A conserved insertion in protein-primed DNA polymerases is involved in primer terminus stabilisation

Journal of Molecular Biology

Volumn 331, Issue 4, 2003, Pages 781-794

  Dufour, Emmanuelle ^a,b   Rodríguez, Irene ^a   Lázaro, José M ^a   De Vega, Miguel ^a   Salas, Margarita ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b Centre National de la Recherche Scientifique   (France)

Author keywords

Bacteriophage 29; Linear DNA replication; Protein priming

Indexed keywords

DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE BETA; EXONUCLEASE; MUTANT PROTEIN; PRIMER DNA; PROTEIN SUBUNIT; SINGLE STRANDED DNA;

ARTICLE; DNA DETERMINATION; DNA REPLICATION; ENZYME ACTIVITY; GENE INSERTION; GENETIC STABILITY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STABILITY; SITE DIRECTED MUTAGENESIS; WILD TYPE;

EUKARYOTA; INSERTION SEQUENCES;

EID: 0043168028     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00788-5     Document Type: Article

References (60)

1. Salas M., Miller J.T., Leis J., DePamphilis M.L. Mechanism for priming DNA synthesis. DePamphilis M.L. DNA Replication in Eukaryotic Cells. 1996;131-176 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
2. van der Vliet P.C. Roles of transcription factors in DNA replication. DePamphilis M.L. DNA Replication in Eukaryotic Cells. 1996;87-118 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. Salas, M. (1999). Mechanisms of initiation of linear DNA replication in prokaryotes. In Genetic Engineering (Setlow, J. K., ed.), vol. 21, pp. 159-171, Kluwer Academic/Plenum Publishers, NY.
4. Serrano M., Gutiérrez C., Freire R., Bravo A., Salas M., Hermoso J.M. Phage ø29 protein p6: a viral histone-like protein. Biochemie. 76:1994;981-991.
5. + ions on ø29 DNA-protein p3 replication: formation of a complex between the terminal protein and the DNA polymerase. J. Virol. 61:1987;3983-3991.
6. Serna-Rico A., Illana B., Salas M., Meijer W.J. The putative coiled coil domain of the ø29 terminal protein is a major determinant involved in recognition of the origin of replication. J. Biol. Chem. 275:2000;40529-40538.
7. González-Huici V., Lázaro J.M., Salas M., Hermoso J.M. Specific recognition of parental terminal protein by DNA polymerase for initiation of protein-primed DNA replication. J. Biol. Chem. 275:2000;14678-14683.
8. González-Huici V., Salas M., Hermoso J.M. Sequence requirements for protein-primed initiation and elongation of phage ø29 DNA replication. J. Biol. Chem. 275:2000;40547-40553.
9. Blanco L., Salas M. Replication of ø29 DNA with purified terminal protein and DNA polymerase: synthesis of full-length ø29 DNA. Proc. Natl Acad. Sci. USA. 82:1985;6404-6408.
10. 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 ø29. Nucl. Acids Res. 13:1985;7715-7728.
11. Méndez J., Blanco L., Esteban J.A., Bernad A., Salas M. Initiation of ø29 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.
12. 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.
13. Blanco L., Bernad A., Lázaro J.M., Martín G., Garmendia C., Salas M. Highly efficient DNA synthesis by the phage ø29 DNA polymerase. Symmetrical mode of DNA replication. J. Biol. Chem. 264:1989;8935-8940.
14. Blanco L., Salas M. Mutational analysis of bacteriophage ø29 DNA polymerase. Methods Enzymol. 262:1995;283-294.
15. Blanco L., Salas M. Relating structure to function in ø29 DNA polymerase. J. Biol. Chem. 271:1996;8509-8512.
16. Bernad A., Blanco L., Lázaro J.M., Martín G., Salas M. A conserved 3′-5′ exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell. 59:1989;219-228.
17. Blanco L., Bernad A., Blasco M.A., Salas M. A general structure for DNA-dependent DNA polymerases. Gene. 100:1991;27-38.
18. Blasco M.A., Blanco L., Parés E., Salas M., Bernad A. Structural and functional analysis of temperature-sensitive mutants of the phage ø29 DNA polymerase. Nucl. Acids Res. 18:1990;4763-4770.
19. Dufour E., Méndez J., Lázaro J.M., de Vega M., Blanco L., Salas M. An aspartic acid residue in TPR-1, a specific region of protein-priming DNA polymerases, is required for the functional interaction with primer terminal protein. J. Mol. Biol. 304:2000;289-300.
20. Wang J., Sattar A.K., 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.
21. Franklin M.C., Wang J., Steitz T.A. Structure of the replicating complex of a pol α family DNA polymerase. Cell. 105:2001;657-667.
22. Chou P.Y., Fasman G.D. Prediction of the secondary structure of proteins from their amino acid sequence. Advan. Enzymol. 47:1978;45-148.
23. 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.
24. Bordo D., Argos P. Suggestions for "safe" residue substitutions in site-directed mutagenesis. J. Biol. Chem. 217:1991;721-729.
25. de Vega M., Lázaro J.M., Salas M., Blanco L. Primer-terminus stabilization at the 3′-5′ exonuclease active site of ø29 DNA polymerase. Involvement of two amino acid residues highly conserved in proofreading DNA polymerases. EMBO J. 15:1996;1182-1192.
26. Creighton S., Bloom L.B., Goodman M.F. Gel fidelity assay measuring nucleotide misinsertion, exonucleolytic proofreading and lesion bypass eficiences. Methods Enzymol. 262:1995;232-256.
27. Saturno J., Blanco L., Salas M., Esteban J.A. A novel kinetic analysis to calculate affinity of proofreading DNA polymerases. Application to ø29 DNA polymerase fidelity mutants. J. Biol. Chem. 270:1995;31235-31243.
28. 2GR. J. Biol. Chem. 269:1994;30030-30038.
29. Blanco L., Bernad A., Esteban J.A., Salas M. DNA-independent deoxynucleotidylation of the ø29 terminal protein by the ø29 DNA polymerase. J. Biol. Chem. 267:1992;1225-1230.
30. Esteban J.A., Soengas M.S., Salas M., Blanco L. 3′-5′ exonuclease active site of ø29 DNA polymerase. Evidence favoring a metal-ion-assisted reaction mechanism. J. Biol. Chem. 269:1994;31946-31954.
31. Esteban J.A., Salas M., Blanco L. Fidelity of ø29 DNA polymerase. Comparison between protein-primed initiation and DNA polymerization. J. Biol. Chem. 268:1993;2719-2726.
32. Truniger V., Blanco L., Salas M. Role of the "YxGG/A" motif of ø29 DNA polymerase in protein-primed replication. J. Mol. Biol. 286:1999;57-69.
33. Truniger V., Lázaro J.M., Esteban F.J., Blanco L., Salas M. A positively charged residue of ø29 DNA polymerase, highly conserved in DNA polymerases from families A and B, is involved in binding the incoming nucleotide. Nucl. Acids Res. 30:2002;1483-1492.
34. Joyce C.M., Steitz T.A. Function and structure relationships in DNA polymerases. Annu. Rev. Biochem. 63:1994;777-822.
35. 2GR. J. Biol. Chem. 269:1994;30030-30038.
36. Truniger V., Lázaro J.M., Salas M., Blanco L. A DNA binding motif coordinating synthesis and degradation in proofreading DNA polymerases. EMBO J. 15:1996;3430-3441.
37. de Vega M., Ilyina T., Lázaro J.M., Salas M., Blanco L. An invariant lysine residue is involved in catalysis at the 3′-5′ exonuclease active site of eukaryotic-type DNA polymerases. J. Mol. Biol. 270:1997;65-78.
38. de Vega M., Blanco L., Salas M. ø29 DNA polymerase residue Ser122, a single-stranded DNA ligand for 3′-5′ exonucleolysis, is required to interact with the terminal protein. J. Biol. Chem. 273:1998;28966-28977.
39. de Vega M., Blanco L., Salas M. Processive proofreading and spatial relationship between polymerase and exonuclease active sites of bacteriophage ø29 DNA polymerase. J. Mol. Biol. 292:1999;39-51.
40. Li Y., Korolev S., Waskman G. Crystal structures of the 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.
41. Blasco M.A., Lázaro J.M., Bernad A., Blanco L., Salas M. ø29 DNA polymerase active site: mutants in conserved residues Tyr254 and Tyr390 are affected in dNTP binding. J. Biol. Chem. 267:1992;19427-19434.
42. 3NSxYG is involved in template-primer binding and dNTP selection. J. Biol. Chem. 268:1993;16763-16770.
43. Saturno J., Lázaro J.M., Esteban J.A., Blanco L., Salas M. ø29 DNA polymerase residue Lys383, invariant at motif B of DNA-dependent polymerases, is involved in dNTP binding. J. Mol. Biol. 269:1997;313-325.
44. 2SLYP is critical for synthetic activities. J. Biol. Chem. 268:1993;24106-24113.
45. Blasco M.A., Méndez J., Lázaro J.M., Blanco L., Salas M. Primer terminus stabilization at the ø29 DNA polymerase active site. Mutational analysis of conserved motif KxY. J. Biol. Chem. 270:1995;2735-2740.
46. Truniger V., Blanco L., Salas M. Analysis of ø29 DNA polymerase by partial proteolysis: binding of terminal protein in the double-stranded DNA channel. J. Mol. Biol. 295:2000;441-453.
47. Eisenbrandt R., Lázaro J.M., Salas M., de Vega M. ø29 DNA polymerase residues Tyr59, His61, and Phe69 of the highly conserved ExoII motif, are essential for interaction with the terminal protein. Nucl. Acids Res. 30:2002;1379-1386.
48. Truniger V., Lázaro J.M., Salas M., Blanco L. ø29 DNA polymerase requires the N-terminal domain to bind terminal protein and DNA primer substrates. J. Mol. Biol. 278:1998;741-755.
49. Soengas M.S., Esteban J.A., Lázaro J.M., Bernad A., Blasco M.A., Salas M., Blanco L. Site-directed mutagenesis at the ExoIII motif of ø29 DNA polymerase. Overlapping structural domains for the 3′-5′ exonuclease and strand displacement activities. EMBO J. 11:1992;4227-4237.
50. Zhu W., Ito J. Family A and family B DNA polymerases are structurally related: evolutionary implications. Nucl. Acids Res. 22:1994;5177-5183.
51. Peñalva M.A., Salas M. Initiation of phage ø29 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.
52. Lázaro J.M., Blanco L., Salas M. Purification of bacteriophage ø29 DNA polymerase. Methods Enzymol. 262:1995;42-49.
53. Studier F.W., Moffat B.A. Use of T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 189:1986;113-130.
54. Zaballos A., Lázaro J.M., Méndez E., Mellado R.P., Salas M. Effects of internal deletions on the priming activity of the phage ø29 terminal protein. Gene. 83:1989;187-195.
55. Ho S.N., Hunt H.D., Horton R.M., Pullen J.K., Pease L.R. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene. 77:1989;51-59.
56. 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.
57. Delarue M., Poch O., Tordo N., Moras D., Argos P. An attempt to unify the structure of polymerases. Protein Eng. 3:1990;461-467.
58. Braithwaite D.K., Ito J. Compilation, alignment, and phylogenetic relationships of DNA polymerases. Nucl. Acids Res. 21:1993;787-802.
59. Rohe M., Schrage K., Meinhardt F. The linear plasmid pMC3-2 from Morchella conica is structurally related to adenoviruses. Curr. Genet. 20:1991;527-533.
60. 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.