Molecular basis of fidelity of DNA synthesis and nucleotide specificity of retroviral reverse transcriptases

Progress in Nucleic Acid Research and Molecular Biology

Volumn 71, Issue , 2002, Pages 91-147

  Menéndez Arias, Luis ^a  

^a CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

RNA DIRECTED DNA POLYMERASE; VIRUS DNA;

AMINO ACID SEQUENCE; BIOSYNTHESIS; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; GENETIC RECOMBINATION; GENETICS; HUMAN IMMUNODEFICIENCY VIRUS 1; METABOLISM; MOLECULAR GENETICS; MUTATION; RETROVIRUS; REVIEW; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; DNA, VIRAL; HIV-1; HIV-1 REVERSE TRANSCRIPTASE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; RECOMBINATION, GENETIC; RETROVIRIDAE; RNA-DIRECTED DNA POLYMERASE; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY;

EID: 0036369217     PISSN: 00796603     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0079-6603(02)71042-8     Document Type: Review

References (263)

1. H.M Temin The control of cellular morphology in embryonic cells infected with Rous sarcoma virus in vitro Virology 10 1960 182 197
2. E Domingo C.K Biebricher M Eigen J.J Holland Quasispecies and RNA Virus Evolution: Principles and Consequences 2001 Landes Bioscience Georgetown, TX
3. B.H Hahn G.M Shaw M.E Taylor R.R Redfield P.D Markham S.Z Salahuddin F Wong-Staal R.C Gallo E.S Parks W.P Parks Genetic variation in HTLV III/LAV over time in patients with AIDS or at risk for AIDS Science 232 1986 1548 1553
4. D.P.W Burns R.C Desrosiers Selection of genetic variants of simian immunodeficiency virus in persistently infected rhesus monkeys J. Virol. 65 1991 1843 1854
5. P.R Johnson T.E Hamm S Goldstein S Kitov V.M Hirsch The genetic fate of molecularly cloned simian immunodeficiency virus in experimentally infected macaques Virology 185 1991 217 228
6. J Overbaugh L.M Rudensey M.D Papenhausen R.E Benveniste W.R Morton Variation in simian immunodeficiency virus env is confined to V1 and V4 during progression to simian AIDS J. Viral. 65 1991 7025 7031
7. B.D Preston J.P Dougherty Mechanisms of retroviral mutation Trends in Microbiol. 4 1996 16 21
8. J.M Leider P Palese F.I Smith Determination of the mutation rate of a retrovirus J. Virol. 62 1988 3084 3091
9. V.K Pathak H.M Temin Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: Deletions and deletions with insertions 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 87 1990 6024 6028
10. J.W Drake A constant rate of spontaneous mutation in DNA-based microbes 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 88 1991 7160 7164
11. T.A Kunkel P.S Alexander The base substitution fidelity of eucaryotic DNA polymerases J. Biol. Chem. 261 1986 160 166
12. T Matsuda K Bebenek C Masutani F Hanaoka T.A Kunkel Low fidelity DNA synthesis by human DNA polymerase-η Nature 404 2000 1011 1013
13. B.D Preston B.J Poiesz L.A Loeb Fidelity of HIV-1 reverse transcriptase Science 242 1988 1168 1171
14. J.D Roberts K Bebenek T.A Kunkel The accuracy of reverse transcriptase from HIV-1 Science 242 1988 1171 1173
15. J.D Roberts B.D Preston L.A Johnston A Soni L.A Loeb T.A Kunkel Fidelity of two retroviral reverse transcriptases during DNA-dependent DNA synthesis in vitro Mol. Cell. Biol. 9 1989 469 476
16. J Weber F Grosse Fidelity of human immunodeficiency virus type 1 reverse transcriptase in copying natural DNA Nucleic Acids Res. 17 1989 1379 1393
17. M Ricchetti H Buc Reverse transcriptases and genomic variability: the accuracy of DNA replication is enzyme specific and sequence dependent EMBO J. 9 1990 1583 1593
18. A Manns H König M Baier R Kurth F Grosse Fidelity of reverse transcriptase of the simian immunodeficiency virus from African green monkey Nucleic Acids Res. 19 1991 533 537
19. L de Mercoryol Y Corda C Job D Job Accuracy of wheat-germ RNA polymerase II: General enzymatic properties and effect of template conformational transition from right-handed B -DNA to left-handed Z-DNA Eur. J. Biochem. 206 1992 49 58
20. C.J Jeon K Agarwal Fidelity of RNA polymerase II transcription controlled by elongation factor TFIIS 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 93 1996 13,677 13,682
21. D.A Erie O Hajiseyedjavadi M.C Young P.H von Hippel Multiple RNA polymerase conformations and GreA: Control of the fidelity of transcription Science 262 1993 867 873
22. M.J Thomas A.A Platas D.K Hawley Transcriptional fidelity and proofreading by RNA polymerase II Cell 93 1998 627 637
23. J.G Levin D.L Hatfield S Oroszlan A Rein Mechanisms of translational suppression used in biosynthesis of reverse transcriptase A.M Skalka S.P Goff Reverse Transcriptase 1993 Cold Spring Harbor Laboratory Press Plainview, New York 5 31
24. S.P Goff Retroviral reverse transcriptase: Synthesis, structure and function J. Acquir Immune Def. Syndr. 3 1990 817 831
25. A Telesnitsky S.P Goff Reverse transcription and the generation of retroviral DNA J Coffin S.H Hughes H Varmus Retroviruses 1997 Cold Spring Harbor Laboratory Press Plainview, New York 121 160
26. F Di Marzo Veronese T.D Copeland A.L DeVico R Rahman S Oroszlan R.C Gallo M.G Sarngadharan Characterization of highly immunogenic p66/p51 as the reverse transcriptase of HTLV-III/LAV Science 231 1986 1289 1291
27. M.M Lightfoote J.E Coligan T.M Folks A.S Fauci M.A Martin S Venkatesan Structural characterization of reverse transcriptase and endonuclease polypeptides of the acquired immunodeficiency syndrome retrovirus J. Virol. 60 1986 771 775
28. S.F.J Le Grice T Naas B Wohlgensinger O Schatz Subunit-selective mutagenesis indicates minimal polymerase activity in heterodimer-associated p51 HIV-I reverse transcriptase EMBO J. 10 1991 3905 3911
29. Z Hostomsky Z Hostomska T.-B Fu J Taylor Reverse transcriptase of human immunodeficiency virus type 1: Functionality of subunits of the heterodimer in DNA synthesis J. Virol. 66 1992 3179 3182
30. D.W Rodgers S.J Gamblin B.A Harris S Ray J.S Culp B Hellmig D.J Woolf C Debouck S.C Harrison The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 92 1995 1222 1226
31. L.A Kohlstaedt J Wang J.M Friedman P.A Rice T.A Steitz Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor Science 256 1992 1783 1790
32. A Jacobo-Molina J Ding R.G Nanni A.D Clark Jr. X Lu C Tantillo R.L Williams G Kamer A.L Ferris P Clark A Hizi S.H Hughes E Arnold Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 90 1993 6320 6324
33. J Ding K Das Y Hsiou S.G Sarafianos A.D Clark Jr. A Jacobo-Mohna C Tantillo S.H Hughes E Arnold 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
34. S.G Sarafianos K Das C Tantillo A.D Clark Jr. J Ding J.M Whitcomb P.L Boyer S.H Hughes E Arnold Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA EMBO J. 20 2001 1449 1461
35. H Huang R Chopra G.L Verdine S.C Harrison Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: Implications for drug resistance Science 282 1998 1669 1675
36. E.J Arts S.F.J Le Grice Interaction of retroviral reverse transcriptase with template-primer duplexes during replication Progr Nucleic Acid Res. Mol. Biol. 58 1998 339 393
37. M Götte X Li M.A Wainberg HIV-1 reverse transcription: A brief overview focused on structure-function relationship between molecules involved in initiation of the reaction Archs. Biochem. Biophys. 365 1999 199 210
38. H Yu A.E Jetzt J.P Dougherty Use of single-cycle analysis to study rates and mechanisms of retroviral mutation Methods: A Comp. Methods Enzymol. 12 1997 325 336
39. J.P Dougherty H.M Temin High mutation rate of a spleen necrosis virus-based retrovvrls vector Molec. Cell. Biol. 6 1986 4387 4395
40. L.M Mansky H.M Temin Lower mutation rate of bovine leukemia virus relative to that of spleen necrosis virus J. Virol. 68 1994 494 499
41. L.M Mansky H.M Temin Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase J. Virol. 69 1995 5087 5094
42. S Parthasarathi A Varela-Echevarría Y Ron B.D Preston J.P Dougherty Genetic rearrangements occurring during a single cycle of murine leukemia virus vector replication: characterization and implications J. Virol. 69 1995 7991 8000
43. L Mansky Forward mutation rate of human immunodeficiency virus type 1 in a T lymphoid cell line AIDS Res. Human Retrovir. 12 1996 307 314
44. A Varela-Echavarría N Garvey B.D Preston J.P Dougherty Comparison of Moloney murine leukemia virus mutation rate with the fidelity of its reverse transcriptase in vitro J. Biol. Chem. 267 1992 24,681 24,688
45. A Varela-Echavarría C.M Prorock Y Ron J.P Dougherty High rate of genetic rearrangement during replication of a Moloney murine leukemia virus-based vector J. Virol. 67 1993 6357 6364
46. L.M Mansky In vivo analysis of human T-cell leukemia virus type 1 reverse transcription accuracy J. Virol. 74 2000 9525 9531
47. R.J Monk F.G Malik D Stokesberry L.H Evans Direct determination of the point mutation rate of a murine retrovirus J. Virol. 66 1992 3683 3689
48. A Gabriel M Willems E.H Mules J.D Boeke Replication infidelity during a single cycle of Tyl retrotransposition 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 93 1996 7767 7771
49. Y Takeuchi T Nagumo H Hoshino Low fidelity of cell-free DNA synthesis by reverse transcriptase of human immunodeficiency virus J. Virol. 62 1988 3900 3902
50. M.S Boosalis J Petruska M.F Goodman DNA polymerase insertion fidelity-Gel assay for site-specific kinetics J. Biol. Chem. 262 1987 14,689 14,696
51. M.F Goodman S Creighton L.B Bloom J Petruska Biochemical basis of DNA replication fidelity Crit. Rev. Biochem. Mol. Biol. 28 1993 83 126
52. A.M Martín-Hernández E Domingo L Menendez-Arias Human immunodeficiency virus type 1 reverse transcriptase: role of Tyr115 in deoxynucleotide binding and misinsertion fidelity of DNA synthesis EMBO J. 15 1996 4434 4442
53. L Menéndez-Arias Studies on the effects of truncating α-helix E' of p66 human immunodeficiency virus type 1 reverse transcriptase on template-primer binding and fidelity of DNA synthesis Biochemistry 37 1998 16,636 16,644
54. L.V Mendelman M.S Boosalis J Petruska M.F Goodman Nearest neighbor influences on DNA polymerase insertion fidelity J. Biol. Chem. 264 1989 14,415 14,423
55. M Bakhanashvili A Hizi Fidelity of the reverse transcriptase of human immunodeficiency virus type 2 FEBS Lett. 306 1992 151 156
56. H Yu M.F Goodman Comparison of HIV-1 and avian myeloblastosis virus reverse transcriptase fidelity on RNA and DNA templates J. Biol. Chem. 267 1992 10,888 10,896
57. M Bakhanashvili A Hizi Fidelity of DNA synthesis exhibited in vitro by the reverse transcriptase of the lentivirus equine infectious anemia virus Biochemistry 32 1993 7559 7567
58. R Taube O Avidan M Bakhanashvili A Hizi DNA synthesis exhibited by the reverse transcriptase of mouse mammary tumor virus: Processivity and fidelity of misinsertion and mispair extension Eur. J. Biochem. 258 1998 1032 1039
59. tG:T mispair formation on RNA and DNA templates with mismatched primers: a kinetic and thermodynamic study EMBO J. 14 1995 4622 4627
60. C.M Malboeuf S.J Isaacs N.H Tran B Kim Thermal effects on reverse transcription: Improvement of accuracy and processivity in cDNA synthesis BioTechniques 30 2001 1074 1084
61. S Moran R.X.-F Ren E.T Kool A thymidine triphosphate shape analog lacking Watson-Crick pairing ability is replicated with high sequence selectivity 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 94 1997 10,506 10,511
62. J.C Morales E.T Kool Efficient replication between non-hydrogen bonded nucleoside shape analogs Nature Struct. Biol. 5 1998 950 954
63. H Echols M.F Goodman Fidelity mechanisms in DNA replication Annu. Rev. Biochem. 60 1991 477 511
64. M.F Goodman Hydrogen bonding revisited: Geometric selection as a principal determinant of DNA replication fidelity 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 94 1997 10,493 10,495
65. M Boutabout M Wilhelm F.-X Wilhelm DNA synthesis fidelity by the reverse transcriptase of the yeast retrotransposon Tyl Nucleic Acids Res. 29 2001 2217 2222
66. F.W Perrino B.D Preston L.L Sandell L.A Loeb Extension of mismatched 3′ termini of DNA is a major determinant of the infidelity of human immunodeficiency virus type 1 reverse transcriptase 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 86 1989 8343 8347
67. G.A Pulsinelli H.M Temin High rate of mismatch extension during reverse transcription in a single round of retrovirus replication 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 91 1994 9490 9494
68. S Creighton M.-H Huang H Cai N Arnheim M.F Goodman Base mispair extension kinetics—Binding of avian myeloblastosis reverse transcriptase to matched and mismatched base pair termini J. Biol. Chem. 267 1992 2633 2639
69. S Zinnen J.-C Hsieh P Modrich Misincorporation and mispaired primer extension by human immunodeficiency virus reverse transcriptase J. Biol. Chem. 269 1994 24,195 24,202
70. L.V Mendelman J Petruska M.F Goodman Base mispair extension kinetics-Comparison of DNA polymerase α and reverse transcriptase J. Biol. Chem. 265 1990 2338 2346
71. M Bakhanashvili A Hizi Fidelity of the RNA-dependent DNA synthesis exhibited by the reverse transcriptases of human immunodeficiency virus types 1 and 2 and of murine leukemia virus: Mispair extension frequencies Biochemistry 31 1992 9393 9398
72. C.E Cases-González M Gutiérrez-Rivas L Menéndez-Arias Coupling ribose selection to fidelity of DNA synthesis: The role of Tyr-115 of human immunodeficiency virus type 1 reverse transcriptase J. Biol. Chem. 275 2000 19,759 19,767
73. K.A Johnson Conformational coupling in DNA polymerase fidelity Annu. Rev. Biochem. 62 1993 685 713
74. W.M Kati K.A Johnson L.F Jerva K.S Anderson Mechanism and fidelity of HIV reverse transcriptase J. Biol. Chem. 267 1992 25,988 25,997
75. S.G Kerr K.S Anderson RNA dependent DNA replication fidelity of HIV-1 reverse transcriptase: Evidence of discrimination between DNA and RNA substrates Biochemistry 36 1997 14,056 14,063
76. T. A. Kunkel and A. Soni, Mutagenesis by transient misalignment. J. Biol. Chem. 263 , 14,784–14,789.
77. K Bebenek J Abbotts J.D Roberts S.H Wilson T.A Kunkel Specificity and mechanism of error-prone replication by human immunodeficiency virus-1 reverse transcriptase J. Biol. Chem. 264 1989 16,948 16,956
78. J.C Boyer K Bebenek T.A Kunkel Unequal human immunodeficiency virus type 1 reverse transcriptase error rates with RNA and DNA templates 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 89 1992 6919 6923
79. K.A Eckert T.A Kunkel Fidelity of DNA synthesis catalyzed by human DNA polymerase α and HIV-1 reverse transcriptase: Effect of reaction pH Nucleic Acids Res. 21 1993 5212 5220
80. W.C Drosopoulos V.R Prasad Increased misincorporation fidelity observed for nucleoside analog resistance mutations M184V and E89G in human immunodeficiency virus type 1 reverse transcriptase does not correlate with the overall error rate measured in vitro J. Virol. 72 1998 4224 4230
81. L.F Rezende W.C Drosopoulos V.R Prasad The influence of 3TC resistance mutation M184I on the fidelity and error specificity of human immunodeficiency virus type 1 reverse transcriptase Nucleic Acids Res. 26 1998 3066 3072
82. J Ji L.A Loeb Fidelity of HIV-1 reverse transcriptase copying RNA in vitro Biochemistry 31 1992 954 958
83. J Ji L.A Loeb Fidelity of HIV-1 reverse transcriptase copying a hypervariable region of the HIV-1 env gene Virology 199 1994 323 330
84. P.L Boyer S.H Hughes Effects of amino acid substitutions at position 115 on the fidelity of human immunodeficiency virus type 1 reverse transcriptase J. Virol. 74 2000 6494 6500
85. L.F Rezende K Curr T Ueno H Mitsuya V.R Prasad The impact of multidideoxynucleoside resistance-conferring mutations in human immunodeficiency virus type 1 reverse transcriptase on polymerase fidelity and error specificity J. Virol. 72 1998 2890 2895
86. W.A Beard S.J Stahl H.-R Kim K Bebenek A Kumar M.-P Strub S.P Becerra T.A Kunkel S.H Wilson Structure/function studies of human immunodeficiency virus type 1 reverse transcriptas—Alanine scanning mutagenesis of an α-helix in the thumb subdomain J. Biol. Chem. 269 1994 28,091 28,097
87. K Bebenek W.A Beard J.R Casas-Finet H.-R Kim T.A Darden S.H Wilson T.A Kunkel Reduced frameshift fidelity and processivity of HIV-1 reverse transcriptase mutants containing alanine substitutions in helix H of the thumb subdomain J. Biol. Chem. 270 1995 19,516 19,523
88. W.A Beard D.T Minnick C.L Wade R Prasad R.L Won A Kumar T.A Kunkel S.H Wilson Role of the “helix clamp” in HIV-1 reverse transcriptase catalytic cycling as revealed by alanine-scanning mutagenesis J. Biol. Chem. 271 1996 12,213 12,220
89. W.A Beard K Bebenek T.A Darden L Li R Prasad T.A Kunkel S.H Wilson Vertical-scanning mutagenesis of a critical tryptophan in the minor groove binding track of HIV-1 reverse transcriptase—Molecular nature of polymerase-nucleic acid interactions J. Biol. Chem. 273 1998 30,435 30,442
90. B Kim T.R Hathaway L.A Loeb Fidelity of mutant HIV-1 reverse transcriptases: Interaction with the single-stranded template influences the accuracy of DNA synthesis Biochemistry 37 1998 5831 5839
91. B Kim J.C Ayran S.G Sagar E.T Adman S.M Fuller N.H Tran J Horrigan New human immunodeficiency virus type 1 reverse transcriptase (HIV-1 RT) mutants with increased fidelity of DNA synthesis—Accuracy, template binding, and processivity J. Biol. Chem. 274 1999 27,666 27,673
92. K Bebenek T.A Kunkel Analyzing fidelity of DNA polymerases Methods Enzymol. 262 1995 217 232
93. T.A Kunkel K Bebenek DNA replication fidelity Annu. Rev. Biochem. 69 2000 497 529
94. K Bebenek T.A Kunkel Frameshift errors initiated by nucleotide misincorporation 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 87 1990 4946 4950
95. K Bebenek J Abbotts S.H Wilson T.A Kunkel Error-prone polymerization by HIV-1 reverse transcriptase—Contribution of template-primer misalignment, miscoding, and termination probability to mutational hot spots J. Biol. Chem. 268 1993 10,324 10,334
96. J.-P Vartanian A Meyerhans B Asjo S Wain-Hobson Selection, recombination, and G → A hypermutation of human immunodeficiency virus type 1 genomes J. Virol. 65 1991 1779 1788
97. T Kim R.A Mudry Jr. C.A Rexrode II V.K Pathak Retroviral mutation rates and A-to-G hypermutations during different stages of retroviral replication J. Virol. 70 1996 7594 7602
98. K Bourara S Litvak A Araya Generation of G-to-A and C-to-U changes in HIV-1 transcripts by RNA editing Science 289 2000 1564 1566
99. J.-P Vartanian A Meyerhans M Sala S Wain-Hobson G → A hypermutation of the human immunodeficiency virus type 1 genome: Evidence for dCTP pool imbalance during reverse transcription 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 91 1994 3092 3096
100. J.E Fitzgibbon S Mazar D.T Dubin A new type of G → A hypermutation affecting human immunodeficiency virus AIDS Res. Human Retrovir. 9 1993 833 838
101. S Wain-Hobson P Sonigo M Guyader A Gazit M Henry Erratic G → A hypermutation within a complete caprine arthritis-encephalitis virus (CAEV) provirus Virology 209 1995 297 303
102. A Hübner M Kruhoffer F Grosse G Krauss Fidelity of human immunodeficiency virus type I reverse transcriptase in copying natural RNA J. Mol. Biol. 223 1992 595 600
103. M Götte M Kameoka N McLellan L Cellai M.A Wainberg Analysis of efficiency and fidelity of HIV-1 (+)-strand DNA synthesis reveals a novel rate-limiting step during retroviral reverse transcription J. Biol. Chem. 276 2001 6711 6719
104. J.M Lanchy C Ehresmann S.F.J Le Grice B Ehresmann R Marquet Binding and kinetic properties of HIV-1 reverse transcriptase markedly differ during initiation and elongation of reverse transcription EMBO J. 15 1996 7178 7187
105. B.B Oude Essink B Berkhout The fidelity of reverse transcription differs in reactions primed with RNA versus DNA primers J. Biomed. Sci. 6 1999 121 132
106. J.A Peliska S.J Benkovic Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase Science 258 1992 1112 1118
107. P.H Patel B.D Preston Marked infidelity of human immunodeficiency virus type 1 reverse transcriptase at RNA and DNA template ends 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 91 1994 549 553
108. J.A Peliska S.J Benkovic Fidelity of in vitro DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase Biochemistry 33 1994 3890 3895
109. D Kulpa R Topping A Telesnitsky Determination of the site of first strand transfer during Moloney murine leukemia virus reverse transcription and identification of strand transfer-associated reverse transcriptase errors EMBO J. 16 1997 856 865
110. C Palaniappan M Wisniewski W Wu P.J Fay R.A Bambara Misincorporation of HIV-1 reverse transcriptase promotes recombination via strand transfer synthesis J. Biol. Chem. 271 1996 22,331 22,338
111. G.J Klarmann C.A Schauber B.D Preston Template-directed pausing of DNA synthesis by HIV-1 reverse transcriptase during polymerization of HIV-1 sequences in vitro J. Biol. Chem. 268 1993 9793 9802
112. W Wu B.M Blumberg P.J Fay R.A Bambara Strand transfer mediated by human immunodeficiency virus reverse transcriptase in vitro is promoted by pausing and results in misincorporation J. Biol. Chem. 270 1995 325 332
113. L Diaz J.J DeStefano Strand transfer is enhanced by mismatched nucleotides at the 3′ primer terminus: a possible link between HIV reverse transcriptase fidelity and recombination Nucleic Acids Res. 24 1996 3086 3092
114. W Wu C Palaniappan R.A Bambara P.J Fay Differences in mutagenesis during minus strand, plus strand and strand transfer (recombination) synthesis of the HIV-1 nef gene in vitro Nucleic Acids Res. 24 1996 1710 1718
115. J.J DeStefano J Ghosh B Prasad A Raja High fidelity of internal strand transfer catalyzed by human immunodeficiency virus reverse transcriptase J. Biol. Chem. 273 1998 1483 1489
116. J Zhang H.M Temin Retrovirus recombination depends on the length of sequence identity and is not error prone J. Virol. 68 1994 2409 2414
117. J.K Pfeiffer R.S Topping N.-H Shin A Telestnitsky Altering the intracellular environment increases the frequency of tandem repeat deletion during Moloney murine leukemia virus reverse transcription J. Virol. 73 1999 8441 8447
118. J.J DeStefano A Raja J.V Cristofaro In vitro strand transfer from broken RNAs results in mismatch but not frameshift mutations Virology 276 2000 7 15
119. J.-L Darlix M Lapadat-Tapolsky H de Rocquigny B.P Roques First glimpses of structure-function relationships of the nucleocapsid protein of retroviruses J. Mol. Biol. 254 1995 523 537
120. A Rein L.E Henderson J.G Levin Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication Trends Biochem. Sci. 23 1998 297 301
121. J.-B Rascle D Ficheux J.-L Darlix Possible roles of nucleocapsid protein of MoMuLV in the specificity of proviral DNA synthesis and in the genetic variability of the virus J. Mol. Biol. 280 1998 215 225
122. M Dettenhofer S Cen B.A Carlson L Kleiman X.-F Fu Association of human immunodeficiency virus type 1 Vif with RNA and its role in reverse transcription J. Virol. 74 2000 8938 8945
123. D.G Vassylyev K Morikawa Precluding uracil from DNA Structure 4 1996 1381 1385
124. J.H Elder D.L Lerner C.S Hasselkus-Light D.J Fontenot E Hunter P.A Luciw R.C Montelaro T.R Phillips Distinct subsets of retroviruses encode dUTPase J. Virol. 66 1992 1791 1794
125. B Köppe L Menéndez-Arias S Oroszlan Expression and purification of the mouse mammary tumor virus gag-pro transframe protein p30 and characterization of its dUTPase activity J. Virol. 68 1994 2313 2319
126. D.L Lerner P.C Wagaman T.R Phillips O Prospero-García S.J Henriksen H.S Fox F.E Bloom J.H Elder Increased mutation frequency of feline immunodeficiency virus lacking a functional deoxyuridine-triphosphatase 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 92 1995 7480 7484
127. M Bouhamdan S Benichou F Rey J.-M Navarro I Agostini B Spire J Camonis G Slupphaug R Vigne R Benarous J Sire Human immunodeficiency virus type 1 Vpr protein binds to the uracil DNA glycosylase DNA repair enzyme J. Virol. 70 1996 697 704
128. L Selig S Benichou M.E Rogel L.I Wu M.A Wodicka J Sire R Benarous M Emerman Uracil DNA glycosylase specifically interacts with Vpr of both human immunodeficiency virus type 1 and simian immunodeficiency virus of sooty mangabeys, but binding does not correlate with cell cycle arrest J. Virol. 71 1997 4842 4846
129. M Bukrinsky A Adzhubei Viral protein R of HIV 1 Rev. Med. Virol. 9 1999 39 49
130. L.A Stark R.T Hay Human immunodeficiency virus type 1 (HIV-1) viral protein R (Vpr) interacts with Lys-tRNA synthetase: Implications for priming of HIV-1 reverse transcription J. Virol. 72 1998 3037 3044
131. F Bachand X.-J Yao M Hrimech N Rougeau E.A Cohen Incorporation of Vpr into human immunodeficiency virus type 1 requires a direct interaction with the p6 domain of the p55 gag precursor J. Biol. Chem. 274 1999 9083 9091
132. L Selig J.-C Pages V Tanchou S Prévéral C Berlioz-Torrent L.X Liu L Erdtman J.-L Darlix R Benarous S Benichou Interaction with the p6 domain of the Gag precursor mediates incorporation into virions of Vpr and Vpx proteins from primate lentiviruses J. Virol. 73 1999 592 600
133. E.S Withers-Ward J.B.M Jowett S.A Stewart Y.-M Me A Garfinkel Y Shibagald S.A Chow N Shah F Hanaoka D.G Sawitz R.W Armstrong L.M Souza I.S.Y Chen Human immunodeficiency virus type 1 Vpr interacts with HHR23A, a cellular protein implicated in nucleotide excision DNA repair J. Virol. 71 1997 9732 9742
134. T Dieckmann E.S Withers-Ward M.A Jarosinski C.-F Liu I.S.Y Chen J Feigon Structure of a human DNA repair protein UBA domain that interacts with HIV-1 Vpr Nature Struct. Biol. 5 1998 1042 1047
135. L.M Mansky S Preveral E Le Rouzic L.C Bernard L Selig C Depienne R Benarous S Benichou Interaction of human immunodeficiency virus type 1 Vpr with the HHR23A DNA repair protein does not correlate with multiple biological functions of Vpr Virology 282 2001 176 185
136. J.B Jowett Y.-M Me I.S.Y Chen The presence of human immunodeficiency virus type 1 Vpr correlates with a decrease in the frequency of mutations in the plasmid shuttle vector J. Virol. 73 1999 7132 7137
137. L Mansky The mutation rate of human immunodeficiency virus type 1 is influenced by the vpr gene Virology 222 1996 391 400
138. L.M Mansky S Preveral L Selig R Benarous S Benichou The interaction of Vpr with uracil DNA glycosylase modulates the human immunodeficiency virus type 1 in vivo mutation rate J. Virol. 74 2000 7039 7047
139. J Balzarini Suppression of resistance to drugs targeted to human immunodeficiency virus reverse transcriptase by combination therapy Biochem. Pharmacol. 58 1999 1 27
140. H Jonckheere J Anné E De Clercq The HIV-1 reverse transcription (RT) process as target for RT inhibitors Med. Res. Rev. 20 2000 129 154
141. E Domingo A Mas E Yuste N Pariente S Sierra M Gutiérrez-Rivas L Menéndez-Arias Virus population dynamics, fitness variations and the control of viral disease: an update Prog. Drug Res. 57 2001 77 115
142. Y Xiong T.H Eickbush Origin and evolution of retroelements based upon their reverse transcriptase sequences EMBO J. 9 1990 3353 3362
143. T.M Nakamura G.B Morin K.B Chapman S.L Weinrich W.H Andrews J Lingner C.B Harley T.R Cech Telomerase catalytic subunit homologs from fission yeast and human Science 277 1997 955 959
144. B Canard K Chowdhury R Sarfati S Doublié C.C Richardson The motif D loop of human immunodeficiency virus type 1 reverse transcriptase is critical for nucleoside ′-triphosphate selectivity J. Biol. Chem. 274 1999 35,768 35,776
145. P.L Boyer A.L Ferris S.H Hughes Cassette mutagenesis of the reverse transcriptase of human immunodeficiency virus type 1 J. Virol. 66 1992 1031 1039
146. P.L Boyer A.L Ferris S.H Hughes Mutational analysis of the fingers domain of human immunodeficiency virus type 1 reverse transcriptase J. Virol. 66 1992 7533 7537
147. P.L Boyer A.L Ferris P Clark J Whitmer P Frank C Tantillo E Arnold S.H Hughes Mutational analysis of the fingers and palm subdomains of human immunodeficiencyvirus type-1 (HIV-1) reverse transcriptase J. Mol. Biol. 243 1994 472 483
148. S.-F Chao V.L Chan P Juranka A.H Kaplan R Swanstrom C.A Hutchison III Mutational sensitivity patterns define critical residues in the palm subdomain of the reverse transcriptase of human immunodeficiency virus type 1 Nucleic Acids Res. 23 1995 803 810
149. B Kim T.R Hathaway L.A Loeb Human immunodeficiency virus reverse transcriptase—Functional mutants obtained by random mutagenesis coupled with genetic selection in Escherichia coli J. Biol. Chem. 271 1996 4872 4878
150. H.-Q Gan P.L Boyer E Arnold S.H Hughes Effects of mutations in the polymerase domain on the polymerase, RNase H and strand transfer activities of human immunodeficiency virus type 1 reverse transcriptase J. Mol. Biol. 277 1998 559 572
151. J.A Wrobel S.-F Chao M.J Conrad J.D Merker R Swanstrom G.J Pielak C.A Hutchison III A genetic approach for identifying critical residues in the fingers and palm subdomains of HIV-1 reverse transcriptase 3rd ed. Proc. Natn. Acad. Sci. U.S.A. 95 1998 638 645
152. B.A Larder S.D Kemp D.J.M Purifoy Infectious potential of human immunodeficiency virus type 1 reverse transcriptase mutants with altered inhibitor sensitivity 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 86 1989 4803 4807
153. N Kaushik N Rege P.N.S Yadav S.G Sarafianos M.J Modak V.N Pandey Biochemical analysis of catalytically crucial aspartate mutants of human immunodeficiency virus type 1 reverse transcriptase Biochemistry 35 1996 11,536 11,546
154. D Harris N Kaushik P.K Pandey P.N.S Yadav V.N Pandey Functional analysis of amino acid residues constituting the dNTP binding pocket of HIV-1 reverse transcriptase J. Biol. Chem. 273 1998 33,624 33,634
155. P.L Boyer S.G Sarafianos E Arnold S.H Hughes Analysis of mutations at positions 115 and 116 in the dNTP binding site of HIV-1 reverse transcriptase 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 97 2000 3056 3061
156. A.M Martín-Hemnández M Gutiérrez-Rivas E Domingo L Menéndez-Arias Mispair extension fidelity of human immunodeficiency virus type 1 reverse transcriptases with amino acid substitutions affecting Tyr115 Nucleic Acids Res. 25 1997 1383 1389
157. A.L Zakharenko D.M Kolpashchikov S.N Khodyreva O.I Lavrik L Menéndez-Arias Investigation of the dNTP-binding site of HIV-1 reverse transcriptase using photoreactive analogs of dNTP Biochemistry (Moscow) 66 2001 999 1007
158. M Ricchetti H Buc A reiterative mode of DNA synthesis adopted by HIV -1 reverse transcriptase after a misincorporation Biochemistry 35 1996 14,970 14,983
159. J.-P Vartanian M Sala M Henry S Wain-Hobson A Meyerhans Manganese cations increase the mutation rate of human immunodeficiency virus type 1 ex vivo J. Gen. Virol. 80 1999 1983 1986
160. H Jonckheere E De Clercq J Anné Fidelity analysis of HIV-1 reverse transcriptase mutants with an altered amino-acid sequence at residues Leu74, Glu89, Tyr115, Tyr183 and Met184 Eur. J. Biochem. 267 2000 2658 2665
161. I Olivares V Sánchez-Merino M.A Martínez E Domingo C López-Galíndez L Menéndez-Arias Second-site reversion of a human immunodeficiency virus type 1 reverse transcriptase mutant that restores enzyme function and replication capacity J. Virol. 73 1999 6293 6298
162. E.K Halvas E.S Svarovskaia V.K Pathak Role of murine leukemia virus reverse transcriptase deoxyribonucleoside triphosphate-binding site in retroviral replication and in vivo fidelity J. Virol. 74 2000 10,349 10,358
163. G Gao M Orlova M.M Georgiadis W.A Hendrickson S.P Goff Conferring RNA polymerase activity to a DNA polymerase: A single residue in reverse transcriptase controls substrate selection 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 94 1997 407 411
164. M Delarue O Poch N Tordo D Moras P Argos An attempt to unify the structure of polymerases Protein Eng. 3 1990 461 467
165. D.K Braithwaite J Ito Compilation, alignment, and phylogenetic relationships of DNA polymerases Nucleic Acids Res. 21 1993 787 802
166. Q Dong W.C Copeland T.S.-F Wang 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 24,163 24,174
167. A.F Gardner W.E Jack Determinants of nucleotide sugar recognition in an archaeon DNA polymerase Nucleic Acids Res. 27 1999 2545 2553
168. A Bonnin J.M Lazaro L Blanco M Salas A single tyrosine prevents insertion of ribonucleotides in the eukaryotic-type φ29 DNA polymerase J. Mol. Biol. 290 1999 241 251
169. M Gutiérrez-Rivas A Ibáñez M.A Martínez E Domingo L Menéndez-Arias Mutational analysis of Phe-160 within the ‘palm’ subdomain of human immunodeficiency virus type 1 reverse transcriptase J. Mol. Biol. 290 1999 615 625
170. N.K.T Back M Nijhuis W Keulen C.A.B Boucher B.B Oude Essink A.B.P van Kuilenburg A.H van Gennip B Berkhout Reduced replication of 3TC-resistant HIV-1 variants in primary cells due to a processivity defect of the reverse trancriptase enzyme EMBO J. 15 1996 4040 4049
171. W Keulen N.K.T Back A van Wijk C.A.B Boucher B Berkhout Initial appearance of the 184Ile variant in lamivudine-treated patients is caused by the mutational bias of human immunodeficiency virus type 1 reverse transcriptase J. Virol. 71 1997 3346 3350
172. S.G Sarafianos K Das A.D Clark Jr. J Ding P.L Boyer S.H Hughes E Arnold Lamivudine (3TC) resistance in HIV-1 reverse transcriptase involves steric hindrance with β-branched amino acids 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 96 1999 10,027 10,032
173. R Krebs U Immendörfer S.H Thrall B.M Wöhrl R.S Goody Single-step kinetics of HIV-1 reverse transcriptase mutants responsible for virus resistance to nucleoside inhibitors zidovudine and 3TC Biochemistry 36 1997 10,292 10,300
174. J.E Wilson A Aulabaugh B Caligan S McPherson J.K Wakefield S Jablonski C.D Morrow J.E Reardon P.A Furman Human immunodeficiency virus type-1 reverse transcriptase—Contribution of Met-184 to binding of nucleoside 5′-triphosphate J. Biol. Chem. 271 1996 13,656 13,662
175. J.Y Feng K.S Anderson Mechanistic studies examining the efficiency and fidelity of DNA synthesis by the 3TC-resistant mutant (184V) of HIV-1 reverse transcriptase Biochemistry 38 1999 9440 9448
176. H.-Q Gao P.L Boyer S.G Sarafianos E Arnold S.H Hughes The role of steric hindrance in 3TC resistance of human immunodeficiency virus type-1 reverse transcriptase J. Mol. Biol. 300 2000 403 418
177. E.K Halvas E.S Svarovskaia E.O Freed V.K Pathak Wild-type and YMDD mutant murine leukemia virus reverse transcriptases are resistant to 2′,3′-dideoxy-3′-thiacytidine J. Virol. 74 2000 6669 6674
178. M.A Wainberg W.C Drosopoulos H Salomon M Hsu G Borkow M.A Parniak Z Gu Q Song J Manne S Islam G Castriota V.R Prasad Enhanced fidelity of 3TC-selected mutant HIV-1 reverse transcriptase Science 271 1996 1282 1285
179. B.D Preston Reverse transcriptase fidelity and HIV-1 variation Science 275 1997 228 229
180. W Keulen M Nijhuis R Schuurman B Berkhout C Boucher Reverse transcriptase fidelity and HIV-1 variation Science 275 1997 229
181. J Balzarini H Pelemans E De Clereq A Karlsson J.-P Kleim Reverse transcriptase fidelity and HIV-1 variation Science 275 1997 229 230
182. H Jonckheere M Witvrouw E De Clereq J Anné Lamivudine resistance of HIV type 1 does not delay development of resistance to nonnucleoside HIV type 1-specific reverse transcriptase inhibitors as compared with wild-type HIV type 1 AIDS Res. Human Retrovir. 14 1998 249 253
183. W Keulen A van Wijk R Schuurman B Berkhout C.A.B Boucher Increased polymerase fidelity of lamivudine-resistant HIV-1 variants does not limit their evolutionary potential AIDS 13 1999 1343 1349
184. V.N Pandey N Kaushik N Rege S.G Sarafianos P.N.S Yadav M.J Modak Role of methionine 184 of human immunodeficiency virus type-1 reverse transcriptase in the polymerase function and fidelity of DNA synthesis Biochemistry 35 1996 2168 2179
185. M.E Hamburgh W.C Drosopoulos V.R Prasad The influence of 3TC-resistance mutations E89G and M184V in the human immunodeficiency virus reverse transcriptase on mispair extension efficiency Nucleic Acids Res. 26 1998 4389 4394
186. M Hsu P Inouye L Rezende N Richard Z Li V.R Prasad M.A Wainberg Higher fidelity of RNA-dependent DNA mispair extension by M184V drug-resistant than wild-type reverse transcriptase of human immunodeficiency virus type 1 Nucleic Acids Res. 25 1997 4532 4536
187. B.B Oude Essink N.K.T Back B Berkhout Increased polymerase fidelity of the 3TC-resistant variants of HIV-1 reverse transcriptase Nucleic Acids Res. 25 1997 3212 3217
188. D Harris P.N.S Yadav V.N Pandey Loss of polymerase activity due to Tyr to Phe substitution in the YMDD motif of human immunodeficiency virus type-1 reverse transcriptase is compensated by Met to Val substitution within the same motif Biochemistry 37 1998 9630 9640
189. L.M Mansky L.C Bernard 3′-azido-3′-deoxythymidine (AZT) and AZT-resistant reverse transcriptase can increase the in vivo mutation rate of human immunodeficiency virus type 1 J. Virol. 74 2000 9532 9539
190. M Bakhanashvili O Avidan A Hizi Mutational studies of human immunodeficiency virus type 1 reverse transcriptase: the involvement of residues 183 and 184 in the fidelity of DNA synthesis FEBS Lett. 391 1996 257 262
191. N Kaushik K Chowdhury V.N Pandey M.J Modak Valine of the YVDD motif of Moloney murine leukemia virus reverse transcriptase: Role in the fidelity of DNA synthesis Biochemistry 39 2000 5155 5165
192. E.K Halvas E.S Svarovskaia V.K Pathak Development of an in vivo assay to identify structural determinants in murine leukemia virus reverse transcriptase important for fidelity J. Virol. 74 2000 312 319
193. T Ueno T Shirasaka H Mitsuya Enzymatic characterization of human immunodeficiency virus type 1 reverse transcriptase resistant to multiple 2′,3′-dideoxynucleoside 5′-triphosphates J. Biol. Chem. 270 1995 23,605 23,611
194. T Ueno H Mitsuya Comparative enzymatic study of HIV-1 reverse transcriptase resistant to 2′,3′-dideoxynucleotide analogs using the single-nucleotide incorporation assay Biochemistry 36 1997 1092 1099
195. N Kaushik T.T Talele P.K Pandey D Harris P.N.S Yadav V.N Pandey Role of glutamine 151 of human immunodeficiency virus type-1 reverse transcriptase in substrate selection as assessed by site-directed mutagenesis Biochemistry 39 2000 2912 2920
196. S Tabor C.C Richardson A single residue in DNA polymerases of the Escherichia coli DNA polymerase I family is critical for distinguishing between deoxy- and dideoxyribonucleotides 3rd ed. Proc. Natn. Acad. Sci. U.S.A. 92 1995 6339 6343
197. S.G Sarafianos V.N Pandey N Kaushik M.J Modak Glutamine 151 participates in the substrate dNTP binding function of HIV-1 reverse transcriptase Biochemistry 34 1995 7207 7216
198. N Kaushik D Harris N Rege M.J Modak P.N.S Yadav V.N Pandey Role of glutamine-151 of human immunodeficiencyvirus type-1 reverse transcriptase in RNA-directed DNA synthesis Biochemistry 36 1997 14,430 14,438
199. K.K Weiss S.J Isaacs N.H Tran E.T Adman B Kim Molecular architecture of the mutagenic active site of human immunodeficiency virus type 1 reverse transcriptase: Roles of the β8-αE loop in fidelity, processivity and substrate interactions Biochemistry 39 2000 10,684 10,694
200. T Shirasaka M.F Kavlick T Ueno W.-Y Gao E Kojima M.L Alcaide S Chokekijchai B.M Roy E Arnold R Yarchoan H Mitsuya Emergence of human immunodeficiency virus type 1 variants with resistance to multiple dideoxynucleosides inpatients receiving therapy with dideoxynucleosides 3rd ed. Proc. Natn. Acad. Sci. U.S.A. 92 1995 2398 2402
201. K Singh N Kaushik J Jin M Madhusudanan M.J Modak Role of Q190 of MuLV RT in ddNTP resistance and fidelity of DNA synthesis: a molecular model of interactions with substrates Protein Eng. 13 2000 635 643
202. Z Gu Q Gao H Fang H Salomon M.A Parniak E Goldberg J Cameron M.A Wainberg Identification of a mutation at codon 65 in the IKKK motif of reverse transcriptase that encodes human immunodeficiency virus resistance to 2′,3′-dideoxycytidine and 2′,3′-dideoxy-3′-thiacytidine Antimicrob. Agents Chemother. 38 1994 275 281
203. Z Gu R.S Fletcher E.J Arts M.A Wainberg M.A Parniak The K65R mutant reverse transcriptase of HIV-1 cross-resistant to 2′,3′-dideoxycytidine, 2′,3′-dideoxy-3′-thiacytidine, and 2′,3′-dideoxyinosine shows reduced sensitivity to specific dideoxynucleoside triphosphate inhibitors in vitro J. Biol. Chem. 269 1994 28,118 28,122
204. D Zhang A.M Caliendo J.J Eron K.M DeVore J.C Kaplan M.S Hirsch R.T D'Aquila Resistance to 2′,3′-dideoxycytidine conferred by a mutation in codon 65 of the human immunodeficiency virus type 1 reverse transcriptase Antimicrob. Agents Chemother. 38 1994 282 287
205. M.A Winters R.W Shafer R.A Jellinger G Mamtora T Gingeras T.C Merigan Human immunodeficiency virus type 1 reverse transcriptase genotype and drug susceptibility changes in infected individuals receiving dideoxyinosine monotherapy for 1 to 2 years Antimicrob. Agents Chemother. 41 1997 757 762
206. Z Gu E.J Arts M.A Parniak M.A Wainberg Mutated K65R recombinant reverse transcriptase of human immunodeficiency virus type 1 shows diminished chain termination in the presence of 2′,3′-dideoxycytidine 5′-triphosphate and other drugs 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 92 1995 2760 2764
207. D Arion G Borkow Z Gu M.A Wainberg M.A Parniak The K65R mutation confers increased DNA polymerase processivity to HIV-1 reverse transcriptase J. Biol. Chem. 271 1996 19,860 19,864
208. N Sluis-Cremer D Arion N Kaushik H Lim Mutational analysis of Lys65 of HIV-1 reverse transcriptase Biochem. J. 348 2000 77 82
209. F.S Shah K.A Curr M.E Hamburgh M Parniak H Mitsuya J.G Arnez V.R Prasad Differential influence of nucleoside analog-resistance mutations K65R and L74V on the overall mutation rate and error specificity of human immunodeficiency virus type 1 reverse transcriptase J. Biol. Chem. 275 2000 27,037 27,044
210. S.G Sarafianos V.N Pandey N Kaushik M.J Modak Site-directed mutagenesis of arginine 72 of HIV-1 reverse transcriptase—Catalytic role and inhibitor sensitivity J. Biol. Chem. 270 1995 19,729 19,735
211. K Chowdhury N Kaushik V.N Pandey M.J Modak Elucidation of the role of Arg 110 of murine leukemia virus reverse transcriptase in the catalytic mechanism: Biochemical characterization of its mutant enzymes Biochemistry 35 1996 16,610 16,620
212. D.A Lewis K Bebenek W.A Beard S.H Wilson T.A Kunkel Uniquely altered DNA replication fidelity conferred by an amino acid change in the nucleotide binding pocket of human immunodeficiency virus type 1 reverse transcriptase J. Biol. Chem. 274 1999 32,924 32,930
213. M.H.St Clair J.L Martin G Tudor-Williams M.C Bach C.L Vavro D.M King P Kellam S.D Kemp B.A Larder Resistance to ddI and sensitivity to AZT induced by a mutation in HIV-1 reverse transcriptase Science 253 1991 1557 1559
214. P.L Sharma C.S Crumpacker Decreased processivity of human immunodeficiency virus type 1 reverse transcriptase (RT) containing didanosine-selected mutation Leu74Val: A comparative analysis of RT variants Leu74Val and lamivudine-selected Met184Val J. Virol. 73 1999 8448 8456
215. T Rubinek M Bakhanashvili R Taube O Avidan A Hizi The fidelity of 3′ misinsertion and mispair extension during RNA synthesis exhibited by two drug-resistant mutants of the reverse transcriptase of human immunodeficiency virus type 1 with Leu74 → Val and Glu89 → Gly Eur. J. Biochem. 247 1997 238 247
216. R Taube O Avidan A Hizi The fidelity of misinsertion and mispair extension throughout DNA synthesis exhibited by mutants of the reverse transcriptase of human immunodeficiency virus type 2 resistant to nucleoside analogs Eur. J. Biochem. 250 1997 106 114
217. V.R Prasad I Lowy T de los Santos L Chiang S.P Goff Isolation and characterization of a dideoxyguanosine triphosphate-resistant HIV-1 reverse transcriptase expressed in bacteria 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 88 1991 11,363 11,367
218. O Avidan A Hizi The processivity of DNA synthesis exhibited by drug-resistant variants of human immunodeficiency virus type-1 reverse transcriptase Nucleic Acids Res. 26 1998 1713 1717
219. Y Quan P Inouye C Liang L Rong M Götte M.A Wainberg Dominance of the E89G substitution in HIV-1 reverse transcriptase in regard to increased polymerase processivity and patterns of pausing J. Biol. Chem. 273 1998 21,918 21,925
220. W.C Drosopoulos V.R Prasad Increased polymerase fidelity of E89G, a nucleoside analog-resistant variant of human immunodeficiency virus type 1 reverse transcriptase J. Virol. 70 1996 4834 4838
221. N Kaushik K Singh I Alluru M.J Modak Tyrosine 222, a member of the YXDD motif of MuLV RT, is catalytically essential and is a major component of the fidelity center Biochemistry 38 1999 2617 2627
222. P.S Jacques B.M Wöhrl M Ottmann J.-L Darlix S.F.J Le Grice Mutating the “primer grip” of p66 HIV-1 reverse transcriptase implicates tryptophan-229 in template-primer utilization J. Biol. Chem. 269 1994 26,472 26,478
223. M Ghosh P.S Jacques D.W Rodgers M Ottman J.-L Darlix S.F.J Le Grice Alterations to the primer grip of p66 HIV-1 reverse transcriptase and their consequences for template-primer utilization Biochemistry 35 1996 8553 8562
224. M Ghosh J Williams M.D Powell J.G Levin S.F.J Le Grice Mutating a conserved motif of the HIV-1 reverse transcriptase palm subdomain alters primer utilization Biochemistry 36 1997 5758 5768
225. C Palaniappan M Wisniewski P.S Jacques S.F.J Le Grice P.J Fay R.A Bambara Mutations within the primer grip region of HIV-1 reverse transcriptase result in loss of RNase H function J. Biol. Chem. 272 1997 11,157 11,164
226. M.D Powell M Ghosh P.S Jacques K.J Howard S.F.J Le Grice J.G Levin Alanine-scanning mutations in the “primer grip” of p66 HIV-1 reverse transcriptase result in selective loss of RNA priming activity J. Biol. Chem. 272 1997 13,262 13,269
227. B.M Wöhrl R Krebs S.H Thrall S.F.J Le Grice A.J Scheidig R.S Goody Kinetic analysis of four HIV-1 reverse transcriptase enzymes mutated in the primer grip region of p66—Implications for DNA synthesis and dimerization J. Biol. Chem. 272 1997 17,581 17,587
228. M Wisniewski C Palaniappan Z Fu S.F.J Le Grice P Fay R.A Bambara Mutations in the primer grip region of HIV reverse transcriptase can increase replication fidelity J. Biol. Chem. 274, 28,175-28,184 1999
229. Q Yu M Ottmann C Pechoux S Le Grice J.-L Darlix Mutations in the primer grip of human immunodeficiency virus type 1 reverse transcriptase impair proviral DNA synthesis and virion maturation J. Virol. 72 1998 7676 7680
230. M Gutiérrez-Rivas L Menéndez-Arias A mutation in the primer grip region of HIV-1 reverse transcriptase that confers reduced fidelity of DNA synthesis Nucleic Acids Res. 29 2001 4963 4972
231. K Bebenek W.A Beard T.A Darden L Li R Prasad B.A Luxon D.G Gorenstein S.H Wilson T.A Kunkel A minor groove binding track in reverse transcriptase Nature Struct. Biol. 4 1997 194 197
232. M.D Powell W.A Beard K Bebenek K.J Howard S.F.J Le Grice T.A Darden T.A Kunkel S.H Wilson J.G Levin Residues in the αH and αI helices of the HIV-1 reverse transcriptase thumb subdomain required for the specificity of RNase H-catalyzed removal of the polypurine tract primer J. Biol. Chem. 274 1999 19,885 19,893
233. M Bakhanashvili A Hizi A possible role for cysteine residues in the fidelity of DNA synthesis exhibited by the reverse transcriptases of human immunodeficiency viruses type 1 and type 2 FEBS Lett. 304 1992 289 293
234. S Loya M Bakhanashvili R Tal S.H Hughes P.L Boyer A Hizi Enzymatic properties of two mutants of reverse transcriptase of human immunodeficiency virus type 1 (Tyrosine 181 → Isoleucine and Tyrosine 188 Leucine) resistant to nonnucleoside inhibitors AIDS Res. Human Retrovir. 10 1994 939 946
235. Y Kew L.R Olsen A.J Japour V.R Prasad Insertions into the β3-β4 hairpin loop of HIV-1 reverse transcriptase reveal a role for fingers subdomain in processive polymerization J. Biol. Chem. 273 1998 7529 7537
236. L.F Rezende Y Kew V.R Prasad The effect of increased processivity on overall fidelity of human immunodeficiency virus type 1 reverse transcriptase J. Biomed. Sci. 8 2001 197 205
237. M Ghosh K.J Howard C.E Cameron S.J Benkovic S.H Hughes S.F.J Le Grice Truncating α-helix E' of p66 human immunodeficiency virus reverse transcriptase modulates RNase H function and impairs DNA strand transfer J. Biol. Chem. 270 1995 7068 7076
238. B.A Larder Interactions between drug resistance mutations in human immunodeficiency virus type 1 reverse transcriptase J. Gen. Virol. 75 1994 951 957
239. P.R Meyer S.E Matsuura A.M Mian A.G So W.A Scott A mechamism of AZT resistance: an increase in nucleotide-dependent primer unblocking by mutant HIV-1 reverse transcriptase Mol. Cell 4 1999 35 43
240. N Sluis-Cremer D Arion M.A Parniak Molecular mechanisms of HIV-1 resistance to nucleoside reverse transcriptase inhibitors (NRTIs) CMLS, Cell. Mol. Life Sci. 57 2000 1408 1422
241. A Mas M Parera C Briones V Soriano M.A Martínez E Domingo L Menéndez-Arias Role of a dipeptide insertion between codons 69 and 70 of HIV-1 reverse transcriptase in the mechanism of AZT resistance EMBO J. 19 2000 5752 5761
242. S.F Lacey J.E Reardon E.S Furfine T.A Kunkel K Bebenek K.A Eckert S.D Kemp B.A Larder Biochemical studies on the reverse transcriptase and RNase H activities from human immunodeficiency virus strains resistant to 3′-azido-3′-deoxythymidine J. Biol. Chem. 267 1992 15,789 15,794
243. J.G Julias T Kim G Arnold V.K Pathak The antiretrovirus drug 3′-azido-3′-deoxythymidine increases the retrovrus mutation rate J. Virol. 71 1997 4254 4263
244. J.M Coffin HIV population dynamics in vivo: implications for genetic variation, pathogenesis and therapy Science 267 1995 483 489
245. T.L Diamond J Kimata B Kim Identification of a simian immunodeficiencyvirus reverse transcriptase variant with enhanced replicational fidelity in the late stage of viral infection J. Biol. Chem. 276 2001 23,624 23,631
246. J.G Juhas V.K Pathak Deoxyribonucleoside triphosphate pool imbalances in vivo are associated with an increased retroviral mutation rate J. Virol. 72 1998 7941 7949
247. W.A O'Brien A Namazi H Kalhor S.-H Mao J.A Zack I.S.Y Chen Kinetics of human immunodeficiency virus type 1 reverse transcriptase in blood mononuclear phagocytes are slowed by limitations of nucleotide precursors J. Virol. 68 1994 1258 1263
248. N.K.T Back B Berkhout Limiting deoxynucleoside triphosphate concentrations emphasize the processivity defect of lamivudine-resistant variants of human immunodeficiency virus type 1 reverse transcriptase Antimicrob. Agents Chemother. 41 1997 2484 2491
249. M.A Martínez J.-P Vartanian S Wain-Hobson Hypermutagenesis of RNA using human immunodeficiency virus type 1 reverse transcriptase and biased dNTP concentrations 3rd ed. Proc. Natn. Acad. Sci. U.S.A. 91 1994 11,787 11,791
250. J.-P Vartanian U Plikat M Henry R Mahieux L Guillemot A Meyerhans S WainHobson HIV genetic variation is directed and restricted by DNA precursor availability J. Mol. Biol. 270 1997 139 151
251. M.A Martínez M Sala J.-P Vartanian S Wain-Hobson Reverse transcriptase and substrate dependence of the RNA hypermutagenesis reaction Nucleic Acids Res. 23 1995 2573 2578
252. J Balzarini M.-J Camarasa M.-J Pérez-Pérez A San-Félix S Velázquez C.-F Perno E De Clercq J.N Anderson A Karlsson Exploitation of the low fidelity of human immunodeficiency virus type 1 (HIV-1) reverse transcriptase and the nucleotide composition bias in the HIV-1 genome to alter the drug resistance development of HIV J. Virol. 75 2001 5772 5777
253. D.G Johns W.-Y Gao Selective depletion of DNA precursors: An evolving strategy for potentiation of dideoxynucleoside activity against human immunodeficiency virus Biochem. Pharmacol. 55 1998 1551 1556
254. J Balzarini Effect of antimetabolite drugs of nucleotide metabolism on the anti-human immunodeficiency virus activity of nucleoside reverse transcriptase inhibitors Pharmacol. Therapeut. 87 2000 175 187
255. J.K Pfeiffer M.M Georgiadis A Telestnitsky Structure-based Moloney murine leukemia virus reverse transcriptase mutants with altered intracellular direct-repeat deletion frequencies J. Virol. 74 2000 9629 9636
256. R.A LaCasse K.M Remington T.W North The mutation frequency of feline immunodeficiency virus enhanced by 3′-azido-3′-deoxythymidine J. Acquir Immune Def. Syndr. Humar Retrovir. 12 1996 26 32
257. J Ji J.-S Hoffmann L.A Loeb Mutagenicity and pausing of HIV reverse transcriptase during HIV plus-strand DNA synthesis Nucleic Acids Res. 22 1994 47 52
258. V.K Pathak H.M Temin 5-Azacytidine and RNA secondary structure increase the retrovirus mutation rate J. Virol. 66 1992 3093 5100
259. J.E Mott J Van Arsdell T Platt Targeted mutagenesis in vitro : lac repressor mutations generated using AMV reverse transcriptase and dBrUTR Nucleic Acids Res. 12 1984 4139 4152
260. 2-dGTP by reverse transcriptases and mammalian DNA polymerases J. Biol. Chem. 272 1997 5892 5898
261. 6-methyldeoxyguanosine triphosphate Mutation Res. 374 1997 41 50
262. L.A Loeb J.M Essigmann F Kazazi J Zhang K.D Rose J.I Mullins Lethal mutagenesis of HIV with mutagenic nucleoside analogs 3rd ed. Proc. Natl. Acad. Sci. U.S.A. 96 1999 1492 1497
263. L.A Loeb J.I Mullins Lethal mutagenesis of HIV by mutagenic ribonucleoside analogs AIDS Res. Human Retrovir. 16 2000 1 3