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Structural studies on MtRecA-nucleotide complexes: insights into DNA and nucleotide binding and the structural signature of NTP recognition.

Datta S, Ganesh N, Chandra NR, Muniyappa K, Vijayan M
Proteins 50 474-85 (2003)
Related entries: 1mo4, 1mo5, 1mo6

Cited: 38 times
EuropePMC logo PMID: 12557189

Abstract

RecA protein plays a crucial role in homologous recombination and repair of DNA. Central to all activities of RecA is its binding to Mg(+2)-ATP. The active form of the protein is a helical nucleoprotein filament containing the nucleotide cofactor and single-stranded DNA. The stability and structure of the helical nucleoprotein filament formed by RecA are modulated by nucleotide cofactors. Here we report crystal structures of a MtRecA-ADP complex, complexes with ATPgammaS in the presence and absence of magnesium as well as a complex with dATP and Mg+2. Comparison with the recently solved crystal structures of the apo form as well as a complex with ADP-AlF4 confirms an expansion of the P-loop region in MtRecA, compared to its homologue in Escherichia coli, correlating with the reduced affinity of MtRecA for ATP. The ligand bound structures reveal subtle variations in nucleotide conformations among different nucleotides that serve in maintaining the network of interactions crucial for nucleotide binding. The nucleotide binding site itself, however, remains relatively unchanged. The analysis also reveals that ATPgammaS rather than ADP-AlF4 is structurally a better mimic of ATP. From among the complexed structures, a definition for the two DNA-binding loops L1 and L2 has clearly emerged for the first time and provides a basis to understand DNA binding by RecA. The structural information obtained from these complexes correlates well with the extensive biochemical data on mutants available in the literature, contributing to an understanding of the role of individual residues in the nucleotide binding pocket, at the molecular level. Modeling studies on the mutants again point to the relative rigidity of the nucleotide binding site. Comparison with other NTP binding proteins reveals many commonalties in modes of binding by diverse members in the structural family, contributing to our understanding of the structural signature of NTP recognition.

Articles - 1mo3 mentioned but not cited (4)

  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)
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  3. 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)
  4. In-vivo studies on Transitmycin, a potent Mycobacterium tuberculosis inhibitor. Mondal R, Dusthackeer V N A, Kannan P, Singh AK, Thiruvengadam K, Manikkam R, A S S, Balasubramanian M, Elango P, Ebenezer Rajadas S, Bharadwaj D, Arumugam GS, Ganesan S, Kumar A K H, Singh M, Patil S, U C A J, Doble M, R B, Tripathy SP, Kumar V. PLoS One 18 e0282454 (2023)


Reviews citing this publication (7)

  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)
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  5. Advances in structural studies of recombination mediator proteins. Korolev S. Biophys Chem 225 27-37 (2017)
  6. Techniques and applications: The heterologous expression of Mycobacterium tuberculosis genes is an uphill road. Bellinzoni M, Riccardi G. Trends Microbiol 11 351-358 (2003)
  7. Allosteric movements in eubacterial RecA. Chandran AV, Vijayan M. Biophys Rev 5 249-258 (2013)

Articles citing this publication (27)

  1. Crystal structure of a Rad51 filament. Conway AB, Lynch TW, Zhang Y, Fortin GS, Fung CW, Symington LS, Rice PA. Nat Struct Mol Biol 11 791-796 (2004)
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  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. Complexes of RecA with LexA and RecX differentiate between active and inactive RecA nucleoprotein filaments. VanLoock MS, Yu X, Yang S, Galkin VE, Huang H, Rajan SS, Anderson WF, Stohl EA, Seifert HS, Egelman EH. J Mol Biol 333 345-354 (2003)
  5. 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)
  6. 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)
  7. Crystal structures of Escherichia coli RecA in a compressed helical filament. Xing X, Bell CE. J Mol Biol 342 1471-1485 (2004)
  8. Crystal structures of Mycobacterium smegmatis RecA and its nucleotide complexes. Datta S, Krishna R, Ganesh N, Chandra NR, Muniyappa K, Vijayan M. J Bacteriol 185 4280-4284 (2003)
  9. Structure of adeno-associated virus type 2 Rep40-ADP complex: insight into nucleotide recognition and catalysis by superfamily 3 helicases. James JA, Aggarwal AK, Linden RM, Escalante CR. Proc Natl Acad Sci U S A 101 12455-12460 (2004)
  10. DNA helicase activity of PcrA is not required for the displacement of RecA protein from DNA or inhibition of RecA-mediated strand exchange. Anand SP, Zheng H, Bianco PR, Leuba SH, Khan SA. J Bacteriol 189 4502-4509 (2007)
  11. 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)
  12. Complementary strand relocation may play vital roles in RecA-based homology recognition. Peacock-Villada A, Yang D, Danilowicz C, Feinstein E, Pollock N, McShan S, Coljee V, Prentiss M. Nucleic Acids Res 40 10441-10451 (2012)
  13. Phosphorylation of Deinococcus radiodurans RecA Regulates Its Activity and May Contribute to Radioresistance. Rajpurohit YS, Bihani SC, Waldor MK, Misra HS. J Biol Chem 291 16672-16685 (2016)
  14. 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)
  15. Modeling the early stage of DNA sequence recognition within RecA nucleoprotein filaments. Saladin A, Amourda C, Poulain P, Férey N, Baaden M, Zacharias M, Delalande O, Prévost C. Nucleic Acids Res 38 6313-6323 (2010)
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  17. Disassembly of Escherichia coli RecA E38K/DeltaC17 nucleoprotein filaments is required to complete DNA strand exchange. Britt RL, Haruta N, Lusetti SL, Chitteni-Pattu S, Inman RB, Cox MM. J Biol Chem 285 3211-3226 (2010)
  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. The SOS Regulatory Network. Simmons LA, Foti JJ, Cohen SE, Walker GC. EcoSal Plus 2008 (2008)
  20. Loop 2 in Saccharomyces cerevisiae Rad51 protein regulates filament formation and ATPase activity. Zhang XP, Galkin VE, Yu X, Egelman EH, Heyer WD. Nucleic Acids Res 37 158-171 (2009)
  21. 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)
  22. 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)
  23. 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)
  24. Micro-homology intermediates: RecA's transient sampling revealed at the single molecule level. Lee AJ, Endo M, Hobbs JK, Davies AG, Wälti C. Nucleic Acids Res 49 1426-1435 (2021)
  25. Phosphorylation of deinococcal RecA affects its structural and functional dynamics implicated for its roles in radioresistance of Deinococcus radiodurans. Sharma DK, Siddiqui MQ, Gadewal N, Choudhary RK, Varma AK, Misra HS, Rajpurohit YS. J Biomol Struct Dyn 38 114-123 (2020)
  26. RecA assembly, one molecule at a time. Egelman EH. Structure 14 1600-1602 (2006)
  27. Computational elucidation of the binding mechanisms of curcumin analogues as bacterial RecA inhibitors. Zhou ZY, Yuan J, Pan Q, Mo XM, Xie YL, Yin F, Li Z, Wong NK. RSC Adv 9 19869-19881 (2019)


Related citations provided by authors (2)

  1. Crystal Structures of Mycobacterium Tuberculosis Reca and its Complex with Adp-Alf4: Implications For Decreased ATPase Activity and Molecular Aggregation. Datta S, Prabu M, Vaze MB, Ganesh N, Chandra NR, MUNIYAPPA K, VIJAYAN M Nucleic Acids Res. 28 4964-4973 (2000)
  2. Functional Characterization of the Precursor and Spliced Forms of Reca Protein of Mycobacterium Tuberculosis.. Ajay Kumar R, Vaze M, Chandra NR, VIJAYAN M, MUNIYAPPA K Biochemistry 35 1793-1802 (1996)

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