The double mutation L109M and R448M of HIV-1 reverse transcriptase decreases fidelity of DNA synthesis by promoting mismatch elongation

References

Álvarez, M., Barrioluengo, V., Afonso-Lehmann, R.N., and Menéndez-Arias, L. (2013). Altered error specificity of RNase H-deficient HIV-1 reverse transcriptases during DNA-dependent DNA synthesis. Nuc. Acids Res. 41, 4601–4612.10.1093/nar/gkt109Search in Google Scholar

Baltimore, D. (1970). Viral RNA-dependent DNA polymerase. Nature 226, 1209–1211.10.1038/2261209a0Search in Google Scholar

Basu, V.P., Song, M., Gao, L., Rigby, S.T., Hanson, M.N., and Bambara, R.A. (2008). Strand transfer events during HIV-1 reverse transcription. Virus Res. 134, 19–38.10.1016/j.virusres.2007.12.017Search in Google Scholar

Beard, W.A., Stahl, S.J., Kim, H.R., Bebenek, K., Kumar, A., Strub, M.P., Becerra, S.P., Kunkel, T.A., and Wilson, S.H. (1994). Structure/function studies of human immunodeficiency virus type 1 reverse transcriptase. Alanine scanning mutagenesis of an α-helix in the thumb subdomain. J. Biol. Chem. 269, 28091–28097.10.1016/S0021-9258(18)46899-8Search in Google Scholar

Bebenek, K., Pedersen, L.C., and Kunkel, T.A. (2011). Replication infidelity via a mismatch with Watson-Crick geometry. Proc. Natl. Acad. Sci. USA 108, 1862–1867.10.1073/pnas.1012825108Search in Google Scholar

Boyer, P.L., Ferris, A.L., Clark, P., Whitmer, J., Frank, P., Tantillo, C., Arnold, E., and Hughes, S.H. (1994). Mutational analysis of the fingers and palm subdomains of HIV-1 RT. J. Mol. Biol. 243, 472–483.10.1006/jmbi.1994.1673Search in Google Scholar

Creighton, S., Bloom, L.B., and Goodman, M.F. (1995). Gel fidelity assay measuring nucleotide misinsertion, exonucleolytic proofreading, and lesion bypass efficiencies. Methods Enzymol. 262, 232–256.10.1016/0076-6879(95)62021-4Search in Google Scholar

Cristofaro, J.V., Rausch, J.W., Le Grice, S.F., and DeStefano, J.J. (2002). Mutations in the ribonuclease H active site of HIV-RT reveal a role for this site in stabilizing enzyme-primer-template binding. Biochemistry 41, 10968–10975.10.1021/bi025871vSearch in Google Scholar PubMed

Das, K., Martinez, S.E., Bandwar, R.P., and Arnold, E. (2014). Structures of HIV-1 RT-RNA/DNA ternary complexes with dATP and nevirapine reveal conformational flexibility of RNA/DNA: insights into requirements for RNase H cleavage. Nuc. Acids Res. 42, 8125–8137.10.1093/nar/gku487Search in Google Scholar PubMed PubMed Central

Delarue, M., Poch, O., Tordo, N., Moras, D., and Argos, P. (1990). An attempt to unify the structure of all polymerases. Protein Engin. 3, 461–467.10.1093/protein/3.6.461Search in Google Scholar PubMed

di Marzo Veronese, F., Copeland, T.D., DeVico, A.L., Rahman, R., Oroszlan, S., Gallo, R.C., and Sarngadharan, M.G. (1986). Characterization of highly immunogenic p66/p51 as the reverse transcriptase of HTLV-III/LAV. Science 231, 1289–1291.10.1126/science.2418504Search in Google Scholar PubMed

Domingo, E. (2000). Viruses at the edge of adaptation. Virology 270, 251–253.10.1006/viro.2000.0320Search in Google Scholar PubMed

Gao, F., Chen, Y., Levy, D.N., Conway, J.A., Kepler, T.B., and Hui, H. (2004). Unselected mutations in the human immunodeficiency virus type 1 genome are mostly nonsynonymous and often deleterious. J. Virol. 78, 2426–2433.10.1128/JVI.78.5.2426-2433.2004Search in Google Scholar PubMed PubMed Central

Garforth, S.J., Domaoal, R.A., Lwatula, C., Landau, M.J., Meyer, A.J., Anderson, K.S., and Prasad, V.R. (2010). K65R andK65A substitutions in HIV-1 reverse transcriptase enhance polymerase fidelity by decreasingboth dNTP misinsertion and mispaired primer extension efficiencies. J. Mol. Biol. 401, 33–44.10.1016/j.jmb.2010.06.001Search in Google Scholar PubMed PubMed Central

Gonzales, M.J., Delwart, E., Rhee, S.-Y., Tsui, R., Zolopa, A.R., Taylor, J., and Shafer, R.W. (2003). Lack of detectable human immunodeficiency virus type 1 superinfection during 1072 person-years of observation. J. Infect. Dis. 188, 397–405.10.1086/376534Search in Google Scholar PubMed PubMed Central

Hu, W.-S. and Hughes, S.H. (2012). HIV-1 Reverse Transcription. Cold Spring Harb. Perspect. Med. 2, 1–22.10.1101/cshperspect.a006882Search in Google Scholar PubMed PubMed Central

Huang, H., Chopra, R., Verdine, G.L., and Harrison, S.C. (1998). Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282, 1669–1675.10.1126/science.282.5394.1669Search in Google Scholar PubMed

Hunter, W.N., Brown, T., Anand, N.N., and Kennard, O. (1986). Structure of an adenine:cytosine base pair in DNA and its implications for mismatch repair. Nature 320, 552–556.10.1038/320552a0Search in Google Scholar PubMed

Jozwiakowski, S.K. and Connolly, B.A. (2009). Plasmid-based lacZα assay for DNA polymerase fidelity: application to archaeal familiy-B DNA polymerase. Nuc. Acids Res. 37, 1–7.10.1093/nar/gkp494Search in Google Scholar PubMed PubMed Central

Julias, J.G., McWilliams, M.J., Sarafianos, S.G., Arnold, E., and Hughes, S.H. (2002). 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. USA 99, 9515–9520.10.1073/pnas.142123199Search in Google Scholar PubMed PubMed Central

Kati, W.M., Jonson, K.A., Jerva, L.F., and Anderson, K.S. (1992). Mechanism and fidelity of HIV reverse transcriptase. J. Biol. Chem. 267, 25988–25997.10.1016/S0021-9258(18)35706-5Search in Google Scholar

Katz, R.A. and Skalka, A.M. (1990). Generation of diversity in retroviruses. Annu. Rev. Genet. 24, 409–445.10.1146/annurev.ge.24.120190.002205Search in Google Scholar PubMed

Klumpp, K., Hang, J.Q., Rajendran, S., Yang, Y., Derosier, A., Wong Kai In, P., Overton, H., Parkes, K.E.B., Cammack, N., and Martin, J.A. (2003). Two-metal ion mechanism of RNA cleavage by HIV RNase H and mechanism-based design of selective HIV RNaseH inhibitors. Nuc. Acids Res. 31, 6852–6859.10.1093/nar/gkg881Search in Google Scholar PubMed PubMed Central

Kohlstaedt, L.A., Wang, J., Friedman, J.M., Rice, P.A., and Steitz, T.A. (1992). Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256, 1783–1790.10.1126/science.1377403Search in Google Scholar PubMed

Mansky, L.M. and Temin, H.M. (1995). Lower in vivo mutation rate of human immunodeficiency type 1 than predicted from the fidelity of purified reverse transcriptase. J. Virol. 69, 5087–5094.10.1128/jvi.69.8.5087-5094.1995Search in Google Scholar PubMed PubMed Central

Mansky, L.M., Le Rouzic, E., Benichou, S., and Gajary, L.C. (2003). Influence of reverse transcriptase variants, drugs, and Vpr on human immunodeficiency virus type 1 mutant frequencies. J. Virol. 77, 2071–2080.10.1128/JVI.77.3.2071-2080.2003Search in Google Scholar

Mbisa, J.L., Nikolenko, G.N., and Pathak, V.K. (2005). Mutations in the RNase H primer grip domain of murine leukemia virus reverse transcriptase decrease efficiency and accuracy of plus-strand DNA transfer. J. Virol. 79, 419–427.10.1128/JVI.79.1.419-427.2005Search in Google Scholar PubMed PubMed Central

Menéndez-Arias, L. (2009). Mutation rates and intrinsic fidelity of retroviral reverse transcriptases. Viruses 1, 1137–1165.10.3390/v1031137Search in Google Scholar PubMed PubMed Central

Nowak, M.A., May, R.M., and Anderson, R.M. (1990). The evolutionary dynamics of HIV-1 quasispecies and the development of immunodeficiency disease. AIDS 4, 1095–1103.10.1097/00002030-199011000-00007Search in Google Scholar PubMed

O’Neil, P.K., Sun, G., Yu, H., Ron, Y., Dougherty, J.P., and Preston, B.D. (2002). Mutational analysis of HIV-1 long terminal repeats to explore the relative contribution of reverse transcriptase and RNA polymerase II to viral mutagenesis. J. Biol. Chem. 277, 38053–38061.10.1074/jbc.M204774200Search in Google Scholar PubMed

Onafuwa-Nuga, A. and Telesnitsky, A. (2009). The remarkable frequency of human immunodeficiency virus type 1 genetic recombination. Microbiol. Mol. Biol. Rev. 73, 451–480.10.1128/MMBR.00012-09Search in Google Scholar PubMed PubMed Central

Patel, S.S., Wong, I., and Johnson, K.A. (1991). Pre-steady state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-deficient mutant. Biochemistry 30, 511–525.10.1021/bi00216a029Search in Google Scholar PubMed

Poch, O., Sauvaget, I., Delarue, M., and Tordo, N. (1989). Identification of four conserved motifs among RNA-dependent polymerase encoding elements. EMBO J. 8, 3867–3874.10.1002/j.1460-2075.1989.tb08565.xSearch in Google Scholar PubMed PubMed Central

Preston, B.D., Poiesz, B.J., and Loeb, L.A. (1988). Fidelity of HIV-1 reverse trancriptase. Science 242, 1168–1171.10.1126/science.2460924Search in Google Scholar PubMed

Rasband, W. (2004). ImageJ software, v 1.32. Available from: http://rsb.info.nih.gov/. Accessed on August 05, 2015.Search in Google Scholar

Reardon, J.E. (1992). Human immunodeficiency virus reverse transcriptase: steady-state and pre-steady-state kinetics of nucleotide incorporation. Biochemistry 31, 4473–4479.10.1021/bi00133a013Search in Google Scholar PubMed

Rhee, S.-Y., Gonzales, M.J., Kantor, R., Betts, B.J., Raveela, J., and Shafer, R.W. (2003). Human immunodeficiency reverse transcriptase and protease database. Nuc. Acids Res. 31, 298–303.10.1093/nar/gkg100Search in Google Scholar PubMed PubMed Central

Rittinger, K., Divita, G., and Goody, R.S. (1995). Human immunodeficiency virus reverse transcriptase substrate-induced conformational changes and the mechanism of inhibition by nonnucleoside inhibitors. Proc. Natl. Acad. Sci. USA 92, 8046–8049.10.1073/pnas.92.17.8046Search in Google Scholar PubMed PubMed Central

Roberts, J.D., Bebenek, K., and Kunkel, T.A. (1988). The accuracy of reverse transcriptase from HIV-1. Science 242, 1171–1173.10.1126/science.2460925Search in Google Scholar PubMed

Sarafianos, S.G., Das, K., Tantillo, C., Clark, A.D., Ding, J., Whitcomb, J.M., Boyer, P.L., Hughes, S.H., and Arnold, E. (2001). Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J. 20, 1449–1461.10.1093/emboj/20.6.1449Search in Google Scholar PubMed PubMed Central

Shafer, R.W. (2006). Rationale and uses of a public HIV drug-resistance database. J. Infect. Dis. 194, S51–S58.10.1086/505356Search in Google Scholar PubMed PubMed Central

Shafer, R.W., Rhee, S.-Y., Kiuchi, M., and Liu, T. (2008). Stanford Drug Resistance Database. Available at: http://hivdb.stanford.edu/. Accessed on August 05, 2015.Search in Google Scholar

Söte, S., Schlicke, M., Kleine, S., and Brakmann, S. (2011). Directed evolution of an error-prone T7 DNA polymerase that attenuates viral replication. ChemBioChem 12, 1551–1558.10.1002/cbic.201000799Search in Google Scholar PubMed

Stumpp, S.N., Heyn, B., and Brakmann, S. (2010). Activity-based selection of HIV-1 reverse transcriptase variants with decreased polymerization fidelity. Biol. Chem. 391, 665–674.10.1515/bc.2010.067Search in Google Scholar PubMed

Temin, H.M. and Mizutani, S. (1970). RNA-dependent DNA polymerase in virions of Rous carcinoma virus. Nature 226, 1211–1213.10.1038/2261211a0Search in Google Scholar PubMed

Watson, J.D. and Crick, F.H. (1953). Molecular structure of nucleic acids: a structure for deoxyribonucleic acid. Nature 171, 737–738.10.1038/171737a0Search in Google Scholar PubMed

Wong, I., Patel, S.S., and Johnson, K.A. (1991). An induced-fit kinetic mechanism for DNA replication fidelity: direct measurement by single-turnover kinetics. Biochemistry 30, 526–537.10.1021/bi00216a030Search in Google Scholar PubMed

Wrobel, J.A., Chao, S.F., Conrad, M.J., Merker, J.D., Swanstrom, R., Pielak, G.J., and Hutchison, C.A. (1998). A genetic approach for identifying critical residues in the fingers and palm subdomains of HIV-1 reverse transcriptase. Proc. Natl. Acad. Sci. USA 95, 638–645.10.1073/pnas.95.2.638Search in Google Scholar PubMed PubMed Central

Zhang, W., Svarovskaia, E.S., Barr, R., and Pathak, V.K. (2002). Y586F mutation in murine leukemia virus reverse transcriptase decreases fidelity of DNA synthesis in regions associated with adenine-thymine tracts. Proc. Natl. Acad. Sci. USA 99, 10090–10095.10.1073/pnas.152186199Search in Google Scholar PubMed PubMed Central