Mutations proximal to the minor groove-binding track of human immunodeficiency virus type 1 reverse transcriptase differentially affect utilization of RNA versus DNA as template

Journal of Virology

Volumn 77, Issue 10, 2003, Pages 5837-5845

  Fisher, Timothy S ^a   Darden, Tom ^b   Prasad, Vinayaka R ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA DIRECTED DNA POLYMERASE; VIRUS DNA; VIRUS RNA;

ARTICLE; CONFORMATION; DNA SYNTHESIS; DNA TEMPLATE; GENE MUTATION; HUMAN IMMUNODEFICIENCY VIRUS 1; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; SYNTHESIS;

BINDING SITES; DNA PRIMERS; DNA, VIRAL; DNA-DIRECTED DNA POLYMERASE; HIV-1; HIV-1 REVERSE TRANSCRIPTASE; HUMANS; MODELS, MOLECULAR; MUTATION; RNA, VIRAL; RNA-DIRECTED DNA POLYMERASE; TEMPLATES, GENETIC;

EID: 0038709523     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.10.5837-5845.2003     Document Type: Article

References (46)

1. Arion, D., G. Borokov, Z. Gu, M. A. Wainberg, and M. A. Parniak. 1996. The K65R mutation confers increased DNA polymerase processivity to HIV-1 reverse transcriptase. J. Biol. Chem. 271:19860-19864.
2. Arts, E. J., X. Li, Z. Gu, L. Kleiman, M. A. Parniak, and M. A. Wainberg. 1994. Comparison of deoxyoligonucleotide and tRNA(Lys-3) as primers in an endogenous human immunodeficiency virus-1 in vitro reverse transcription/template-switching reaction. J. Biol. Chem. 269:14672-14680.
3. Beard, W. A., K. Bebenek, T. A. Darden, L. Li, R. Prasad, T. A. Kunkel, and S. H. Wilson. 1998. Vertical-scanning mutagenesis of a critical tryptophan in the minor groove binding track of HIV-1 reverse transcriptase. Molecular nature of polymerase-nucleic acid interactions. J. Biol. Chem. 273:30435-30442.
4. Beard, W. A., S. J. Stahl, H. R. Kim, K. Bebenek, A. Kumar, M. P. Strub, S. P. Becerra, T. A. Kunkel, and S. H. Wilson. 1994. Structure-function studies of human immunodeficiency virus type 1 reverse transcriptase: alanine scanning mutagenesis of an alpha-helix in the thumb subdomain. J. Biol. Chem. 269:28091-28097.
5. Bebenek, K., J. Abbotts, S. H. Wilson, and T. A. Kunkel. 1993. Error-prone polymerization by HIV-1 reverse transcriptase. J. Biol. Chem. 268:10324-10334.
6. Boyer, P. L., S. G. Sarafianos, E. Arnold, and S. H. Hughes. 2000. Analysis of mutations at postions 115 and 116 in the dNTP binding site of HIV-1 reverse transcriptase. Proc. Natl. Acad. Sci. USA 97:3056-3061.
7. Boyer, P. L., C. Tantillo, A. Jacobo-Molina, R. G. Nanni, J. Ding, E. Arnold, and S. H. Hughes. 1994. Sensitivity of wild-type human immunodeficiency virus type 1 reverse transcriptase to dideoxynucleotides depends on template length; the sensitivity of drug-resistant mutants does not. Proc. Natl. Acad. Sci. USA 91:4882-4886.
8. Cheatham, T. E., III, P. Cieplak, and P. A. Kollman. 1999. A modified version of the Cornell et al. force field with improved sugar pucker phases and helical repeat. J. Biomol. Struct. Dyn. 16:845-862.
9. DeStefano, J. J., R. A. Bambara, and P. J. Fay. 1993. Parameters that influence the binding of human immunodeficiency virus reverse transcriptase to nucleic acid structures. Biochemistry 32:6908-6915.
10. Ding, J., K. Das, Y. Hsiou, S. G. Sarafianos, A. D. Clark, A. Jacobo-Molina, C. Tantillo, S. H. Hughes, and E. Arnold. 1998. Structure and functional implication 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 Å resolution. J. Mol. Biol. 284:1095-1111.
11. Ding, J., S. H. Hughes, and E. Arnold. 1997. Protein-nucleic acid interactions and DNA conformation in a complex of human immunodeficiency virus type 1 reverse transcriptase with a double-stranded DNA template-primer. Biopolymers 44:125-138.
12. Drosopoulos, W. C., and V. R. Prasad. 1998. The 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 rates measured in vitro. J. Virol. 72:4224-4230.
13. Drosopoulos, W. C., and V. R. Prasad. 1996. Increased polymerase fidelity of E89G, a nucleoside analog-resistant variant of human immunodeficiency virus type 1 (HIV-1) reverse transcriptase. J. Virol. 70:4834-4838.
14. Essmann, U. A. 1995. A smooth particle mesh method. J. Chem. Phys. 103:8577-8593.
15. Fisher, T. S., P. Joshi, and V. R. Prasad. 2002. Mutations that confer resistance to template-analog inhibitors of human immunodeficiency virus (HIV) type 1 reverse transcriptase lead to severe defects in HIV replication. J. Virol. 76:4068-4072.
16. 2-guanine adducts. J. Biol. Chem. 272:8525-8530.
17. Gao, G., and S. P. Goff. 1998. Replication defect of Moloney murine leukemia virus with a mutant reverse transcriptase that can incorporate ribonucleotides and deoxyribonucleotides. J. Virol. 72:5905-5911.
18. Gao, G., M. Orlova, M. M. Georgiadis, W. A. Hendrickson, and S. P. Goff. 1997. Conferring RNA polymerase activity to a DNA polymerase: a single residue in reverse transcriptase controls substrate selection. Proc. Natl. Acad. Sci. USA 94:407-411.
19. Ghosh, M., P. S. Jacques, D. W. Rodgers, M. Ottman, J.-L. Darlix, and S. F. J. Le Grice. 1996. Alterations to the primer grip of p66 HIV-1 reverse transcriptase and their consequences for template-primer utilization. Biochemistry 35:8553-8562.
20. Ghosh, M., J. Williams, M. D. Powell, J. G. Levin, and S. F. Le Grice. 1997. Mutating a conserved motif of the HIV-1 reverse transcriptase palm subdomain alters primer utilization. Biochemistry 36:5758-5768.
21. 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.
22. Jacobo-Molina, A., J. Ding, R. G. Nanni, A. D. Clark, Jr., X. Lu, C. Tantillo, R. L. Williams, G. Kamer, A. L. Ferris, P. Clark, 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.
23. Jacques, P. S., B. M. Wohrl, M. Ottman, J.-L. Darlix, and S. F. J. Le Grice. 1994. Mutating the "primer grip" of p66 HIV-1 reverse transcriptase implicates tryptophan-229 in template-primer utilization. J. Biol. Chem. 269:26472-26478.
24. 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.
25. Kew, Y., L. Olsen, A. Japour, and V. R. Prasad. 1998. Insertions into the β3-β4 hairpin loop of HIV-1 reverse transcriptase reveal a role for fingers subdomain in processive polymerization. J. Biol. Chem. 273:7529-7537.
26. Kew, Y., Q. Song, and V. Prasad. 1994. Subunit selective mutagenesis of Glu89 residue in human immunodeficiency virus reverse transcriptase. J. Biol. Chem. 269:15331-15336.
27. 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.
28. Klarmann, G. J., R. A. Smith, R. F. Schinazi, T. W. North, and B. D. Preston. 2000. Site-specific incorporation of nucleoside analogs by HIV-1 reverse transcriptase and the template grip mutant P157S. Template interactions influence substrate recognition at the polymerase active site. J. Biol. Chem. 275:359-366.
29. Kraulis, P. J. 1991. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24:946-950.
30. Latham, G. J., E. Forgacs, W. A. Beard, R. Prasad, K. Bebenek, T. A. Kunkel, S. H. Wilson, and R. S. Lloyd. 2000. 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. J. Biol. Chem. 275:15025-15033.
31. Li, M. D., D. L. Bronson, T. D. Lemke, and A. J. Faras. 1995. Phylogenetic analyses of 55 retroelements on the basis of the nucleotide and product amino acid sequences of the pol gene. Mol. Biol. Evol. 12:657-670.
32. Merritt, E. A., and D. J. Bacon. 1997. Raster3D: photorealistic molecular graphics, p. 505-524. In C. W. Carter, Jr. (ed.), Macromolecular crystallography, part B, vol. 277. Academic Press, Inc., New York, N.Y.
33. Oude Essink, B. B., N. K. T. Back, and B. Berkhout. 1997. Increased polymerase fidelity of the 3TC-resistant variants of HIV-1 reverse transcriptase. Nucleic Acids Res. 25:3212-3217.
34. Patel, P. H., and L. A. Loeb. 2001. Getting a grip on how DNA polymerases function. Nat. Struct. Biol. 8:656-659.
35. Pearlman, D. A. 1995. AMBER, a package of computer programs for applying molecular mechanics, normal mode of analysis, molecular dynamics, and free energy calculations to simulate the structural and energetic properties of molecules. Comp. Phys. Commun. 91:1-41.
36. Powell, M. D., M. Ghosh, P. S. Jacques, K. J. Howard, S. F. LeGrice, and J. G. Levin. 1997. Alanine-scanning mutations in the "primer grip" of p66 HIV-1 reverse transcriptase result in selective loss of RNA priming activity. J. Biol. Chem. 272:13262-13269.
37. Prasad, V. R., I. Lowy, T. De Los Santos, L. Chiang, and S. P. Goff. 1991. Isolation and characterization of a dideoxyguanosine triphosphate-resistant HIV-1 reverse transcriptase expressed in bacteria. Proc. Natl. Acad. Sci. USA 88:11363-11367.
38. Rubinek, T., M. Bakhanashvili, R. Taube, O. Avidan, and A. Hizi. 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 Leu74Val and Glu89Gly. Eur. J. Biochem. 247:238-247.
39. Sarafianos, S. G., K. Das, J. Ding, P. L. Boyer, S. H. Hughes, and E. Arnold. 1999. Touching the heart of HIV-1 drug resistance: the fingers close down on the dNTP at the polymerase active site. Chem. Biol. 6:R137-R146.
40. Sarafianos, S. G., K. Das, C. Tantillo, A. D. Clark, Jr., 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.
41. Sarafianos, S. G., V. N. Pandey, N. Kaushik, and M. J. Modak. 1995. Glutamine 151 participates in the substrate dNTP binding function of HIV-1 reverse transcriptase. Biochemistry 34:7207-7216.
42. Schneider, D. J., J. Feigon, Z. Hostomsky, and L. Gold. 1995. High-affinity ssDNA inhibitors of the reverse transcriptase of type 1 human immunodeficiency virus. Biochemistry 34:9599-9610.
43. Telesnitsky, A., and S. P. Goff. 1998. Reverse transcriptase and the generation of retroviral DNA, p. 121-160. In J. M. Coffin (ed.), Retroviruses. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
44. Wainberg, M. A., W. C. Drosopoulos, H. Salomon, M. Hsu, G. Borkow, M. Parniak, Z. Gu, Q. Song, J. Manne, S. Islam, G. Castriota, and V. R. Prasad. 1996. Enhanced fidelity of 3TC-selected mutant HIV-1 reverse transcriptase. Science 271:1282-1285. (Comments, 275:228-231, 1997.)
45. Wisniewski, M., C. Palaniappan, Z. Fu, S. F. Le Grice, P. Fay, and R. A. Bambara. 1999. Mutations in the primer grip region of HIV reverse transcriptase can increase replication fidelity. J. Biol. Chem. 274:28175-28184.
46. Wohrl, B. M., R. Krebs, S. H. Thrall, S. F. LeGrice, A. J. Scheidig, and R. S. Goody. 1997. Kinetic analysis of four HIV-1 reverse transcriptase enzymes mutated in the primer grip region of p66: implications for DNA synthesis and dimerization. J. Biol. Chem. 272:17581-17587.