Elucidating the kinetic mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase B1

Biochemistry

Volumn 48, Issue 31, 2009, Pages 7502-7511

  Brown, Jessica A ^a   Suo, Zucai ^a,b,c  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINARY COMPLEXES; COFACTORS; CONFORMATIONAL CHANGE; DISSOCIATION RATES; DNA POLYMERASE; DNA POLYMERIZATION; ELEMENTARY STEPS; EXONUCLEASE; IN-VIVO; INDUCED FIT; KINETIC EVIDENCE; KINETIC MECHANISM; PHOSPHODIESTER BONDS; POLYMERASE ACTIVE SITE; POLYMERIZATION REACTION; PROCESSIVITY; SULFOLOBUS SOLFATARICUS; TERNARY COMPLEX; TRANSIENT-STATE KINETIC TECHNIQUES;

ACTIVATION ENERGY; CHEMICAL BONDS; CONFORMATIONS; DISSOCIATION; GENES; NUCLEIC ACIDS; NUCLEOTIDES; POLYMERIZATION; POLYMERS;

DNA;

DNA POLYMERASE; DNA POLYMERASE B1; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; DISSOCIATION; DNA SYNTHESIS; ENZYME KINETICS; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; REACTION ANALYSIS; SULFOLOBUS SOLFATARICUS;

CATALYSIS; DNA POLYMERASE BETA; DNA, ARCHAEAL; EXODEOXYRIBONUCLEASES; KINETICS; POLYMERS; SULFOLOBUS SOLFATARICUS;

SULFOLOBUS SOLFATARICUS;

EID: 68249105256     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9005336     Document Type: Article

References (58)

1. She, Q., Singh, R. K., Confalonieri, F., Zivanovic, Y., Allard, G., Awayez, M. J., Chan-Weiher, C. C., Clausen, I. G., Curtis, B. A., De Moors, A., Erauso, G., Fletcher, C., Gordon, P. M., Heikamp-de Jong, I., Jeffries, A. C., Kozera, C. J., Medina, N., Peng, X., Thi-Ngoc, H. P., Redder, P., Schenk, M. E., Theriault, C., Tolstrup, N., Charlebois,R. L., Doolittle, W. F., Duguet, M., Gaasterland, T., Garrett, R. A., Ragan, M. A., Sensen, C. W., and Van der Oost, J. (2001) The complete genome of the crenarchaeon Sulfolobus solfataricus P2. Proc. Natl. Acad. Sci. U.S.A. 98, 7835-7840
2. Boudsocq, F., Iwai, S., Hanaoka, F., and Woodgate, R. (2001) Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): An archaeal DinB-like DNA polymerase with lesion-bypass properties akin to eukaryotic poleta. Nucleic Acids Res. 29, 4607-4616 (Pubitemid 33095021)
3. De Felice, M., Medagli, B., Esposito, L., De Falco, M., Pucci, B., Rossi, M., Gruz, P., Nohmi, T., and Pisani, F. M. (2007) Biochemical evidence of a physical interaction between Sulfolobus solfataricus B-family and Y-family DNA polymerases. Extremophiles 11, 277-282 (Pubitemid 46318134)
4. Lou, H., Duan, Z., Sun, T., and Huang, L. (2004) Cleavage of double-stranded DNA by the intrinsic 30-50 exonuclease activity of DNA polymerase B1 from the hyperthermophilic archaeon Sulfolobus solfataricus at high temperature. FEMS Microbiol. Lett. 231, 111-117
5. Gruz, P., Shimizu, M., Pisani, F. M., De Felice, M., Kanke, Y., and Nohmi, T. (2003) Processing of DNA lesions by archaeal DNA polymerases from Sulfolobus solfataricus. Nucleic Acids Res. 31, 4024-4030 (Pubitemid 37442282)
6. Kuchta, R. D., Mizrahi, V., Benkovic, P. A., Johnson, K. A., and Benkovic, S. J. (1987) Kinetic mechanism of DNA polymerase I (Klenow). Biochemistry 26, 8410-8417
7. Kuchta, R. D., Benkovic, P., and Benkovic, S. J. (1988) Kinetic mechanism whereby DNA polymerase I (Klenow) replicates DNA with high fidelity. Biochemistry 27, 6716-6725 (Pubitemid 18232773)
8. Dahlberg, M. E., and Benkovic, S. J. (1991) Kinetic mechanism of DNA polymerase I (Klenow fragment): Identification of a second conformational change and evaluation of the internal equilibrium constant. Biochemistry 30, 4835-4843.
9. Eger, B. T., and Benkovic, S. J. (1992) Minimal kinetic mechanism for misincorporation by DNA polymerase I (Klenow fragment). Biochemistry 31, 9227-9236.
10. Frey, M. W., Sowers, L. C., Millar, D. P., and Benkovic, S. J. (1995) The nucleotide analog 2-aminopurine as a spectroscopic probe of nucleotide incorporation by the Klenow fragment of Escherichia coli polymerase I and bacteriophage T4 DNA polymerase. Biochemistry 34, 9185-9192.
11. Joyce, C. M., Potapova, O., Delucia, A. M., Huang, X., Basu, V. P., and Grindley, N. D. (2008) Fingers-closing and other rapid conformational changes in DNA polymerase I (Klenow fragment) and their role in nucleotide selectivity. Biochemistry 47, 6103-6116. (Pubitemid 351812823)
12. Patel, S. S., Wong, I., and Johnson, K. A. (1991) Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant. Biochemistry 30, 511-525.
13. Wong, I., Patel, S. S., and Johnson, K. A. (1991) An induced-fit kinetic mechanism for DNA replication fidelity: Direct measurement by single-turnover kinetics. Biochemistry 30, 526-537.
14. Tsai, Y. C., and Johnson, K. A. (2006) A new paradigm for DNA polymerase specificity. Biochemistry 45, 9675-9687.
15. Kati, W. M., Johnson, K. A., Jerva, L. F., and Anderson, K. S. (1992) Mechanism and fidelity of HIV reverse transcriptase. J. Biol. Chem. 267, 25988-25997.
16. Hsieh, J. C., Zinnen, S., and Modrich, P. (1993) Kinetic mechanism of the DNA-dependent DNA polymerase activity of human immunodeficiency virus reverse transcriptase. J. Biol. Chem. 268, 24607-24613.
17. Zinnen, S., Hsieh, J. C., and Modrich, P. (1994) Misincorporation and mispaired primer extension by human immunodeficiency virus reverse transcriptase. J. Biol. Chem. 269, 24195-24202.
18. Capson, T. L., Peliska, J. A., Kaboord, B. F., Frey, M. W., Lively, C., Dahlberg, M., and Benkovic, S. J. (1992) Kinetic characterization of the polymerase and exonuclease activities of the gene 43 protein of bacteriophage T4. Biochemistry 31, 10984-10994
19. Frey, M. W., Nossal, N. G., Capson, T. L., and Benkovic, S. J. (1993) Construction and characterization of a bacteriophage T4 DNA polymerase deficient in 3′→5′ exonuclease activity. Proc. Natl. Acad. Sci. U.S.A. 90, 2579-2583
20. Wu, P., Nossal, N., and Benkovic, S. J. (1998) Kinetic characterization of a bacteriophage T4 antimutator DNA polymerase. Biochemistry 37, 14748-14755 (Pubitemid 28487582)
21. Hariharan, C., and Reha-Krantz, L. J. (2005) Using 2-aminopurine fluorescence to detect bacteriophage T4 DNA polymerase-DNA complexes that are important for primer extension and proofreading reactions. Biochemistry 44, 15674-15684 (Pubitemid 41746898)
22. Hariharan, C., Bloom, L. B., Helquist, S. A., Kool, E. T., and Reha-Krantz, L. J. (2006) Dynamics of nucleotide incorporation: Snapshots revealed by 2-aminopurine fluorescence studies. Biochemistry 45, 2836-2844. (Pubitemid 43334532)
23. Washington, M. T., Prakash, L., and Prakash, S. (2001) Yeast DNA polymerase η utilizes an induced-fit mechanism of nucleotide incorporation. Cell 107, 917-927. (Pubitemid 34084982)
24. Fiala, K. A., and Suo, Z. (2004) Pre-Steady-State Kinetic Studies of the Fidelity of Sulfolobus solfataricus P2 DNA Polymerase IV. Biochemistry 43, 2106-2115. (Pubitemid 38233272)
25. Fiala,K. A., and Suo, Z. (2004) Mechanism ofDNAPolymerization Catalyzed by Sulfolobus solfataricus P2 DNA Polymerase IV. Biochemistry 43, 2116-2125. (Pubitemid 38233273)
26. Fiala, K. A., Sherrer, S. M., Brown, J. A., and Suo, Z. (2008) Mechanistic consequences of temperature on DNA polymerization catalyzed by a Y-family DNA polymerase. Nucleic Acids Res. 36, 1990-2001.
27. Savino, C., Federici, L., Johnson, K. A., Vallone, B., Nastopoulos, V., Rossi, M., Pisani, F. M., and Tsernoglou, D. (2004) Insights into DNAreplication: The crystal structure ofDNApolymerase B1 from the archaeon Sulfolobus solfataricus. Structure 12, 2001-2008. (Pubitemid 39469397)
28. Duggin, I. G., and Bell, S. D. (2006) The chromosome replication machinery of the archaeon Sulfolobus solfataricus. J. Biol. Chem. 281, 15029-15032.
29. Dionne, I., Nookala, R. K., Jackson, S. P., Doherty, A. J., and Bell, S. D. (2003) A heterotrimeric PCNA in the hyperthermophilic archaeon Sulfolobus solfataricus. Mol. Cell 11, 275-282. (Pubitemid 36126608)
30. Dionne, I., Brown, N. J.,Woodgate, R., and Bell, S. D. (2008) On the mechanism of loading the PCNA sliding clamp by RFC. Mol. Microbiol. 68, 216-222.
31. Xing, G., Kirouac, K., Shin, Y. J., Bell, S. D., and Ling, H. (2009) Structural insight into recruitment of translesion DNA polymerase Dpo4 to sliding clamp PCNA. Mol. Microbiol. 71, 678-691.
32. Zhang, L., Brown, J. A., Newmister, S. A., and Suo, Z. (2009) Polymerization Fidelity of a Replicative DNA Polymerase from the Hyperthermophilic Archaeon Sulfolobus solfataricus P2. Biochemistry (DOI 10.1021/bi900532w).
33. Eckstein, F. (1985) Nucleoside phosphorothioates. Annu. Rev. Biochem. 54, 367-402.
34. Liu, J., and Tsai,M. D. (2001) DNA polymerase β: Pre-steady-state kinetic analyses of dATPRS stereoselectivity and alteration of the stereoselectivity by various metal ions and by site-directed mutagenesis. Biochemistry 40, 9014-9022.
35. Arnold, J. J., Ghosh, S. K., and Cameron, C. E. (1999) Poliovirus RNA-dependent RNA polymerase (3D(pol)). Divalent cation modulation of primer, template, and nucleotide selection. J. Biol. Chem. 274, 37060-37069.
36. Barshop, B. A., Wrenn, R. F., and Frieden, C. (1983) Analysis of numerical methods for computer simulation of kinetic processes: Development of KINSIM;a flexible, portable system. Anal. Biochem. 130, 134-145.
37. Zimmerle, C. T., and Frieden, C. (1989) Analysis of progress curves by simulations generated by numerical integration. Biochem. J. 258, 381-387.
38. Herschlag, D., Piccirilli, J. A., and Cech, T. R. (1991) Ribozymecatalyzed and nonenzymatic reactions of phosphate diesters: Rate effects upon substitution of sulfur for a nonbridging phosphoryl oxygen atom. Biochemistry 30, 4844-4854.
39. Fiala,K. A., and Suo, Z. (2004) Mechanism of DNA Polymerization Catalyzed by Sulfolobus solfataricus P2 DNA Polymerase IV. Biochemistry 43, 2116-2125. (Pubitemid 38233273)
40. Joyce, C. M., and Benkovic, S. J. (2004) DNA polymerase fidelity: Kinetics, structure, and checkpoints. Biochemistry 43, 14317-14324. (Pubitemid 39491965)
41. Florian, J., Goodman, M. F., and Warshel, A. (2003) Computer simulation of the chemical catalysis of DNA polymerases: Discriminating between alternative nucleotide insertion mechanisms for T7 DNA polymerase. J. Am. Chem. Soc. 125, 8163-8177.
42. Pauling, L. (1946) Molecular Architecture and Biological Reactions. Chem. Eng. News 24, 1375-1377.
43. Radhakrishnan, R., and Schlick, T. (2006) Correct and incorrect nucleotide incorporation pathways in DNA polymerase β. Biochem. Biophys. Res. Commun. 350, 521-529.
44. Washington, M. T., Johnson, R. E., Prakash, L., and Prakash, S. (2003) The mechanism of nucleotide incorporation by human DNA polymerase η differs from that of the yeast enzyme. Mol. Cell. Biol. 23, 8316-8322.
45. Pelletier, H., Sawaya, M. R., Wolfle, W., Wilson, S. H., and Kraut, J. (1996) Crystal structures of human DNA polymerase β complexed with DNA: implications for catalytic mechanism, processivity, and fidelity. Biochemistry 35, 12742-12761. (Pubitemid 26337329)
46. Li, Y., Korolev, S., and 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. (Pubitemid 29002718)
47. 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. (Pubitemid 28099004)
48. Franklin, M. C., Wang, J., and Steitz, T. A. (2001) Structure of the replicating complex of a pol R family DNA polymerase. Cell 105, 657-667. (Pubitemid 32524118)
49. Johnson, S. J., Taylor, J. S., and Beese, L. S. (2003) Processive DNA synthesis observed in a polymerase crystal suggests a mechanism for the prevention of frameshift mutations. Proc. Natl. Acad. Sci. U.S.A. 100, 3895-3900.
50. Garcia-Diaz, M., Bebenek, K., Krahn, J. M., Kunkel, T. A., and Pedersen, L. C. (2005) A closed conformation for the Pol λ catalytic cycle. Nat. Struct. Mol. Biol. 12, 97-98.
51. Wong, J. H., Fiala, K. A., Suo, Z., and Ling, H. (2008) Snapshots of a Y-family DNA polymerase in replication: Substrate-induced conformational transitions and implications for fidelity of Dpo4. J. Mol. Biol. 379, 317-330.
52. Rothwell, P. J., Mitaksov, V., and Waksman, G. (2005) Motions of the fingers subdomain of klentaq1 are fast and not rate limiting: Implications for the molecular basis of fidelity in DNA polymerases. Mol. Cell 19, 345-355. (Pubitemid 41074890)
53. Pal, S. K., and Zewail, A. H. (2004) Dynamics of water in biological recognition. Chem. Rev. 104, 2099-2123.
54. Mace, D. C., and Alberts, B. M. (1984) Characterization of the stimulatory effect of T4 gene 45 protein and the gene 44/62 protein complex on DNA synthesis by T4 DNA polymerase. J. Mol. Biol. 177, 313-327.
55. Tabor, S., Huber, H. E., and Richardson, C. C. (1987) Escherichia coli thioredoxin confers processivity on the DNA polymerase activity of the gene 5 protein of bacteriophage T7. J. Biol. Chem. 262, 16212-16223.
56. Huber, H. E., Tabor, S., and Richardson, C. C. (1987) Escherichia coli thioredoxin stabilizes complexes of bacteriophage T7 DNA polymerase and primed templates. J. Biol. Chem. 262, 16224-16232.
57. Johnson, A. A., Tsai, Y., Graves, S. W., and Johnson, K. A. (2000) Human mitochondrial DNA polymerase holoenzyme: Reconstitution and characterization. Biochemistry 39, 1702-1708. (Pubitemid 30108960)
58. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2001) Crystal structure of a Y-familyDNApolymerase in action:Amechanism for error-prone and lesion-bypass replication. Cell 107, 91-102. (Pubitemid 32972040)