Reduced replication of 3TC-resistant HIV-1 variants in primary cells due to a processivity defect of the reverse transcriptase enzyme

EMBO Journal

Volumn 15, Issue 15, 1996, Pages 4040-4049

  Back, Nicole K T ^a   Nijhuis, Monique ^b   Keulen, Wilco ^b   Boucher, Charles A B ^b   Oude Essink, Belinda B ^a   Van Kuilenburg, André B P ^c   Van Gennip, Albert H ^c   Berkhout, Ben ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UTRECHT UNIVERSITY   (Netherlands)

^c ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

Drug resistance; Enzyme processivity; Virus fitness

Indexed keywords

COMPLEMENTARY DNA; ISOLEUCINE; LAMIVUDINE; METHIONINE; RNA DIRECTED DNA POLYMERASE; VALINE; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; DRUG RESISTANCE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; KINETICS; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION; RNA PROCESSING; T LYMPHOCYTE; VIROGENESIS; VIRUS INFECTION; VIRUS MUTANT; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 0029757751     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00777.x     Document Type: Article

References (70)

1. Argos, P. (1988) A sequence motif in many polymerases. Nucleic Acids Res., 16, 9909-9916.
2. Baltimore, D. and Smoler, D. (1971) Primer requirement and template specificity of the DNA polymerase of RNA tumor viruses. Proc. Natl Acad. Sci. USA, 68, 1507-1511.
3. Bebenek, K., Abbotts, J., Roberts, J.D., Wilson, S.N. and Kunkel, T.A. (1989) Specificity and mechanism of error-prone replication by human immunodeficiency virus-1 reverse transcriptase. J. Biol. Chem., 264, 16948-16956.
4. Boucher, C.A.B., Cammack, N., Schipper, P., Schuurman, R., Rouse, P.L. and Cameron, J.M. (1993) High level resistance to (-) enantiomeric 2′-deoxy-3′-thiacytidine (3TC) in vitro is due to one amino acid substitution in the catalytic site of HIV-1 reverse transcriptase. Antimicrob. Agents Chemother., 37, 2231-2234.
5. Boyer, P.L. and Hughes, S.H. (1995) Analysis of mutations at position 184 in reverse transcriptase of human immunodeficiency virus type 1. Antimicrob. Agents Chemother., 39, 1624-1628.
6. Boyer, P.L., Ferris, A.L. and Hughes, S.H. (1992) Cassette mutagenesis of the reverse transcriptase of human immunodeficiency virus type 1. J. Virol., 66, 1031-1039.
7. Bray, G. and Brent, T.P. (1972) Deoxyribonucleoside 5′-triphosphate pool fluctuations during the mammalian cell cycle. Biochim. Biophys. Acta, 269, 184-191.
8. Chou, P.Y. and Fasman, G.D. (1978) Prediction of the secondary structure of proteins from their amino acid sequence. In Meister, A. (ed.), Advances in Enzymolology and Related Areas of Molecular Biology. John Wiley & Sons, New York, pp. 45-148.
9. Coates, J.A.V. et al. (1992a) (-)-2′-deoxy-3′-thiacytidine is a potent, highly selective inhibitor of human immunodeficiency virus type 1 and type 2 replication in vitro. Antimicrob. Agents Chemother., 36, 733-739.
10. Coates, J.A.V., Cammack, N., Jenkinson, H.J., Mutton, I.M., Pearson, B.A., Storer, R., Cameron, J.M. and Penn, C.R. (1992b) The separated enantiomers of 2′-deoxy-3′-thiacytidine (BCH 189) both inhibit human immunodeficiency virus replication in vitro. Antimicrob. Agents Chemother., 36, 202-205.
11. Coffin, J.M. (1995) HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science, 267, 483-489.
12. Cohen, A., Barankiewicz, J., Ledermann, H.M. and Gelfand, E.W. (1983) Purine and pyrimidine metabolism in human lymphocytes. Regulation of deoxyribonucleotide metabolism. J. Biol. Chem., 258, 12334-12340.
13. Dahbo, Y. and Eriksson, S. (1985) On the mechanism of deoxyribonucleoside toxicity in human T-lymphoblastoid cells. Reversal of growth inhibition by addition of cytidine. Eur. J. Biochem., 150, 429-434.
14. de Jong, J.J., Goudsmit, J., Keulen, W., Klaver, B., Krone, W., Tersmette, M. and de Ronde, A. (1992) Human immunodeficiency virus type 1 clones chimeric for the envelope V3 domain differ in syncytium formation and replication capacity. J. Virol., 66, 757-765.
15. de Korte, D., Haverkort, W.A., Van Gennip, A.H. and Roos, D. (1985) Nucleotide profiles of normal human blood cells determined by high performance liquid chromatography. Anal. Biochem., 147, 197-209.
16. Dudding, L.R., Nkabinde, N.C. and Mizrahi, V. (1991) Analysis of the RNA- and DNA-dependent DNA polymerase activities of point mutants of HIV-1 reverse transcriptase lacking ribonuclease H activity. Biochemistry, 30, 10498-10506.
17. Erice, A. and Balfour, H.H., Jr (1994) Resistance of human immunodeficiency virus type 1 to antiretroviral agents: a review. Clin. Inf. Dis., 18, 149-156.
18. Gao, Q., Gu, Z., Parniak, M.A., Cameron, J., Cammack, N., Boucher, C.A.B. and Wainberg, M.A. (1993a) The same mutation that encodes low-level human immunodeficiency virus type 1 resistance to 2′,3′-dideoxyinosine and 2′,3′-dideoxycytidine confers high-level resistance to the (-) enantiomer of 2′,3′-dideoxy-3′-thiacytidine. Antimicrob. Agents. Chemother., 37, 1390-1392.
19. Gao, W.Y., Cara, A., Gallo, R.C. and Lori, F. (1993b) Low levels of deoxynucleotides in peripheral blood lymphocytes: a strategy to inhibit human immunodeficiency virus type I replication. Proc. Natl Acad. Sci. USA, 90, 8925-8928.
20. Garrett, C. and Santi, D.V. (1979) A rapid and sensitive high pressure liquid chromatography assay for deoxyribonucleoside triphosphates in cell extracts. Anal. Biochem., 99, 268-273.
21. Goodman, M.F., Creighton, S., Bloom, L.B. and Petruska, J. (1993) Biochemical basis of DNA replication fidelity. Crit. Rev. Biochem. Mol. Biol., 28, 83-126.
22. Gürtler, L.G., Hauser, P.H., Eberle, J., von Brunn, A., Knapp, S., Zekeng, L., Tsague, J.M. and Kaptue, L. (1994) A new subtype of human immunodeficiency virus type 1 (MVP-5180) from Cameroon. J. Virol., 68, 1581-1585.
23. Ho, D.D., Neumann, A.U., Perelson, A.S., Chen, W., Leonard, J.M. and Markowitz, M. (1995) Rapid turnover of plasma virions and CD4 lymphocytes in HIV-1 infection. Nature, 373, 123-126.
24. Huber, H.E., McCoy, J.M., Seehra, J.S. and Richardson, C.C. (1989) Human immunodeficiency virus 1 reverse transcriptase; template binding, processivity, strand displacement synthesis, and template switching. J. Biol. Chem., 264, 4669-4678.
25. Inokuchi, Y. and Hirashima, A. (1987) Interference with viral infection by defective RNA replicase. J. Virol., 61, 3946-3949.
26. Jablonski, S.A., Luo, M. and Morrow, C.D. (1991) Enzymatic activity of poliovirus RNA polymerase mutants with single amino acid changes in the conserved YGDD amino acid motif. J. Virol., 65, 4565-4572.
27. Jacobo-Molina, A. et al. (1993) Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA. Proc. Natl Acad. Sci. USA, 90, 6320-6324.
28. Kamer, G. and Argos, P. (1984) Primary structural comparison of RNA-dependent polymerases from plant, animal and bacterial viruses. Nucleic Acids Res., 12, 7269-7283.
29. Kellam, P. and Larder, B.A. (1994) Recombinant virus assay: a rapid, phenotypic assay for assessment of drug susceptibility of human immunodeficiency virus type 1 isolates. Antimicrob. Agents Chemother., 38, 23-30.
30. Keulen, W., Boucher, C. and Berkhout, B. (1996) Nucleotide substitution patterns can predict the requirements for drug-resistance of HIV-1 proteins. Antiviral Res., in press.
31. Klarmann, G.J., Schauber, C.A. and Preston, B.D. (1993) Template-directed pausing of DNA synthesis by HIV-1 reverse transcriptase during polymerization of HIV-1 sequences in vitro. J. Biol. Chem., 268, 9793-9802.
32. 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.
33. Kornberg, A. and Baker, T.A. (1992) DNA Replication. 2nd edn. W.H. Freeman and Company, New York.
34. Kunkel, T.A. (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl Acad. Sci. USA, 82, 488-492.
35. Kunkel, T.A., Patel, S.S. and Johnson, K.A. (1994) Error-prone replication of repeated DNA sequences by T7 DNA polymerase in the absence of its processivity subunit. Proc. Natl Acad. Sci. USA, 91, 6830-6834.
36. Larder, B.A. (1994) Interactions between drug resistance mutations in human immunodeficiency virus type 1 reverse transcriptase. J. Gen. Virol., 75, 951-957.
37. Larder, B.A. and Kemp, S.D. (1989) Multiple mutations in HIV-1 reverse transcriptase confer high-level resistance to zidovudine (AZT). Science, 246, 1155-1158.
38. Larder, B.A., Kemp, S.D. and Purifoy, D.J.M. (1989) Infectious potential of human immunodeficiency virus type 1 reverse transcriptase mutants with altered inhibitor sensitivity. Proc. Natl Acad. Sci. USA, 86, 4803-4807.
39. Larder, B.A., Chesebro, B. and Richman, D.D. (1990) Susceptibilities of zidovudine-susceptible and -resistant human immunodeficiency virus isolates to antiviral agents determined by using a quantitative plaque reduction assay. Antimicrob. Agents Chemother., 34, 436-441.
40. Larder, B.A., Kemp, S.D. and Harrigan, P.R. (1995) Potential mechanism for sustained antiretroviral efficacy of AZT-3TC combination therapy. Science, 269, 696-699.
41. Le Grice, S.F.J., Naas, T. Wohlgensinger, B. and Schatz, O. (1991) Subunit-selective, mutagenesis indicates minimal polymerase activity in heterodimer-associated p51 HIV-1 reverse transcriptase. EMBO J., 10, 3905-3911.
42. Lori, F. and Gallo, R.C. (1995) Hydroxyurea and AIDS: an old drug finds a new application? AIDS Res. Hum. Retrovirus, 11, 1149-1151.
43. Lori, F., Malykh, A., Cara, A., Sun, D., Weinstein, J.N., Lisziewicz, J. and Gallo, R.C. (1994) Hydroxyurea as an inhibitor of human immunodeficiency virus type I replication. Science, 266, 801-805.
44. Lowe, D.M., Parmar, V., Kemp, S.D. and Larder, B.A. (1991) Mutational analysis of two conserved sequence motifs in HIV-1 reverse transcriptase. FEBS Lett., 282, 231-234.
45. Majumbar, C., Abbotts, J., Broder, S. and Wilson, S.H. (1988) Studies on the mechanism of human immunodeficiency virus reverse transcriptase; steady-state kinetics, processivity, and polynucleotide inhibition. J. Biol. Chem., 263, 15657-15665.
46. McKeating, J.A., McKnight, A. and Moore, J.P. (1991) Differential loss of envelope glycoprotein gp120 from virions of human immunodeficiency virus type 1 isolates: effects on infectivity and neutralization. J. Virol., 65, 852-860.
47. Meyerhans, A., Vartanian, J.-P., Hultgren, C., Plikat, U., Karlsson, A., Wang, L., Eriksson, S. and Wain-Hobson, S. (1994) Restriction and enhancement of human immunodeficiency virus type 1 replication by modulation of intracellular deoxynucleoside triphosphate pools. J. Virol., 68, 535-540.
48. Moore, J.P., McKeating, J.A., Weiss, R.A. and Sattentau, Q.J. (1990) Dissociation of gp120 from HIV-1 virions induced by soluble CD4. Science, 250, 1139-1142.
49. Myers, G., Korber, B., Wain-Hobson, S. and Smith, R.F. (1993) Human Retrovirus and AIDS 1993 I-II, Theoretical Biology and Biophysics. Los Alamos National Laboratory, Los Alamos, NM.
50. Paul, A.V., Cao, X., Harris, K.S., Lama, J. and Wimmer, E. (1994) Studies with poliovirus polymerase 3Dpol. Stimulation of poly(U) synthesis in vitro by purified poliovirus protein 3AB. J. Biol. Chem., 269, 29173-29181.
51. Pelletier, H., Sawaya, M.R., Kumar, A., Wilson, S.H. and Kraut, J. (1994) Structure of ternary complexes of rat DNA polymerase β, a DNA template-primer, and ddCTP. Science, 264, 1891-1903.
52. Poch, O., Sauvaget, I., Delarue, M. and Tordo, N. (1989) Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J., 8, 3867-3874.
53. Rocancourt, D., Bonnerot, C., Jouin, H., Emerman, M. and Nicolas, J.-F. (1990) Activation of a β-galactosidase recombinant provirus: application to titration of human immunodeficiency virus (HIV) and HIV-infected cells. J. Virol., 64, 2660-2668.
54. Rodgers, D.W., Gamblin, S.J., Harris, B.A., Ray, S., Culp, J.S., Hellmig, B., Woolf, D.J., Debouck, C. and Harrison, S.C. (1995) The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1. Proc. Natl Acad. Sci. USA, 92, 1222-1226.
55. Sawaya, M.R., Pelletier, H., Kumar, A., Wilson, S.H. and Kraut, J. (1994) Crystal structure of rat DNA polymerase β: evidence for a common polymerase mechanism. Science, 264, 1930-1935.
56. Schinazi, R.F. et al. (1992) Activities of the four optical isomers of 2′,3′-dideoxy-3′-thiacytidine (BCH-189) against human immunodeficiency virus type 1 in human lymphocytes. Antimicrob. Agents Chemother., 36, 672-676.
57. Schinazi, R.F. et al. (1993) Characterization of human immunodeficiency viruses resistant to oxathiolane-cytosine nucleosides. Antimicrob. Agents Chemother., 37, 875-881.
58. Schmidt, N.J. (1979) Cell culture techniques for diagnostic virology. In Lennette, E.H. and Schmidt, N.J. (eds), Diagnostic Procedures for Viral, Rickettsial and Chlamydial Infections. American Public Health Association Inc., Washington, pp. 65-139.
59. Schuurman, R. et al. (1995) Rapid changes in human immunodeficiency virus type I RNA load and appearance of drug-resistant virus populations in persons treated with lamivudine (3TC). J. Infect. Dis.. 171, 1411-1419.
60. Shimizu, K., Handa, H., Nakada, S. and Nagata, K. (1994) Regulation of influenza virus RNA polymerase activity by cellular and viral factors. Nucleic Acids Res., 22, 5047-5053.
61. Smith, P.K. et al. (1985) Measurement of protein using bicinchoninic acid. Anal. Biochem., 150, 76-85.
62. Tisdale, M., Kemp, S.D., Parry, N.R. and Larder, B.A. (1993) Rapid in vitro selection of human immunodeficiency virus type 1 resistant to 3′-thiacytidine inhibitors due to a mutation in the YMDD region of reverse transcriptase. Proc. Natl Acad. Sci. USA, 90, 5653-5656.
63. van Leeuwen, R. et al. (1995) Evaluation of safety and efficacy of 3TC (lamivudine) in patients with asymptomatic or mildly symptomatic HIV-1 infection; a phase I/II study. J. Infect. Dis., 171, 1161-1171.
64. Wainberg, M.A. et al. (1995) Development of HIV-1 resistance to (-)2′-deoxy-3′-thiacytidine in patients with AIDS or advanced AIDS-related complex. AIDS, 9, 351-357.
65. Wainberg, M.A. et al. (1996) Enhanced fidelity of 3TC-selected mutant HIV-1 reverse transcriptase. Science, 271, 1282-1285.
66. Wakefield, J.K., Jablonski, S.A. and Morrow, C.D. (1992) In vitro enzymatic activity of human immunodeficiency virus type 1 reverse transcriptase mutants in the highly conserved YMDD amino acid motif correlates with the infectious potential of the proviral genome. J. Virol., 66, 6806-6812.
67. Wei, X. et al. (1995) Viral dynamics in human immunodeficiency virus type 1 infection. Nature, 373, 117-126.
68. Willey, R.L., Smith, D.H., Lasky, L.A., Theodore, T.S., Earl, P.L., Moss, B., Capon, D.J. and Martin, M.A. (1988) In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J. Virol., 62, 139-147.
69. Zack, J.A., Arrigo, S.J., Weitsman, S.R., Go, A.S., Haislip, A. and Chen, I.S.Y. (1990) HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell, 61, 213-222.
70. Zack, J.A., Haislip, A.M., Krogstad, P. and Chen, I.S.Y. (1992) Incompletely reverse-transcribed human immunodeficiency virus type 1 genomes in quiescent cells can function as intermediates in the retroviral life cycle. J. Virol., 66, 1717-1725.