochemistry, 52, 4056–4065. doi:10.1021/bi400191z
   PubMed Web of Science ®Google Scholar
• Prabu, J. R., Manjunath, G. P., Chandra, N. R., Muniyappa, K., & Vijayan, M. (2008). Functionally important movements in RecA molecules and filaments: Studies involving mutation and environmental changes. Acta Crystallographica Section D – Biological Crystallography, 64, 1146–1157. doi:10.1107/S0907444908028448
   PubMedGoogle Scholar
• Prabu, J. R., Thamotharan, S., Khanduja, J. S., Chandra, N. R., Muniyappa, K., & Vijayan, M. (2009). Crystallographic and modelling studies on Mycobacterium tuberculosis RuvA. Biochimica et Biophysica Acta (BBA) – Proteins and Proteomics, 1794, 1001–1009. doi:10.1016/j.bbapap.2009.04.003
   PubMed Web of Science ®Google Scholar
• Rajan, R., & Bell, C. E. (2004). Crystal structure of RecA from Deinococcus radiodurans: Insights into the structural basis of extreme radioresistance. Journal of Molecular Biology, 344, 951–963. doi:10.1016/j.jmb.2004.09.087
   PubMed Web of Science ®Google Scholar
• Roy, S., Saraswathi, R., Chatterji, D., & Vijayan, M. (2008). Structural studies on the second Mycobacterium smegmatis Dps: Invariant and variable features of structure, assembly and function. Journal of Molecular Biology, 375, 948–959. doi:10.1016/j.jmb.2007.10.023
   PubMed Web of Science ®Google Scholar
• Seitz, E. M., Brockman, J. P., Sandler, S. J., Clark, A. J., & Kowalczykowski, S. C. (1998). RadA protein is an archaeal RecA protein homolog that catalyzes DNA strand exchange. Genes & Development, 12, 1248–1253.10.1101/gad.12.9.1248
   PubMed Web of Science ®Google Scholar
• Selvaraj, M., Roy, S., Singh, N. S., Sangeetha, R., Varshney, U., & Vijayan, M. (2007). Structural plasticity and enzyme action: Crystal structures of mycobacterium tuberculosis peptidyl-tRNA hydrolase. Journal of Molecular Biology, 372, 186–193. doi:10.1016/j.jmb.2007.06.053
   PubMed Web of Science ®Google Scholar
• Shvetsov, A. V., Lebedev, D. V., Chervyakova, D. B., Bakhlanova, I. V., Yung, I. A., Radulescu, A., … Isaev-Ivanov, V. V. (2014). Structure of RecX protein complex with the presynaptic RecA filament: Molecular dynamics simulations and small angle neutron scattering. FEBS Letters, 588, 948–955.10.1016/j.febslet.2014.01.053
   PubMed Web of Science ®Google Scholar
• Story, R. M., & Steitz, T. A. (1992). Structure of the recA protein-ADP complex. Nature, 355, 374–376. doi:10.1038/355374a0
   PubMed Web of Science ®Google Scholar
• Story, R. M., Weber, I. T., & Steitz, T. A. (1992). The structure of the E. coli recA protein monomer and polymer. Nature, 355, 318–325. doi:10.1038/355318a0
   PubMed Web of Science ®Google Scholar
• Terwilliger, T. C., Park, M. S., Waldo, G. S., Berendzen, J., Hung, L. W., Kim, C. Y., … Rupp, B. (2003). The TB structural genomics consortium: A resource for Mycobacterium tuberculosis biology. Tuberculosis, 83, 223–249.10.1016/S1472-9792(03)00051-9
   PubMed Web of Science ®Google Scholar
• Vijayan, M. (2005). Structural biology of mycobacterial proteins: The Bangalore effort. Tuberculosis, 85, 357–366. doi:10.1016/j.tube.2005.08.011
   PubMed Web of Science ®Google Scholar
• Xing, X., & Bell, C. E. (2004a). Crystal structures of Escherichia coli RecA in a compressed helical filament. Journal of Molecular Biology, 342, 1471–1485. doi:10.1016/j.jmb.2004.07.091
   PubMed Web of Science ®Google Scholar
• Xing, X., & Bell, C. E. (2004b). Crystal structures of Escherichia coli RecA in complex with MgADP and MnAMP-PNP. Biochemistry, 43, 16142–16152. doi:10.1021/bi048165y
   PubMed Web of Science ®Google Scholar
• Yu, X., Shvetsov, A., Karelov, D., Lebedev, D., Radulescu, A., Petukhov, M., & Isaev-Ivanov, V. (2012). Correlated motion of protein subdomains and large-scale conformational flexibility of RecA protein filament. In Journal of Physics: Conference Series (Vol. 340, p. 012094). Prague, Czech Republic: IOP Publishing.
   Google Scholar
• Yu, X., VanLoock, M. S., Yang, S., Reese, J. T., & Egelman, E. H. (2004). What is the structure of the RecA-DNA filament? Current Protein & Peptide Science, 5, 73–79. doi:10.2174/1389203043486883
   PubMed Web of Science ®Google Scholar