DNA binding mediates conformational changes and metal ion coordination in the active site of PcrA helicase

Journal of Molecular Biology

Volumn 290, Issue 1, 1999, Pages 137-148

  Soultanas, Panos ^a   Dillingham, Mark S ^a   Velankar, Sameer S ^a   Wigley, Dale B ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

ATP hydrolysis; Crystal structure; Helicase; Mutagenesis; PcrA

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; HELICASE; MAGNESIUM ION; METAL ION; SINGLE STRANDED DNA;

ARTICLE; BINDING SITE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN DNA BINDING;

EID: 0033516596     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2873     Document Type: Article

References (39)

1. Bennet W. S., Steitz T. A. Structure of a complex between yeast hexokinase A and glucose. J. Mol. Biol. 140:1980;183-230.
2. Berchtold H., Reshetnikova L., Reiser C. O. A., Schirmer N. K., Sprinzl M., Hilgenfeld R. Crystal structure of active elongation factor Tu reveals major domain rearrangements. Nature. 365:1993;126-132.
3. Bird L. E., Brannigan J. A., Subramanya H. S., Wigley D. B. Characterisation of Bacillus stearothermophilus PcrA helicase: evidence against an active rolling mechanism. Nucl. Acids Res. 26:1998;2686-2693.
4. Brosh R. M. Jr, Matson S. W. Mutations in motif II of Escherichia coli DNA helicase II render the enzyme nonfunctional in both mismatch repair and excision repair with differential effects on the unwinding reaction. J. Bacteriol. 177:1995;5612-5621.
5. Brunger At. T., Karplus M., Petsko G. A. Crystallographic refinement by simulated annealing: application to crambin. Acta Crystallog. sect. A. 45:1989;50-61.
6. Crute J. J., Mocarski E. S., Lehman I. R. A DNA helicase induced by herpes simplex virus type I. Nucl. Acids Res. 16:1988;6585-6596.
7. George J. W., Brosh R. M. Jr, Matson S. W. A dominant negative allele of the Escherichia coli uvrD gene encoding DNA helicase II. J. Mol. Biol. 235:1994;424-435.
8. Gorbalenya A. E., Koonin E. V. Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin Struct. Biol. 3:1993;419-429.
9. Gross C. H., Shuman S. Mutational analysis of vaccinia virus nucleoside triphosphate phosphohydrolase II, a DExH box RNA helicase. J. Virol. 69:1995;4727-4736.
10. Håkansson K., Doherty A. J., Shuman S., Wigley D. B. X-ray crystallography reveals a large conformational change during guanyl transfer by mRNA capping enzymes. Cell. 89:1997;545-553.
11. Hall M. C., Matson S. W. Mutation of a highly conserved arginine in motif IV of Escherichia coli DNA helicase II results in an ATP-binding defect. J. Biol. Chem. 272:1997;18614-18620.
12. Hall M. C., Özsoy A. Z., Matson S. W. Site-directed mutations in Motif VI of Escherichia coli DNA helicase II result in multiple biochemical defects: evidence for the involvement of motif VI in the coupling of ATPase and DNA binding activities via conformational changes. J. Mol. Biol. 277:1998;257-271.
13. Korangy F., Julin D. A. Enzymatic effects of a lysine-to-glutamine mutation in the ATP-binding consensus sequence in the RecD subunit of the RecBCD enzyme from Escherichia coli. J. Biol. Chem. 267:1992;1733-1740.
14. Korolev S., Hsieh J., Gauss G. H., Lohman T. M., Waksman G. Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell. 90:1996;635-647.
15. La Cour T. F. M., Nybord J., Thirup S., Clarke B. F. C. Structural details of the binding guanosine diphosphate to elongation factor Tu from E. coli as studied by X-ray crystallography. EMBO J. 4:1985;2385-2388.
16. Laemmli U. K. Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
17. Lanzetta P. A., Alvarez L. J., Reinach P. S., Candia O. A. An improved assay for nanomole amounts of inorganic phosphate. Anal. Biochem. 100:1979;95-97.
18. Lohman T. M., Bjornson K. P. Mechanisms of helicase-catalyzed DNA unwinding. Annu. Rev. Biochem. 65:1996;169-214.
19. McPherson M. J., Quirke P., Taylor G. R. PCR, A Practical Approach. 1992;IRL Press, Oxford. p. 207-209.
20. Myles G. M., Hearst J. E., Sancar A. Site-specific mutagenesis of conserved residues within Walker A and B sequences of Escherichia coli UvrA protein. Biochemistry. 30:1991;3824-3834.
21. Noel J. P., Hamm H. E., Sigler P. B. The 2.2 Å crystal structure of transducin-α complexed with GTPγS. Nature. 366:1993;654-663.
22. Notarnicola S. M., Richardson C. C. The nucleotide binding site of helicase/primase of bacteriophage T7. Interactions of mutant and wild-type proteins. J. Biol. Chem. 268:1993;27198-27207.
23. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
24. Pai E. F., Kabsh W., Krengel U., Holmes K. C., John J., Wittinghoffer A. Structure of the guanine-nucleotide-binding domain of the Ha-ras oncogene product p21 in the triphosphate conformation. Nature. 341:1989;209-214.
25. Parsonage D., Al-Shawi M. K., Senior A. E. Directed mutations of strongly conserved lysing 155 in the catalytic nucleotide-binding domain of β-subunit of F1-ATPase from Escherichia coli. J. Biol. Chem. 263:1988;4740-4744.
26. Patel S. S., Hingorani M. M., Ng W. M. The K318A mutant bacteriophage T7 DNA primase-helicase protein is deficient in helicase but not primase activity and inhibits primase-helicas protein wild-type activities by heterooligomer formation. Biochemistry. 33:1994;7857-7868.
27. Pause A., Sonenburg N. Mutational analysis of a DEAD box RNA helicase: the mammalian translation initiation factor elF-4A. EMBO J. 7:1992;2643-2654.
28. Pullman M. E., Penefsky H. S., Datta A., Racker E. Partial resolution of the enzymes catalyzing oxidative phosphorylation. J. Biol. Chem. 235:1960;3322-3329.
29. Rehrauer W. M., Kowalczykowski S. C. Alteration of the nucleoside triphosphate (NTP) catalytic domain within Escherichia coli recA protein attenuates NTP hydrolysis but not joint molecule formation. J. Biol. Chem. 268:1993;1292-1297.
30. Roussel A., Cambillau C. TURBO-FRODO. Silicon Graphics Geometry Partner Directory. 1989;Silicon Graphics, Mountain View, CA. p. 77-78.
31. Rozen F. J., Pelletier J., Trachsel H., Sonenberg N. A lysine substitution in the ATP-binding site of eucaryotic initiation factor 4A abrogates nucleotide-binding activity. Mol. Cell. Biol. 9:1989;4061-4063.
32. Schulz G. E. Binding of nucleotides by proteins. Curr. Opin. Struct. Biol. 2:1992;61-67.
33. Schulz G. E., Muller W. C., Diederichs K. Induced-fit movements in adenylate kinases. J. Mol. Biol. 213:1990;627-630.
34. Soultanas P., Dillingham M. S., Wigley D. B. Escherichia coli ribosomal protein L3 stimulates the helicase activity of the Bacillus stearothermophilus PcrA helicase. Nucl. Acid Res. 26:1998;2374-2379.
35. Story R. M., Steitz T. A. Structure of the recA protein-ADP complex. Nature. 355:1992;374-376.
36. Subramanya H. S., Bird L. E., Brannigan J. A., Wigley D. B. Crystal structure of a DExx box DNA helicase. Nature. 384:1996;379-383.
37. Sung P., Higgins D., Prakash L., Prakash S. Mutation of lysine-48 to arginine in the yeast RAD3 protein abolishes its ATPase and DNA helicase activities but not the ability to bind ATP. EMBO J. 7:1988;3263-3269.
38. Velankar S. S., Soultanas P., Dillingham M. S., Subramanya H. S., Wigley D. B. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell. 97:1999;75-84.
39. Walker J. E., Saraste M., Runswick M. J., Gray N. J. Distantly related sequences in the A- and B-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J. 1:1982;945-951.