Two Positively Charged Residues of φ29 DNA Polymerase, Conserved in Protein-primed DNA Polymerases, are Involved in Stabilisation of the Incoming Nucleotide

Journal of Molecular Biology

Volumn 335, Issue 2, 2004, Pages 481-494

  Truniger, Verónica ^a,b   Lázaro, José M ^a   Salas, Margarita ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

Author keywords

dNTP binding; Motif B; Pre motif B; Protein priming; 29 DNA polymerase

Indexed keywords

AMINO ACID; DEOXYRIBONUCLEOTIDE; DNA; DNA BINDING PROTEIN; DNA POLYMERASE; DOUBLE STRANDED DNA; LYSINE; MUTANT PROTEIN; NUCLEOTIDE; PHOSPHATE; PROTEIN P6; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE; ENZYME ACTIVE SITE; NUCLEOTIDE SEQUENCE; PHENOTYPE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN MOTIF; SITE DIRECTED MUTAGENESIS; SURFACE CHARGE; WILD TYPE;

EID: 0345735667     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.10.024     Document Type: Article

References (59)

1. Salas M. Protein-priming of DNA replication. Annu. Rev. Biochem. 60:1991;39-71.
2. Salas M. Mechanisms of initiation of linear DNA replication in prokaryotes. Genet. Eng. 21:1999;159-171.
3. Méndez J., Blanco L., Salas M. Protein-primed DNA replication: a transition between two modes of priming by a unique DNA polymerase. EMBO J. 16:1997;2519-2527.
4. Brautigam C., 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.
5. Kunkel T.A., Wilson S. DNA polymerases on the move. Nature Struct. Biol. 5:1998;95-99.
6. Li Y., Waksman G. Crystal structures of ddATP-, ddCTP- and ddGTP-trapped ternary complex of Klentaq 1: insights into nucleotide incorporation and selectivity. Protein Sci. 6:2001;1225-1233.
7. Patel P., Suzuki M., Adman E., Shinkai A., Loeb L. Prokaryotic DNA polymerase I: evolution, structure and "base flipping" mechanism for nucleotide selection. J. Mol. Biol. 308:2001;823-837.
8. Franklin M., Wang J., Steitz T. Structure of the replicating complex of Pol α family DNA polymerase. Cell. 105:2001;657-667.
9. Delarue M., Poch O., Tordo N., Moras D., Argos P. An attempt to unify the structure of polymerases. Protein Eng. 6:1990;461-467.
10. 390 are affected in dNTP binding. J. Biol. Chem. 267:1992;19427-19434.
11. 3NSxYG" is involved in template-primer binding and dNTP selection. J. Biol. Chem. 268:1993;16763-16770.
12. Carroll S., Cowart M., Benkovic S. A mutant of DNA polymerase I (Klenow fragment) with reduced fidelity. Biochemistry. 30:1991;804-813.
13. Saturno J., Blanco L., Salas M., Esteban J.A. A novel kinetic analysis to calculate nucleotide affinity of proofreading DNA polymerases. Application to φ29 DNA polymerase fidelity mutants. J. Biol. Chem. 270:1995;31235-31243.
14. Bell J., Eckert K., Joyce C., Kunkel T. Base miscoding and strand misalignment errors by mutator Klenow polymerases with amino acid substitutions at tyrosine 766 in the O helix of the fingers subdomain. J. Biol. Chem. 272:1997;7345-7351.
15. Yang G., Lin T., Karam J., Konigsberg W.H. Steady-state kinetic characterization of RB69 DNA polymerase mutants that affect dNTP incorporation. Biochemistry. 38:1999;8094-8101.
16. Pavlov Y., Shcherbakova P., Kunkel T. In vivo consequences of putative active site mutations in yeast DNA polymerases α, ε, δ, and ζ Genetics. 159:2001;47-64.
17. Truniger V., Lázaro J.M., Vega de M., Blanco L., Salas M. φ29 DNA polymerase residue Leu384, highly conserved in motif B of eukaryotic type DNA replicases, is involved in nucleotide insertion fidelity. J. Biol. Chem. 278:2003;33482-33491.
18. Saturno J., Lázaro J.M., Esteban F.J., Blanco L., Salas M. φ29 DNA polymerase residue Lys383, invariant at motif B of DNA-dependent polymerases, is involved in dNTP binding. J. Mol. Biol. 269:1997;313-325.
19. Patel P., Kawate H., Adman E., Ashbach M., Loeb L. A single highly mutable catalytic site amino acid is critical for DNA polymerase fidelity. J. Biol. Chem. 276:2001;5044-5051.
20. Shinkai A., Loeb L. In vivo mutagenesis by Escherichia coli DNA polymerase I. Ile709 in motif A functions in base selection. J. Biol. Chem. 276:2001;46759-46764.
21. Li Y., Korolev S., Waksman G. Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. EMBO J. 17:1998;7514-7525.
22. Doublié S., Tabor S., Long A., Richardson C., Ellenberger T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature. 391:1998;251-258.
23. Truniger V., Lázaro J.M., Esteban F.J., Blanco L., Salas M. A positively charged residue of φ29 DNA polymerase, highly conserved in DNA polymerases from families A and B, is involved in binding the incoming nucleotide. Nucl. Acids Res. 30:2002;1482-1493.
24. Wang J., Sattar A.K.M.A., Wang C.C., Karam J.D., Konigsberg W.H., Steitz T.A. Crystal structure of a pol α family replication DNA polymerase from bacteriophage, RB69. Cell. 89:1997;1087-1099.
25. Hopfner K.P., Eichinger A., Engh R., Laue F., Ankanbauer W., Huber R., Angerer B. Crystal structure of a thermostable type B DNA polymerase from Thermococcus gorgonarius. Proc. Natl Acad. Sci. USA. 96:1999;3600-3605.
26. Zhao Y., Jeruzalmi D., Moarefi I., Leighton L., Lasken R., Kuriyan J. Crystal structure of an archebacterial DNA polymerase. Structure. 7:1999;1189-1199.
27. Rodriguez C.A., Park H., Mao C., Beese L. Crystal structure of a pol α family DNA polymerase from the hyperthermophilic archaeon Thermococcus sp. 9oN-7. J. Mol. Biol. 299:2000;447-462.
28. Hashimoto H., Nishioka M., Fujiwara S., Takagi M., Imanaka T., Inoue T., Kai Y. Crystal structure of DNA polymerase from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1. J. Mol. Biol. 306:2001;469-477.
29. Bordo D., Argos P. Suggestions for "safe" residue substitutions in site-directed mutagenesis. J. Mol. Biol. 217:1991;721-729.
30. Chou P.Y., Fasman G.D. Prediction of the secondary structure of proteins from their amino acid sequence. Advan. Enzymol. 47:1978;45-148.
31. Garnier J., Osguthorpe D.J., Robson B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J. Mol. Biol. 120:1978;97-120.
32. 2GR" J. Biol. Chem. 269:1994;30030-30038.
33. Clark J.M. Novel non-templated nucleotide addition reactions catalyzed by procaryotic and eucaryotic DNA polymerases. Nucl. Acids Res. 16:1988;9677-9686.
34. Blasco M.A., Bernad A., Blanco L., Salas M. Characterization and mapping of the pyrophosphorolytic activity of the phage φ29 DNA polymerase. J. Biol. Chem. 266:1991;7904-7909.
35. Blanco L., Bernad A., Lázaro J.M., Martín G., Garmendia C., Salas M. Highly efficient DNA synthesis by the phage φ29 DNA polymerase. Symmetrical mode of DNA replication. J. Biol. Chem. 267:1989;1225-1230.
36. Méndez J., Blanco L., Esteban J.A., Bernad A., Salas M. Initiation of φ29 DNA replication occurs at the second 3′ nucleotide of the linear template: a sliding-back mechanism for protein-primed DNA replication. Proc. Natl Acad. Sci. USA. 89:1992;9579-9583.
37. Hermoso J.M., Méndez E., Soriano F., Salas M. Location of the serine residue involved in the linkage between the terminal protein and the DNA of phage φ29. Nucl. Acids Res. 13:1985;7715-7728.
38. Blanco L., Salas M. Characterization and purification of a phage φ29-encoded DNA polymerase required for the initiation of replication. Proc. Natl Acad. Sci. USA. 82:1984;6404-6408.
39. Blanco L., Bernad A., Esteban J.A., Salas M. DNA-independent deoxynucleotidylation of the φ29 terminal protein by the φ29 DNA polymerase. J. Biol. Chem. 267:1992;1225-1230.
40. Serrano M., Gutiérrez C., Freire R., Bravo A., Salas M., Hermoso J.M. Phage φ29 protein p6: a viral histone-like protein. Biochimie. 76:1994;981-991.
41. Blanco L., Gutiérrez J., Lázaro J.M., Bernad A., Salas M. Replication of phage φ29 DNA in vitro: role of the viral protein p6 in initiation and elongation. Nucl. Acids Res. 14:1986;4923-4937.
42. Suzuki M., Baskin D., Hood L., Loeb L. Random mutagenesis of Thermus aquaticus DNA polymerase I: concordance of immutable sites in vivo with the crystal structure. Proc. Natl Acad. Sci. USA. 93:1996;9670-9675.
43. Truniger V., Lázaro J.M., Blanco L., Salas M. A highly conserved lysine residue in φ29 DNA polymerase is important for correct binding of the templating nucleotide during initiation of φ29 DNA replication. J. Mol. Biol. 318:2002;83-96.
44. Peñalva M.A., Salas M. Initiation of phage φ29 DNA replication in vitro: formation of a covalent complex between the terminal protein p3 and 5′-dAMP. Proc. Natl Acad. Sci. USA. 79:1982;5522-5526.
45. Zaballos A., Salas M. Functional domains in the bacteriophage φ29 terminal protein for the interaction with the φ29 DNA polymerase and with DNA. Nucl. Acids Res. 17:1989;10353-10366.
46. Pastrana R., Lázaro J.M., Blanco L., García J.A., Méndez E., Salas M. Overproduction and purification of protein p6 of Bacillus subtilis phage φ29: role in the initiation of DNA replication. Nucl. Acids Res. 13:1985;3083-3100.
47. Lázaro J.M., Blanco L., Salas M. Purification of bacteriophage φ29 DNA polymerase. Methods Enzymol. 262:1995;42-49.
48. Tabor S., Richardson C.C. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl Acad. Sci. USA. 82:1985;1074-1078.
49. Horton R., Hunt H., Ho S., Pullen J., Pease L. Engineering hybrid genes without the use of restriction enzymes: gene splicing by overlap extension. Gene. 77:1989;61-68.
50. Studier F.W., Moffatt B.A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:1986;113-130.
51. Carthew R.W., Chodosch L.A., Sharp P.A. A RNA polymerase II transcription factor binds to an upstream element in the adenovirus major late promoter. Cell. 43:1985;439-448.
52. McDonnell M.W., Simon M.N., Studier F.W. Analysis of restriction fragments of T7 DNA and determination of molecular weights by electrophoresis in neutral and alkaline gels. J. Mol. Biol. 110:1977;119-146.
53. Truniger V., Blanco L., Salas M. Role of the "YxGG/A" motif of φ29 DNA polymerase in protein-primed replication. J. Mol. Biol. 286:1999;57-69.
54. Blanco L., Bernad A., Salas M. Transition from initiation to elongation in protein-primed φ29 DNA replication: salt-dependent stimulation by the viral protein p6. J. Virol. 62:1988;4167-4172.
55. Sambrook J., Russell D. Molecular Cloning. A Laboratory Manual. 3rd edit. 2001;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
56. Braithwaite D.K., Ito J. Compilation, alignment and phylogenetic relationships of DNA polymerases. Nucl. Acids Res. 21:1993;787-802.
57. Hermanns J., Osiewacz H.D. The linear mitochondrial plasmid pAL2-1 of a long-lived Podospora anserina mutant is an invertron encoding a DNA and a RNA polymerase. Curr. Genet. 22:1992;491-500.
58. Illana B., Blanco L., Salas M. Functional characterization of the genes coding for the terminal protein and DNA polymerase from bacteriophage GA-1. Evidence for a sliding back mechanism during protein-primed GA-1 DNA replication. J. Mol. Biol. 264:1996;453-464.
59. Blanco L., Salas M. Mutational analysis of bacteriophage φ29 DNA polymerase. Methods Enzymol. 262:1995;283-294.