Fidelity of Dpo4: Effect of metal ions, nucleotide selection and pyrophosphorolysis

EMBO Journal

Volumn 24, Issue 17, 2005, Pages 2957-2967

  Vaisman, Alexandra ^a   Ling, Hong ^b,c   Woodgate, Roger ^a   Yang, Wei ^b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

Base stacking; Fidelity; Metal ion; Mismatch; Pyrophosphorolysis

Indexed keywords

DNA POLYMERASE; DNA POLYMERASE IV; MAGNESIUM ION; MANGANESE; METAL ION; NUCLEOTIDE; PYROPHOSPHATE; UNCLASSIFIED DRUG; CATION; DEOXYGUANOSINE PHOSPHATE; DEOXYGUANOSINE TRIPHOSPHATE; DNA DIRECTED DNA POLYMERASE; MAGNESIUM;

ARTICLE; BASE MISPAIRING; CATALYSIS; CHEMICAL REACTION; CONFORMATIONAL TRANSITION; CRYSTAL STRUCTURE; DNA SYNTHESIS; POLYMERIZATION; PRIORITY JOURNAL; PYROPHOSPHOROLYSIS; SYNTHESIS; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; KINETICS; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BASE PAIR MISMATCH; BINDING SITES; CATALYSIS; CATIONS; CRYSTALLOGRAPHY, X-RAY; DEOXYGUANINE NUCLEOTIDES; DIPHOSPHATES; DNA-DIRECTED DNA POLYMERASE; KINETICS; MAGNESIUM; MANGANESE; MODELS, MOLECULAR; NUCLEOTIDES; PROTEIN CONFORMATION;

EID: 27144542782     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600786     Document Type: Article

References (47)

1. Arion D, Kaushik N, McCormick S, Borkow G, Parniak MA (1998) Phenotypic mechanism of HIV-1 resistance to 3′-azido-3′-deoxythymidine (AZT): increased polymerization processivity and enhanced sensitivity to pyrophosphate of the mutant viral reverse transcriptase. Biochemistry 37: 15908-15917
2. Bebenek K, Kunkel TA (2004) Functions of DNA polymerases. Adv Protein Chem 69: 137-165
3. Boudsoçq F, Iwai S, Hanaoka F, 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
4. Boudsoçq F, Kokoska RJ, Plosky BS, Vaisman A, Ling H, Kunkel TA, Yang W, Woodgate R (2004) Investigating the role of the little finger domain of Y-family DNA polymerases in low fidelity synthesis and translesion replication. J Biol Chem 279: 32932-32940
5. Brieba LG, Eichman BF, Kokoska RJ, Doublie S, Kunkel TA, Ellenberger T (2004) Structural basis for the dual coding potential of 8-oxoguanosine by a high-fidelity DNA polymerase. EMBO J 23: 3452-3461
6. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang JS, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr D 54 (Part 5): 905-921
7. Dahlberg ME, Benkovic SJ (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
8. Deutscher MP, Kornberg A (1969) Enzymatic synthesis of deoxyribonucleic acid. 28. The pyrophosphate exchange and pyrophosphorolysis reactions of deoxyribonucleic acid polymerase. J Biol Chem 244: 3019-3028
9. Doublie S, Sawaya MR, Ellenberger T (1999) An open and closed case for all polymerases. Struct Fold Des 7: R31-R35
10. Doublie S, Tabor S, Long AM, Richardson CC, Ellenberger T (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature 391: 251-258
11. Dutta S, Li Y, Johnson D, Dzantiev L, Richardson CC, Romano LJ, Ellenberger T (2004) Crystal structures of 2-acetylaminofluorene and 2-aminofluorene in complex with T7 DNA polymerase reveal mechanisms of mutagenesis. Proc Natl Acad Sci USA 101: 16186-16191
12. Fiala KA, Suo Z (2004) Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry 43: 2116-2125
13. Franklin MC, Wang J, Steitz TA (2001) Structure of the replicating complex of a pol α family DNA polymerase. Cell 105: 657-667
14. Friedberg EC, Walker GC, Siede W (1995) DNA Repair and Mutagenesis. Washington, DC: ASM Press
15. Glick E, Chau JS, Vigna KL, McCulloch SD, Adman ET, Kunkel TA, Loeb LA (2003) Amino acid substitutions at conserved tyrosine 52 alter fidelity and bypass efficiency of human DNA polymerase η. J Biol Chem 278: 19341-19346
16. Huang H, Chopra R, Verdine GL, Harrison SC (1998) Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282: 1669-1675
17. Johnson SJ, Beese LS (2004) Structures of mismatch replication errors observed in a DNA polymerase. Cell 116: 803-816
18. Jones TA, Zou J-Y, Cowan SW (1991) Improved methods for building models in electron density maps and the location of errors in these models. Acta Crystallogr A 47: 110-119
19. 2+ requirements. EMBO J 15: 2547-2555
20. Kool ET (2002) Active site tightness and substrate fit in DNA replication. Annu Rev Biochem 71: 191-219
21. Kunkel TA, Bebenek K (2000) DNA replication fidelity. Annu Rev Biochem 69: 497-529
22. Kunkel TA, Loeb LA (1979) On the fidelity of DNA replication. Effect of divalent metal ion activators and deoxyrionucleoside triphosphate pools on in vitro mutagenesis. J Biol Chem 254: 5718-5725
23. Lecomte P, Doubleday OP, Radman M (1986) Evidence for an intermediate in DNA synthesis involving pyrophosphate exchange. A possible role in fidelity. J Mol Biol 189: 643-652
24. Li Y, Dutta S, Doublie S, Bdour HM, Taylor JS, Ellenberger T (2004) Nucleotide insertion opposite a cis-syn thymine dimer by a replicative DNA polymerase from bacteriophage T7. Nat Struct Mol Biol 11: 784-790
25. 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
26. Ling H, Boudsocq F, Plosky BS, Woodgate R, Yang W (2003) Replication of a cis-syn thymine dimer at atomic resolution. Nature 424: 1083-1087
27. Ling H, Boudsocq F, Woodgate R, 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
28. Ling H, Boudsocq F, Woodgate R, Yang W (2004a) Snapshots of replication through an abasic lesion; structural basis for base substitutions and frameshifts. Mol Cell 13: 751-762
29. Ling H, Sayer JM, Plosky BS, Yagi H, Boudsocq F, Woodgate R, Jerina DM, Yang W (2004b) Crystal structure of a benzo[a]pyrene diol epoxide adduct in a ternary complex with a DNA polymerase. Proc Natl Acad Sci USA 101: 2265-2269
30. Meyer PR, Matsuura SE, Mian AM, So AG, Scott WA (1999) A mechanism of AZT resistance: an increase in nucleotide-dependent primer unblocking by mutant HIV-1 reverse transcriptase. Mol Cell 4: 35-43
31. Nair DT, Johnson RE, Prakash S, Prakash L, Aggarwal AK (2004) Replication by human DNA polymerase-ι occurs by Hoogsteen base-pairing. Nature 430: 377-380
32. Natrajan G, Lamers MH, Enzlin JH, Winterwerp HH, Perrakis A, Sixma TK (2003) Structures of Escherichia coli DNA mismatch repair enzyme MutS in complex with different mismatches: a common recognition mode for diverse substrates. Nucleic Acids Res 31: 4814-4821
33. Obmolova G, Ban C, Hsieh P, Yang W (2000) Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407: 703-710
34. Ohmori H, Friedberg EC, Fuchs RP, Goodman MF, Hanaoka F, Hinkle D, Kunkel TA, Lawrence CW, Livneh Z, Nohmi T, Prakash L, Prakash S, Todo T, Walker GC, Wang Z, Woodgate R (2001) The Y-family of DNA polymerases. Mol Cell 8: 7-8
35. Otwinowski Z, Minor W (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276: 307-326
36. Rozovskaia TA, Tarusova NB, Minasian S, Atrazhev AM, Kukhanova MK (1989) [Analogs of pyrophosphate in a pyrophosphorolysis reaction catalyzed by DNA polymerases]. Mol Biol (Mosk) 23: 862-871
37. Shah AM, Li SX, Anderson KS, Sweasy JB (2001) Y265H mutator mutant of DNA polymerase β. Proper teometric alignment is critical for fidelity. J Biol Chem 276: 10824-10831
38. Silvian LF, Toth EA, Pham P, Goodman MF, Ellenberger T (2001) Crystal structure of a DinB family error-prone DNA polymerase from Sulfolobus solfataricus. Nat Struct Biol 8: 984-989
39. Trincao J, Johnson RE, Wolfle WT, Escalante CR, Prakash S, Prakash L, Aggarwal AK (2004) Dpo4 is hindered in extending a G.T mismatch by a reverse wobble. Nat Struct Mol Biol 11: 457-462
40. Uljon SN, Johnson RE, Edwards TA, Prakash S, Prakash L, Aggarwal AK (2004) Crystal structure of the catalytic core of human DNA polymerase κ. Structure (Camb) 12: 1395-1404
41. Vaisman A, Tissier A, Frank EG, Goodman MF, Woodgate R (2001) Human DNA polymerase ι promiscuous mismatch extension. J Biol Chem 276: 30615-30622
42. Vermote CL, Vipond IB, Halford SE (1992) EcoRV restriction endonuclease: communication between DNA recognition and catalysis. Biochemistry 31: 6089-6097
43. Villani G, Tanguy Le Gac N, Wasungu L, Burnouf D, Fuchs RP, Boehmer PE (2002) Effect of manganese on in vitro replication of damaged DNA catalyzed by the herpes simplex virus type-1 DNA polymerase. Nucleic Acids Res 30: 3323-3332
44. Vipond IB, Moon BJ, Halford SE (1996) An isoleucine to leucine mutation that switches the cofactor requirement of the EcoRV restriction endonuclease from magnesium to manganese. Biochemistry 35: 1712-1721
45. Yang L, Arora K, Beard WA, Wilson SH, Schlick T (2004) Critical role of magnesium ions in DNA polymerase β's closing and active site assembly. J Am Chem Soc 126: 8441-8453
46. Yang W (2003) Damage repair DNA polymerases Y. Curr Opin Struct Biol 13: 23-30
47. Zhou BL, Pata JD, Steitz TA (2001) Crystal structure of a DinB lesion bypass DNA polymerase catalytic fragment reveals a classic polymerase catalytic domain. Mol Cell 8: 427-437