Formation of purine-purine mispairs by Sulfolobus solfataricus DNA polymerase IV

Biochemistry

Volumn 47, Issue 31, 2008, Pages 8157-8164

  DeCarlo, Lindsey ^a   Gowda, A S Prakasha ^a   Suo, Zucai ^b   Spratt, Thomas E ^a  

^a PENN STATE MILTON S HERSHEY MEDICAL CENTER   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONCENTRATION (PROCESS); DNA; GENES; HYDROGEN; HYDROGEN BONDS; NONMETALS; ORGANIC ACIDS; RATE CONSTANTS;

ACTIVE SITES; BASE PAIRS; DNA CONCENTRATION; DNA DAMAGES; DNA POLYMERASES; FIRST ORDER EQUATIONS; FIRST-ORDER RATE CONSTANTS; MODIFIED NUCLEOTIDES; PROTEIN-DNA INTERACTIONS; SULFOLOBUS SOLFATARICUS; TIME COURSES; WATSON-CRICK BASE PAIRS;

NUCLEIC ACIDS;

ADENINE; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE ETA; DNA POLYMERASE; DNA POLYMERASE IV; GUANINE; NUCLEOTIDE; PURINE;

AMINO ACID SUBSTITUTION; ARTICLE; BASE MISPAIRING; BASE PAIRING; CONFORMATION; DNA DAMAGE; GEOMETRY; HYDROGEN BOND; KINETICS; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS; SULFOLOBUS SOLFATARICUS;

ADENINE; ARCHAEAL PROTEINS; BASE PAIR MISMATCH; BASE PAIRING; DNA DAMAGE; DNA POLYMERASE BETA; DNA REPLICATION; GUANINE; HYDROGEN BONDING; KINETICS; MOLECULAR STRUCTURE; PURINES; SULFOLOBUS SOLFATARICUS;

SULFOLOBUS SOLFATARICUS;

EID: 48649102536     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800820m     Document Type: Article

References (43)

1. Kool, E. T. (2002) Active site tightness and substrate fit in DNA replication. Annu. Rev. Biochem. 71, 191-219.
2. Kool, E. T., and Sintim, H. O. (2006) The difluorotoluene debate: A decade later. Chem. Commun., 3665-3675.
3. Prakash, S., Johnson, R. E., and Prakash, L. (2005) Eukaryotic Translesion Synthesis DNA Polymerases: Specificity of Structure and Function. Annu. Rev. Biochem. 74, 317-353.
4. 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.
5. Mizrahi, V., Henrie, R. N., Marlier, J. F., Johnson, K. A., and Benkovic, S. J. (1985) Rate-limiting steps in the DNA polymerase I reaction pathway. Biochemistry 24, 4010-4018.
6. 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.
7. Fiala, K. A., and Suo, Z. (2004) Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry 43, 2116-2125.
8. Trincao, J., Johnson, R. E., Wolfle, W. T., Escalante, C. R., Prakash, S., Prakash, L., and Aggarwal, A. K. (2004) Dpo4 is hindered in extending a G·T mismatch by a reverse wobble. Nat. Struct. Mol. Biol. 11, 457-462.
9. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2001) Crystal structure of a Y-family DNA polymerase in action: A mechanism for error-prone and lesion-bypass replication. Cell 107, 91-102.
10. Vaisman, A., Ling, H., Woodgate, R., and Yang, W. (2005) Fidelity of Dpo4: Effect of metal ions, nucleotide selection and pyrophosphorolysis. EMBO J. 24, 2957-2967.
11. Ling, H., Sayer, J. M., Plosky, B. S., Yagi, H., Boudsocq, F., Woodgate, R., Jerina, D. M., and Yang, W. (2004) Crystal structure of a benzo[a]pyrene diol epoxide adduct in a ternary complex with a DNA polymerase. Proc. Natl. Acad. Sci. U.S.A. 101, 2265-2269.
12. Ling, H., Boudsocq, F., Plosky, B. S., Woodgate, R., and Yang, W. (2003) Replication of a cis-syn thymine dimer at atomic resolution. Nature 424, 1083-1087.
13. Ling, H., Boudsocq, F., Woodgate, R., and Yang, W. (2004) Snapshots of replication through an abasic lesion: Structural basis for base substitutions and frameshifts. Mol. Cell 13, 751-762.
14. Rechkoblit, O., Malinina, L., Cheng, Y., Kuryavyi, V., Broyde, S., Geacintov, N. E., and Patel, D. J. (2006) Stepwise Translocation of Dpo4 Polymerase during Error-Free Bypass of an oxoG Lesion. PLoS Biol. 4.
15. Zang, H., Goodenough, A. K., Choi, J. Y., Irimia, A., Loukachevitch, L. V., Kozekov, I. D., Angel, K. C., Rizzo, C. J., Egli, M., and Guengerich, F. P. (2005) DNA Adduct Bypass Polymerization by Sulfolobus solfataricus DNA Polymerase Dpo4: Analysis and Crystal Structures of Multiple Base Pair Substitution and Frameshift Products with the Adduct 1,N2-Ethenoguanine. J. Biol. Chem. 280, 29750-29764.
16. Wolfle, W. T., Washington, M. T., Kool, E. T., Spratt, T. E., Helquist, S. A., Prakash, L., and Prakash, S. (2005) Evidence for a Watson-Crick Hydrogen Bonding Requirement in DNA Synthesis by Human DNA Polymerase kappa. Mol. Cell. Biol. 25, 7137-7143.
17. Hwang, H., and Taylor, J. S. (2005) Evidence for Watson-Crick and not Hoogsteen or wobble base pairing in the selection of nucleotides for insertion opposite pyrimidines and a thymine dimer by yeast DNA pol η. Biochemistry 44, 4850-4860.
18. Kim, T. W., Brieba, L. G., Ellenberger, T., and Kool, E. T. (2006) Functional Evidence for a Small and Rigid Active Site in a High Fidelity DNA Polymerase: Probing T7 DNA Polymerase with Variably Sized Base Pairs. J. Biol. Chem. 281, 2289-2295.
19. Mizukami, S., Kim, T. W., Helquist, S. A., and Kool, E. T. (2006) Varying DNA base-pair size in subangstrom increments: Evidence for a loose, not large, active site in low-fidelity Dpo4 polymerase. Biochemistry 45, 2772-2778.
20. Dunn, D. B., and Hall, R. H. (1986) In Handbook of Biochemistry and Molecular Biology (Fasman, G. D., Ed.) pp 65-215, CRC Press, Boca Raton, FL.
21. Borer, P. (1977) Optical properties of nucleic acids, absorption, and circular dichroism spectra. In Handbook of Biochemistry and Molecular Biology (Fasman, G. D., Ed.) pp 589, CRC Press, Boca Raton, FL.
22. 6-alkylguanine-DNA alkyltransferase. Biochemistry 33, 11364-11371.
23. Gervais, V., Cognet, J. A., Le Bret, M., Sowers, L. C., and Fazakerley, G. V. (1995) Solution structure of two mismatches A·A and T·T in the K-ras gene context by nuclear magnetic resonance and molecular dynamics. Eur. J. Biochem. 228, 279-290.
24. Gao, X., and Patel, D. J. (1988) G(syn)-A(anti) mismatch formation in DNA dodecamers at acidic pH: pH-dependent transition of G-A mispairs detected by proton NMR. J. Am. Chem. Soc. 110, 5178-5182.
25. Leonard, G. A., Booth, E. D., and Brown, T. (1990) Structural and thermodynamic studies on the adenine.guanine mismatch in B-DNA. Nucleic Acids Res. 18, 5617-5623.
26. Brown, T., Leonard, G. A., Booth, E. D., and Chambers, J. (1989) Crystal structure and stability of a DNA duplex containing A(anti)·G(syn) base-pairs. J. Mol. Biol. 207, 455-457.
27. 2 dodecamer. Biochem. J. 279 (Part 1), 269-281.
28. Kan, L. S., Chandrasegaran, S., Pulford, S. M., and Miller, P. S. (1983) Detection of a guanine X adenine base pair in a decadeoxyribonucleotide by proton magnetic resonance spectroscopy. Proc. Natl. Acad. Sci U.S.A. 80, 4263-4265.
29. Johnson, S. J., and Beese, L. S. (2004) Structures of mismatch replication errors observed in a DNA polymerase. Cell 116, 803-816.
30. Prive, G. G., Heinemann, U., Chandrasegaran, S., Kan, L. S., Kopka, M. L. and Dickerson, R. E. (1987) Helix geometry, hydration, and G·A mismatch in a B-DNA decamer. Science 238, 498-504.
31. Hunter, W. N., Brown, T., and Kennard, O. (1986) Structural features and hydration of d(C-G-C-G-A-A-T-T-A-G-C-G); a double helix containing two G.A mispairs. J. Biomol. Struct. Dyn. 4, 173-191.
32. Brown, T., Hunter, W. N., Kneale, G., and Kennard, O. (1986) Molecular structure of the G·A base pair in DNA and its implications for the mechanism of transversion mutations. Proc. Natl. Acad. Sci U.S.A. 83, 2402-2406.
33. Cognet, J. A., Gabarro-Arpa, J., Le Bret, M., van der marel, G. A., van Boom, J. H., and Fazakerley, G. V. (1991) Solution conformation of an oligonucleotide containing a G·G mismatch determined by nuclear magnetic resonance and molecular mechanics. Nucleic Acids Res. 19, 6771-6779.
34. Skelly, J. V., Edwards, K. J., Jenkins, T. C., and Neidle, S. (1993) Crystal structure of an oligonucleotide duplex containing G·G base pairs: Influence of mispairing on DNA backbone conformation. Proc. Natl. Acad. Sci. U.S.A. 90, 804-808.
35. Faibis, V., Cognet, J. A., Boulard, Y., Sowers, L. C., and Fazakerley, G. V. (1996) Solution structure of two mismatches G·G and I·I in the K-ras gene context by nuclear magnetic resonance and molecular dynamics. Biochemistry 35, 14452-14464.
36. Johnson, R. E., Prakash, L., and Prakash, S. (2005) Biochemical evidence for the requirement of Hoogsteen base pairing for replication by human DNA polymerase ι. Proc. Natl. Acad. Sci. U.S.A. 102, 10466-10471.
37. Kretulskie, A. M., and Spratt, T. E. (2006) Structure of purine-purine mispairs during misincorporation and extension by E. coli DNA polymerase I. Biochemistry 45, 3740-3746.
38. 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.
39. Potapova, O., Chan, C., DeLucia, A. M., Helquist, S. A., Kool, E. T., Grindley, N. D. F., and Joyce, C. M. (2006) DNA Polymerase Catalysis in the Absence of Watson-Crick Hydrogen Bonds: Analysis by Single-Turnover Kinetics. Biochemistry 45, 890-898.
40. Irimia, A., Eoff, R. L., Pallan, P. S., Guengerich, F. P., and Egli, M. (2007) Structure and Activity of Y-class DNA Polymerase DPO4 from Sulfolobus solfataricus with Templates Containing the Hydrophobic Thymine Analog 2,4-Difluorotoluene. J. Biol. Chem. 282, 36421-36433.
41. Potapova, O., Grindley, N. D. F., and Joyce, C. M. (2002) The Mutational Specificity of the Dbh Lesion Bypass Polymerase and Its Implications. J. Biol. Chem. 277, 28157-28166.
42. Kim, T. W., Delaney, J. C., Essigmann, J. M., and Kool, E. T. (2005) Probing the active site tightness of DNA polymerase in subangstrom increments. Proc. Natl. Acad. Sci. U.S.A. 102, 15803-15808.
43. Bevington, P. (1969) Propagation of Errors. In Data Reduction and Error Analysis for the Physical Sciences, pp 56-65, McGraw-Hill, New York.