Structure and mechanism of DNA polymerases

Advances in Protein Chemistry

Volumn 71, Issue , 2005, Pages 401-440

  Rothwell, Paul J ^a   Waksman, Gabriel ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; DNA POLYMERASE; MOLECULAR MOTOR; MUTAGENIC AGENT; NUCLEOTIDE; PRIMER DNA; RNA DIRECTED DNA POLYMERASE;

BACTERIOPHAGE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DNA BINDING; DNA DAMAGE; DNA REPLICATION; DNA SYNTHESIS; DNA TEMPLATE; ENZYME ACTIVITY; ENZYME STRUCTURE; HUMAN; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; REVIEW; STRUCTURE ANALYSIS; ULTRAVIOLET RADIATION;

ANIMALS; CATALYSIS; DNA; DNA-DIRECTED DNA POLYMERASE; HUMANS; NUCLEOTIDES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY;

EID: 26844566830     PISSN: 00653233     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0065-3233(04)71011-6     Document Type: Review

References (154)

1. Abbotts J., Sen Gupta D.N., Zmudzka B., Widen S.G., Notario V., and Wilson S.H. Expression of human DNA polymerase β in Escherichia coli and characterization of the recombinant enzyme Biochemistry 27 1988 901 909
2. Ahn J., Werneburg B.G., and Tsai M.D. DNA polymerase β: Structure-fidelity relationship from pre-steady-state kinetic analyses of all possible correct and incorrect base pairs for wild type and R283A mutant Biochemistry 36 1997 1100 1107
3. Andricioaei I., Goel A., Herschbach D., and Karplus M. Dependence of DNA polymerase replication rate on external forces: A model based on molecular dynamics simulations Biophys. J. 87 2004 1478 1497
4. Astatke M., Grindley N.D., and Joyce C.M. Deoxynucleoside triphosphate and pyrophosphate binding sites in the catalytically competent ternary complex for the polymerase reaction catalyzed by DNA polymerase I (Klenow fragment) J. Biol. Chem. 270 1995 1945 1954
5. Basu A., and Modak M.J. Identification and amino acid sequence of the deoxynucleoside triphosphate binding site in Escherichia coli DNA polymerase I Biochemistry 26 1987 1704 1709
6. Beese L.S., Derbyshire V., and Steitz T.A. Structure of DNA polymerase I Klenow fragment bound to duplex DNA Science 260 1993 352 355
7. Beese L.S., Friedman J.M., and Steitz T.A. Crystal structures of the Klenow fragment of DNA polymerase I complexed with deoxynucleoside triphosphate and pyrophosphate Biochemistry 32 1993 14095 14101
8. Bork P., Hofmann K., Bucher P., Neuwald A., Altschul S., and Koonin E. A superFamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins FASEB J. 11 1997 68 76
9. Boudsocq F., Iwai S., Hanaoka F., and Woodgate R. Sulfolobus solfataricus P2 DNA polymerase IV (Dpo4): An archaeal DNA polymerase with lesion-bypass properties akin to eukaryotic pol η Nucleic Acids Res. 15 2001 4607 4613
10. Braithwaite D.K., and Ito J. Compilation, alignment, and phylogenetic relationships of DNA polymerases Nucleic Acids Res. 21 1993 787 802
11. Bruskov V.I., and Poltev V.I. On molecular mechanisms of nucleic acid synthesis. Fidelity aspects: 2. Contribution of protein-nucleotide recognition J. Theor. Biol. 78 1979 29 41
12. Burgers P.M., Koonin E.V., Bruford E., Blanco L., Burtis K.C., Christman M.F., Copeland W.C., Friedberg E.C., Hanaoka F., Hinkle D.C., Lawrence C.W., Nakanishi M., Ohmori H., Prakash L., Prakash S., Reynaud C.A., Sugino A., Todo T., Wang Z., Weill J.C., and Woodgate R. Eukaryotic DNA polymerases: Proposal for a revised nomenclature J. Biol. Chem. 276 2001 43487 43490
13. Cann I.K., Komori K., Toh H., Kanai S., and Ishino Y. A heterodimeric DNA polymerase: Evidence that members of Euryarchaeota possess a distinct DNA polymerase Proc. Natl. Acad. Sci. USA 95 1998 14250 14255
14. Capson T.L., Peliska J.A., Kaboord B.F., Frey M.W., Lively C., Dahlberg M., and Benkovic S.J. Kinetic characterization of the polymerase and exonuclease activities of the gene 43 protein of bacteriophage T4 Biochemistry 31 1992 10984 10994
15. Carroll S.S., Cowaet M., and Benkovic S.J. A mutant of DNA polymerase I (Klenow Fragment) with reduced fidelity Biochemistry 30 1991 804 813
16. Dahlberg M.E., and Benkovic S.J. Kinetic mechanism of DNA polymerase I (Klenow fragment): Identification of a second conformational change and evaluation of the internal equilibrium constant Biochemistry 30 1991 4835 4843
17. Das D., and Georgiadis M.M. The crystal structure of the monomeric reverse transcriptase from Moloney murine leukemia virus Structure 12 2004 819 829
18. Delarue M., Poch O., Tordo N., Moras D., and Argos P. An attempt to unify the structure of polymerases Protein Eng. 3 1990 461 467
19. Dianov G.L., Sleeth K.M., Dianova II, and Allinson S.L. Repair of abasic sites in DNA Mutat. Res. 531 2003 157 163
20. Ding J., Das K., Hsiou Y., Sarafianos S.G., Clark A.D. Jr., Jacobo-Molina A., Tantillo C., Hughes S.H., and Arnold E. Structure and functional implications of the polymerase active site region in a complex of HIV-1 RT with a double-stranded DNA template-primer and an antibody Fab fragment at 2.8 Å resolution J. Mol. Biol. 284 1998 1095 1111
21. Ding J., Das K., Moereels H., Koymans L., Andries K., Janssen P.A., Hughes S.H., and Arnold E. Structure of HIV-1 RT/TIBO R 86183 complex reveals similarity in the binding of diverse nonnucleoside inhibitors Nat. Struct. Biol. 2 1995 407 415
22. Ding J., Das K., Tantillo C., Zhang W., Clark A.D. Jr., Jessen S., Lu X., Hsiou Y., Jacobo-Molina A., Andries K., Pauwels R., Moereels H., Koymans L., Janssen P.A.J., Smith R.H. Jr., Kroeger Koepke M., Michejda C.J., Hughes S.H., and Arnold E. Structure of HIV-1 reverse transcriptase in a complex with the non-nucleoside inhibitor alpha-APA R 95845 at 2.8 Å resolution Structure 3 1995 365 379
23. Divita G., Rittinger K., Geourjon C., Deleage G., and Goody R.S. Dimerization kinetics of HIV-1 and HIV-2 reverse transcriptase: A two step process J. Mol. Biol. 245 1995 508 521
24. Divita G., Rittinger K., Restle T., Immendorfer U., and Goody R.S. Conformational stability of dimeric HIV-1 and HIV-2 reverse transcriptases Biochemistry 34 1995 16337 16346
25. Dominguez O., Ruiz J.F., Lain de Lera T., Garcia-Diaz M., Gonzalez M.A., Kirchhoff T., Martinez A.C., Bernad A., and Blanco L. DNA polymerase μ (Pol μ), homologous to TdT, could act as a DNA mutator in eukaryotic cells EMBO J. 19 2000 1731 1742
26. Dong Q., Copeland W.C., and Wang T.S. Mutational studies of human DNA polymerase α: Identification of residues critical for deoxynucleotide binding and misinsertion fidelity of DNA synthesis J. Biol. Chem. 268 1993 24163 24174
27. Donlin M.J., Patel S.S., and Johnson K.A. Kinetic partitioning between the exonuclease and polymerase sites in DNA error correction Biochemistry 30 1991 538 546
28. Doublie S., Tabor S., Long A.M., Richardson C.C., and Ellenberger T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution Nature 391 1998 251 258
29. Dunlap C.A., and Tsai M.D. Use of 2-aminopurine and tryptophan fluorescence as probes in kinetic analyses of DNA polymerase β Biochemistry 41 2002 11226 11235
30. Echols H., and Goodman M.F. Fidelity mechanism in DNA replication Annu. Rev. Biochem. 60 1991 477 511
31. Eger B.T., and Benkovic S.J. Minimal kinetic mechanism for misincorporation by DNA polymerase I (Klenow fragment) Biochemistry 31 1992 9227 9236
32. Engel J.D., and von Hippel P.H. D(M6ATP) as a probe of the fidelity of base incorporation into polynucleotides by Escherichia coli DNA polymerase I J. Biol. Chem. 253 1978 935 939
33. Eom S.H., Wang J., and Steitz T.A. Structure of Taq ploymerase with DNA at the polymerase active site Nature 382 1996 278 281
34. Esnouf R., Ren J., Ross C., Jones Y., Stammers D., and Stuart D. Mechanism of inhibition of HIV-1 reverse transcriptase by non-nucleoside inhibitors Nat. Struct. Biol. 2 1995 303 308
35. Fiala K.A., and Suo Z. Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV Biochemistry 43 2004 2116 2125
36. Fiala K.A., and Suo Z. Pre-steady-state kinetic studies of the fidelity of Sulfolobus solfataricus P2 DNA polymerase IV Biochemistry 43 2004 2106 2115
37. Franklin M.C., Wang J., and Steitz T.A. Structure of the replicating complex of a pol α Family DNA polymerase Cell 105 2001 657 667
38. Freemont P.S., Friedman J.M., Beese L.S., Sanderson M.R., and Steitz T.A. Cocrystal structure of an editing complex of Klenow fragment with DNA Proc. Natl. Acad. Sci. USA 85 1988 8924 8928
39. Frey M.W., Sowers L.C., Millar D.P., and Benkovic S.J. 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 1995 9185 9192
40. Friedberg E.C., Feaver W.J., and Gerlach V.L. The many faces of DNA polymerases: Strategies for mutagenesis and for mutational avoidance Proc. Natl. Acad. Sci. USA 97 2000 5681 5683
41. Friedberg E.C., and Gerlach V.L. Novel DNA polymerases offer clues to the molecular basis of mutagenesis Cell 98 1999 413 416
42. Garcia-Diaz M., Dominguez O., Lopez-Fernandez L.A., de Lera L.T., Saniger M.L., Ruiz J.F., Parraga M., Garcia-Ortiz M.J., Kirchhoff T., and del Mazo J. DNA polymerase λ (Pol λ), a novel eukaryotic DNA polymerase with a potential role in meiosis J. Mol. Biol. 301 2000 851 867
43. Gillin F.D., and Nossal N.G. Control of mutation frequency by bacteriophage T4 DNA polymerase: II. Accuracy of nucleotide selection by the L88 mutator, CB120 antimutator, and wild type phage T4 DNA polymerases J. Biol. Chem. 251 1976 5225 5232
44. Goodman M.F., and Tippin B. Sloppier copier DNA polymerases involved in genome repair Curr. Opin. Genet. Dev. 10 2000 162 168
45. Gotte M., Li X., and Wainberg M.A. HIV-1 reverse transcription: A brief overview focused on structure-function relationships among molecules involved in initiation of the reaction Arch. Biochem. Biophys. 365 1999 199 210
46. Greider C.W., and Blackburn E.H. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts Cell 43 1985 405 413
47. Greider C.W., and Blackburn E.H. A telomeric sequence in the RNA of Tetrahymena telomerase required for telomere repeat synthesis Nature 337 1989 331 337
48. Guajardo R., and Sousa R. A model for the mechanism of polymerase translocation J. Mol. Biol. 265 1997 8 19
49. Hashimoto H., Nishioka M., Fujiwara S., Takagi M., Imanaka T., Inoue T., and Kai Y. Crystal structure of DNA polymerase from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1 J. Mol. Biol. 306 2001 469 477
50. Hogg M., Wallace S.S., and Doublie S. Crystallographic snapshots of a replicative DNA polymerase encountering an abasic site EMBO J. 23 2004 1483 1493
51. Hopfner K.P., Eichinger A., Engh R.A., Laue F., Ankenbauer W., Huber R., and Angerer B. Crystal structure of a thermostable type B DNA polymerase from Thermococcus gorgonarius Proc. Natl. Acad. Sci. USA 96 1999 3600 3605
52. Hsieh J.C., Zinnen S., and Modrich P. Kinetic mechanism of the DNA-dependent DNA polymerase activity of human immunodeficiency virus reverse transcriptase J. Biol. Chem. 268 1993 24607 24613
53. Hsiou Y., Ding J., Das K., Clark A.D. Jr., Hughes S.H., and Arnold E. Structure of unliganded HIV-1 reverse transcriptase at 2.7 Å resolution: Implications of conformational changes for polymerization and inhibition mechanisms Structure 4 1996 853 860
54. Huang H., Chopra R., Verdine G.L., and Harrison S.C. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: Implications for drug resistance Science 282 1998 1669 1675
55. Ito J., and Braithwaite D.K. Compilation and alignment of DNA polymerase sequences Nucl. Acids Res. 19 1991 4045 4057
56. Jacobo-Molina A., Ding J., Nanni R.G., Clark A.D. Jr., Lu X., Tantillo C., Williams R.L., Kamer G., Ferris A.L., Clark P., Hizi A., Hughes S.H., and Arnold E. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA Proc. Natl. Acad. Sci. USA 90 1993 6320 6324
57. Jaeger J., Restle T., and Steitz T.A. The structure of HIV-1 reverse transcriptase complexed with an RNA pseudoknot inhibitor EMBO J. 17 1998 4535 4542
58. Jezewska M.J., Galletto R., and Bujalowski W. Dynamics of gapped DNA recognition by human polymerase β J. Biol. Chem. 277 2002 20316 20327
59. Jezewska M.J., Rajendran S., and Bujalowski W. Energetics and specificity of Rat DNA polymerase β interactions with template-primer and gapped DNA substrates J. Biol. Chem. 276 2001 16123 16136
60. Jezewska M.J., Rajendran S., and Bujalowski W. Interactions of the 8-kDa domain of rat DNA polymerase β with DNA Biochemistry 40 2001 3295 3307
61. Johnson R.E., Washington M.T., Prakash S., and Prakash L. Bridging the gap: A family of novel DNA polymerases that replicate faulty DNA Proc. Natl. Acad. Sci. USA 96 1999 12224 12226
62. Joyce C.M., and Steitz T.A. Function and structure relationships in DNA polymerases Annu. Rev. Biochem. 63 1994 777 822
63. Kati W.M., Johnson K.A., Jerva L.F., and Anderson K.S. Mechanism and fidelity of HIV reverse transcriptase J. Biol. Chem. 267 1992 25988 25997
64. Kelman Z., and O'Donnell M. DNA polymerase III holoenzyme: Structure and function of a chromosomal replicating machine Ann. Rev. Biochem. 64 1995 171 200
65. Kensch O., Restle T., Wöhrl B.M., Goody R.S., and Steinhoff H.J. Temperature-dependent equilibrium between the open and closed conformation of the p66 subunit of HIV-1 reverse transcriptase revealed by site-directed spin labelling J. Mol. Biol. 301 2000 1029 1039
66. Kiefer J.R., Mao C., Braman J.C., and Beese L.S. Visualizing DNA replication in a catalytically active Bacillus DNA polymerase crystal Nature 391 1998 304 307
67. Kim S.J., Beard W.A., Harvey J., Shock D.D., Knutson J.R., and Wilson S.H. Rapid segmental and subdomain motions of DNA polymerase β J. Biol. Chem. 278 2003 5072 5081
68. Kim Y., Eom S.H., Wang J., Lee D.S., Suh S.W., and Steitz T.A. Crystal structure of Thermus aquaticus DNA polymerase Nature 376 1995 612 616
69. Klenow H., and Overgaard-Hansen K. Proteolytic cleavage of DNA polymerase from Escherichia coli B into an exonuclease unit and a polymerase unit FEBS Lett. 6 1970 25 27
70. Kohlstaedt L.A., Wang J., Friedman J.M., Rice P.A., and Steitz T.A. Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor Science 256 1992 1783 1790
71. Kornberg A. "DNA Replication." 1980 W. H. Freeman San Francisco
72. Kornberg A., and Baker T.A. "DNA Replication." 1992 W. H. Freeman New York
73. Kornberg A., Lehman I.R., Bessman M.J., and Simms E.S. Enzymic synthesis of deoxyribonucleic acid Biochim. Biophys. Acta 21 1956 197 198
74. Korolev S., Nayal M., Barnes W.M., Di Cera E., and Waksman G. Crystal structure of the large fragment of Thermus aquaticus DNA polymerase I at 2.5 A resolution: Structural basis for thermostability Proc. Natl. Acad. Sci. USA 92 1995 9264 9268
75. Krahn J.M., Beard W.A., Miller H., Grollman A.P., and Wilson S.H. Structure of DNA polymerase β with the mutagenic DNA lesion 8-oxodeoxyguanine reveals structural insights into its coding potential Structure 11 2003 121 127
76. Kraynov V.S., Werneburg B.G., Zhong X., Lee H., Ahn J., and Tsai M.D. DNA polymerase β: Analysis of the contributions of tyrosine-271 and asparagine-279 to substrate specificity and fidelity of DNA replication by pre-steady-state kinetics Biochem. J. 323 1997 103 111
77. Kuchta R.D., Benkovic P., and Benkovic S.J. Kinetic mechanism whereby DNA polymerase I (Klenow) replicates DNA with high fidelity Biochemistry 27 1988 6716 6725
78. Kuchta R.D., Mizrahi V., Benkovic P.A., Johnson K.A., and Benkovic S.J. Kinetic mechanism of DNA polymerase I (Klenow) Biochemistry 26 1987 8410 8417
79. Kumar A., Abbotts J., Karawya E.M., and Wilson S.H. Identification and properties of the catalytic domain of mammalian DNA polymerase β Biochemistry 29 1990 7156 7159
80. Lehman I.R., Zimmerman S.B., Adler J., Bessman M.J., Simms E.S., and Kornberg A. Enzymatic synthesis of deoxyribonucleic acid: V. Chemical composition of enzymatically synthesized deoxyribonucleic acid Proc. Natl. Acad. Sci. USA 44 1958 1191 1196
81. Li Y., Dutta S., Doublie S., Bdour H.M., Taylor J.S., and Ellenberger T. Nucleotide insertion opposite a cis-syn thymine dimer by a replicative DNA polymerase from bacteriophage T7 Nat. Struct. Mol. Biol. 11 2004 784 790
82. Li Y., Kong Y., Korolev S., and Waksman G. Crystal structures of the Klenow fragment of Thermus aquaticus DNA polymerase I complexed with deoxyribonucleoside triphosphates Protein Sci. 7 1998 1116 1123
83. Li Y., Korolev S., and Waksman G. 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 1998 7514 7525
84. Li Y., and Waksman G. Crystal structures of a ddATP-, ddTTP-, ddCTP-, and ddGTP-trapped ternary complex of Klentaq1: Insights into the nucleotide incorporation and selectivity Protein Sci. 10 2001 1225 1233
85. Li Y., and Waksman G. Structural studies of the Klentaq1 DNA polymerase Curr. Organic Chem. 5 2001 871 883
86. Lin T.C., Karam G., and Konigsberg W.H. Isolation, characterization, and kinetic properties of truncated forms of T4 DNA polymerase that exhibit 3′-5′ exonuclease activity J. Biol. Chem. 269 1994 19286 19294
87. Ling H., Boudsocq F., Plosky B.S., Woodgate R., and Yang W. Replication of a cis-syn thymine dimer at atomic resolution Nature 424 2003 1083 1087
88. Ling H., Boudsocq F., Woodgate R., and Yang W. Crystal structure of a Y-Family DNA polymerase in action: A mechanism for error-prone and lesion-bypass replication Cell 107 2001 91 102
89. Ling H., Sayer J.M., Plosky B.S., Yagi H., Boudsocq F., Woodgate R., Jerina D.M., and Yang W. Crystal structure of a benzo[a]pyrene diol epoxide adduct in a ternary complex with a DNA polymerase Proc. Natl. Acad. Sci. USA 101 2004 2265 2269
90. Loeb L.A., and Kunkel T.A. Fidelity of DNA synthesis Ann. Rev. Biochem. 52 1982 429 447
91. Lu H., Macosko J., Habel-Rodriguez D., Keller R.W., Brozik J.A., and Keller D.J. Closing of the fingers domain generates motor forces in the HIV reverse transcriptase J. Biol. Chem. 279 2004 54529 54532
92. Madrid M., Jacobo-Molina A., Ding J., and Arnold E. Major subdomain rearrangement in HIV-1 reverse transcriptase simulated by molecular dynamics Proteins 35 1999 332 337
93. Maier D., Bensimon D., and Croquette V. Replication by a single DNA polymerase of a stretched single-stranded DNA Proc. Natl. Acad. Sci. USA 97 2000 12002 12007
94. Martins A., Ribeiro G., Marques M.I., and Costa J.V. Genetic identification and nucleotide sequence of the DNA polymerase gene of African swine fever virus Nucleic Acids Res. 22 1994 208 213
95. Matsumoto Y., and Bogenhagen D.F. Repair of a synthetic abasic site involves concerted reactions of DNA synthesis followed by excision and ligation Mol. Cell. Biol. 11 1991 4441 4447
96. Matsumoto Y., and Kim K. Excision of deoxyribose phosphate residues by DNA polymerase β during DNA repair Science 269 1995 699 702
97. Nair D.T., Johnson R.E., Prakash S., Prakash L., and Aggarwal A.K. Replication by human DNA polymerase-ι occurs by Hoogsteen base-pairing Nature 430 2004 377 380
98. Ollis D.L., Brick P., Hamlin R., Xuong N.G., and Steitz T.A. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP Nature 313 1985 762 766
99. Pata J.D., Stirtan W.G., Goldstein S.W., and Steitz T.A. Structure of HIV-1 reverse transcriptase bound to an inhibitor active against mutant reverse transcriptases resistant to other nonnucleoside inhibitors Proc. Natl. Acad. Sci. USA 101 2004 10548 10553
100. Patel S.S., Wong I., and Johnson K.A. Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant Biochemistry 30 1991 511 525
101. Pavlov A.R., and Karam J.D. Binding specificity of T4 DNA polymerase to RNA J. Biol. Chem. 269 1994 12968 12972
102. Pelletier H., Sawaya M.R., Kumar A., Wilson S.H., and Kraut J. Structures of ternary complexes of rat DNA polymerase β, a DNA template-primer, and ddCTP Science 264 1994 1891 1903
103. Pelletier H., Sawaya M.R., Wolfle W., Wilson S.H., and Kraut J. Crystal structures of human DNA polymerase β complexed with DNA: Implications for catalytic mechanism, processivity, and fidelity Biochemistry 35 1996 12742 12761
104. Petruska J., Sowers L.C., and Goodman M.F. Comparison of nucleotide interactions in water, proteins, and vacuum: Model for DNA polymerase fidelity Proc. Natl. Acad. Sci. USA 83 1986 1559 1562
105. Prasad R., Widen S., Singhal R., Watkins J., Prakash L., and Wilson S. Yeast open reading frame YCR14C encodes a DNA β-polymerase-like enzyme Nucl. Acids Res. 21 1993 5301 5307
106. Purohit V., Grindley N.D., and Joyce C.M. Use of 2-aminopurine fluorescence to examine conformational changes during nucleotide incorporation by DNA polymerase I (Klenow fragment) Biochemistry 42 2003 10200 10211
107. Rajendran S., Jezewska M.J., and Bujalowski W. Human DNA polymerase β recognizes single-stranded DNA using two different binding modes J. Biol. Chem. 273 1998 31021 31031
108. Rajendran S., Jezewska M.J., and Bujalowski W. Recognition of template-primer and gapped DNA substrates by the human DNA polymerase β J. Mol. Biol. 308 2001 477 500
109. Ren J., Bird L.E., Chamberlain P.P., Stewart-Jones G.B., Stuart D.I., and Stammers D.K. Structure of HIV-2 reverse transcriptase at 2.35-Å resolution and the mechanism of resistance to non-nucleoside inhibitors Proc. Natl. Acad. Sci. USA 99 2002 14410 14415
110. Ren J., Esnouf R., Garman E., Somers D., Ross C., Kirby I., Keeling J., Darby G., Jones Y., and Stuart D. High resolution structures of HIV-1 RT from four RT-inhibitor complexes Nat. Struct. Biol. 2 1995 293 302
111. Ren J., Esnouf R.M., Hopkins A.L., Warren J., Balzarini J., Stuart D.I., and Stammers D.K. Crystal structures of HIV-1 reverse transcriptase in complex with carboxanilide derivatives Biochemistry 37 1998 14394 14403
112. Ren J., Nichols C.E., Chamberlain P.P., Weaver K.L., Short S.A., and Stammers D.K. Crystal structures of HIV-1 reverse transcriptases mutated at codons 100, 106 and 108 and mechanisms of resistance to non-nucleoside inhibitors J. Mol. Biol. 336 2004 569 578
113. Rittinger K., Divita G., and Goody R.S. Human immunodeficiency virus reverse transcriptase substrate-induced conformational changes and the mechanism of inhibition by nonnucleoside inhibitors Proc. Natl. Acad. Sci. USA 92 1995 8046 8049
114. Rodgers D.W., Gamblin S.J., Harris B.A., Ray S., Culp J.S., Hellmig B., Woolf D.J., Debouck C., and Harrison S.C. The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1 Proc. Natl. Acad. Sci. USA 92 1995 1222 1226
115. Rodriguez A.C., Park H.W., Mao C., and Beese L.S. Crystal structure of a pol α Family DNA polymerase from the hyperthermophilic archaeon Thermococcus sp. 9 degrees N-7 J. Mol. Biol. 299 2000 447 462
116. Roth M.J., Tanese N., and Goff S.P. Purification and characterization of murine retroviral reverse transcriptase expressed in Escherichia coli J. Biol. Chem. 260 1985 9326 9335
117. Rothwell P.J., Berger S., Kensch O., Felekyan S., Antonik M., Wohrl B.M., Restle T., Goody R.S., and Seidel C.A. Multiparameter single-molecule fluorescence spectroscopy reveals heterogeneity of HIV-1 reverse transcriptase:primer/template complexes Proc. Natl. Acad. Sci. USA 100 2003 1655 1660
118. Sarafianos S.G., Clark A.D. Jr., Das K., Tuske S., Birktoft J.J., Ilankumaran P., Ramesha A.R., Sayer J.M., Jerina D.M., Boyer P.L., Hughes S.H., and Arnold E. Structures of HIV-1 reverse transcriptase with pre- and post-translocation AZTMP-terminated DNA EMBO J. 21 2002 6614 6624
119. Sarafianos S.G., Das K., Tantillo C., Clark A.D. Jr., Ding J., Whitcomb J.M., Boyer P.L., Hughes S.H., and Arnold E. Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA EMBO J. 20 2001 1449 1461
120. Sawaya M.R., Pelletier H., Kumar A., Wilson S.H., and Kraut J. Crystal structure of rat DNA polymerase β: Evidence for a common polymerase mechanism Science 264 1994 1930 1935
121. Sawaya M.R., Prasad R., Wilson S.H., Kraut J., and Pelletier H. Crystal structures of human DNA polymerase β complexed with gapped and nicked DNA: Evidence for an induced fit mechanism Biochemistry 36 1997 11205 11215
122. Shah A.M., Maitra M., and Sweasy J.B. Variants of DNA polymerase β extend mispaired DNA due to increased affinity for nucleotide substrate Biochemistry 42 2003 10709 10717
123. Silvian L.F., Toth E.A., Pham P., Goodman M.F., and Ellenberger T. Crystal structure of a DinB Family error-prone DNA polymerase from Sulfolobus solfataricus Nat. Struct. Biol. 8 2001 984 989
124. Sloane D.L., Goodman M.F., and Echols H. The fidelity of base selection by the polymerase subunit of DNA polymerase III holoenzyme Nucleic Acids Res. 16 1988 6465 6475
125. Sluis-Cremer N., Arion D., and Parniak M.A. Molecular mechanisms of HIV-1 resistance to nucleoside reverse transcriptase inhibitors (NRTIs) Cell Mol. Life Sci. 57 2000 1408 1422
126. Smerdon S.J., Jager J., Wang J., Kohlstaedt L.A., Chirino A.J., Friedman J.M., Rice P.A., and Steitz T.A. Structure of the binding site for nonnucleoside inhibitors of the reverse transcriptase of human immunodeficiency virus type 1 Proc. Natl. Acad. Sci. USA 91 1994 3911 3915
127. Steitz T.A. DNA- and RNA-dependent DNA polymerases Curr. Opin. Struct. Biol. 3 1993 31 38
128. Steitz T.A. A unified polymerase mechanism for nonhomologous DNA and RNA polymerases Science 266 1994 2022 2026
129. Steitz T.A. A mechanism for all polymerases Nature 391 1998 231 232
130. Suzuki M., Baskin D., Hood L., and Loeb L.A. Random mutagenesis of Thermus aquaticus DNA polymerase I: Concordance of immutable sites in vivo with the crystal structure Proc. Natl. Acad. Sci. USA 93 1996 9670 9675
131. Tabor S., Huber H.E., and Richardson C.C. Escherichia coli thioredoxin confers processivity on the DNA polymerase activity of the gene 5 protein of bacteriophage T7 J. Biol. Chem. 262 1987 16212 16223
132. Topal M.D., Di Guiseppi S.R., and Sinha N.K. Molecular basis for substitution mutations: Effect of primer terminal and template residues on nucleotide selection by phage T4 DNA polymerase in vitro J. Biol. Chem. 255 1980 11717 11724
133. Trincao J., Johnson R.E., Escalante C.R., Prakash S., Prakash L., and Aggarwal A.K. Structure of the catalytic core of S. cerevisiae DNA polymerase η: Implications for translesion DNA synthesis Mol. Cell 8 2001 417 426
134. Tuerk C., Eddy S., Parma D., and Gold L. Autogenous translational operator recognized by bacteriophage T4 DNA polymerase J. Mol. Biol. 213 1990 749 761
135. Uemori T., Sato Y., Doi H., and Ishino Y. A novel DNA polymerase in the hyperthermophilic acrhaeon, Pyrococcus furiosus: Gene cloning, expression and characterization Genes to Cell 2 1997 499 512
136. Uljon S.N., Johnson R.E., Edwards T.A., Prakash S., Prakash L., and Aggarwal A.K. Crystal structure of the catalytic core of human DNA polymerase κ Structure 12 2004 1395 1404
137. Vande Berg B.J., Beard W.A., and Wilson S.H. DNA structure and aspartate 276 influence nucleotide binding to human DNA polymerase β. Implication for the identity of the rate-limiting conformational change J. Biol. Chem. 276 2001 3408 3416
138. Wang C.C., Pavlov A., and Karam J.D. Evolution of RNA-binding specificity in T4 DNA polymerase J. Biol. Chem. 272 1997 17703 17710
139. Wang J., Sattar A.K., Wang C.C., Karam J.D., Konigsberg W.H., and Steitz T.A. Crystal structure of a pol α Family replication DNA polymerase from bacteriophage RB69 Cell 89 1997 1087 1099
140. Washington M.T., Prakash L., and Prakash S. Yeast DNA polymerase η utilizes an induced-fit mechanism of nucleotide incorporation Cell 107 2001 917 927
141. Watson J.D., and Crick F.H. Genetical implications of the structure of deoxyribonucleic acid Nature 171 1953 964 967
142. Watson J.D., and Crick F.H. Molecular structure of nucleic acids: A structure for deoxyribose nucleic acid Nature 171 1953 737 738
143. Werneburg B.G., Ahn J., Zhong X., Hondal R.J., Kraynov V.S., and Tsai M.D. DNA polymerase β: Pre-steady-state kinetic analysis and roles of arginine-283 in catalysis and fidelity Biochemistry 35 1996 7041 7050
144. Wöhrl B.M., Krebs R., Goody R.S., and Restle T. Refined model for primer/template binding by HIV-1 reverse transcriptase: Pre-steady-state kinetic analyses of primer/template binding and nucleotide incorporation events distinguish between different binding modes depending on the nature of the nucleic acid substrate J. Mol. Biol. 292 1999 333 344
145. Wong I., Patel S.S., and Johnson K.A. An induced-fit kinetic mechanism for DNA replication fidelity: Direct measurement by single-turnover kinetics Biochemistry 30 1991 526 537
146. Woodgate R. A plethora of lesion-replicating DNA polymerases Genes Dev. 13 1999 2191 2195
147. Wuite G.J.L., Smith S.B., Young M., Keller D., and Bustamante C. Single-molecule studies of the effect of template tension on T7 DNA polymerase activity Nature 404 2000 103 106
148. Yang G., Franklin M., Li J., Lin T.C., and Konigsberg W. Correlation of the kinetics of finger domain mutants in RB69 DNA polymerase with its structure Biochemistry 41 2002 2526 2534
149. Yang L., Arora K., Beard W.A., Wilson S.H., and Schlick T. Critical role of magnesium ions in DNA polymerase β's closing and active site assembly J. Am. Chem. Soc. 126 2004 8441 8453
150. Yang L., Beard W.A., Wilson S.H., Broyde S., and Schlick T. Polymerase β simulations suggest that Arg258 rotation is a slow step rather than large subdomain motions per se J. Mol. Biol. 317 2002 651 671
151. Yang W. Damage repair DNA polymerases Y Curr. Opin. Struct. Biol. 13 2003 23 30
152. Zhao Y., Jeruzalmi D., Moarefi I., Leighton L., Lasken R., and Kuriyan J. Crystal structure of an archaebacterial DNA polymerase Structure Fold Des. 7 1999 1189 1199
153. Zhong X., Patel S.S., Werneburg B.G., and Tsai M.D. DNA polymerase β: Multiple conformational changes in the mechanism of catalysis Biochemistry 36 1997 11891 11900
154. Zhou B.L., Pata J.D., and Steitz T.A. Crystal structure of a DinB lesion bypass DNA polymerase catalytic fragment reveals a classic polymerase catalytic domain Mol. Cell 8 2001 427 437