Modular architecture of the bacteriophage T7 primase couples RNA primer synthesis to DNA synthesis

Molecular Cell

Volumn 11, Issue 5, 2003, Pages 1349-1360

  Kato, Masato ^a   Ito, Takuhiro ^a   Wagner, Gerhard ^a   Richardson, Charles C ^a   Ellenberger, Tom ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DNA PRIMASE; NUCLEOTIDE; ZINC;

ARCHITECTURE; ARTICLE; BACTERIOPHAGE T7; BIOCHEMISTRY; CRYSTAL STRUCTURE; DNA BINDING; DNA SYNTHESIS; DNA TEMPLATE; GENE LOCUS; MOLECULAR DYNAMICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PROKARYOTE; PROTEIN DOMAIN; RNA SYNTHESIS;

BACTERIA (MICROORGANISMS); PROKARYOTA;

EID: 0038054465     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00195-3     Document Type: Article

References (74)

1. Aravind L., Leipe D.D., Koonin E.V. Toprim - a conserved catalytic domain in type IA and II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins. Nucleic Acids Res. 26:1998;4205-4213.
2. Augustin M.A., Huber R., Kaiser J.T. Crystal structure of a DNA-dependent RNA polymerase (DNA primase). Nat. Struct. Biol. 8:2001;57-61.
3. Bailey S. The CCP4 suite-programs for protein crystallography. Acta Crystallogr. D50:1994;760-763.
4. Benkovic S.J., Valentine A.M., Salinas F. Replisome-mediated DNA replication. Annu. Rev. Biochem. 70:2001;181-208.
5. Berger J.M., Gamblin S.J., Harrison S.C., Wang J.C. Structure and mechanism of DNA topoisomerase II. Nature. 379:1996;225-232.
6. Bernstein J.A., Richardson C.C. A 7-kDa region of the bacteriophage T7 gene 4 protein is required for primase but not for helicase activity. Proc. Natl. Acad. Sci. USA. 85:1988;396-400.
7. Bird L.E., Hakansson K., Pan H., Wigley D.B. Characterization and crystallization of the helicase domain of bacteriophage T7 gene 4 protein. Nucleic Acids Res. 25:1997;2620-2626.
8. Bird L.E., Pan H., Soultanas P., Wigley D.B. Mapping protein-protein interactions within a stable complex of DNA primase and DnaB helicase from Bacillus stearothermophilus. Biochemistry. 39:2000;171-182.
9. Brautigam C.A., Steitz T.A. Structural and functional insights provided by crystal structures of DNA polymerases and their substrate complexes. Curr. Opin. Struct. Biol. 8:1998;54-63.
10. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S.et al. Crystallography & NMR system. a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54:1998;905-921.
11. Carson M. Ribbons. Carter C.W. Jr., Sweet R.M. Methods in Enzymology. 1997;Academic Press, Orlando. 493-505.pp.
12. Chang P., Marians K.J. Identification of a region of Escherichia coli DnaB required for functional interaction with DnaG at the replication fork. J. Biol. Chem. 275:2000;26187-26195.
13. Chowdhury K., Tabor S., Richardson C.C. A unique loop in the DNA-binding crevice of bacteriophage T7 DNA polymerase influences primer utilization. Proc. Natl. Acad. Sci. USA. 97:2000;12469-12474.
14. Cowtan K., Main P. Phase combination and cross validation in iterated density-modification calculation. Acta Crystallogr. D52:1996;43-48.
15. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., Bax A. NMRPipe. a multidimensional spectral processing system based on UNIX pipes J. Biomol. NMR. 6:1995;277-293.
16. Doublie S., Ellenberger T. The mechanism of action of T7 DNA polymerase. Curr. Opin. Struct. Biol. 8:1998;704-712.
17. Dunn J.J., Studier F.W. Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J. Mol. Biol. 166:1983;477-535.
18. Egelman H.H., Yu X., Wild R., Hingorani M.M., Patel S.S. Bacteriophage T7 helicase/primase proteins form rings around single-stranded DNA that suggest a general structure for hexameric helicases. Proc. Natl. Acad. Sci. USA. 92:1995;3869-3873.
19. Farrow N.A., Muhandiram R., Singer A.U., Pascal S.M., Kay C.M., Gish G., Shoelson S.E., Pawson T., Forman-Kay J.D., Kay L.E. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry. 33:1994;5984-6003.
20. Frick D.N., Richardson C.C. Interaction of bacteriophage T7 gene 4 primase with its template recognition site. J. Biol. Chem. 274:1999;35889-35898.
21. Frick D.N., Richardson C.C. DNA primases. Annu. Rev. Biochem. 70:2001;39-80.
22. Frick D.N., Baradaran K., Richardson C.C. An N-terminal fragment of the gene 4 helicase/primase of bacteriophage T7 retains primase activity in the absence of helicase activity. Proc. Natl. Acad. Sci. USA. 95:1998;7957-7962.
23. Fujiyama A., Kohara Y., Okazaki T. Initiation sites for discontinuous DNA synthesis of bacteriophage T7. Proc. Natl. Acad. Sci. USA. 78:1981;903-907.
24. Gnatt A.L., Cramer P., Fu J., Bushnell D.A., Kornberg R.D. Structural basis of transcription. an RNA polymerase II elongation complex at 3.3 Å resolution Science. 292:2001;1876-1882.
25. Godson G.N., Schoenich J., Sun W., Mustaev A.A. Identification of the magnesium ion binding site in the catalytic center of Escherichia coli primase by iron cleavage. Biochemistry. 39:2000;332-339.
26. Griep M.A. Primase structure and function. Indian J. Biochem. Biophys. 32:1995;171-178.
27. Guo S., Tabor S., Richardson C.C. The linker region between the helicase and primase domains of the bacteriophage T7 gene 4 protein is critical for hexamer formation. J. Biol. Chem. 274:1999;30303-30309.
28. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:1993;123-138.
29. Ilyina T.V., Gorbalenya A.E., Koonin E.V. Organization and evolution of bacterial and bacteriophage primase-helicase systems. J. Mol. Evol. 34:1992;351-357.
30. Johnson B.A., Blevins R.A. NMRView. a computer program for the visualization and analysis of NMR data J. Biomol. NMR. 4:1994;603-614.
31. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A. 47(Pt 2):1991;110-119.
32. Kato M., Frick D.N., Lee J., Tabor S., Richardson C.C., Ellenberger T. A complex of the bacteriophage T7 primase-helicase and DNA polymerase directs primer utilization. J. Biol. Chem. 276:2001;21809-21820.
33. Keck J.L., Berger J.M. Primus inter pares (first among equals). Nat. Struct. Biol. 8:2001;2-4.
34. Keck J.L., Roche D.D., Lynch A.S., Berger J.M. Structure of the RNA polymerase domain of E. coli primase. Science. 287:2000;2482-2486.
35. Kraulis P.J. Molscript. a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallogr. 24:1991;946-950.
36. Kusakabe T., Richardson C.C. The role of the zinc motif in sequence recognition by DNA primases. J. Biol. Chem. 271:1996;19563-19570.
37. Kusakabe T., Richardson C.C. Gene 4 DNA primase of bacteriophage T7 mediates the annealing and extension of ribo-oligonucleotides at primase recognition sites. J. Biol. Chem. 272:1997;12446-12453.
38. Kusakabe T., Baradaran K., Lee J., Richardson C.C. Roles of the helicase and primase domain of the gene 4 protein of bacteriophage T7 in accessing the primase recognition site. EMBO J. 17:1998;1542-1552.
39. Kusakabe T., Hine A.V., Hyberts S.G., Richardson C.C. The Cys4 zinc finger of bacteriophage T7 primase in sequence-specific single-stranded DNA recognition. Proc. Natl. Acad. Sci. USA. 96:1999;4295-4300.
40. Lee J., Chastain P.D., Kusakabe T., Griffith J.D., Richardson C.C. Coordinated leading and lagging strand DNA synthesis on a minicircular template. Mol. Cell. 1:1998;1001-1010.
41. Lee S.J., Richardson C.C. Essential lysine residues in the RNA polymerase domain of the gene 4 primase-helicase of bacteriophage T7. J. Biol. Chem. 276:2001;49419-49426.
42. Lee S.J., Richardson C.C. Interaction of adjacent primase domains within the hexameric gene 4 helicase-primase of bacteriophage T7. Proc. Natl. Acad. Sci. USA. 99:2002;12703-12708.
43. Lima C.D., Wang J.C., Mondragon A. Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature. 367:1994;138-146.
44. Marintcheva B., Weller S.K. A tale of two HSV-1 helicases. roles of phage and animal virus helicases in DNA replication and recombination Prog. Nucleic Acid Res. Mol. Biol. 70:2001;77-118.
45. Matson S.W., Tabor S., Richardson C.C. The gene 4 protein of bacteriophage T7. Characterization of helicase activity. J. Biol. Chem. 258:1983;14017-14024.
46. Mendelman L.V., Richardson C.C. Requirements for primer synthesis by bacteriophage T7 63-kDa gene 4 protein. Roles of template sequence and T7 56-kDa gene 4 protein. J. Biol. Chem. 266:1991;23240-23250.
47. Mendelman L.V., Beauchamp B.B., Richardson C.C. Requirement for a zinc motif for template recognition by the bacteriophage T7 primase. EMBO J. 13:1994;3909-3916.
48. Mondragon A., DiGate R. The structure of Escherichia coli DNA topoisomerase III. Struct. Fold. Des. 7:1999;1373-1383.
49. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53:1997;240-255.
50. Mustaev A.A., Godson G.N. Studies of the functional topography of the catalytic center of Escherichia coli primase. J. Biol. Chem. 270:1995;15711-15718.
51. Nicholls A., Sharp K.A., Honig B. Protein folding and association. insights from the interfacial and thermodynamic properties of hydrocarbons Proteins. 11:1991;281-296.
52. Nichols M.D., DeAngelis K., Keck J.L., Berger J.M. Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo11. EMBO J. 18:1999;6177-6188.
53. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Carter C.W. Jr., Sweet R.M. Methods in Enzymology. 1997;Academic Press, Orlando. 307-326.pp.
54. Pan H., Wigley D.B. Structure of the zinc-binding domain of Bacillus stearothermophilus DNA primase. Struct. Fold. Des. 8:2000;231-239.
55. Patel S.S., Rosenberg A.H., Studier F.W., Johnson K.A. Large scale purification and biochemical characterization of T7 primase/helicase proteins. Evidence for homodimer and heterodimer formation. J. Biol. Chem. 267:1992;15013-15021.
56. Podobnik M., McInerney P., O'Donnell M., Kuriyan J. A TOPRIM domain in the crystal structure of the catalytic core of Escherichia coli primase confirms a structural link to DNA topoisomerases. J. Mol. Biol. 300:2000;353-362.
57. Powers L., Griep M.A. Escherichia coli primase zinc is sensitive to substrate and cofactor binding. Biochemistry. 38:1999;7413-7420.
58. Qian X., Jeon C., Yoon H., Agarwal K., Weiss M.A. Structure of a new nucleic-acid-binding motif in eukaryotic transcriptional elongation factor TFIIS. Nature. 365:1993;277-279.
59. Richardson C.C. Bacteriophage T7. minimal requirements for the replication of a duplex DNA molecule Cell. 33:1983;315-317.
60. Rosenberg A.H., Griffin K., Washington M.T., Patel S.S., Studier F.W. Selection, identification, and genetic analysis of random mutants in the cloned primase/helicase gene of bacteriophage T7. J. Biol. Chem. 271:1996;26819-26824.
61. Sawaya M.R., Guo S., Tabor S., Richardson C.C., Ellenberger T. Crystal structure of the helicase domain from the replicative helicase-primase of bacteriophage T7. Cell. 99:1999;167-177.
62. Singleton M.R., Sawaya M.R., Ellenberger T., Wigley D.B. Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides. Cell. 101:2000;589-600.
63. Steitz T.A. A mechanism for all polymerases. Nature. 391:1998;231-232.
64. Sun W., Schoneich J., Godson G.N. A mutant Escherichia coli primase defective in elongation of primer RNA chains. J. Bacteriol. 181:1999;3761-3767.
65. Tabor S., Richardson C.C. Template recognition sequence for RNA primer synthesis by gene 4 protein of bacteriophage T7. Proc. Natl. Acad. Sci. USA. 78:1981;205-209.
66. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55:1999;849-861.
67. Urlacher T.M., Griep M.A. Magnesium acetate induces a conformational change in Escherichia coli primase. Biochemistry. 34:1995;16708-16714.
68. Valentine A.M., Ishmael F.T., Shier V.K., Benkovic S.J. A zinc ribbon protein in DNA replication. primer synthesis and macromolecular interactions by the bacteriophage T4 primase Biochemistry. 40:2001;15074-15085.
69. Van Duyne G.D., Standaert R.F., Karplus P.A., Schreiber S.L., Clardy J. Atomic structures of the human immunophilin FKBP-12 complexes with FK506 and rapamycin. J. Mol. Biol. 229:1993;105-124.
70. VanLoock M.S., Chen Y.J., Yu X., Patel S.S., Egelman E.H. The primase active site is on the outside of the hexameric bacteriophage T7 gene 4 helicase-primase ring. J. Mol. Biol. 311:2001;951-956.
71. Vassylyev D.G., Sekine S., Laptenko O., Lee J., Vassylyeva M.N., Borukhov S., Yokoyama S. Crystal structure of a bacterial RNA polymerase holoenzyme at 2.6 Å resolution. Nature. 417:2002;712-719.
72. von Hippel P.H., Jing D.H. Structural biology. Bit players in the trombone orchestra. Science. 287:2000;2435-2436.
73. Yuzhakov A., Kelman Z., O'Donnell M. Trading places on DNA-a three-point switch underlies primer handoff from primase to the replicative DNA polymerase. Cell. 96:1999;153-163.
74. Ziegelin G., Linderoth N.A., Calendar R., Lanka E. Domain structure of phage P4 alpha protein deduced by mutational analysis. J. Bacteriol. 177:1995;4333-4341.