Influence of reverse transcriptase variants, drugs, and Vpr on human immunodeficiency virus type 1 mutant frequencies

Journal of Virology

Volumn 77, Issue 3, 2003, Pages 2071-2080

  Mansky, Louis M ^a,c   Le Rouzic, Erwann ^b   Benichou, Serge ^b   Gajary, Lisa C ^a  

^a THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

^b INSTITUT COCHIN   (France)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3' AZIDO 2',3' DIDEOXYCYTIDINE; AMINO ACID; BETA GALACTOSIDE; HYDROXYUREA; RNA DIRECTED DNA POLYMERASE; THYMIDINE; TIOGUANINE; URACIL DNA GLYCOSYLTRANSFERASE; VPR PROTEIN; ZIDOVUDINE;

AMINO ACID SUBSTITUTION; ANTIBIOTIC RESISTANCE; ARTICLE; EVOLUTION; HIGHLY ACTIVE ANTIRETROVIRAL THERAPY; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; MUTATION RATE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; VIRUS MUTANT;

AMINO ACID SUBSTITUTION; ANTI-HIV AGENTS; GENE PRODUCTS, VPR; HIV-1; HIV-1 REVERSE TRANSCRIPTASE; MUTATION; THIOGUANINE;

EID: 0037302270     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.3.2071-2080.2003     Document Type: Article

References (68)

1. Abbas, U. L., and J. W. Mellors. 2002. Interruption of antiretroviral therapy to augment immune control of chronic HIV-1 infection: risk without reward. Proc. Natl. Acad. Sci. USA 99:13377-13378.
2. Bebenek, K., W. A. Beard, J. R. Casas-Finet, H.-R. Kim, T. A. Darden, S. H. Wilson, and T. A. Kunkel. 1995. Reduced frameshift fidelity and processivity of HIV-1 reverse transcriptase mutants containing alanine substitutions in helix H of the thumb subdomain. J. Biol. Chem. 270:19516-19523.
3. Biron, F., F. Lucht, D. Peyramond, A. Fresard, T. Vallet, F. Nugier, J. Grange, S. Malley, F. Hamedi-Sangsari, and J. Vila. 1996. Pilot clinical trial of the combination of hydroxyurea and didanosine in HIV-1 infected individuals. Antivir. Res. 29:111-113.
4. Bouhamdan, M., S. Benichou, F. Rey, J.-M. Navarro, I. Agostini, B. Spire, J. Camonis, G. Slupphaug, R. Vigne, R. Benarous, and J. Sire. 1996. Human immunodeficiency virus type 1 Vpr protein binds to the uracil DNA glycosylase DNA repair enzyme. J. Virol. 70:697-704.
5. Boyer, P. L., and S. H. Hughes. 2000. Effects of amino acid substitutions at position 115 on the fidelity of human immunodeficiency virus type 1 reverse transcriptase. J. Virol. 74:6494-6500.
6. Cases-Gonzalez, C. E., M. Gutierrez-Rivas, and L. Menendez-Arias. 2000. Coupling ribose selection to fidelity of DNA synthesis. The role of Tyr-115 of human immunodeficiency virus type 1 reverse transcriptase. J. Biol. Chem. 275:19759-19767.
7. Coffin, J. 1995. HIV population dynamics in vivo: implications for genetic variation, pathogenesis, and therapy. Science 267:483-489.
8. Cohen, A., J. Barankiewicz, H. M. Lederman, and E. W. Gelfand. 1983. Purine and pyrimidine metabolism in human T lymphocytes. Regulation of deoxyribonucleotide metabolism. J. Biol. Chem. 258:12334-12340.
9. Cohen, E. A., G. Dehni, J. G. Sodroski, and W. A. Haseltine. 1990. Human immunodeficiency virus vpr product is a virion-associated regulatory protein. J. Virol. 64:3097-3099.
10. Diamond, T. L., J. Kimata, and B. Kim. 2001. Identification of a simian immunodeficiency virus reverse transcriptase variant with enhanced replicational fidelity in the late stage of viral infection. J. Biol. Chem. 276:23624-23631.
11. Drosopoulos, W. C., and V. R. Prasad. 1998. 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. 72:4224-4230.
12. Drosopoulos, W. C., and V. R. Prasad. 1996. Increased polymerase fidelity of E89G, a nucleoside analog-resistant variant of human immunodeficiency virus type 1 reverse transcriptase. J. Virol. 70:4834-4838.
13. Elion, G. B. 1989. The purine path to chemotherapy. Science 244:41-47.
14. Frost, S. D. W., M.-J. Dumaurier, S. Wain-Hobson, and A. J. Leigh Brown 2001. Genetic drift and within-host metapopulation dynamics of HIV-1 infection. Proc. Natl. Acad. Sci. USA 98:6975-6980.
15. Gao, W. Y., A. Cara, R. C. Gallo, and F. Lori. 1993. Low levels of deoxynucleotides in peripheral blood lymphocytes: a strategy to inhibit human immunodeficiency virus type 1 replication. Proc. Natl. Acad. Sci. USA 90:8925-8928.
16. Gao, W. Y., D. G. Johns, and H. Mitsuya. 1994. Anti-human immunodeficiency virus type 1 activity of hydroxyurea in combination with 2′,3′-dideoxynucleosides. Mol. Pharmacol. 46:767-772.
17. Giacca, M., S. Zanussi, M. Comar, C. Simonelli, E. Vaccher, P. de Paoli, and U. Tirelli. 1996. Treatment of human immunodeficiency virus infection with hydroxyurea: virologic and clinical evaluation. J. Infect. Dis. 174:204-209.
18. Gu, Z., R. S. Fletcher, E. J. Arts, M. A. Wainberg, and M. A. Parniak. 1994. The K65R mutant reverse transcriptase of HIV-1 cross-resistant to 2́, 3́-dideoxycytidine, 2′,3′-dideoxy.3′-thiacytidine, and 2′,3′-dideoxyinosine shows reduced sensitivity to specific dideoxynucleoside triphosphate inhibitors in vitro. J. Biol. Chem. 269:28118-28122.
19. Gu, Z., Q. Gao, H. Fang, H. Salomon, M. A. Parniak, E. Goldberg, J. Cameron, and M. A. Wainberg. 1994. Identification of a mutation at codon 65 in the IKKK motif of reverse transcriptase that encodes human immunodeficiency virus resistance to 2·,3·-dideoxycytidine and 2′,3′-dideoxy-3·-thiacytidine. Antimicrob. Agents Chemother. 38:275-281.
20. Gutierrez-Rivas, M., and L. Menendez-Arias. 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.
21. Harrigan, P. R., C. Stone, P. Griffin, I. Najera, S. Bloor, S. D. Kemp, M. Tisdale, and B. A. Larder. 2000. Resistance profile of the human immunodeficiency virus type 1 reverse transcriptase inhibitor abacavir (1592U89) after monotherapy and combination therapy. J. Infect. Dis. 181:912-920.
22. Hogg, R. S., K. V. Heath, B. Yip, K. J. Craib, M. V. O'Shaughnessy, M. T. Schechter, and J. S. Montaner. 1998. Improved survival among HIV-infected individuals following initiation of antiretroviral therapy. JAMA 279: 450-454.
23. Hu, W.-S., and H. M. Temin. 1990. Genetic consequences of packaging two RNA genomes in one retroviral particle: pseudodiploidy and high rate of genetic recombination. Proc. Natl. Acad. Sci. USA 87:1556-1560.
24. Huang, H., R. Chopra, G. L. Verdine, and S. C. Harrison. 1998. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282:1669-1675.
25. Ito, W., H. Ishiguro, and Y. Kurosawa. 1991. A general method for introducing a series of mutations into cloned DNA using the polymerase chain reaction. Gene 102:67-70.
26. Jacobo-Molina, A., J. Ding, R. G. Nanni, A. D. Clark, Jr., X. Lu, C. Tantillo, R. L. Williams, R. L. Kamer, A. L. Ferris, P. Clark, A. Hizi, S. H. Hughes, and E. Arnold. 1993. Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0A resolution shows bend DNA. Proc. Natl. Acad. Sci. USA 90:6320-6324.
27. Jonckheere, H., E. De Clercq, and J. Anne. 2000. 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. 267:2658-2665.
28. Julias, J. G., and V. K. Pathak. 1998. Deoxyribonucleoside triphosphate pool imbalances in vivo are associated with an increased retroviral mutation rate. J. Virol. 72:7941-7949.
29. Kim, B., J. C. Ayran, S. G. Sager, E. T. Adman, S. M. Fuller, N. H. Tran, and J. Horrigan. 1999. New human immunodeficiency virus type 1 reverse transcriptase (HIV-1 RT) mutants with increased fidelity of DNA synthesis. J. Biol. Chem. 274:27666-27673.
30. Kim, B., T. R. Hathaway, and L. A. Loeb. 1998. Fidelity of mutant HIV-1 reverse transcriptases: interaction with the single-stranded template influences the accuracy of DNA synthesis. Biochemistry 37:5831-5839.
31. Kohlstaedt, L. A., J. Wang, J. M. Friedman, P. A. Rice, and T. A. Steitz. 1992. Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256:1783-1790.
32. Kohlstaedt, L. A., J. Wang, P. A. Rice, J. M. Friedman, and T. A. Steitz. 1993. The structure of HIV-1 reverse transcriptase, p. 223-249. In A. M. Skalka and S. P. Goff (ed.), Reverse transcriptase. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
33. Krynetskaia, N. F., J. Y. Feng, E. Y. Krynetski, J. V. Garcia, J. C. Panetta, K. S. Anderson, and W. E. Evans. 2001. Deoxythioguanosine triphosphate impairs HIV replication: a new mechanism for an old drug. FASEB J. 15:1902-1908.
34. Landau, N. R., K. A. Page, and D. R. Littman. 1991. Pseudotyping with human T-cell leukemia virus type I broadens the human immunodeficiency virus host range. J. Virol. 65:162-169.
35. Le Grice, S. F. J. 1993. Human immunodeficiency virus reverse transcriptase, p. 163-191. In A. M. Skalka and S. P. Goff (ed.), Reverse transcriptase. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
36. Leigh Brown, A. J. 1997. Analysis of HIV-1 env gene sequences reveals evidence for a low effective number in the viral population. Proc. Natl. Acad. Sci. USA 94:1862-1865.
37. Lori, F., A. G. Malykh, A. Foli, R. Maserati, A. De Antoni, L. Minoli, D. Padrini, A. Degli Antoni, E. Barchi, H. Jessen, M. A. Wainberg, R. C. Gallo, and J. Lisziewicz. 1997. Combination of a drug targeting the cell with a drug targeting the virus controls human immunodeficiency virus type 1 resistance. AIDS Res. Hum. Retrovir. 13:1403-1409.
38. Lu, Y.-L., P. Spearman, and L. Ratner. 1993. Human immunodeficiency virus type I viral protein R localization in infected cells and virions. J. Virol. 67:6542-6550.
39. Mansky, L. M. 1996. The mutation rate of human immunodeficiency virus type 1 is influenced by the vpr gene. Virology 222:391-400.
40. Mansky, L. M. 1994. Retroviral-vector-mediated gene transfer, p. 27B:5.1-27B:5.10. In J. B. Griffiths, A. Doyle, and D. G. Newell (ed.), Cell and tissue culture: laboratory procedures, 6th ed. John Wiley & Sons, New York, N.Y.
41. Mansky, L. M. 1998. Retrovirus mutation rates and their role in genetic variation. J. Gen. Virol. 79:1337-1345.
42. Mansky, L. M., and L. C. Bernard. 2000.3′-Azido-3′-deoxythymidine (AZT) and AZT-resistant reverse transcriptase can increase the in vivo mutation rate of human immunodeficiency type 1. J. Virol. 74:9532-9539.
43. Mansky, L. M., D. K. Pearl, and L. C. Gajary. 2002. Combination of drugs and drug-resistant reverse transcriptase results in a multiplicative increase of human immunodeficiency virus type 1 mutant frequencies. J. Virol. 76:9253-9259.
44. Mansky, L. M., S. Preveral, L. Selig, R. Benarous, and S. Benichou. 2000. The interaction of Vpr with uracil DNA glycosylase modulates the human immunodeficiency virus type 1 in vivo mutation rate. J. Virol. 74:7039-7047.
45. Mansky, L. M., and H. M. Temin. 1995. Lower in vivo mutation rate of human immunodeficiency virus type 1 than predicted from the fidelity of purified reverse transcriptase. J. Virol. 69:5087-5094.
46. Mansky, L. M., and H. M. Temin. 1994. Lower mutation rate of bovine leukemia virus relative to that of spleen necrosis virus. J. Virol. 68:494-499.
47. Meyerhans, A., J.-P. Vartanian, C. Hultgren, U. Plikat, A. Karlsson, L. Wang, S. Eriksson, and S. Wain-Hobson. 1994. Restriction and enhancement of human immunodeficiency virus type 1 replication by modulation of intracellular deoxynucleoside triphosphate pools. J. Virol. 68:535-540.
48. O'Neil, P. K., G. Sun, H. Yu, Y. Ron, J. P. Dougherty, and B. D. Preston. 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.
49. Palella, F. J., K. M. Delaney, A. C. Moorman, M. O. Loveless, J. Fuhrer, G. A. Satten, D. J. Aschman, and S. D. Holmberg. 1998. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. N. Engl. J. Med. 338:853-860.
50. Paxton, W., R. I. Connor, and N. R. Landau. 1993. Incorporation of Vpr into human immunodeficiency virus type 1 virions: requirement for the p6 region of gag and mutational analysis. J. Virol. 67:7229-7237.
51. Prasad, V. R., I. Lowy, T. de los Santos, L. Chiang, and S. P. Goff. 1991. Isolation and characterization of a dideoxyguanosine triphosphate-resistant mutant of human immunodeficiency virus reverse transcriptase. Proc. Natl. Acad. Sci. USA 88:11363-11367.
52. Preston, B. D. 1997. Reverse transcriptase fidelity and HIV-1 variation. Science 275:228-231.
53. Refaeli, Y., D. N. Levy, and D. B. Weiner. 1995. The glucocorticoid receptor type II complex is a target of the HIV-1 vpr gene product. Proc. Natl. Acad. Sci. USA 92:3621-3625.
54. Reichard, P. 1988. Interactions between deoxyribonucleotide and DNA synthesis. Ann. Rev. Biochem. 57:349-374.
55. Sarafianos, S. G., K. Das, C. Tantillo, A. D. Clark, J. Ding, J. M. Whitcomb, P. L. Boyer, S. H. Hughes, and E. Arnold. 2001. Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J. 20:1449-1461.
56. Selig, L., S. Benichou, M. E. Rogel, L. I. Wu, M. A. Vodicka, J. Sire, R. Benarous, and M. Emerman. 1997. Uracil DNA glycosylase specifically interacts with Vpr of both human immunodeficiency virus type 1 and simian immunodeficiency virus of sooty mangabeys, but binding does not correlate with cell cycle arrest. J. Virol. 71:4842-4846.
57. Selig, L., J.-C. Pages, V. Tanchou, S. Preveral, C. Berlioz-Torrent, L. X. Liu, L. Erdtmann, J.-L. Darlix, R. Benarous, and S. Benichou. 1999. Interaction with the p6 domain of the Gag precursor mediates incorporation into virions of Vpr and Vpx proteins from primate lentiviruses. J. Virol. 73:592-600.
58. Shah, F. S., K. A. Curr, M. E. Hamburgh, M. Parniak, H. Mitsuya, J. G. Arnez, and V. R. Prasad. 2000. Differential influence of nucleoside analogresistance 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.
59. Shirasaka, T., M. F. Kavlick, T. Ueno, W. Y. Gao, E. Kojima, M. L. Alcaide, S. Chokekijchai, B. M. Roy, E. Arnold, R. Yarchoan, et al. 1995. Emergence of human immunodeficiency virus type 1 variants with resistance to multiple dideoxynucleosides in patients receiving therapy with dideoxynucleosides. Proc. Natl. Acad. Sci. USA 92:2398-2402.
60. Snyder, R. D. 1988. Consequences of the depletion of cellular deoxynucleoside triphosphate pools on the excision-repair process in cultured human fibroblasts. Mutat. Res. 200:193-199.
61. Srinivas, R. V., and A. Fridland. 1998. Antiviral activities of 9-R-2-phosphonomethoxypropyl adenine (PMPA) and bis(isopropyloxymethylcarbonyl)PMPA against various drug-resistant human immunodeficiency virus strains. Antimicrob. Agents Chemother. 42:1484-1487.
62. St. Clair, M. H., J. L. Martin, G. Tudor-Williams, M. C. Bach, C. L. Vavro, D. M. King, P. Kellam, S. D. Kemp, and B. A. Larder. 1991. Resistance to ddI and sensitivity to AZT induced by a mutation in HIV-1 reverse transcriptase. Science 253:1557-1559.
63. gag expressed in bacteria. Virology 150:283-290.
64. Telesnitsky, A., and S. P. Goff. 1997. Reverse transcriptase and the generation of retroviral DNA, p. 121-160. In J. M. Coffin, S. H. Hughes, and H. E. Varmus (ed.), Retroviruses. Cold Spring Harbor Press, Plainview, N.Y.
65. Weiss, K. K., S. J. Isaacs, N. H. Tran, E. T. Adman, and B. Kim. 2000. Molecular architecture of the mutagenic active site of human immunodeficiency virus type 1 reverse transcriptase: roles of the β8-α loop in fidelity, processivity, and substrate interactions. Biochemistry 39:10684-10694.
66. Wisniewski, M., C. Palaniappan, Z. Fu, S. F. Le Grice, P. Fay, and R. A. Bambara. 1999. Mutation in the primer grip region of HIV reverse transcriptase can increase replication fidelity. J. Biol. Chem. 274:28175-28184.
67. Zhang, W. H., E. S. Svarovskaia, R. Barr, and V. K. Pathak. 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.
68. Zhao, L.-J., S. Mukherjee, and O. Narayan. 1994. Biochemical mechanism of HIV-1 Vpr function. J. Biol. Chem. 269:15577-15582.