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Crystal structures of Escherichia coli RecA in a compressed helical filament.

Xing X, Bell CE
J Mol Biol 342 1471-85 (2004)
Related entries: 1u94, 1u99

Cited: 39 times
EuropePMC logo PMID: 15364575

Abstract

The X-ray crystal structure of uncomplexed Escherichia coli RecA protein has been determined in three new crystal forms at resolutions of 1.9 A, 2.0 A, and 2.6 A. The RecA protein used for this study contains the extra residues Gly-Ser-His-Met at the N terminus, but retains normal ssDNA-dependent ATPase and coprotease activities. In all three crystals, RecA is packed in a right-handed helical filament with a pitch of approximately 74 A. These RecA filaments are compressed relative to the original crystal structure of RecA, which has a helical pitch of 82.7 A. In the structures of the compressed RecA filament, the monomer-monomer interface and the core domain are essentially the same as in the RecA structure with the 83 A pitch. The change in helical pitch is accommodated by a small movement of the N-terminal domain, which is reoriented to preserve the contacts it makes at the monomer-monomer interface. The new crystal structures show significant variation in the orientation and conformation of the C-terminal domain, as well as in the inter-filament packing interactions. In crystal form 2, a calcium ion is bound closely to a beta-hairpin of the C-terminal domain and to Asp38 of a neighboring filament, and residues 329-331 of the C-terminal tail become ordered to contact a neighboring filament. In crystal forms 3 and 4, a sulfate ion or a phosphate anion is bound to the same site on RecA as the beta-phosphate group of ADP, causing an opening of the P-loop. Altogether, the structures show the conformational variability of RecA protein in the crystalline state, providing insight into many aspects of RecA function.

Reviews - 1u98 mentioned but not cited (1)

  1. Allosteric movements in eubacterial RecA. Chandran AV, Vijayan M. Biophys Rev 5 249-258 (2013)

Articles - 1u98 mentioned but not cited (1)

  1. Structural and Functional Studies of H. seropedicae RecA Protein - Insights into the Polymerization of RecA Protein as Nucleoprotein Filament. Leite WC, Galvão CW, Saab SC, Iulek J, Etto RM, Steffens MB, Chitteni-Pattu S, Stanage T, Keck JL, Cox MM. PLoS One 11 e0159871 (2016)


Reviews citing this publication (8)

  1. Regulation of bacterial RecA protein function. Cox MM. Crit Rev Biochem Mol Biol 42 41-63 (2007)
  2. Motoring along with the bacterial RecA protein. Cox MM. Nat Rev Mol Cell Biol 8 127-138 (2007)
  3. Deposition diseases and 3D domain swapping. Bennett MJ, Sawaya MR, Eisenberg D. Structure 14 811-824 (2006)
  4. Structure and mechanism of Escherichia coli RecA ATPase. Bell CE. Mol Microbiol 58 358-366 (2005)
  5. Common mechanisms of DNA translocation motors in bacteria and viruses using one-way revolution mechanism without rotation. Guo P, Zhao Z, Haak J, Wang S, Wu D, Meng B, Weitao T. Biotechnol Adv 32 853-872 (2014)
  6. Advances in structural studies of recombination mediator proteins. Korolev S. Biophys Chem 225 27-37 (2017)
  7. Homologous Recombination under the Single-Molecule Fluorescence Microscope. Gibbs DR, Dhakal S. Int J Mol Sci 20 E6102 (2019)
  8. Generation and Repair of Postreplication Gaps in Escherichia coli. Cox MM, Goodman MF, Keck JL, van Oijen A, Lovett ST, Robinson A. Microbiol Mol Biol Rev 87 e0007822 (2023)

Articles citing this publication (29)

  1. Intracellular protein and DNA dynamics in competent Bacillus subtilis cells. Kidane D, Graumann PL. Cell 122 73-84 (2005)
  2. Essential roles for imuA'- and imuB-encoded accessory factors in DnaE2-dependent mutagenesis in Mycobacterium tuberculosis. Warner DF, Ndwandwe DE, Abrahams GL, Kana BD, Machowski EE, Venclovas C, Mizrahi V. Proc Natl Acad Sci U S A 107 13093-13098 (2010)
  3. Separation of recombination and SOS response in Escherichia coli RecA suggests LexA interaction sites. Adikesavan AK, Katsonis P, Marciano DC, Lua R, Herman C, Lichtarge O. PLoS Genet 7 e1002244 (2011)
  4. The Rad51/RadA N-terminal domain activates nucleoprotein filament ATPase activity. Galkin VE, Wu Y, Zhang XP, Qian X, He Y, Yu X, Heyer WD, Luo Y, Egelman EH. Structure 14 983-992 (2006)
  5. Crystal structure of RecA from Deinococcus radiodurans: insights into the structural basis of extreme radioresistance. Rajan R, Bell CE. J Mol Biol 344 951-963 (2004)
  6. Crystal structure of the left-handed archaeal RadA helical filament: identification of a functional motif for controlling quaternary structures and enzymatic functions of RecA family proteins. Chen LT, Ko TP, Chang YC, Lin KA, Chang CS, Wang AH, Wang TF. Nucleic Acids Res 35 1787-1801 (2007)
  7. Conformational flexibility revealed by the crystal structure of a crenarchaeal RadA. Ariza A, Richard DJ, White MF, Bond CS. Nucleic Acids Res 33 1465-1473 (2005)
  8. Finding of widespread viral and bacterial revolution dsDNA translocation motors distinct from rotation motors by channel chirality and size. De-Donatis GM, Zhao Z, Wang S, Huang LP, Schwartz C, Tsodikov OV, Zhang H, Haque F, Guo P. Cell Biosci 4 30 (2014)
  9. Cleavage of bacteriophage lambda cI repressor involves the RecA C-terminal domain. Galkin VE, Yu X, Bielnicki J, Ndjonka D, Bell CE, Egelman EH. J Mol Biol 385 779-787 (2009)
  10. Crystallographic identification of an ordered C-terminal domain and a second nucleotide-binding site in RecA: new insights into allostery. Krishna R, Manjunath GP, Kumar P, Surolia A, Chandra NR, Muniyappa K, Vijayan M. Nucleic Acids Res 34 2186-2195 (2006)
  11. Probing adenosine nucleotide-binding proteins with an affinity-labeled nucleotide probe and mass spectrometry. Qiu H, Wang Y. Anal Chem 79 5547-5556 (2007)
  12. 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. Krishna R, Prabu JR, Manjunath GP, Datta S, Chandra NR, Muniyappa K, Vijayan M. J Mol Biol 367 1130-1144 (2007)
  13. Molecular determinants of the DprA-RecA interaction for nucleation on ssDNA. Lisboa J, Andreani J, Sanchez D, Boudes M, Collinet B, Liger D, van Tilbeurgh H, Guérois R, Quevillon-Cheruel S. Nucleic Acids Res 42 7395-7408 (2014)
  14. Structure of the hDmc1-ssDNA filament reveals the principles of its architecture. Okorokov AL, Chaban YL, Bugreev DV, Hodgkinson J, Mazin AV, Orlova EV. PLoS One 5 e8586 (2010)
  15. Structural biology of mycobacterial proteins: the Bangalore effort. Vijayan M. Tuberculosis (Edinb) 85 357-366 (2005)
  16. Loss of genes for DNA recombination and repair in the reductive genome evolution of thioautotrophic symbionts of Calyptogena clams. Kuwahara H, Takaki Y, Shimamura S, Yoshida T, Maeda T, Kunieda T, Maruyama T. BMC Evol Biol 11 285 (2011)
  17. Structure of a hyper-cleavable monomeric fragment of phage lambda repressor containing the cleavage site region. Ndjonka D, Bell CE. J Mol Biol 362 479-489 (2006)
  18. Inter-subunit interactions that coordinate Rad51's activities. Grigorescu AA, Vissers JH, Ristic D, Pigli YZ, Lynch TW, Wyman C, Rice PA. Nucleic Acids Res 37 557-567 (2009)
  19. Structure of RadB recombinase from a hyperthermophilic archaeon, Thermococcus kodakaraensis KOD1: an implication for the formation of a near-7-fold helical assembly. Akiba T, Ishii N, Rashid N, Morikawa M, Imanaka T, Harata K. Nucleic Acids Res 33 3412-3423 (2005)
  20. Probing the DNA sequence specificity of Escherichia coli RECA protein. Rajan R, Wisler JW, Bell CE. Nucleic Acids Res 34 2463-2471 (2006)
  21. Two modes of binding of DinI to RecA filament provide a new insight into the regulation of SOS response by DinI protein. Galkin VE, Britt RL, Bane LB, Yu X, Cox MM, Egelman EH. J Mol Biol 408 815-824 (2011)
  22. Role of allosteric switch residue histidine 195 in maintaining active-site asymmetry in presynaptic filaments of bacteriophage T4 UvsX recombinase. Farb JN, Morrical SW. J Mol Biol 385 393-404 (2009)
  23. Structural studies on Mycobacterium tuberculosis RecA: molecular plasticity and interspecies variability. Chandran AV, Prabu JR, Nautiyal A, Patil KN, Muniyappa K, Vijayan M. J Biosci 40 13-30 (2015)
  24. Structure and interactions of RecA: plasticity revealed by molecular dynamics simulations. Chandran AV, Jayanthi S, Vijayan M. J Biomol Struct Dyn 36 98-111 (2018)
  25. Ion specific influences on the stability and unfolding transitions of a naturally aggregating protein; RecA. Cannon WR, Talley ND, Danzig BA, Liu X, Martinez JS, Shreve AP, MacDonald G. Biophys Chem 163-164 56-63 (2012)
  26. Conformational flexibility of RecA protein filament: transitions between compressed and stretched states. Petukhov M, Lebedev D, Shalguev V, Islamov A, Kuklin A, Lanzov V, Isaev-Ivanov V. Proteins 65 296-304 (2006)
  27. Structural insights into the inhibition of bacterial RecA by naphthalene polysulfonated compounds. Zhou Z, Pan Q, Lv X, Yuan J, Zhang Y, Zhang MX, Ke M, Mo XM, Xie YL, Liu Y, Chen T, Liang M, Yin F, Liu L, Zhou Y, Qiao K, Liu R, Li Z, Wong NK. iScience 24 101952 (2021)
  28. A rationally designed peptide enhances homologous recombination in vitro and resistance to DNA damaging agents in vivo. Chen LT, Wang AH. Nucleic Acids Res 38 4361-4371 (2010)
  29. MAW point mutation impairs H. Seropedicae RecA ATP hydrolysis and DNA repair without inducing large conformational changes in its structure. Leite WC, Penteado RF, Gomes F, Iulek J, Etto RM, Saab SC, Steffens MBR, Galvão CW. PLoS One 14 e0214601 (2019)


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