Viral reverse transcriptases show selective high affinity binding to DNA-DNA primer-templates that resemble the polypurine tract

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Nair, Gauri R ^a   Dash, Chandravanu ^b,c   Le Grice, Stuart F J ^b   DeStefano, Jeffrey J ^a  

^a Bldg 142   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c MEHARRY MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; DOUBLE STRANDED DNA; GUANINE; PRIMER DNA; RNA DIRECTED DNA POLYMERASE;

3' UNTRANSLATED REGION; AMINO TERMINAL SEQUENCE; ARTICLE; AVIAN MYELOBLASTOSIS VIRUS; BINDING AFFINITY; CONTROLLED STUDY; DNA SEQUENCE; DNA TEMPLATE; ENZYME BINDING; MOLONEY LEUKEMIA ONCOVIRUS; NONHUMAN; PROTEIN DNA BINDING; RETROPOSON; SEQUENCE ANALYSIS;

AVIAN MYELOBLASTOSIS VIRUS; BASE SEQUENCE; DNA PRIMERS; DNA, VIRAL; GC RICH SEQUENCE; MOLONEY MURINE LEUKEMIA VIRUS; PROTEIN BINDING; RETROELEMENTS; RNA-DIRECTED DNA POLYMERASE; SUBSTRATE SPECIFICITY;

AVIAN MYELOBLASTOSIS VIRUS; MOLONEY MURINE LEUKEMIA VIRUS;

EID: 84864412192     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041712     Document Type: Article

References (50)

1. Goff SP, Telesnitsky A, (1997) Reverse transcriptase and the generation of retroviral DNA. In: Coffin JM, Hughes SH, Varmus HE, editors. Retroviruses Cold Spring Harbor, NY Cold Spring Harbor Press pp. 121-160.
2. Arhel NJ, Souquere-Besse S, Charneau P, (2006) Wild-type and central DNA flap defective HIV-1 lentiviral vector genomes: intracellular visualization at ultrastructural resolution levels. Retrovirology 3: 38.
3. Park F, Kay MA, (2001) Modified HIV-1 based lentiviral vectors have an effect on viral transduction efficiency and gene expression in vitro and in vivo. Mol Ther 4: 164-173.
4. Skasko M, Kim B, (2008) Compensatory role of human immunodeficiency virus central polypurine tract sequence in kinetically disrupted reverse transcription. J Virol 82: 7716-7720.
5. Zennou V, Petit C, Guetard D, Nerhbass U, Montagnier L, et al. (2000) HIV-1 genome nuclear import is mediated by a central DNA flap. Cell 101: 173-185.
6. Jacob DT, DeStefano JJ, (2008) A new role for HIV nucleocapsid protein in modulating the specificity of plus strand priming. Virology 378: 385-396.
7. Post K, Kankia B, Gopalakrishnan S, Yang V, Cramer E, et al. (2009) Fidelity of plus-strand priming requires the nucleic acid chaperone activity of HIV-1 nucleocapsid protein. Nucleic Acids Res 37: 1755-1766.
8. Powell MD, Levin JG, (1996) Sequence and structural determinants required for priming of plus-strand DNA synthesis by the human immunodeficiency virus type 1 polypurine tract. J Virol 70: 5288-5296.
9. Kelleher CD, Champoux JJ, (2000) RNA degradation and primer selection by Moloney murine leukemia virus reverse transcriptase contribute to the accuracy of plus strand initiation. J Biol Chem 275: 13061-13070.
10. Schultz SJ, Zhang M, Kelleher CD, Champoux JJ, (1999) Polypurine tract primer generation and utilization by Moloney murine leukemia virus reverse transcriptase. J Biol Chem 274: 34547-34555.
11. Klarmann GJ, Yu H, Chen X, Dougherty JP, Preston BD, (1997) Discontinuous plus-strand DNA synthesis in human immunodeficiency virus type 1-infected cells and in a partially reconstituted cell-free system. J Virol 71: 9259-9269.
12. Kung HJ, Fung YK, Majors JE, Bishop JM, Varmus HE, (1981) Synthesis of plus strands of retroviral DNA in cells infected with avian sarcoma virus and mouse mammary tumor virus. J Virol 37: 127-138.
13. Miller MD, Wang B, Bushman FD, (1995) Human immunodeficiency virus type 1 preintegration complexes containing discontinuous plus strands are competent to integrate in vitro. J Virol 69: 3938-3944.
14. Kvaratskhelia M, Budihas SR, Le Grice SF, (2002) Pre-existing distortions in nucleic acid structure aid polypurine tract selection by HIV-1 reverse transcriptase. J Biol Chem 277: 16689-16696.
15. Rausch JW, Le Grice SF, (2004) 'Binding, bending and bonding': polypurine tract-primed initiation of plus-strand DNA synthesis in human immunodeficiency virus. Int J Biochem Cell Biol 36: 1752-1766.
16. Cote ML, Pflomm M, Georgiadis MM, (2003) Staying straight with A-tracts: a DNA analog of the HIV-1 polypurine tract. J Mol Biol 330: 57-74.
17. Jones FD, Hughes SH, (2007) In vitro analysis of the effects of mutations in the G-tract of the human immunodeficiency virus type 1 polypurine tract on RNase H cleavage specificity. Virology 360: 341-349.
18. Julias JG, McWilliams MJ, Sarafianos SG, Alvord WG, Arnold E, et al. (2004) Effects of mutations in the G tract of the human immunodeficiency virus type 1 polypurine tract on virus replication and RNase H cleavage. J Virol 78: 13315-13324.
19. Brinson RG, Turner KB, Yi-Brunozzi HY, Le Grice SF, Fabris D, et al. (2009) Probing anomalous structural features in polypurine tract-containing RNA-DNA hybrids with neomycin B. Biochemistry 48: 6988-6997.
20. Dash C, Marino JP, Le Grice SF, (2006) Examining Ty3 polypurine tract structure and function by nucleoside analog interference. J Biol Chem 281: 2773-2783.
21. Turner KB, Yi-Brunozzi HY, Brinson RG, Marino JP, Fabris D, et al. (2009) SHAMS: combining chemical modification of RNA with mass spectrometry to examine polypurine tract-containing RNA/DNA hybrids. RNA 15: 1605-1613.
22. DeStefano JJ, (1995) The orientation of binding of human immunodeficiency virus reverse transcriptase on nucleic acid hybrids. Nucleic Acids Res 23: 3901-3908.
23. DeStefano JJ, Bambara RA, Fay PJ, (1993) Parameters that influence the binding of human immunodeficiency virus reverse transcriptase to nucleic acid structures. Biochemistry 32: 6908-6915.
24. DeStefano JJ, Cristofaro JV, Derebail S, Bohlayer WP, Fitzgerald-Heath MJ, (2001) Physical mapping of HIV reverse transcriptase to the 5′ end of RNA primers. J Biol Chem 276: 32515-32521.
25. Palaniappan C, Kim JK, Wisniewski M, Fay PJ, Bambara RA, (1998) Control of initiation of viral plus strand DNA synthesis by HIV reverse transcriptase. J Biol Chem 273: 3808-3816.
26. Abbondanzieri EA, Bokinsky G, Rausch JW, Zhang JX, Le Grice SF, et al. (2008) Dynamic binding orientations direct activity of HIV reverse transcriptase. Nature 453: 184-189.
27. DeStefano JJ, Cristofaro JV, (2006) Selection of primer-template sequences that bind human immunodeficiency virus reverse transcriptase with high affinity. Nucleic Acids Res 34: 130-139.
28. Pullen KA, Rattray AJ, Champoux JJ, (1993) The sequence features important for plus strand priming by human immunodeficiency virus type 1 reverse transcriptase. J Biol Chem 268: 6221-6227.
29. Gorshkova II, Rausch JW, Le Grice SF, Crouch RJ, (2001) HIV-1 reverse transcriptase interaction with model RNA-DNA duplexes. Anal Biochem 291: 198-206.
30. Patel PH, Jacobo-Molina A, Ding J, Tantillo C, Clark AD Jr, et al. (1995) Insights into DNA polymerization mechanisms from structure and function analysis of HIV-1 reverse transcriptase. Biochemistry 34: 5351-5363.
31. Rausch JW, Grice MK, Henrietta M, Nymark M, Miller JT, et al. (2000) Interaction of p55 reverse transcriptase from the Saccharomyces cerevisiae retrotransposon Ty3 with conformationally distinct nucleic acid duplexes. J Biol Chem 275: 13879-13887.
32. DeStefano JJ, Nair GR, (2008) Novel aptamer inhibitors of human immunodeficiency virus reverse transcriptase. Oligonucleotides 18: 133-144.
33. Cristofaro JV, Rausch JW, Le Grice SF, DeStefano JJ, (2002) Mutations in the ribonuclease H active site of HIV-RT reveal a role for this site in stabilizing enzyme-primer-template binding. Biochemistry 41: 10968-10975.
34. Schatz O, Cromme FV, Gruninger-Leitch F, Le Grice SFJ, (1989) Point mutations in conserved amino acid residues within the C-terminal domain of HIV-1 reverse transcriptase specifically repress RNase H function. FEBS Letters 257: 311-314.
35. Hansen LJ, Chalker DL, Sandmeyer SB, (1988) Ty3, a yeast retrotransposon associated with tRNA genes, has homology to animal retroviruses. Mol Cell Biol 8: 5245-5256.
36. Telesnitsky A, Goff SP, (1993) Reverse Transcriptase; In: Shalka AM, Goff SP, editors. Cold Spring Harbor, N. Y. Cold Spring Harbor Laboratory Press pp. 49-83.
37. Xiong Y, Eickbush TH, (1990) Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9: 3353-3362.
38. Nakamura TM, Morin GB, Chapman KB, Weinrich SL, Andrews WH, et al. (1997) Telomerase catalytic subunit homologs from fission yeast and human. Science 277: 955-959.
39. Boeke JD, Stoye JP, (1997) Retrotransposons, endognous retroviruses, and the evolution of retroelements. In: Coffin JM, Hughes SH, Varmus HE, editors. Retroviruses Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press pp. 343-435.
40. Michalowski D, Chitima-Matsiga R, Held DM, Burke DH, (2008) Novel bimodular DNA aptamers with guanosine quadruplexes inhibit phylogenetically diverse HIV-1 reverse transcriptases. Nucleic Acids Res 36: 7124-7135.
41. Schneider DJ, Feigon J, Hostomsky Z, Gold L, (1995) High-affinity ssDNA inhibitors of the reverse transcriptase of type 1 human immunodeficiency virus. Biochemistry 34: 9599-9610.
42. Sissi C, Gatto B, Palumbo M, (2011) The evolving world of protein-G-quadruplex recognition: A medicinal chemist's perspective. Biochimie 93: 1219-1230.
43. Doolittle RF, Feng DF, Johnson MS, McClure MA, (1989) Origins and evolutionary relationships of retroviruses. Q Rev Biol 64: 1-30.
44. McClure MA, (1991) Evolution of retroposons by acquisition or deletion of retrovirus-like genes. Mol Biol Evol 8: 835-856.
45. Oh J, Chang KW, Alvord WG, Hughes SH, (2006) Alternate polypurine tracts affect rous sarcoma virus integration in vivo. J Virol 80: 10281-10284.
46. Robson ND, Telesnitsky A, (2000) Selection of optimal polypurine tract region sequences during Moloney murine leukemia virus replication. J Virol 74: 10293-10303.
47. Sambrook J, Russell DW, (2001) Molecular Cloning: A Laboratory Manual Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press.
48. Peliska JA, Benkovic SJ, (1992) Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase. Science 258: 1112-1118.
49. Hsieh JC, Zinnen S, Modrich P, (1993) Kinetic mechanism of the DNA-dependent DNA polymerase activity of human immunodeficiency virus reverse transcriptase. J Biol Chem 268: 24607-24613.
50. Reardon JE, (1992) Human Immunodeficiency Virus Reverse Transcriptase: Steady-State and Pre-Steady-State Kinetics of Nucleotide Incorporation. Biochemistry 31: 4473-4479.