p66 Trp24 and Phe61 Are Essential for Accurate Association of HIV-1 Reverse Transcriptase with Primer/Template

Journal of Molecular Biology

Volumn 373, Issue 1, 2007, Pages 127-140

  Agopian, Audrey ^a   Depollier, Julien ^a   Lionne, Corinne ^b   Divita, Gilles ^a  

^a Centre National de la Recherche Scientifique   (France)

^b University of Montpellier I and II   (France)

Author keywords

DNA polymerase; HIV; peptide based inhibitors; pre steady state kinetics; reverse transcriptase

Indexed keywords

PROTEIN P51; PROTEIN P66; RNA DIRECTED DNA POLYMERASE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; DIMERIZATION; ENZYME ACTIVITY; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 34548550779     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.07.044     Document Type: Article

References (46)

1. Telesnitsky A., and Goff S.P. Reverse transcriptase and the generation of retroviral DNA. In: Coffin J.M., Hughes S.H., and Varmus H.E. (Eds). Retroviruses (1997), Cold Spring Harbor Laboratory Press, Plainview, NY 121-160
2. Le Grice S.F.J. Human immunodeficiency virus reverse transcriptase. In: Skala A., and Goff S.P. (Eds). Reverse Transcriptase (1993), Cold Spring Harbor Laboratory Press, Plainview, NY 163-191
3. Richman D.D. Antiretroviral drug resistance: mechanisms, pathogenesis, clinical significance. Adv. Exp. Med. Biol. 394 (1996) 383-395
4. Parniak M.A., and Sluis-Cremer N. Inhibitors of HIV-1 reverse transcriptase. Adv. Pharmacol. 49 (2000) 67-196
5. Menendez-Arias L. Targeting HIV: antiretroviral therapy and development of drug resistance. Trends Pharmacol. Sci. 23 (2002) 381-388
6. De Clercq E. Strategies in the design of antiviral drugs. Nat. Rev. Drug Discov. 1 (2002) 13-25
7. Sarafianos S.G., Das K., Hughes S.H., and Arnold E. Taking aim at a moving target: designing drugs to inhibit drug-resistant HIV-1 reverse transcriptase. Curr. Opin. Struct. Biol. 14 (2004) 716-730
8. Sluis-Cremer N., and Tachedjian G. Modulation of the oligomeric structures of HIV-1 retroviral enzymes by synthetic peptides and small molecules. Eur. J. Biochem. 269 (2002) 5103-5111
9. Camarasa M.J., Velazquez S., San-Felix A., Perez-Perez M.J., and Gago F. Dimerization inhibitors of HIV-1 reverse transcriptase, protease and integrase: a single mode of inhibition for the three HIV enzymes?. Antiviral Res. 1 (2006) 260-267
10. Divita G., Restle T., Goody R.S., Chermann J.C., and Baillon J.G. Inhibition of human immunodeficiency virus type 1 reverse transcriptase dimerization using synthetic peptides derived from the connection domain. J. Biol. Chem. 269 (1994) 13080-13083
11. Kohlstaedt L.A., Wang J., Friedman J.M., Rice P.A., and Steitz T.A. Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256 (1992) 1783-1790
12. Jacobo-Molina A., Ding J., Nanni R.G., Clark Jr. A.D., Lu X., Tantillo C., et al. 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 (1993) 6320-6324
13. di Marzo Veronese F., Copeland T.D., DeVico A.L., Rahman R., Oroszlan S., Gallo R.C., and Sarngadharan M.G. Characterization of highly immunogenic p66/p51 as the reverse transcriptase of HTLV-III/LAV. Science 231 (1986) 1289-1291
14. Restle T., Müller B., and Goody R.S. Dimerization of human immunodeficiency virus type 1 reverse transcriptase. A target for chemotherapeutic intervention. J. Biol. Chem. 265 (1990) 8986-8988
15. Divita G., Rittinger K., Geourjon C., Deleage G., and Goody R.S. Dimerization kinetics of HIV-1 and HIV-2 reverse transcriptase: a two step process. J. Mol. Biol. 245 (1995) 508-521
16. Restle T., Müller B., and Goody R.S. RNase H activity of HIV reverse transcriptases is confined exclusively to the dimeric forms. FEBS Letters 300 (1992) 97-100
17. Müller B., Restle T., Weiss S., Gautel M., Sczakiel G., and Goody R.S. Co-expression of the subunits of the heterodimer of HIV-1 reverse transcriptase in Escherichia coli. J. Biol. Chem. 264 (1989) 13975-13978
18. Divita G., Baillon J.G., Rittinger K., Chermann J.C., and Goody R.S. Interface peptides as structure-based human immunodeficiency virus reverse transcriptase inhibitors. J. Biol. Chem. 270 (1995) 28642-28646
19. Tachedjian G., Orlova M., Sarafianos S.G., Arnold E., and Goff S.P. Nonnucleoside reverse transcriptase inhibitors are chemical enhancers of dimerization of the HIV type 1 reverse transcriptase. Proc. Natl Acad. Sci. USA 98 (2001) 7188-7193
20. Morris M.C., Robert-Hebmann V., Chaloin L., Mery J., Heitz F., Devaux C., et al. A new potent HIV-1 reverse transcriptase inhibitor: a synthetic peptide derived from the interface subunit domain. J. Biol. Chem. 274 (1999) 24941-24946
21. Depollier J., Hourdou M.L., Aldrian-Herrada G., Rothwell P., Restle T., and Divita G. Insight into the mechanism of a peptide inhibitor of HIV reverse transcriptase dimerization. Biochemistry 44 (2005) 1909-1918
22. Kati W.M., Johnson K.A., Jerva L.F., and Anderson K.S. Mechanism and fidelity of HIV reverse transcriptase. J. Biol. Chem. 267 (1992) 25988-25997
23. Rittinger K., Divita G., and Goody R.S. Human immunodeficiency virus reverse transcriptase substrate-induced conformational changes and the mechanism of inhibition by nonnucleoside inhibitors. Proc. Natl Acad. Sci. USA 92 (1995) 8046-8049
24. Spence R.A., Kati W.M., Anderson K.S., and Johnson K.A. Mechanism of inhibition of HIV-1 reverse transcriptase by nonnucleoside inhibitors. Science 267 (1995) 988-993
25. Sarafianos S.G., Clark Jr. A.D., Das K., Tuske S., Birktoft J.J., Ilankumaran P., et al. Structures of HIV-1 reverse transcriptase with pre- and post-translocation AZTMP-terminated DNA. EMBO J. 21 (2002) 6614-6624
26. Huang H., Chopra R., Verdine G.L., and Harrison S.C. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282 (1998) 1669-1675
27. Rodgers D.W., Gamblin S.J., Harris B.A., Ray S., Culp J.S., Hellmig B., et al. The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1. Proc. Natl Acad. Sci. USA 92 (1995) 1222-1226
28. Hsiou Y., Ding J., Das K., Clark Jr. A.D., Hughes S.H., and Arnold E. Structure of unliganded HIV-1 reverse transcriptase at 2.7 A resolution: implications of conformational changes for polymerization and inhibition mechanisms. Structure 4 (1996) 853-860
29. Esnouf R., Ren J., Ross C., Jones D., Stammers D., and Stuart D. Mechanism of inhibition of HIV-1 reverse transcriptase by non-nucleoside inhibitors. Nat. Struct. Biol. 2 (1995) 303-308
30. Tuske S., Sarafianos S.G., Clark Jr. A.D., Ding J., Naeger L.K., White K.L., et al. Structures of HIV-1 RT-DNA complexes before and after incorporation of the anti-AIDS drug tenofovir. Nat. Struct. Mol. Biol. (2004) 469-474
31. Tachedjian G., Aronson H.E., and Goff S.P. Analysis of mutations and suppressors affecting interactions between the subunits of the HIV type 1 reverse transcriptase. Proc. Natl Acad. Sci. USA 97 (2000) 6334-6339
32. Fisher T.S., Darden T., and Prasad V.R. Substitutions at Phe61 in the beta3-beta4 hairpin of HIV-1 reverse transcriptase reveal a role for the Fingers subdomain in strand displacement DNA synthesis. J. Mol. Biol. 325 (2003) 443-459
33. Fisher T.S., and Prasad V.R. Substitutions of Phe61 located in the vicinity of template 5′-overhang influence polymerase fidelity and nucleoside analog sensitivity of HIV-1 reverse transcriptase. J. Biol. Chem. 277 (2002) 22345-22352
34. Dash C., Fisher T.S., Prasad V.R., and Le Grice S.F. Examining interactions of HIV-1 reverse transcriptase with single-stranded template nucleotides by nucleoside analog interference. J. Biol. Chem. 281 (2006) 27873-27881
35. Garforth S.J., Kim T.W., Parniak M.A., Kool E.T., and Prasad V.R. 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 (2006) 38-49
36. Müller B., Restle T., Reinstein J., and Goody R.S. Interaction of fluorescently labeled dideoxynucleotides with HIV-1 reverse transcriptase. Biochemistry 30 (1991) 3709-3715
37. Divita G., Müller B., Immendorfer U., Gautel M., Rittinger K., Restle T., and Goody R.S. Kinetics of interaction of HIV reverse transcriptase with primer/template. Biochemistry 32 (1993) 7966-7971
38. Wohrl B.M., Krebs R., Goody R.S., and Restle T. Refined model for primer/template binding by HIV-1 reverse transcriptase: pre-steady-state kinetic analyses of primer/template binding and nucleotide incorporation events distinguish between different binding modes depending on the nature of the nucleic acid substrate. J. Mol. Biol. 292 (1999) 333-344
39. Divita G., Rittinger K., Restle T., Immendorfer U., and Goody R.S. Conformational stability of dimeric HIV-1 and HIV-2 reverse transcriptases. Biochemistry 34 (1995) 16337-16346
40. Ren J., Bird L.E., Chamberlain P.P., Stewart-Jones G.B., Stuart D.I., and Stammers D.K. Structure of HIV-2 reverse transcriptase at 2.35 A resolution and the mechanism of resistance to non-nucleoside inhibitors. Proc. Natl Acad. Sci. USA 99 (2002) 14410-14415
41. Sarafianos S.G., Clark Jr. A.D., Tuske S., Squire C.J., Das K., Sheng D., et al. Trapping HIV-1 reverse transcriptase before and after translocation on DNA. J. Biol. Chem. 278 (2003) 16280-16288
42. Peletskaya E.N., Kogon A.A., Tuske S., Arnold E., and Hughes S.H. Nonnucleoside inhibitors binding affects the interactions of the finger subdomain of human immunodeficiency virus type 1 reverse transcriptase with DNA. J. Virol. 78 (2004) 3387-3397
43. Wohrl B.M., Tantillo C., Arnold E., and Le Grice S.F. An expanded model of replicating human immunodeficiency virus reverse transcriptase. Biochemistry 34 (1995) 5343-5356
44. Kew Y., Olsen L.R., Japour A.J., and Prasad V.R. Insertions into the beta3-beta4 hairpin loop of HIV-1 reverse transcriptase reveal a role for fingers subdomain in processive polymerization. J. Biol. Chem. 273 (1998) 7529-7537
45. Prasad V.R., Lowy I., de los Santos T., Chiang L., and Goff S.P. Isolation and characterization of a dideoxyguanosine triphosphate-resistant mutant of human immunodeficiency virus reverse transcriptase. Proc. Natl Acad. Sci. USA 88 (1991) 11363-11367
46. Barman T.E., and Travers F. The rapid-flow-quench method in the study of fast reactions in biochemistry: extension to subzero conditions. Methods Biochem. Anal. 31 (1985) 1-59