Examining the ribonuclease H primer grip of HIV-1 reverse transcriptase by charge neutralization of RNA/DNA hybrids

Nucleic Acids Research

Volumn 36, Issue 20, 2008, Pages 6363-6371

  Dash, Chandravanu ^a   Scarth, Brian J ^b   Badorrek, Christopher ^a   Götte, Matthias ^b   Le Grice, Stuart F J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

METHYLPHOSPHONIC ACID; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DNA FOOTPRINTING; DNA RNA HYBRIDIZATION; DNA STRAND; DOWNSTREAM PROCESSING; ENZYME ACTIVE SITE; ENZYME LOCALIZATION; ENZYME MECHANISM; NONHUMAN; PRIORITY JOURNAL; STRUCTURAL GENE;

DNA; DNA FOOTPRINTING; DNA PRIMERS; HIV REVERSE TRANSCRIPTASE; MODELS, MOLECULAR; ORGANOPHOSPHORUS COMPOUNDS; RIBONUCLEASE H; RNA;

BACILLUS HALODURANS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 56649096052     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn678     Document Type: Article

References (39)

1. Huang,H., Chopra,R., Verdine,G.L. and Harrison,S.C. (1998) Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science, 282, 1669-1675.
2. Jacobo-Molina,A., Ding,J., Nanni,R.G., Clark,A.D. Jr, Lu,X., Tantillo,C., Williams,R.L., Kamer,G., Ferris,A.L., Clark,P. et al. (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.
3. Kohlstaedt,L.A., Wang,J., Friedman,J.M., Rice,P.A. and Steitz,T.A. (1992) Crystal structure at 3.5A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science, 256, 1783-1790.
4. 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 immunode.ciency virus type 1. Proc. Natl Acad. Sci. USA, 92, 1222-1226.
5. Sarafianos,S.G., Das,K., Tantillo,C., Clark,A.D. Jr, Ding,J., Whitcomb,J.M., Boyer,P.L., Hughes,S.H. and Arnold,E. (2001) Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J., 20, 1449-1461.
6. Curr,K., Tripathi,S., Lennerstrand,J., Larder,B.A. and Prasad,V.R. (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.
7. Boyer,P.L., Sarafianos,S.G., Arnold,E. and Hughes,S.H. (2002) Nucleoside analog resistance caused by insertions in the fingers of human immunodeficiency virus type 1 reverse transcriptase involves ATP-mediated excision. J. Virol., 76, 9143-9151.
8. Boyer,P.L., Ferris,A.L., Clark,P., Whitmer,J., Frank,P., Tantillo,C., Arnold,E. and Hughes,S.H. (1994) Mutational analysis of the fingers and palm subdomains of human immunodeficiency virus type-1 (HIV-1) reverse transcriptase. J. Mol. Biol., 243, 472-483.
9. Wohrl,B.M., Krebs,R., Thrall,S.H., Le Grice,S.F., Scheidig,A.J. and Goody,R.S. (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.
10. Ghosh,M., Jacques,P.S., Rodgers,D.W., Ottman,M., Darlix,J.L. and Le Grice,S.F. (1996) Alterations to the primer grip of p66 HIV-1 reverse transcriptase and their consequences for template-primer utilization. Biochemistry, 35, 8553-8562.
11. Jacques,P.S., Wohrl,B.M., Ottmann,M., Darlix,J.L. and Le Grice,S.F. (1994) Mutating the 'primer grip' of p66 HIV-1 reverse transcriptase implicates tryptophan-229 in template-primer utilization. J. Biol. Chem., 269, 26472-26478.
12. Chao,S.F., Chan,V.L., Juranka,P., Kaplan,A.H., Swanstrom,R. and Hutchison,C.A. 3rd (1995) Mutational sensitivity patterns define critical residues in the palm subdomain of the reverse transcriptase of human immunodeficiency virus type 1. Nucleic Acids Res., 23, 803-810.
13. Rausch,J.W., Lener,D., Miller,J.T., Julias,J.G., Hughes,S.H. and Le Grice,S.F. (2002) Altering the RNase H primer grip of human immunodeficiency virus reverse transcriptase modifies cleavage specificity. Biochemistry, 41, 4856-4865.
14. Julias,J.G., McWilliams,M.J., Sarafianos,S.G., Alvord,W.G., Arnold,E. and Hughes,S.H. (2003) Mutation of amino acids in the connection domain of human immunodeficiency virus type 1 reverse transcriptase that contact the template-primer affects RNase H activity. J. Virol., 77, 8548-8554.
15. Nowotny,M., Gaidamakov,S.A., Crouch,R.J. and Yang,W. (2005) Crystal structures of RNase H bound to an RNA/DNA hybrid: Substrate specificity and metal-dependent catalysis. Cell, 121, 1005-1016.
16. Nowotny,M., Gaidamakov,S.A., Ghirlando,R., Cerritelli,S.M., Crouch,R.J. and Yang,W. (2007) Structure of human RNase H1 complexed with an RNA/DNA hybrid: Insight into HIV reverse transcription. Mol. Cell, 28 264-276.
17. Nowotny,M. and Yang,W. (2006) Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. EMBO J. 25, 1924-1933.
18. Cannistraro,V.J. and Taylor,J.S. (2004) DNA-thumb interactions and processivity of T7 DNA polymerase in comparison to yeast polymerase eta. J. Biol. Chem., 279, 18288-18295.
19. Cannistraro,V.J. and Taylor,J.S. (2007) Ability of polymerase eta and T7 DNA polymerase to bypass bulge structures. J. Biol. Chem., 282 11188-11196.
20. Liu,J., Declais,A.C. and Lilley,D.M. (2006) Mechanistic aspects of the DNA junction-resolving enzyme T7 endonuclease I. Biochemistry, 45, 3934-3942.
21. Tian,L., Claeboe,C.D., Hecht,S.M. and Shuman,S. (2004) Remote phosphate contacts trigger assembly of the active site of DNA topoisomerase IB. Structure, 12, 31-40.
22. Hardwidge,P.R., Zimmerman,J.M. and Maher,L.J. 3rd (2002) Charge neutralization and DNA bending by the Escherichia coli catabolite activator protein. Nucleic Acids Res., 30, 1879-1885.
23. Kosikov,K.M., Gorin,A.A., Lu,X.J., Olson,W.K. and Manning,G.S. (2002) Bending of DNA by asymmetric charge neutralization: All-atom energy simulations. J. Am. Chem. Soc., 124, 4838-4847.
24. Okonogi,T.M., Alley,S.C., Harwood,E.A., Hopkins,P.B. and Robinson,B.H. (2002) Phosphate backbone neutralization increases duplex DNA flexibility: A model for protein binding. Proc. Natl Acad. Sci. USA 99, 4156-4160.
25. Zuker,M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
26. Le Grice,S.F., Cameron,C.E. and Benkovic,S.J. (1995) Purification and characterization of human immunodeficiency virus type 1 reverse transcriptase. Methods Enzymol., 262, 130-144.
27. Dash,C., Rausch,J.W. and Le Grice,S.F.J. (2004) Using pyrrolodeoxycytosine to probe RNA/DNA hybrids containing the human immunodeficiency virus type-1 3′ polypurine tract. Nucleic Acids Res., 32, 1539-1547.
28. Gotte,M., Maier,G., Gross,H.J. and 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.
29. Marchand,B. and Gotte,M. (2003) Site-specific footprinting reveals differences in the translocation status of HIV-1 reverse transcriptase. Implications for polymerase translocation and drug resistance. J. Biol. Chem., 278, 35362-35372.
30. Xu,Y., Potapova,O., Leschziner,A.E., Grindley,N.D. and Joyce,C.M. (2001) Contacts between the 50 nuclease of DNA polymerase I and its DNA substrate. J. Biol. Chem., 276, 30167-30177.
31. Peliska,J.A. and Benkovic,S.J. (1992) Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase. Science, 258, 1112-1118.
32. Schultz,S.J., Zhang,M. and Champoux,J.J. (2006) Sequence, distance, and accessibility are determinants of 50-end-directed cleavages by retroviral RNases H. J. Biol. Chem., 281, 1943-1955.
33. Strauss-Soukup,J.K., Rodrigues,P.D. and Maher,L.J. 3rd (1998) Effect of base composition on DNA bending by phosphate neutralization. Biophys. Chem., 72, 297-306.
34. Lener,D., Kvaratskhelia,M. and Le Grice,S.F. (2003) Nonpolar thymine isosteres in the Ty3 polypurine tract DNA template modulate processing and provide a model for its recognition by Ty3 reverse transcriptase. J. Biol. Chem., 278, 26526-26532.
35. Yi-Brunozzi,H.Y., Brinson,R.G., Brabazon,D.M., Lener,D., Le Grice,S.F. and Marino,J.P. (2008) High-resolution NMR analysis of the conformations of native and base analog substituted retroviral and LTR-retrotransposon PPT primers. Chem. Biol., 15, 254-262.
36. Marchand,B., Tchesnokov,E.P. and Gotte,M. (2007) The pyrophosphate analogue foscarnet traps the pre-translocational state of HIV-1 reverse transcriptase in a Brownian ratchet model of polymerase translocation. J. Biol. Chem., 282, 3337-3346.
37. 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.
38. Reardon,J.E. (1993) Human immunodeficiency virus reverse transcriptase. A kinetic analysis of RNA-dependent and DNA-dependent DNA polymerization. J. Biol. Chem., 268, 8743-8751.
39. Nowotny,M., Cerritelli,S.M., Ghirlando,R., Gaidamakov,S.A., Crouch,R.J. and Yang,W. (2008) Specific recognition of RNA/DNA hybrid and enhancement of human RNase H1 activity by HBD. EMBO J., 27, 1172-1181.