φ29 DNA polymerase residue Phe128 of the highly conserved (S/T)Lx2h motif is required for a stable and functional interaction with the terminal protein

Journal of Molecular Biology

Volumn 325, Issue 1, 2003, Pages 85-97

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

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

DNA polymerase; Linear DNA replication; Protein priming; Site directed mutagenesis; Terminal protein

Indexed keywords

AMINO ACID; DNA POLYMERASE; GLUTAMIC ACID; PHENYLALANINE; DNA DIRECTED DNA POLYMERASE; PRIMER DNA; TERMINAL PROTEIN, BACILLUS PHAGE PHI29; VIRUS PROTEIN;

ARTICLE; BACTERIOPHAGE; BINDING AFFINITY; DNA REPLICATION; DNA TEMPLATE; MUTATION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; AMINO ACID SEQUENCE; BACILLUS PHAGE; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

BACTERIOPHAGE PHI29; EUKARYOTA;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BACILLUS PHAGES; CONSERVED SEQUENCE; DNA PRIMERS; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; MUTAGENESIS, SITE-DIRECTED; MUTATION; PHENYLALANINE; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPLATES, GENETIC; VIRAL PROTEINS;

EID: 0037207455     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01130-0     Document Type: Article

References (56)

1. Kornberg, A. & Baker, T. (1992). DNA Replication, 2nd Edit., Freeman, San Francisco.
2. Salas, M. (1991). Protein-priming of DNA replication. Annu. Rev. Biochem. 60, 39-71.
3. Salas, M., Miller, J. T., Leis, J. & DePamphilis, M. L. (1996). Mechanisms for priming DNA synthesis. In DNA Replication in Eukaryotic Cells (DePamphilis, M. L., ed.), pp. 131-176, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Serrano, M., Salas, M. & Hermoso, J. M. (1990). A novel nucleoprotein complex at a replication origin. Science, 248, 1012-1016.
5. Blanco, L. & Salas, M. (1984). Characterization and purification of a phage φ29-encoded DNA polymerase required for the initiation of replication. Proc. Natl. Acad. Sci. USA, 81, 5325-5329.
6. Méndez, J., Blanco, L., Esteban, J. A., Bernad, A. & Salas, M. (1992). Initiation of φ29 DNA replication occurs at the second 3(0)nucleotide of the linear template: A sliding-back mechanism for protein-primed DNA replication. Proc. Natl. Acad. Sci. USA, 89, 9579-9583.
7. Illana, B., Blanco, L. & Salas, M. (1996). 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, 453-464.
8. Caldentey, J., Blanco, L., Bamford, D. H. & Salas, M. (1993). In vitro replication of bacteriophage PRD1 DNA. Characterization of the protein-primed initiation site. Nucl. Acids Res. 21, 3725-3730.
9. Martín, A. C., Blanco, L., García, P., Salas, M. & Méndez, J. (1996). In vitro protein-primed initiation of pneumococcal phage Cp-1 DNA replication occurs at the third 3′ nucleotide of the linear template: A stepwise sliding-back mechanism. J. Mol. Biol. 260, 369-377.
10. King, A. J. & Van der Vliet, P. C. (1994). A precursor terminal protein trinucleotide intermediate during initiation of adenovirus DNA-replication - Regeneration of molecular ends in vitro by a jumping back mechanism. EMBO J. 13, 5786-5792.
11. Méndez, J., Blanco, L. & Salas, M. (1997). Protein-primed DNA replication: A transition between two modes of priming by a unique DNA polymerase. EMBO J. 16, 2519-2527.
12. Blanco, L., Bernad, A., Lázaro, J. M., Martín, G., Garmendia, C. & Salas, M. (1989). Highly efficient DNA synthesis by the phage φ29 DNA polymerase. J. Biol. Chem. 264, 8935-8940.
13. 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 Publishers/Plenum Press, New York.
14. Van der Vliet, P. C. (1996). Roles of transcription factors in DNA replication. In DNA Replication in Eukaryotic Cells (DePamphilis, M. L., ed.), pp. 87-118, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
15. Blanco, L. & Salas, M. (1996). Relating structure to function in φ29 DNA polymerase. J. Biol. Chem. 271, 8509-8512.
16. 2GR. J. Biol. Chem. 269, 30030-30038.
17. Truniger, V., Blanco, L. & Salas, M. (1999). Role of the "YxGG/A" motif of φ29 DNA polymerase in protein-primed replication. J. Mol. Biol. 286, 57-69.
18. Dufour, E., Méndez, J., Lázaro, J. M., de Vega, M., Blanco, L. & Salas, M. (2000). 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, 289-300.
19. Truniger, V., Lázaro, J. M., Salas, M. & Blanco, L. (1998). φ29 DNA polymerase requires the N-terminal domain to bind terminal protein and DNA primer substrates. J. Mol. Biol. 278, 741-755.
20. de Vega, M., Blanco, L. & Salas, M. (1998). φ29 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, 28966-28977.
21. Eisenbrandt, R., Lázaro, J. M., Salas, M. & de Vega, M. (2002). φ29 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, 1379-1386.
22. de Vega, M., Lázaro, J. M., Salas, M. & Blanco, L. (1998). Mutational analysis of φ29 DNA polymerase residues acting as ssDNA ligands for 3′-5′ exonucleolysis. J. Mol. Biol. 279, 807-822.
23. Derbyshire, V., Pinsonneault, J. K. & Joyce, C. M. (1995). Structure-function analysis of the 3′-5φ exonucleases of DNA polymerases. Methods Enzymol. 262, 363-385.
24. Chou, P. Y. & Fasman, G. D. (1978). Prediction of the secondary structures of proteins from their amino acid sequence. Advan. Enzymol. 47, 45-48.
25. Garnier, J., Osguthorpe, D. J. & Robson, B. (1978). Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J. Mol. Biol. 120, 97-120.
26. Bordo, D. & Argos, P. (1991). Suggestions for "safe" residue substitutions in site-directed mutagenesis. J. Biol. Chem. 217, 721-729.
27. Lázaro, J. M., Blanco, L. & Salas, M. (1995). Purification of f29 DNA polymerase. Methods Enzymol. 262, 42-49.
28. Soengas, M. S., Gutiérrez, C. & Salas, M. (1995). Helix-destabilizing activity of φ29 single-stranded DNA binding protein: Effect on the elongation rate during strand displacement DNA replication. J. Mol. Biol. 253, 517-529.
29. Blanco, L., Bernad, A., Esteban, J. A. & Salas, M. (1992). DNA-independent deoxynucleotydilation of the φ29 terminal protein by the φ29 DNA polymerase. J. Biol. Chem. 267, 1225-1230.
30. Bernad, A., Blanco, L., Lázaro, J. M., Martín, G. & Salas, M. (1989). A conserved 3′-5′ exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell, 59, 219-228.
31. Soengas, M. S., Esteban, J. A., Lázaro, J. M., Bernad, A., Blasco, M. A., Salas, M. & Blanco, L. (1992). Site-directed mutagenesis at the Exo III motif of φ29 DNA polymerase. Overlapping structural domains for the 3′-5′ exonuclease and strand-displacement activities. EMBO J. 11, 4227-4237.
32. Esteban, J. A., Soengas, M. S., Salas, M. & Blanco, L. (1994). 3′-5′ Exonuclease active site of φ29 DNA polymerase. Evidence favoring a metal ion-assisted reaction mechanism. J. Biol. Chem. 244, 31946-31954.
33. de Vega, M., Ilyina, T., Lázaro, J. M., Salas, M. & Blanco, L. (1997). An invariant lysine residue is involved in catalysis at the 3′-5′ exonuclease active site of eukaryotic-type DNA polymerases. J. Mol. Biol. 270, 65-78.
34. de Vega, M., Lázaro, J. M., Salas, M. & Blanco, L. (1996). Primer terminus stabilization at the 3′-5′ exonuclease active site of φ29 DNA polymerase. Involvement of two amino acid residues highly conserved in proofreading DNA polymerases. EMBO J. 15, 1182-1192.
35. de Vega, M., Lázaro, J. M. & Salas, M. (2000). Phage φ29 DNA polymerase residues involved in the proper stabilization of the primer-terminus at the 3′-5′ exonuclease active site. J. Mol. Biol. 304, 1-9.
36. Serna-Rico, A., Illana, B., Salas, M. & Meijer, W. J. J. (2000). The putative coiled coil domain of the φ29 terminal protein is a major determinant involved in recognition of the origin of replication. J. Biol. Chem. 275, 40529-40538.
37. González-Huici, V., Salas, M. & Hermoso, J. M. (2000). Sequence requirements for protein-primed initiation and elongation of phage φ29 DNA replication. J. Biol. Chem. 275, 40547-40553.
38. Beese, L. S., Derbyshire, V. & Steitz, T. A. (1993). Structure of DNA polymerase Klenow fragment bound to duplex DNA. Science, 260, 352-355.
39. Kim, Y., Eom, S. H., Wang, J., Lee, D. S., Sush, S. W. & Steitz, T. A. (1995). Crystal structure of Thermus aquaticus DNA polymerase. Nature, 376, 612-616.
40. Li, Y., Korolev, S. & Waksman, G. (1998). 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, 7514-7525.
41. Doublié, S., Tabor, S., Long, A. M., Richardson, C. C. & Ellenberger, T. (1998). Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature, 391, 251-258.
42. Kiefer, J. R., Mao, C., Hansen, C. J., Basehore, S. L., Hogrefe, H. H., Braman, J. C. & Beese, L. S. (1997). Crystal structure of a thermostable Bacillus DNA polymerase I large fragment at 2.1 Å resolution. Structure, 5, 95-108.
43. Wang, J., Sattar, A. K., Wang, C. C., Karam, J. D., Konigsberg, W. H. & Steitz, T. A. (1997). Crystal structure of a Pol α family replication DNA polymerase from bacteriophage RB69. Cell, 89, 1087-1099.
44. Hopfner, K. P., Eichinger, A., Engh, R. A., Laue, F., Ankenbauer, W., Huber, R. & Angerer, B. (1999). Crystal structure of a thermostable type B DNA polymerase from Thermococcus gorgonarius. Proc. Natl. Acad. Sci. USA, 96, 3600-3605.
45. Hashimoto, H., Nishioka, M., Fujiwara, S., Takagi, M., Imanaka, T., Inoue, T. & Kai, Y. (2001). Crystal structure of DNA polymerase from hypertermophilic archeon Pyrococcus kodakaraensis KOD1. J. Mol. Biol. 306, 469-477.
46. Rodriguez, A. C., Park, H. W., Mao, C. & Beese, L. S. (2000). Crystal structure of a Pol α family DNA polymerase from the hypertermophilic archeon Thermococcus sp. 9 degrees N-7. J. Mol. Biol. 299, 447-462.
47. Zhao, Y., Jeruzalmi, D., Moarefi, I., Leighton, L., Lasken, R. & Kuriyan, J. (1999). Crystal structure of an archaebacterial DNA polymerase. Structure, 7, 1189-1199.
48. Zaballos, A., Lázaro, J. M., Méndez, E., Mellado, R. P. & Salas, M. (1989). Effects of internal deletions on the priming activity of the phage φ29 terminal protein. Gene, 83, 187-195.
49. Martín, G., Lázaro, J. M., Méndez, E. & Salas, M. (1989). Characterization of phage φ29 protein p5 as a single-stranded DNA binding protein. Function in f29 DNA-protein p3 replication. Nucl. Acids Res. 17, 3663-3672.
50. Pastrana, R., Lázaro, J. M., Blanco, L., García, J. A., Méndez, E. & Salas, M. (1985). Overproduction and purification of protein p6 of Bacillus subtilis phage φ29: Role in the initiation of DNA replication. Nucl. Acids Res. 13, 3083-3100.
51. Inciarte, M. R., Lázaro, J. M., Salas, M. & Viñuela, E. (1976). Physical map of bacteriophage φ29. Virology, 74, 314-323.
52. Peñalva, M. A. & Salas, M. (1982). 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, 5522-5526.
53. Carthew, R. W., Chodosch, L. A. & Sharp, P. A. (1985). A RNA polymerase II transcription factor binds to an upstream element in the adenovirus major late promoter. Cell, 43, 439-448.
54. McDonnell, M. W., Simon, M. N. & Studier, F. W. (1994). Analysis of restriction fragments of T7 DNA and determination of molecular weights by electrophoresis in neutral and alkaline agarose gels. J. Membr. Biol. 110, 119-146.
55. Blanco, L., Lázaro, J. M., de Vega, M., Bonnin, A. & Salas, M. (1994). Terminal protein-primed DNA amplification. Proc. Natl. Acad. Sci. USA, 91, 12198-12202.
56. 2SLYP" is critical for synthetic activities. J. Biol. Chem. 268, 24106-24113.