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Science 25 November 1988:
Vol. 242. no. 4882, pp. 1171 - 1173
DOI: 10.1126/science.2460925
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Articles

Science, Vol 242, Issue 4882, 1171-1173
Copyright © 1988 by American Association for the Advancement of Science

articles

The accuracy of reverse transcriptase from HIV-1

JD Roberts, K Bebenek, and TA Kunkel

Laboratory of Molecular Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, NC 27709.

A study was conducted to determine the fidelity of DNA synthesis catalyzed in vitro by the reverse transcriptase from a human immunodeficiency virus type 1 (HIV-1). Like other retroviral reverse transcriptases, the HIV-1 enzyme does not correct errors by exonucleolytic proofreading. Measurements with M13mp2-based fidelity assays indicated that the HIV-1 enzyme, isolated either from virus particles or from Escherichia coli cells infected with a plasmid expressing the cloned gene, was exceptionally inaccurate, having an average error rate per detectable nucleotide incorporated of 1/1700. It was, in fact, the least accurate reverse transcriptase described to date, one-tenth as accurate as the polymerases isolated from avian myeloblastosis or murine leukemia viruses, which have average error rates of approximately 1/17,000 and approximately 1/30,000, respectively. DNA sequence analyses of mutations generated by HIV-1 polymerase showed that base substitution, addition, and deletion errors were all produced. Certain template positions were mutational hotspots where the error rate could be as high as 1 per 70 polymerized nucleotides. The data are consistent with the notion that the exceptional diversity of the HIV-1 genome results from error-prone reverse transcription.


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J. Virol. 74, 9306-9312
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J. Virol. 74, 6494-6500
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J. Biol. Chem. 274, 32924-32930
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Mutations in the Primer Grip Region of HIV Reverse Transcriptase Can Increase Replication Fidelity.
M. Wisniewski, C. Palaniappan, Z. Fu, S. F. J. Le Grice, P. Fay, and R. A. Bambara (1999)
J. Biol. Chem. 274, 28175-28184
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W.-Y. Gao, D. G. Johns, M. Tanaka, and H. Mitsuya (1999)
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Coevolutionary analysis of resistance-evading peptidomimetic inhibitors of HIV-1 protease.
C. D. Rosin, R. K. Belew, G. M. Morris, A. J. Olson, and D. S. Goodsell (1999)
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Lethal mutagenesis of HIV with mutagenic nucleoside analogs.
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D. Harris, N. Kaushik, P. K. Pandey, P. N. S. Yadav, and V. N. Pandey (1998)
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Unblocking of chain-terminated primer by HIV-1 reverse transcriptase through a nucleotide-dependent mechanism.
P. R. Meyer, S. E. Matsuura, A. G. So, and W. A. Scott (1998)
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Deoxyribonucleoside Triphosphate Pool Imbalances In Vivo Are Associated with an Increased Retroviral Mutation Rate.
J. G. Julias and V. K. Pathak (1998)
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Dominance of the E89G Substitution in HIV-1 Reverse Transcriptase in Regard to Increased Polymerase Processivity and Patterns of Pausing.
Y. Quan, P. Inouye, C. Liang, L. Rong, M. Gotte, and M. A. Wainberg (1998)
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A. B. van 't Wout, H. Blaak, L. J. Ran, M. Brouwer, C. Kuiken, and H. Schuitemaker (1998)
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L. F. Rezende, K. Curr, T. Ueno, H. Mitsuya, and V. R. Prasad (1998)
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Insertions into the beta 3-beta 4 Hairpin Loop of HIV-1 Reverse Transcriptase Reveal a Role for Fingers Subdomain in Processive Polymerization.
Y. Kew, L. R. Olsen, A. J. Japour, and V. R. Prasad (1998)
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A. Bhui-Kaur, M. F. Goodman, and J. Tower (1998)
Mol. Cell. Biol. 18, 1436-1443
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Flexible Positioning of the Telomerase-Associated Nuclease Leads to Preferential Elimination of Nontelomeric DNA.
E. C. Greene, J. Bednenko, and D. E. Shippen (1998)
Mol. Cell. Biol. 18, 1544-1552
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High Fidelity of Internal Strand Transfer Catalyzed by Human Immunodeficiency Virus Reverse Transcriptase.
J. DeStefano, J. Ghosh, B. Prasad, and A. Raja (1998)
J. Biol. Chem. 273, 1483-1489
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Hydrogen bonding revisited: Geometric selection as a principal determinant of DNA replication fidelity.
M. F. Goodman (1997)
PNAS 94, 10493-10495
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Stereoisomers of Deoxynucleoside 5'-Triphosphates as Substrates for Template-dependent and -independent DNA Polymerases.
D. G. Semizarov, A. A. Arzumanov, N. B. Dyatkina, A. Meyer, S. Vichier-Guerre, G. Gosselin, B. Rayner, J.-L. Imbach, and A. A. Krayevsky (1997)
J. Biol. Chem. 272, 9556-9560
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Differential Tolerance to DNA Polymerization by HIV-1 Reverse Transcriptase on N6 Adenine C10R and C10S Benzo[a]pyrene-7,8-dihydrodiol 9,10-Epoxide-adducted Templates.
P. Chary, C. M. Harris, T. M. Harris, and R. S. Lloyd (1997)
J. Biol. Chem. 272, 5805-5813
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Incorporation of the Guanosine Triphosphate Analogs 8-Oxo-dGTP and 8-NH2-dGTP by Reverse Transcriptases and Mammalian DNA Polymerases.
A. S. Kamath-Loeb, A. Hizi, H. Kasai, and L. A. Loeb (1997)
J. Biol. Chem. 272, 5892-5898
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Evolutionary mechanisms and population dynamics of the third variable envelope region of HIV within single hosts.
Y. Yamaguchi and T. Gojobori (1997)
PNAS 94, 1264-1269
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Misincorporation by HIV-1 Reverse Transcriptase Promotes Recombination via Strand Transfer Synthesis.
C. Palaniappan, M. Wisniewski, W. Wu, P. J. Fay, and R. A. Bambara (1996)
J. Biol. Chem. 271, 22331-22338
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Enzyme-DNA Interactions Required for Efficient Nucleotide Incorporation and Discrimination in Human DNA Polymerase beta.
W. A. Beard, W. P. Osheroff, R. Prasad, M. R. Sawaya, M. Jaju, T. G. Wood, J. Kraut, T. A. Kunkel, and S. H. Wilson (1996)
J. Biol. Chem. 271, 12141-12144
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Role of the ``Helix Clamp'' in HIV-1 Reverse Transcriptase Catalytic Cycling as Revealed by Alanine-scanning Mutagenesis.
W. A. Beard, D. T. Minnick, C. L. Wade, R. Prasad, R. L. Won, A. Kumar, T. A. Kunkel, and S. H. Wilson (1996)
J. Biol. Chem. 271, 12213-12220
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Enzymatic Characterization of Human Immunodeficiency Virus Type 1 Reverse Transcriptase Resistant to Multiple 2`,3`-Dideoxynucleoside 5`-Triphosphates.
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Reduced Frameshift Fidelity and Processivity of HIV-1 Reverse Transcriptase Mutants Containing Alanine Substitutions in Helix H of the Thumb Subdomain.
K. Bebenek, W. A. Beard, J. R. Casas-Finet, H.-R. Kim, T. A. Darden, S. H. Wilson, and T. A. Kunkel (1995)
J. Biol. Chem. 270, 19516-19523
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Influence of Human Immunodeficiency Virus Nucleocapsid Protein on Synthesis and Strand Transfer by the Reverse Transcriptase in Vitro.
L. Rodrguez-Rodrguez, Z. Tsuchihashi, G. M. Fuentes, R. A. Bambara, and P. J. Fay (1995)
J. Biol. Chem. 270, 15005-15011
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Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase.
J. Peliska and S. Benkovic (1992)
Science 258, 1112-1118
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Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor.
L. Kohlstaedt, J Wang, J. Friedman, P. Rice, and T. Steitz (1992)
Science 256, 1783-1790
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Selective transmission of human immunodeficiency virus type-1 variants from mothers to infants.
S. Wolinsky, C. Wike, B. Korber, C Hutto, W. Parks, L. Rosenblum, K. Kunstman, M. Furtado, and J. Munoz (1992)
Science 255, 1134-1137
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Antigenic diversity thresholds and the development of AIDS.
M. Nowak, R. Anderson, A. McLean, T. Wolfs, J Goudsmit, and R. May (1991)
Science 254, 963-969
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Resistance to ddI and sensitivity to AZT induced by a mutation in HIV-1 reverse transcriptase.
M. St Clair, J. Martin, G Tudor-Williams, M. Bach, C. Vavro, D. King, P Kellam, S. Kemp, and B. Larder (1991)
Science 253, 1557-1559
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DNA polymerase fidelity and the polymerase chain reaction..
K A Eckert and T A Kunkel (1991)
Genome Res. 1, 17-24
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Molecular targets for AIDS therapy.
H Mitsuya, R Yarchoan, and S Broder (1990)
Science 249, 1533-1544
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Multiple mutations in HIV-1 reverse transcriptase confer high-level resistance to zidovudine (AZT).
B. Larder and S. Kemp (1989)
Science 246, 1155-1158
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Vertical-scanning Mutagenesis of a Critical Tryptophan in the "Minor Groove Binding Track" of HIV-1 Reverse Transcriptase. MAJOR GROOVE DNA ADDUCTS IDENTIFY SPECIFIC PROTEIN INTERACTIONS IN THE MINOR GROOVE.
G. J. Latham, E. Forgacs, W. A. Beard, R. Prasad, K. Bebenek, T. A. Kunkel, S. H. Wilson, and R. S. Lloyd (2000)
J. Biol. Chem. 275, 15025-15033
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Analysis of Efficiency and Fidelity of HIV-1 (+)-Strand DNA Synthesis Reveals a Novel Rate-limiting Step during Retroviral Reverse Transcription.