Lys66 residue as a determinant of high mismatch extension and misinsertion rates of HIV-1 reverse transcriptase

FEBS Journal

Volumn 279, Issue 21, 2012, Pages 4010-4024

  Lwatula, Chisanga ^a   Garforth, Scott J ^a   Prasad, Vinayaka R ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

HIV 1; misinsertion efficiency; mismatch extension efficiency; polymerase fidelity; reverse transcriptase

Indexed keywords

AMINO ACID; EFAVIRENZ; LYS66 RESIDUE; RNA DIRECTED DNA POLYMERASE; RNA DIRECTED DNA POLYMERASE INHIBITOR; STAVUDINE TRIPHOSPHATE; TENOFOVIR DIPHOSPHATE; UNCLASSIFIED DRUG; ZIDOVUDINE 5' TRIPHOSPHATE;

AMINO ACID SUBSTITUTION; ANTIVIRAL RESISTANCE; ANTIVIRAL SUSCEPTIBILITY; ARTICLE; BINDING KINETICS; CONTROLLED STUDY; ESCHERICHIA COLI; MISINSERTION; MISMATCH EXTENSION; NONHUMAN; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; STEADY STATE; VIRUS MUTANT; WILD TYPE;

AMINO ACID SUBSTITUTION; ANTI-HIV AGENTS; DNA MISMATCH REPAIR; DRUG RESISTANCE, VIRAL; HIV REVERSE TRANSCRIPTASE; HUMANS; HYDROXYL RADICAL; LYSINE; MUTAGENESIS, INSERTIONAL; MUTATION; NUCLEOSIDES; PROTEIN CONFORMATION; STRUCTURE-ACTIVITY RELATIONSHIP; TEMPLATES, GENETIC;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84867580173     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08807.x     Document Type: Article

References (48)

1. Kohlstaedt LA, Wang J, Friedman JM, Rice PA, &, Steitz TA, (1992) Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256, 1783-1790.
2. Sawaya MR, Prasad R, Wilson SH, Kraut J, &, Pelletier H, (1997) Crystal structures of human DNA polymerase beta complexed with gapped and nicked DNA: evidence for an induced fit mechanism. Biochemistry 36, 11205-11215.
3. Rittinger K, Divita G, &, Goody RS, (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.
4. Doublié S, Tabor S, Long AM, Richardson CC, &, Ellenberger T, (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 A resolution. Nature 391, 251-258.
5. Mansky LM, &, Temin HM, (1995) Lower in vivo mutation rate of human immunodeficiency virus type 1 than that predicted from the fidelity of purified reverse transcriptase. J Virol 69, 5087-5094.
6. Coffin JM, (1995) HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267, 483-489.
7. Preston BD, Poiesz BJ, &, Loeb LA, (1988) Fidelity of HIV-1 reverse transcriptase. Science 242, 1168-1171.
8. Hsieh JC, Zinnen S, &, Modrich P, (1993) Kinetic mechanism of the DNA-dependent DNA polymerase activity of human immunodeficiency virus reverse transcriptase. J Biol Chem 268, 24607-24613.
9. Kati WM, Johnson KA, Jerva LF, &, Anderson KS, (1992) Mechanism and fidelity of HIV reverse transcriptase. J Biol Chem 267, 25988-25997.
10. Joyce CM, &, Benkovic SJ, (2004) DNA polymerase fidelity: kinetics, structure, and checkpoints. Biochemistry 43, 14317-14324.
11. Zinnen S, Hsieh JC, &, Modrich P, (1994) Misincorporation and mispaired primer extension by human immunodeficiency virus reverse transcriptase. J Biol Chem 269, 24195-24202.
12. Huang H, Chopra R, Verdine GL, &, Harrison SC, (1998) Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282, 1669.
13. Sarafianos SG, Clark AD, Das K, Tuske S, Birktoft JJ, Ilankumaran P, Ramesha AR, Sayer JM, Jerina DM, Boyer PL, et al,. (2002) Structures of HIV-1 reverse transcriptase with pre- and post-translocation AZTMP-terminated DNA. EMBO J 21, 6614-6624.
14. Boyer PL, Sarafianos SG, Arnold E, &, Hughes SH, (2001) Selective excision of AZTMP by drug-resistant human immunodeficiency virus reverse transcriptase. J Virol 75, 4832-4842.
15. Roberts JD, Bebenek K, &, Kunkel TA, (1988) The accuracy of reverse transcriptase from HIV-1. Science 242, 1171-1173.
16. Yu H, &, Goodman MF, (1992) Comparison of HIV-1 and avian myeloblastosis virus reverse transcriptase fidelity on RNA and DNA templates. J Biol Chem 267, 10888-10896.
17. Perrino FW, Preston BD, Sandell LL, &, Loeb LA, (1989) Extension of mismatched 3' termini of DNA is a major determinant of the infidelity of human immunodeficiency virus type 1 reverse transcriptase. Proc Natl Acad Sci USA 86, 8343-8347.
18. Shah FS, Curr KA, Hamburgh ME, Parniak M, Mitsuya H, Arnez JG, &, Prasad VR, (2000) 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, 27037-27044.
19. Garforth SJ, Kim TW, Parniak MA, Kool ET, &, Prasad VR, (2007) Site-directed mutagenesis in the fingers subdomain of HIV-1 reverse transcriptase reveals a specific role for the beta3-beta4 hairpin loop in dNTP selection. J Mol Biol 365, 38-49.
20. Tuske S, Sarafianos SG, Clark AD, Ding J, Naeger LK, White KL, Miller MD, Gibbs CS, Boyer PL, Clark P, et al,. (2004) Structures of HIV-1 RT-DNA complexes before and after incorporation of the anti-AIDS drug tenofovir. Nat Struct Mol Biol 11, 469-474.
21. Das K, Bandwar RP, White KL, Feng JY, Sarafianos SG, Tuske S, Tu X, Clark AD, Boyer PL, Hou X, et al,. (2009) Structural basis for the role of the K65R mutation in HIV-1 reverse transcriptase polymerization, excision antagonism, and tenofovir resistance. J Biol Chem 284, 35092-35100.
22. Das K, Martinez SE, Bauman JD, &, Arnold E, (2012) HIV-1 reverse transcriptase complex with DNA and nevirapine reveals non-nucleoside inhibition mechanism. Nat Struct Mol Biol 19, 253-259.
23. Rubinek T, Bakhanashvili M, Taube R, Avidan O, &, Hizi A, (1997) The fidelity of 3' misinsertion and mispair extension during DNA 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, 238-247.
24. Matamoros T, Kim B, &, Menéndez-Arias L, (2008) Mechanistic insights into the role of Val75 of HIV-1 reverse transcriptase in misinsertion and mispair extension fidelity of DNA synthesis. J Mol Biol 375, 1234-1248.
25. Sluis-Cremer N, Arion D, Kaushik N, Lim H, &, Parniak MA, (2000) Mutational analysis of Lys65 of HIV-1 reverse transcriptase. Biochem J 348 (Pt 1), 77-82.
26. Garforth SJ, Domaoal RA, Lwatula C, Landau MJ, Meyer AJ, Anderson KS, &, Prasad VR, (2010) K65R and K65A Substitutions in HIV-1 Reverse Transcriptase Enhance Polymerase Fidelity by Decreasing Both dNTP Misinsertion and Mispaired Primer Extension Efficiencies. J Mol Biol 401, 33-44.
27. Kim B, Hathaway TR, &, Loeb LA, (1998) Fidelity of mutant HIV-1 reverse transcriptases: interaction with the single-stranded template influences the accuracy of DNA synthesis. Biochemistry 37, 5831-5839.
28. Jacobo-Molina A, Ding J, Nanni RG, Clark AD, Lu X, Tantillo C, Williams RL, Kamer G, Ferris AL, &, Clark P, (1993) 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 USA 90, 6320-6324.
29. Ding J, Das K, Hsiou Y, Sarafianos SG, Clark AD, Jacobo-Molina A, Tantillo C, Hughes SH, &, Arnold E, (1998) 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, 1095-1111.
30. Xiong Y, &, Eickbush TH, (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9, 3353-3362.
31. Rhee SY, Gonzales MJ, Kantor R, Betts BJ, Ravela J, &, Shafer RW, (2003) Human immunodeficiency virus reverse transcriptase and protease sequence database. Nucleic Acids Res 31, 298-303.
32. Shafer RW, Jung DR, &, Betts BJ, (2000) Human immunodeficiency virus type 1 reverse transcriptase and protease mutation search engine for queries. Nat Med 6, 1290-1292.
33. Mendelman LV, Petruska J, &, Goodman MF, (1990) Base mispair extension kinetics. Comparison of DNA polymerase alpha and reverse transcriptase. J Biol Chem 265, 2338-2346.
34. Müller B, Restle T, Reinstein J, &, Goody RS, (1991) Interaction of fluorescently labeled dideoxynucleotides with HIV-1 reverse transcriptase. Biochemistry 30, 3709-3715.
35. Pandey VN, Kaushik N, Rege N, Sarafianos SG, Yadav PN, &, Modak MJ, (1996) Role of methionine 184 of human immunodeficiency virus type-1 reverse transcriptase in the polymerase function and fidelity of DNA synthesis. Biochemistry 35, 2168-2179.
36. Rezende LF, Drosopoulos WC, &, Prasad VR, (1998) 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, 3066-3072.
37. Gutiérrez-Rivas M, &, Menéndez-Arias L, (2001) A mutation in the primer grip region of HIV-1 reverse transcriptase that confers reduced fidelity of DNA synthesis. Nucleic Acids Res 29, 4963-4972.
38. Drosopoulos WC, &, Prasad VR, (1996) Increased polymerase fidelity of E89G, a nucleoside analog-resistant variant of human immunodeficiency virus type 1 reverse transcriptase. J Virol 70, 4834-4838.
39. Margot NA, Isaacson E, McGowan I, Cheng AK, Schooley RT, &, Miller MD, (2002) Genotypic and phenotypic analyses of HIV-1 in antiretroviral- experienced patients treated with tenofovir DF. AIDS 16, 1227-1235.
40. Wainberg MA, Miller MD, Quan Y, Salomon H, Mulato AS, Lamy PD, Margot NA, Anton KE, &, Cherrington JM, (1999) In vitro selection and characterization of HIV-1 with reduced susceptibility to PMPA. Antivir Ther 4, 87-94.
41. White KL, Margot NA, Wrin T, Petropoulos CJ, Miller MD, &, Naeger LK, (2002) Molecular mechanisms of resistance to human immunodeficiency virus type 1 with reverse transcriptase mutations K65R and K65R+M184V and their effects on enzyme function and viral replication capacity. Antimicrob Agents Chemother 46, 3437-3446.
42. Parikh UM, Koontz DL, Chu CK, Schinazi RF, &, Mellors JW, (2005) In vitro activity of structurally diverse nucleoside analogs against human immunodeficiency virus type 1 with the K65R mutation in reverse transcriptase. Antimicrob Agents Chemother 49, 1139-1144.
43. Curr K, Tripathi S, Lennerstrand J, Larder BA, &, Prasad VR, (2006) Influence of naturally occurring insertions in the fingers subdomain of human immunodeficiency virus type 1 reverse transcriptase on polymerase fidelity and mutation frequencies in vitro. J Gen Virol 87, 419-428.
44. Boyer PL, Ferris AL, &, Hughes SH, (1992) Cassette mutagenesis of the reverse transcriptase of human immunodeficiency virus type 1. J Virol 66, 1031-1039.
45. Le Grice SF, Cameron CE, &, Benkovic SJ, (1995) Purification and characterization of human immunodeficiency virus type 1 reverse transcriptase. Methods Enzymol 262, 130-144.
46. Götte M, Maier G, Gross HJ, &, Heumann H, (1998) Localization of the active site of HIV-1 reverse transcriptase-associated RNase H domain on a DNA template using site-specific generated hydroxyl radicals. J Biol Chem 273, 10139-10146.
47. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, &, Ferrin TE, (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612.
48. Dunbrack RL, &, Cohen FE, (1997) Bayesian statistical analysis of protein side-chain rotamer preferences. Protein Sci 6, 1661-1681.