Retroviral mutation rates and reverse transcriptase fidelity

Frontiers in Bioscience

Volumn , Issue 4, 2003, Pages

  Svarovskaia, Evguenia S ^a   Cheslock, Sara R ^a,b   Zhang, Wen Hui ^a   Hu, Wei Shau ^a   Pathak, Vinay K ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

dNTP Binding Site; Fidelity; Genetic Variation; Misinsertions; Mismatch Extension; Mutation Rate; Retrovirus; Reverse Transcriptase; Review; RNA Polymerase II; RNase H Primer Grip; Template Primer Structure; Transcription Fidelity

Indexed keywords

DNA POLYMERASE; RIBONUCLEASE; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE; VIRUS PROTEIN; ZIDOVUDINE;

CHEMICAL MODIFICATION; DNA REPAIR; DNA SYNTHESIS; DNA TEMPLATE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; GENETIC VARIABILITY; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMAL; MUTATION RATE; NONHUMAN; PROTEIN FUNCTION; REPORTER GENE; RETROVIRUS; REVERSE TRANSCRIPTION; REVIEW; RNA TRANSCRIPTION; VIRUS MUTATION; VIRUS REPLICATION; ANIMAL; CHEMISTRY; GENETICS; MOLECULAR GENETICS; MUTAGENESIS; NUCLEOTIDE SEQUENCE;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA; RNA VIRUSES; UNIDENTIFIED RETROVIRUS;

ANIMALS; BASE SEQUENCE; HUMANS; MOLECULAR SEQUENCE DATA; MUTAGENESIS; RETROVIRIDAE; RNA-DIRECTED DNA POLYMERASE;

EID: 0347117654     PISSN: 27686701     EISSN: 27686698     Source Type: Journal    
DOI: None     Document Type: Review

References (145)

1. Ho, D. D., A. U. Neumann, A. S. Perelson, W. Chen, J. M. Leonard & M. Markowitz: Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature 373, 123-6 (1995)
2. Coffin, J. M.: HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267, 483-9 (1995)
3. Wei, X., S. K. Ghosh, M. E. Taylor, V. A. Johnson, E. A. Emini, P. Deutsch, J. D. Lifson, S. Bonhoeffer, M. A. Nowak, B. H. Hahn & et al.: Viral dynamics in human immunodeficiency virus type 1 infection. Nature 373, 117-22 (1995)
4. Schuitemaker, H., M. Koot, N. A. Kootstra, M. W. Dercksen, R. E. de Goede, R. P. van Steenwijk, J. M. Lange, J. K. Schattenkerk, F. Miedema & M. Tersmette: Biological phenotype of human immunodeficiency virus type 1 clones at different stages of infection: progression of disease is associated with a shift from monocytotropic to T-cell-tropic virus population. J Virol 66, 1354-60 (1992)
5. Connor, R. I., K. E. Sheridan, D. Ceradini, S. Choe & N. R. Landau: Change in coreceptor use coreceptor use correlates with disease progression in HIV-1-infected individuals. J Exp Med 185, 621-8 (1997)
6. Jekle, A., B. Schramm, P. Jayakumar, V. Trautner, D. Schols, E. De Clercq, J. Mills, S. M. Crowe & M. A. Goldsmith: Coreceptor phenotype of natural human immunodeficiency virus with nef deleted evolves in vivo, leading to increased virulence. J Virol 76, 6966-73 (2002)
7. Robertson, D. L., J. P. Anderson, J. A. Bradac, J. K. Carr, B. Foley, R. K. Funkhouser, F. Gao, B. H. Hahn, M. L. Kalish, C. Kuiken, G. H. Learn, T. Leitner, F. McCutchan, S. Osmanov, M. Peeters, D. Pieniazek, M. Salminen, P. M. Sharp, S. Wolinsky & B. Korber: HIV-1 nomenclature proposal. Science 288, 55-6 (2000)
8. Gaschen, B., J. Taylor, K. Yusim, B. Foley, F. Gao, D. Lang, V. Novitsky, B. Haynes, B. H. Hahn, T. Bhattacharya & B. Korber: Diversity considerations in HIV-1 vaccine selection. Science 296, 2354-60 (2002)
9. McMichael, A., M. Mwau & T. Hanke: HIV T cell vaccines, the importance of clades. Vaccine 20, 1918-21 (2002)
10. Schinazi, R. F., B. A. Larder & J. W. Mellors: Mutations in retroviral genes assosiated with drug resistance: 2000-2001 update. International Antiviral News 8, 65-91 (2000)
11. Roberts, J. D., K. Bebenek & T. A. Kunkel: The accuracy of reverse transcriptase from HIV-1. Science 242, 1171-3 (1988)
12. Pathak, V. K. & 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. Proc Natl Acad Sci U S A 87, 6024-8 (1990)
13. Pathak, V. K. & H. M. Temin: Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: substitutions, frameshifts, and hypermutations. Proc Natl Acad Sci U S A 87, 6019-23 (1990)
14. Mansky, L. M. & 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, 5087-94 (1995)
15. Mansky, L. M.: In vivo analysis of human T-cell leukemia virus type 1 reverse transcription accuracy. J Virol 74, 9525-31 (2000)
16. Mansky, L. M. & H. M. Temin: Lower mutation rate of bovine leukemia virus relative to that of spleen necrosis virus. J Virol 68, 494-9 (1994)
17. Hu, W. S., E. H. Bowman, K. A. Delviks & V. K. Pathak: Homologous recombination occurs in a distinct retroviral subpopulation and exhibits high negative interference. J Virol 71, 6028-36 (1997)
18. Hu, W. S. & H. M. Temin: Genetic consequences of packaging two RNA genomes in one retroviral particle: pseudodiploidy and high rate of genetic recombination. Proc Natl Acad Sci U S A 87, 1556-60 (1990)
19. Hu, W. S. & H. M. Temin: Retroviral recombination and reverse transcription. Science 250, 1227-33 (1990)
20. Anderson, J. A., E. H. Bowman & W. S. Hu: Retroviral recombination rates do not increase linearly with marker distance and are limited by the size of the recombining subpopulation. J Virol 72, 1195-202 (1998)
21. Anderson, J. A., R. J. Teufel, 2nd, P. D. Yin & W. S. Hu: Correlated template-switching events during minus-strand DNA synthesis: a mechanism for high negative interference during retroviral recombination. J Virol 72, 1186-94 (1998)
22. Rouzine, I. M., A. Rodrigo & J. M. Coffin: Transition between stochastic evolution and deterministic evolution in the presence of selection: general theory and application to virology. Microbiol Mol Biol Rev 65, 151-85 (2001)
23. Rous, P. & J. B. Murphy: Variations in a chicken sarcoma caused by a filterable agent. J Exptl Med 17, 219-231 (1913)
24. Duran-Reynals, F.: The reciprocal infection of ducks and chickens with tumor-inducing viruses. Cancer Research 2, 343-369 (1942)
25. Temin, H. M. & H. Rubin: Characteristics of an assay for Rous sarcoma virus and Rous sarcoma cells in tissue culture. Virology 6, 669-688 (1958)
26. Temin, H. M.: The control of cellular morphology in embryonic cells infected with Rous Sarcoma Virus in vitro. Virology 10, 182-197 (1960)
27. Baltimore, D.: RNA-dependent DNA polymerase in virions of RNA tumour viruses. Nature 226, 1209-11 (1970)
28. Temin, H. M. & S. Mizutani: RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 226, 1211-3 (1970)
29. Springgate, C. F., N. Battula & L. A. Loeb: Infidelity of DNA synthesis by reverse transcriptase. Biochem Biophys Res Commun 52, 401-6 (1973)
30. Battula, N. & L. A. Loeb: The infidelity of avian myeloblastosis virus deoxyribonucleic acid polymerase in polynucleotide replication. J Biol Chem 249, 4086-93 (1974)
31. Battula, N. & L. A. Loeb: On the fidelity of DNA replication. Characterization of polynucleotides with errors in base-pairing synthesized by avian myeloblastosis virus deoxyribonucleic acid polymerase. J Biol Chem 250, 4405-9 (1975)
32. Mizutani, S. & H. M. Temin: Incorporation of noncomplementary nucleotides at high frequencies by ribodeoxyvirus DNA polymerases and Escherichia coli DNA polymerase I. Biochemistry 15, 1510-6 (1976)
33. Coffin, J. M., P. N. Tsichlis, C. S. Barker, S. Voynow & H. L. Robinson: Variation in avian retrovirus genomes. Ann N Y Acad Sci 354, 410-25 (1980)
34. Gojobori, T. & S. Yokoyama: Rates of evolution of the retroviral oncogene of Moloney murine sarcoma virus and of its cellular homologues. Proc Natl Acad Sci U S A 82, 4198-201 (1985)
35. Steinhauer, D. A. & J. J. Holland: Rapid evolution of RNA viruses. Annu Rev Microbiol 41, 409-33 (1987)
36. Eigen, M.: Selforganization of matter and the evolution of biological macromolecules. Naturwissenschaften 58, 465-523 (1971)
37. Weymouth, L. A. & L. A. Loeb: Mutagenesis during in vitro DNA synthesis. Proc Natl Acad Sci U S A 75, 1924-8 (1978)
38. Kunkel, T. A.: The mutational specificity of DNA polymerases-alpha and -gamma during in vitro DNA synthesis. J Biol Chem 260, 12866-74 (1985)
39. Kunkel, T. A. & A. Soni: Exonucleolytic proofreading enhances the fidelity of DNA synthesis by chick embryo DNA polymerase-gamma. J Biol Chem 263, 4450-9 (1988)
40. Watanabe, S. & H. M. Temin: Encapsidation sequences for spleen necrosis virus, an avian retrovirus, are between the 5′ long terminal repeat and the start of the gag gene. Proc Natl Acad Sci U S A 79, 5986-90 (1982)
41. Mann, R., R. C. Mulligan & D. Baltimore: Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus. Cell 33, 153-9 (1983)
42. Gilboa, E., S. W. Mitra, S. Goff & D. Baltimore: A detailed model of reverse transcription and tests of crucial aspects. Cell 18, 93-100 (1979)
43. Abergel, C., D. L. Robertson & J. M. Claverie: "Hidden" dUTPase sequence in human immunodeficiency virus type 1 gp120. J Virol 73, 751-3 (1999)
44. Petursson, G., P. Turelli, S. Matthiasdottir, G. Georgsson, O. S. Andresson, S. Torsteinsdottir, R. Vigne, V. Andresdottir, E. Gunnarsson, G. Agnarsdottir & G. Querat: Visna virus dUTPase is dispensable for neuropathogenicity. J Virol 72, 1657-61 (1998)
45. Turelli, P., G. Petursson, F. Guiguen, J. F. Mornex, R. Vigne & G. Querat: Replication properties of dUTPase-deficient mutants of caprine and ovine lentiviruses. J Virol 70, 1213-7 (1996)
46. Turelli, P., F. Guiguen, J. F. Mornex, R. Vigne & G. Querat: dUTPase-minus caprine arthritis-encephalitis virus is attenuated for pathogenesis and accumulates G-to-A substitutions. J Virol 71, 4522-30 (1997)
47. Elder, J. H., 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, 1791-4 (1992)
48. Threadgill, D. S., W. K. Steagall, M. T. Flaherty, F. J. Fuller, S. T. Perry, K. E. Rushlow, S. F. Le Grice & S. L. Payne: Characterization of equine infectious anemia virus dUTPase: growth properties of a dUTPase-deficient mutant. J Virol 67, 2592-600 (1993)
49. Mansky, L. M., 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, 7039-47 (2000)
50. Zhang, W. H., C. K. Hwang, W. S. Hu, R. J. Gorelick & V. K. Pathak: Zinc finger domain of murine leukemia virus nucleocapsid protein enhances the rate of viral DNA synthesis in vivo. J Virol 76, 7473-84 (2002)
51. Julias, J. G. & V. K. Pathak: Deoxyribonucleoside triphosphate pool imbalances in vivo are associated with an increased retroviral mutation rate. J Virol 72, 7941-9 (1998)
52. Bowman, R. R., W. S. Hu & V. K. Pathak: Relative rates of retroviral reverse transcriptase template switching during RNA- and DNA-dependent DNA synthesis. J Virol 72, 5198-206 (1998)
53. Glickman, B. W., V. A. Saddi & J. Curry: International Commission for Protection Against Environmental Mutagens and Carcinogens. Working paper no. 2. Spontaneous mutations in mammalian cells. Mutat Res 304, 19-32 (1994)
54. Kim, T., R. A. Mudry, Jr., C. A. Rexrode, 2nd & V. K. Pathak: Retroviral mutation rates and A-to-G hypermutations during different stages of retroviral replication. J Virol 70, 7594-602 (1996)
55. de Mercoyrol, L., 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, 49-58 (1992)
56. Jeon, C. & K. Agarwal: Fidelity of RNA polymerase II transcription controlled by elongation factor TFIIS. Proc Natl Acad Sci USA 93, 13677-82 (1996)
57. Thomas, M. J., A. A. Platas & D. K. Hawley: Transcriptional fidelity and proofreading by RNA polymerase II. Cell 93, 627-37 (1998)
58. Erie, D. A., O. Hajiseyedjavadi, M. C. Young & P. H. von Hippel: Multiple RNA polymerase conformations and GreA: control of the fidelity of transcription. Science 262, 867-73 (1993)
59. Shaw, R. J., N. D. Bonawitz & D. Reines: Use of an in vivo reporter assay to test for transcriptional and translational fidelity in yeast. J Biol Chem 277, 24420-6 (2002)
60. Linton, M. F., M. Raabe, V. Pierotti & S. G. Young: Reading-frame restoration by transcriptional slippage at long stretches of adenine residues in mammalian cells. J Biol Chem 272, 14127-32 (1997)
61. Wagner, L. A., R. B. Weiss, R. Driscoll, D. S. Dunn & R. F. Gesteland: Transcriptional slippage occurs during elongation at runs of adenine or thymine in Escherichia coli. Nucleic Acids Res 18, 3529-35 (1990)
62. Hajjar, A. M. & M. L. Linial: Modification of retroviral RNA by double-stranded RNA adenosine deaminase. J Virol 69, 5878-82 (1995)
63. Felder, M. P., D. Laugier, B. Yatsula, P. Dezelee, G. Calothy & M. Marx: Functional and biological properties of an avian variant long terminal repeat containing multiple A to G conversions in the U3 sequence. J Virol 68, 4759-67 (1994)
64. Julias, J. G., T. Kim, G. Arnold & V. K. Pathak: The antiretrovirus drug 3′-azido-3′-deoxythymidine increases the retro virus mutation rate. J Virol 71, 4254-63 (1997)
65. LaCasse, R. A., K. M. Remington & T. W. North: The mutation frequency of feline immunodeficiency virus enhanced by 3′-azido-3′- deoxythymidine. J Acquir Immune Defic Syndr Hum Retrovirol 12, 26-32 (1996)
66. Mansky, L. M. & 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, 9532-9 (2000)
67. Dougherty, J. P. & H. M. Temin: Determination of the rate of base-pair substitution and insertion mutations in retrovirus replication. J Virol 62, 2817-22 (1988)
68. Bebenek, K., 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, 16948-56 (1989)
69. Gabriel, A., M. Willems, E. H. Mules & J. D. Boeke: Replication infidelity during a single cycle of Tyl retrotransposition. Proc Natl Acad Sci USA 93, 7767-71 (1996)
70. Preston, B. D., B. J. Poiesz & L. A. Loeb: Fidelity of HIV-1 reverse transcriptase. Science 242, 1168-71 (1988)
71. Dougherty, J. P. & H. M. Temin: High mutation rate of a spleen necrosis virus-based retrovirus vector. Mol Cell Biol 6, 4387-95 (1986)
72. Ji, J. P. & L. A. Loeb: Fidelity of HIV-1 reverse transcriptase copying RNA in vitro. Biochemistry 31, 954-8 (1992)
73. Roberts, J. D., B. D. Preston, L. A. Johnston, A. Soni, L. A. Loeb & T. A. Kunkel: Fidelity of two retro viral reverse transcriptases during DNA-dependent DNA synthesis in vitro. Mol Cell Biol 9, 469-76 (1989)
74. Boyer, P. L. & 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, 6494-500 (2000)
75. Stuke, A. W., O. Ahmad-Omar, K. Hoefer, G. Hunsmann & K. D. Jentsch: Mutations in the SIV env and the M13 lacZa gene generated in vitro by reverse transcriptases and DNA polymerases. Arch Virol 142, 1139-54 (1997)
76. Bakhanashvili, M. & A. Hizi: The fidelity of the reverse transcriptases of human immunodeficiency viruses and murine leukemia virus, exhibited by the mispair extension frequencies, is sequence dependent and enzyme related. FEBS Lett 319, 201-5 (1993)
77. Varela-Echavarria, A., 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, 24681-8 (1992)
78. Yu, H. & M. F. Goodman: Comparison of HIV-1 and avian myeloblastosis virus reverse transcriptase fidelity on RNA and DNA templates. J Biol Chem 267, 10888-96 (1992)
79. Eckert, K. A. & T. A. Kunkel: Fidelity of DNA synthesis catalyzed by human DNA polymerase alpha and HIV-1 reverse transcriptase: effect of reaction pH. Nucleic Acids Res 21, 5212-20 (1993)
80. Brosius, S., F. Grosse & G. Krauss: Subspecies of DNA polymerase alpha from calf thymus with different fidelity in copying synthetic template-primers. Nucleic Acids Res 11, 193-202 (1983)
81. Beckman, R. A., A. S. Mildvan & L. A. Loeb: On the fidelity of DNA replication: manganese mutagenesis in vitro. Biochemistry 24, 5810-7 (1985)
82. Bebenek, K., J. D. Roberts & T. A. Kunkel: The effects of dNTP pool imbalances on frameshift fidelity during DNA replication. J Biol Chem 267, 3589-96 (1992)
83. Pham, P. T., M. W. Olson, C. S. McHenry & R. M. Schaaper: The base substitution and frameshift fidelity of Escherichia coli DNA polymerase III holoenzyme in vitro. J Biol Chem 273, 23575-84 (1998)
84. Halvas, E. K., 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, 10349-58 (2000)
85. Halvas, E. K., 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, 312-9 (2000)
86. Parthasarathi, S., A. Varela-Echavarria, 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, 7991-8000 (1995)
87. Kati, W. M., K. A. Johnson, L. F. Jerva & K. S. Anderson: Mechanism and fidelity of HIV reverse transcriptase. J Biol Chem 267, 25988-97 (1992)
88. Kerr, S. G. & K. S. Anderson: RNA dependent DNA replication fidelity of HIV-1 reverse transcriptase: evidence of discrimination between DNA and RNA substrates. Biochemistry 36, 14056-63 (1997)
89. Bakhanashvili, M. & A. Hizi: Fidelity of DNA synthesis exhibited in vitro by the reverse transcriptase of the lentivirus equine infectious anemia virus. Biochemistry 32, 7559-67 (1993)
90. Bakhanashvili, M. & 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, 289-93 (1992)
91. Bakhanashvili, M. & A. Hizi: Fidelity of the reverse transcriptase of human immunodeficiency virus type 2. FEBS Lett 306, 151-6 (1992)
92. Pathak, V. K. & W. S. Hu: "Might as well jump!" Template switching by retroviral reverse transcriptase, defective genome formation, and recombination. Seminars in virology 8, 141-150 (1997)
93. Pathak, V. K. & H. M. Temin: 5-Azacytidine and RNA secondary structure increase the retrovirus mutation rate. J Virol 66, 3093-100 (1992)
94. Burns, D. P. & H. M. Temin: High rates of frameshift mutations within homo-oligomeric runs during a single cycle of retroviral replication. J Virol 68, 4196-203 (1994)
95. Martinez, M. A., J. P. Vartanian & S. Wain-Hobson: Hypermutagenesis of RNA using human immunodeficiency virus type 1 reverse transcriptase and biased dNTP concentrations. Proc Natl Acad Sci USA 91, 11787-91 (1994)
96. Temin, H. M.: Retrovirus variation and reverse transcription: abnormal strand transfers result in retrovirus genetic variation. Proc Natl Acad Sci U S A 90, 6900-3 (1993)
97. Ding, J., K. Das, Y. Hsiou, S. G. Sarafianos, A. D. Clark, Jr., A. Jacobo-Molina, 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 A resolution. J Mol Biol 284, 1095-111 (1998)
98. Huang, H., 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, 1669-75 (1998)
99. Sarafianos, S. G., 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, 1449-61 (2001)
100. Jacobo-Molina, A., J. Ding, R. G. Nanni, A. D. Clark, Jr., X. Lu, C. Tantillo, R. L. Williams, G. Kamer, A. L. Ferris, P. Clark & et al.: Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA. Proc Natl Acad Sci U S A 90, 6320-4 (1993)
101. Smerdon, S. J., J. Jager, J. Wang, L. A. Kohlstaedt, A. J. Chirino, J. M. Friedman, P. A. Rice & T. A. Steitz: Structure of the binding site for nonnucleoside inhibitors of the reverse transcriptase of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 91, 3911-5 (1994)
102. Georgiadis, M. M., S. M. Jessen, C. M. Ogata, A. Telesnitsky, S. P. Goff & W. A. Hendrickson: Mechanistic implications from the structure of a catalytic fragment of Moloney murine leukemia virus reverse transcriptase. Structure 3, 879-92 (1995)
103. Najmudin, S., M. L. Cote, D. Sun, S. Yohannan, S. P. Montano, J. Gu & M. M. Georgiadis: Crystal structures of an N-terminal fragment from Moloney murine leukemia virus reverse transcriptase complexed with nucleic acid: functional implications for template-primer binding to the fingers domain. J Mol Biol 296, 613-32 (2000)
104. Zhang, W. H., E. S. Svarovskaia, R. Barr & V. K. Pathak: Y586F mutation in murine leukemia virus reverse transcriptase decreases fidelity of DNA synthesis in regions associated with adenine-thymine tracts. Proc Natl Acad Sci U S A 99, 10090-5 (2002)
105. Kaushik, N., 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, 5155-65 (2000)
106. Taube, R., 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, 106-14 (1997)
107. Wisniewski, M., C. Palaniappan, Z. Fu, S. F. 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, 28175-84 (1999)
108. Gutierrez-Rivas, M. & L. Menendez-Arias: A mutation in the primer grip region of HIV-1 reverse transcriptase that confers reduced fidelity of DNA synthesis. Nucleic Acids Res 29, 4963-72 (2001)
109. Hermann, T., T. Meier, M. Gotte & H. Heumann: The 'helix clamp' in HIV-1 reverse transcriptase: a new nucleic acid binding motif common in nucleic acid polymerases. Nucleic Acids Res 22, 4625-33 (1994)
110. Hermann, T. & H. Heumann: Strained template under the thumbs. How reverse transcriptase of human immunodeficiency virus type 1 moves along its template. Eur J Biochem 242, 98-103 (1996)
111. Bebenek, K., W. A. Beard, T. A. Darden, L. Li, R. Prasad, B. A. Luton, D. G. Gorenstein, S. H. Wilson & T. A. Kunkel: A minor groove binding track in reverse transcriptase. Nat Struct Biol 4, 194-7 (1997)
112. Julias, J. G., M. J. McWilliams, S. G. Sarafianos, E. Arnold & S. H. Hughes: Mutations in the RNase H domain of HIV-1 reverse transcriptase affect the initiation of DNA synthesis and the specificity of RNase H cleavage in vivo. Proc Natl Acad Sci U S A 99, 9515-20 (2002)
113. Timsit, Y.: DNA structure and polymerase fidelity. J Mol Biol 293, 835-53 (1999)
114. Leider, J. M., P. Palese & F. I. Smith: Determination of the mutation rate of a retrovirus. J Virol 62, 3084-91 (1988)
115. Ji, J. & L. A. Loeb: Fidelity of HIV-1 reverse transcriptase copying a hypervariable region of the HIV-1 env gene. Virology 199, 323-30 (1994)
116. Bakhanashvili, M. & 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, 9393-8 (1992)
117. Avidan, O., M. E. Meer, I. Oz & A. Hizi: The processivity and fidelity of DNA synthesis exhibited by the reverse transcriptase of bovine leukemia virus. Eur J Biochem 269, 859-67 (2002)
118. Boutabout, M., M. Wilhelm & F. X. Wilhelm: DNA synthesis fidelity by the reverse transcriptase of the yeast retrotransposon Tyl. Nucleic Acids Res 29, 2217-22 (2001)
119. Diamond, T. L., J. Kimata & B. Kirn: Identification of a simian immunodeficiency virus reverse transcriptase variant with enhanced replicational fidelity in the late stage of viral infection. J Biol Chem 276, 23624-31 (2001)
120. Taube, R., 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, 1032-9 (1998)
121. Fisher, T. S. & V. R. Prasad: Substitutions of Phe61 located in the vicinity of template 5′ overhang influence polymerase fidelity and nucleoside analog sensitivity of HIV-1 reverse transcriptase. J Biol Chem (2002)
122. Shah, F. S., 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, 27037-44 (2000)
123. Lewis, D. A., 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, 32924-30 (1999)
124. Jonckheere, H., E. De Clercq & J. Anne: 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, 2658-65 (2000)
125. Kirn, B., 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, 5831-9 (1998)
126. Kim, B., 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, 27666-73 (1999)
127. Drosopoulos, W. C. & 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, 4224-30 (1998)
128. Hamburgh, M. E., 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, 4389-94 (1998)
129. Drosopoulos, W. C. & V. R. Prasad: Increased polymerase fidelity of E89G, a nucleoside analog-resistant variant of human immunodeficiency virus type 1 reverse transcriptase. J Virol 70, 4834-8 (1996)
130. Cases-Gonzalez, C. E., M. Gutierrez-Rivas & L. Menendez-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, 19759-67 (2000)
131. Martin-Hernandez, A. M., M. Gutierrez-Rivas, E. Domingo & L. Menendez-Arias: Mispair extension fidelity of human immunodeficiency virus type 1 reverse transcriptases with amino acid substitutions affecting Tyr115. Nucleic Acids Res 25, 1383-9 (1997)
132. Rezende, L. F., 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, 2890-5 (1998)
133. Weiss, K. K., R. A. Bambara & B. Kim: Mechanistic role of residue Q151 in error prone DNA synthesis by human immunodeficiency virus type 1 reverse transcriptase (HIV-1 RT): Pre-steady state kinetic study of the Q151N HIV-1 RT mutant with increased fidelity. J Biol Chem (2002)
134. Weiss, K. K., 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 beta 8-alpha E loop in fidelity, processivity, and substrate interactions. Biochemistry 39, 10684-94 (2000)
135. Gutierrez-Rivas, M., A. Ibanez, M. A. Martinez, E. Domingo & L. Menendez-Arias: Mutational analysis of Phe160 within the "palm" subdomain of human immunodeficiency virus type 1 reverse transcriptase. J Mol Biol 290, 615-25 (1999)
136. Bakhanashvili, M., 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, 257-62 (1996)
137. Hsu, M., 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, 4532-6 (1997)
138. Oude Essink, B. B., N. K. Back & B. Berkhout: Increased polymerase fidelity of the 3TC-resistant variants of HIV-1 reverse transcriptase. Nucleic Acids Res 25, 3212-7 (1997)
139. Wainberg, M. A., W. C. Drosopoulos, H. Salomon, M. Hsu, G. Borkow, M. 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, 1282-5 (1996)
140. Pandey, V. N., N. Kaushik, N. Rege, S. G. Sarafianos, P. N. 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, 2168-79 (1996)
141. Feng, J. Y. & 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, 9440-8 (1999)
142. Rezende, L. F., W. C. Drosopoulos & V. R. Prasad: The influence of 3TC resistance mutation M1841 on the fidelity and error specificity of human immunodeficiency virus type 1 reverse transcriptase. Nucleic Acids Res 26, 3066-72 (1998)
143. Oude Essink, B. B. & B. Berkhout: The fidelity of reverse transcription differs in reactions primed with RNA versus DNA primers. J Biomed Sci 6, 121-32 (1999)
144. Bebenek, K., 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, 19516-23 (1995)
145. Beard, W. A., 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, 12213-20 (1996)