Functional characterization of highly processive protein-primed DNA polymerases from phages Nf and GA-1, endowed with a potent strand displacement capacity

Nucleic Acids Research

Volumn 34, Issue 20, 2006, Pages 6051-6063

  Longás, Elisa ^a   de Vega, Miguel ^a   Lázaro, José M ^a   Salas, Margarita ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; DNA POLYMERASE; DOUBLE STRANDED DNA; PHOSPHODIESTERASE I; SPLEEN EXONUCLEASE;

ARTICLE; BACTERIOPHAGE; BACTERIOPHAGE GA 1; BACTERIOPHAGE NF; CONTROLLED STUDY; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME STRUCTURE; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN POLYMERIZATION; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; BACILLUS PHAGES; DNA; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; EXONUCLEASES; MOLECULAR SEQUENCE DATA; VIRAL PROTEINS;

BACILLUS PHAGE PHI29;

EID: 33845637871     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl769     Document Type: Article

References (78)

1. Kornberg,A. and Baker,T. (1992) DNA Replication, 2nd edn. W.H. Freeman, New York.
2. Salas,M. (1999) Mechanisms of initiation of linear DNA replication in prokaryotes. Genet. Eng. (NY), 21, 159-171.
3. Brenkman,A.B., Breure,E.C. and van der Vliet,P.C. (2002) Molecular architecture of adenovirus DNA polymerise and location of the protein primer. J. Virol., 76, 8200-8207.
4. Rademaker,H.J., Fallaux,F.L, Van den Wollenberg,D.J., De Jong,R.N., Van der Vliet,P.C. and Hoeben,R.C. (2006) Relaxed template specificity in fowl adenovirus 1 DNA replication initiation. J. Gen. Virol., 87, 553-562.
5. Caldentey,J., Blanco,L., Bamford,D.H. and Salas,M. (1993) In vitro replication of bacteriophage PRD1 DNA. Characterization of the protein-primed initiation site. Nucleic Acids Res., 21, 3725-3730.
6. Mana,B., Blanco,L. and 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.
7. King,A.J. and 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.
8. Martín,A.C., Blanco,L., Garcia,P., Salas,M. and 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.
9. Méndez,J., Blanco,L., Esteban,J.A., Bernad,A. and Salas,M. (1992) 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, 9579-9583.
10. Blanco,L., Bernad,A., Lázaro,J.M., Martín,G., Garmendia,C. and Salas,M. (1989) Highly efficient DNA synthesis by the phage φ29 DNA polymerise. Symmetrical mode of DNA replication. J. Biol. Chem., 264, 8935-8940.
11. Kamtekar,S., Berman,A.J., Wang,J., Lázaro,J.M., de Vega,M., Blanco,L., Salas,M. and Steitz,T.A. (2004) Insights into strand displacement and processivity from the crystal structure of the protein-primed DNA polymerase of bacteriophage φ29. Mol. Cell, 16, 609-618.
12. Blasco,M.A., Blanco,L., Parés,E., Salas,M. and Bernad,A. (1990) Structural and functional analysis of temperature-sensitive mutants of the phage φ29 DNA polymerase. Nucleic Acids Res., 18, 4763-4770.
13. Dufour,E., Méndez,J., Lázaro,J.M., de Vega,M., Blanco,L. and 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.
14. Kamtekar,S., Berman,A.J., Wang,J., Lázaro,J.M., de Vega,M., Blanco,L., Salas,M. and Steitz,T.A. (2006) The φ29 DNA polymerase:pRotein-primer structure suggests a model for the initiation to elongation transition. EMBO J., 25, 1335-1343.
15. Rodríguez,I., Lázaro,J.M., Blanco,L., Kamtekar,S., Berman,A.J., Wang,J., Steitz,T.A., Salas,M. and de Vega,M. (2005) A specific subdomain in φ29 DNA polymerase confers both processivity and strand-displacement capacity. Proc. Natl Acad. Sci. USA, 102, 6407-6412.
16. González-Huici,V., Lázaro,J.M., Salas,M. and Hermoso,J.M. (2000) Specific recognition of parental terminal protein by DNA polymerase for initiation of protein-primed DNA replication. J. Biol. Chem., 275, 14678-14683.
17. Meijer,W.J., Horcajadas,J.A. and Salas,M. (2001) φ29 family of phages. Microbiol. Mol. Biol. Rev., 65, 261-287.
18. Peñalva,M.A. and 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.
19. Lázaro,J.M., Blanco,L. and Salas,M. (1995) Purification of bacteriophage φ29 DNA polymerase. Methods Enzymol., 262, 42-49.
20. Studier,F.W. and Moffatt,B.A. (1986) Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol., 189, 113-130.
21. Inciarte,M.R., Viñuela,E. and Salas,M. (1976) Transcription in vitro of φ29 DNA and EcoRI fragments by Bacillus subtilis RNA polymerase. Eur. J. Biochem., 71, 77-83.
22. Tabor,S. and Richardson,C.C. (1985) A bacteriophage T7 RNA polymerase/ promoter system for controlled exclusive expression of specific genes. Proc. Natl Acad. Sci. USA, 82, 1074-1078.
23. Freire,R., Serrano,M., Salas,M. and Hermoso,J.M. (1996) Activation of replication origins in φ29-related phages requires the recognition of initiation proteins to specific nucleoprotein complexes. J. Biol. Chem., 271, 31000-31007.
24. de Vega,M., Lázaro,J.M., Salas,M. and 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.
25. Kumar,J.K., Chiu,E.T., Tabor,S. and Richardson,C.C. (2004) A unique region in bacteriophage t7 DNA polymerase important for exonucleolytic hydrolysis of DNA. J. Biol. Chem., 279, 42018-42025.
26. Carthew,R.W., Chodosh,L.A. and Sharp,P.A. (1985) An RNA polymerase II transcription factor binds to an upstream element in the adenovirus major late promoter. Cell, 43, 439-448.
27. Méndez,J., Blanco,L., Lázaro,J.M. and Salas,M. (1994) Primer-terminus stabilization at the φ29 DNA polymerase active site. Mutational analysis of conserved motif TX2GR. J. Biol. Chem., 269, 30030-30038.
28. Garmendia,C., Bernad,A., Esteban,J.A., Blanco,L. and Salas,M. (1992) The bacteriophage φ29 DNA polymerase, a proofreading enzyme. J. Biol. Chem., 267, 2594-2599.
29. de Vega,M., Blanco,L. and 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.
30. McDonell,M.W., Simon,M.N. and Studier,F.W. (1977) Analysis of restriction fragments of T7 DNA and determination of molecular weights by electrophoresis in neutral and alkaline gels. J. Mol. Biol., 110, 119-146.
31. Esteban,J.A., Bernad,A., Salas,M. and Blanco,L. (1992) Metal activation of synthetic and degradatioe activities of φ29 DNA polymerase, a model enzyme for protein-primed DNA replication. Biochemistry, 31, 350-359.
32. Salas,M. (1991) Protein-priming of DNA replication. Annu. Rev. Biochem., 60, 39-71.
33. Salas,M., Miller,J., Leis,J. and DePamphilis,M. (1996) Mechanisms for Priming DNA Synthesis. Cold Spring Harbor Laboratory Press, New York.
34. Bernad,A., Zaballos,A., Salas,M. and Blanco,L. (1987) Structural and functional relationships between prokaryotic and eukaryotic DNA polymerases. EMBO J., 6, 4219-4225.
35. Gonzalez-Huici,V., Salas,M. and Hermoso,J.M. (2000) Sequence requirements for protein-primed initiation and elongation of phage φ29 DNA replication. J. Biol. Chem., 275, 40547-40553.
36. Guex,N. and Peitsch,M.C. (1997) SWISS-MODEL and the Swiss-Pdb Viewer: An environment for comparative protein modeling. Electrophoresis, 18, 2714-2723.
37. Schwede,T., Kopp,J., Guex,N. and Peitsch,M.C. (2003) SWISS-MODEL: An automated protein homology-modeling server. Nucleic Acids Res., 31, 3381-3385.
38. Bernad,A., Blanco,L., Lázaro,J.M., Martín,G. and Salas,M. (1989) A conserved 3′-5′ exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell, 59, 219-228.
39. Derbyshire,V., Freemont,P.S., Sanderson,M.R., Beese,L., Friedman,J.M., Joyce,C.M. and Steitz,T.A. (1988) Genetic and crystallographic studies of the 3′,5′-exonucleolytic site of DNA polymerase I. Science, 240, 199-201.
40. Beese,L.S. and Steitz,T.A. (1991) Structural basis for the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I: A two metal ion mechanism. EMBO J., 10, 25-33.
41. de Vega,M., Lázaro,J.M. and Salas,M. (2000) Phage φ29 DNA polymerase residues involved in the proper stabilisation of the primer-terminus at the 3′-5′ exonuclease active site. J. Mol. Biol., 304, 1-9.
42. de Vega,M., Lázaro,J.M., Salas,M. and Blanco,L. (1998) Mutational analysis of φ29 DNA polymerase residues acting as ssDNA ligands for 3′-5′ exonucleolysis. J. Mol. Biol., 279, 807-822.
43. Eisenbrandt,R., LáAzaro,J.M., Salas,M. and 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. Nucleic Acids Res., 30, 1379-1386.
44. de Vega,M., Ilyina,T., Lázaro,J.M., Salas,M. and 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.
45. 2h motif is required for a stable and functional interaction with the terminal protein. J. Mol. Biol., 325, 85-97.
46. Rodríguez,I., Lázaro,J.M., Salas,M. and de Vega,M. (2004) φ29 DNA polymerise-terminal protein interaction. Involvement of residues specifically conserved among protein-primed DNA polymerises. J. Mol. Biol., 337, 829-841.
47. Beese,L.S., Derbyshire,V. and Steitz,T.A. (1993) Structure of DNA polymerase I Klenow fragment bound to duplex DNA. Science, 260, 352-355.
48. Doublie,S., Tabor,S., Long,A.M., Richardson,C.C. and Ellenberger,T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature, 391, 251-258.
49. Eom,S.H., Wang,J. and Steitz,T.A. (1996) Structure of Taq polymerise with DNA at the polymerase active site. Nature, 382, 278-281.
50. Franklin,M.C., Wang,J. and Steitz,T.A. (2001) Structure of the replicating complex of a pol α family DNA polymerase. Cell, 105, 657-667.
51. Kiefer,J.R., Mao,C., Braman,J.C. and Beese,L.S. (1998) Visualizing DNA replication in a catalytically active Bacillus DNA polymerase crystal. Nature, 391, 304-307.
52. Blanco,L. and Salas,M. (1996) Relating structure to function in φ29 DNA polymerise. J. Biol. Chem., 271, 8509-8512.
53. Joyce,C.M. and Steitz,T.A. (1994) Function and structure relationships in DNA polymerases. Annu. Rev. Biochem., 63, 777-822.
54. Pelletier,H., Sawaya,M.R., Wolfle,W., Wilson,S.H. and Kraut,J. (1996) Crystal structures of human DNA polymerise beta complexed with DNA: implications for catalytic mechanism, processivity, and fidelity. Biochemistry, 35, 12742-12761.
55. Saturno,J., Lázaro,J.M., Blanco,L. and Salas,M. (1998) Role of the first aspartate residue of the 'YxDTDS' motif of φ29 DNA polymerase as a metal ligand during both TP-primed and DNA-primed DNA synthesis. J. Mol. Biol., 283, 633-642.
56. Steitz,T.A. (1998) A mechanism for all polymerases. Nature, 391, 231-232.
57. Brenkman,A.B., Heideman,M.R., Truniger,V., Salas,M. and van der Vliet,P.C. (2001) The (I/Y)XGG motif of adenovirus DNA polymerase affects template DNA binding and the transition from initiation to elongation. J. Biol. Chem., 276, 29846-29853.
58. Truniger,V., Blanco,L. and Salas,M. (1999) Role of the 'YxGG/A' motif of φ29 DNA polymerase in protein-primed replication. J. Mol. Biol., 286, 57-69.
59. Saturno,J., Lázaro,J.M., Esteban,F.J., Blanco,L. and Salas,M. (1997) φ29 DNA polymerase residue Lys383, invariant at motif B of DNA-dependent polymerases, is involved in dNTP binding. J. Mol. Biol., 269, 313-325.
60. Truniger,V., Lázaro,J.M., Blanco,L. and Salas,M. (2002) A highly conserved lysine residue in φ29 DNA polymerise is important for correct binding of the templating nucleotide during initiation of phi29 DNA replication. J. Mol. Biol., 318, 83-96.
61. Truniger,V., Lázaro,J.M. and Salas,M. (2004) Two positively charged residues of φ29 DNA polymerase, conserved in protein-primed DNA polymerases, are involved in stabilisation of the incoming nucleotide. J. Mol. Biol., 335, 481-494.
62. Pérez-Arnaiz,P., Lázaro,J.M., Salas,M. and de Vega,M. (2006) Involvement of φ29 DNA polymerase thumb subdomain in the proper coordination of synthesis and degradation during DNA replication. Nucleic Acids Res., 34, 3107-3115.
63. Dufour,E., Rodríguez,I., Lázaro,J.M., de Vega,M. and Salas,M. (2003) A conserved insertion in protein-primed DNA polymerases is involved in primer terminus stabilisation. J. Mol. Biol., 331, 781-794.
64. Brutlag,D. and Kornberg,A. (1972) Enzymatic synthesis of deoxyribonucleic acid. XXXVI. A proofreading function for the 3′ leads to 5′ exonuclease activity in deoxyribonucleic acid polymerases. J. Biol. Chem., 247, 241-248.
65. Kunkel,T.A. (1988) Exonucleolytic proofreading. Cell, 53, 837-840.
66. Cowart,M., Gibson,K.J., Allen,D.J. and Benkovic,S.J. (1989) DNA substrate structural requirements for the exonuclease and polymerase activities of procaryotic and phage DNA polymerases. Biochemistry, 28, 1975-1983.
67. Franklin,M.C., Wang,J. and Steitz,T.A. (2001) Structure of the replicating complex of a pol alpha family DNA polymerase. Cell, 105, 657-667.
68. Freemont,P.S., Friedman,J.M., Beese,L.S., Sanderson,M.R. and Steitz,T.A. (1988) Cocrystal structure of an editing complex of Klenow fragment with DNA. Proc. Natl Acad. Sci. USA, 85, 8924-8928.
69. Wang,J., Sattar,A.K., Wang,C.C., Karam,J.D., Konigsberg,W.H. and Steitz,T.A. (1997) Crystal structure of a pol alpha family replication DNA polymerase from bacteriophage RB69. Cell, 89, 1087-1099.
70. Watson,J., Baker,T., Bell,S., Gann,A., Levine,M. and Losick,R. (2004) Molecular Biology of the Gene, 5th edn. Cold Spring Harbor Lab. Press, Plainview, New York.
71. García,P., Hermoso,J.M., García,J.A., García,E., López,R. and Salas,M. (1986) Formation of a covalent complex between the terminal protein of pneumococcal bacteriophage Cp-1 and 5′-dAMP. J. Virol., 58, 31-35.
72. Savilahti,H., Caldentey,J., Lundstrom,K., Syvaoja,J.E. and Bamdord,D.H. (1991) Overexpression, purification, and characterization of Escherichia coli bacteriophage PRD1 DNA polymerase. In vitro synthesis of full-length PRD1 DNA with purified proteins. J. Biol. Chem., 266, 18737-18744.
73. Zhu,W. and Ito,J. (1994) Purification and characterization of PRD1 DNA polymerase. Biochim. Biophys. Acta., 1219, 267-276.
74. Dekker,J., Kanellopoulos,P.N., Loonstra,A.K., van Oosterhout,J.A., Leonard,K., Tucker,P.A. and van der Vliet,P.C. (1997) Multimerization of the adenovims DNA-binding protein is the driving force for ATP-independent DNA unwinding during strand displacement synthesis. EMBO J., 16, 1455-1463.
75. King,A.J., Teertstra,W.R., Blanco,L., Salas,M. and van der Vliet,P.C. (1997) Processive proofreading by the adenovirus DNA polymerase. Association with the priming protein reduces exonucleolytic degradation. Nucleic Acids Res., 25, 1745-1752.
76. Blanco,L., Gutiérrez,J., Lázaro,J.M., Bernad,A. and Salas,M. (1986) Replication of phage φ29 DNA in vitro: Role of the viral protein p6 in initiation and elongation. Nucleic Acids Res., 14, 4923-4937.
77. de Jong,R.N., van der Vliet,P.C. and Brenkman,A.B. (2003) Adenovims DNA replication: Protein priming, jumping back and the role of the DNA binding protein DBP. Curr. Top. Microbiol. Immunol., 272, 187-211.
78. van Breukelen,B., Brenkman,A.B., Holthuizen,P.E. and van der Vliet,P.C. (2003) Adenovirus type 5 DNA binding protein stimulates binding of DNA polymerase to the replication origin. J. Virol., 77, 915-922.