Sequence and structural determinants required for priming of plus- strand DNA synthesis by the human immunodeficiency virus type 1 polypurine tract

Journal of Virology

Volumn 70, Issue 8, 1996, Pages 5288-5296

  Powell, Michael D ^a   Levin, Judith G ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS DNA;

ARTICLE; DNA SYNTHESIS; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEQUENCE ANALYSIS; VIRUS DNA CELL DNA INTERACTION; VIRUS TRANSCRIPTION;

EID: 0029955712     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.70.8.5288-5296.1996     Document Type: Article

References (64)

1. Ben-Artzi, H., E. Zeelon, B. Amit, A. Wortzel, M. Gorecki, and A. Panet. 1993. RNase H activity of reverse transcriptases on substrates derived from the 5′ end of retroviral genome. J. Biol. Chem. 268:16465-16471.
2. Boone, L. R., and A. M. Skalka. 1993. Strand displacement synthesis by reverse transcriptase, p. 119-133. In A. M. Skalka and S. P. Goff (ed.), Reverse transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
3. Bowman, E. H., V. K. Pathak, and W.-S. Hu. 1996. Efficient initiation and strand transfer of polypurine tract-primed plus-strand DNA prevent strand transfer of internally initiated plus-strand DNAs. J. Virol. 70:1687-1694.
4. Chakrabarti, L., M. Guyader, M. Alizon, M. D. Daniel, R. C. Desrosiers, P. Tiollais, and P. Sonigo. 1987. Sequence of simian immunodeficiency virus from macaque and its relationship to other human and simian retroviruses. Nature (London) 328:543-547.
5. Champoux, J. J. 1993. Roles of ribonuclease H in reverse transcription, p. 103-117. In A. M. Skalka and S. P. Goff (ed.), Reverse transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
6. Champoux, J. J., E. Gilboa, and D. Baltimore. 1984. Mechanism of RNA primer removal by the RNase H activity of avian myeloblastosis virus reverse transcriptase. J. Virol. 49:686-691.
7. Charneau, P., M. Alizon, and F. Clavel. 1992. A second origin of DNA plus-strand synthesis is required for optimal human immunodeficiency virus replication. J. Virol. 66:2814-2820.
8. Charneau, P., and F. Clavel. 1991. A single-stranded gap in human immunodeficiency virus unintegrated linear DNA defined by a central copy of the polypurine tract. J. Virol. 65:2415-2421.
9. Charneau, P., G. Mirambeau, P. Roux, S. Paulous, H. Buc, and F. Clavel. 1994. HIV-1 reverse transcription. A termination step at the center of the genome. J. Mol. Biol. 241:651-662.
10. Cirino, N. M., C. E. Cameron, J. S. Smith, J. W. Rausch, M. J. Roth, S. J. Benkovic, and S. F. J. Le Grice. 1995. Divalent cation modulation of the ribonuclease functions of human immunodeficiency virus reverse transcriptase. Biochemistry 34:9936-9943.
11. Collett, M. S., P. Dierks, J. T. Parsons, and A. J. Faras. 1978. RNase H hydrolysis of the 5′ terminus of the avian sarcoma virus genome during reverse transcription. Nature (London) 272:181-184.
12. DeStefano, J. J., R. G. Buiser, L. M. Mallaber, T. W. Myers, R. A. Bambara, and P. J. Fay. 1991. Polymerization and RNase H activities of reverse transcriptases from avian myeloblastosis, human immunodeficiency, and Moloney murine leukemia viruses are functionally uncoupled. J. Biol. Chem. 266:7423-7431.
13. Fedoroff, O. Y., M. Salazar, and B. R. Reid. 1993. Structure of a DNA:RNA hybrid duplex. Why RNase H does not cleave pure RNA. J. Mol. Biol. 233:509-523.
14. Finston, W. I., and J. J. Champoux. 1984. RNA-primed initiation of Moloney murine leukemia virus plus strands by reverse transcriptase in vitro. J. Virol. 51:26-33.
15. Fu, T.-B., and J. Taylor. 1992. When retroviral reverse transcriptases reach the end of their RNA templates. J. Virol. 66:4271-4278.
16. Fuentes, G. M., L. Rodriguez-Rodriguez, P. J. Fay, and R. A. Bambara. 1995. Use of an oligoribonucleotide containing the polypurine tract sequence as a primer by HIV reverse transcriptase. J. Biol. Chem. 270:28169-28176.
17. Furfine, E. S., and J. E. Reardon. 1991. Reverse transcriptase · RNase H from the human immunodeficiency virus. Relationship of the DNA polymerase and RNA hydrolysis activities. J. Biol. Chem. 266:406-412.
18. Gilboa, E., S. W. Mitra, S. Goff, and D. Baltimore. 1979. A detailed model of reverse transcription and tests of crucial aspects. Cell 18:93-100.
19. Gopalakrishnan, V., J. A. Peliska, and S. J. Benkovic. 1992. Human immunodeficiency virus type 1 reverse transcriptase: spatial and temporal relationship between the polymerase and RNase H activities. Proc. Natl. Acad. Sci. USA 89:10763-10767.
20. Guo, J., W. Wu, Z. Y. Yuan, K. Post, R. J. Crouch, and J. G. Levin. 1995. Defects in primer-template binding, processive DNA synthesis, and RNase H activity associated with chimeric reverse transcriptases having the murine leukemia virus polymerase domain joined to Escherichia coli RNase H. Biochemistry 34:5018-5029.
21. Guyader, M., M. Emerman, P. Sonigo, F. Clavel, L. Montagnier, and M. Alizon. 1987. Genome organization and transactivation of the human immunodeficiency virus type 2. Nature (London) 326:662-669.
22. Hansen, L. J., and S. B. Sandmeyer. 1990. Characterization of a transpositionally active Ty3 element and identification of the Ty3 integrase protein. J. Virol. 54:2599-2607.
23. Herr, W. 1984. Nucleotide sequence of AKV murine leukemia virus. J. Virol. 49:471-478.
24. Hu, W.-S., and H. M. Temin. 1990. Retroviral recombination and reverse transcription. Science 250:1227-1233.
25. Huber, H. E., and C. C. Richardson. 1990. Processing of the primer for plus strand DNA synthesis by human immunodeficiency virus 1 reverse transcriptase. J. Biol. Chem. 265:10565-10573.
26. Hung, S.-H., Q. Yu, D. M. Gray, and R. L. Ratliff. 1994. Evidence from CD spectra that d(purine) · r(pyrimidine) and r(purine) · d(pyrimidine) hybrids are in different structural classes. Nucleic Acids Res. 22:4326-4334.
27. Hungnes, O., E. Tjøtta, and B. Grinde. 1991. The plus strand is discontinuous in a subpopulation of unintegrated HIV-1 DNA. Arch. Virol. 116:133-141.
28. Hungnes, O., E. Tjøtta, and B. Grinde. 1992. Mutations in the central polypurine tract of HIV-1 result in delayed replication. Virology 190:440-442.
29. 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, 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 3.0 Å resolution shows bent DNA. Proc. Natl. Acad. Sci. USA 90:6320-6324.
30. Katz, R. A., and A. M. Skalka. 1994. The retroviral enzymes. Annu. Rev. Biochem. 63:133-173.
31. Kohlstaedt, L. A., J. Wang, J. M. Friedman, P. A. Rice, and T. A. Steitz. 1992. Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256:1783-1790.
32. Pro during murine leukemia virus assembly. J. Virol. 38:403-408.
33. Luo, G., L. Sharmeen, and J. Taylor. 1990. Specificities involved in the initiation of retroviral plus-strand DNA. J. Virol. 64:592-597.
34. Luo, G., and J. Taylor. 1990. Template switching by reverse transcriptase during DNA synthesis. J. Virol. 64:4321-4328.
35. Lys into human immunodeficiency virus type 1 particles. J. Virol. 68:2065-2072.
36. Miller, M. D., B. Wang, and F. D. Bushman, 1995. Human immunodeficiency virus type 1 preintegration complexes containing discontinuous plus strands are competent to integrate in vitro. J. Virol. 69:3938-3944.
37. Myers, G., B. Korber, B. H. Hahn, K.-T. Jeang, J. W. Mellors, F. E. Mc-Cutchan, L. E. Henderson, and G. N. Pavlakis. 1995. Human retroviruses and AIDS. A compilation and analysis of nucleic acid and amino acid sequences, p. I-A-376-379. Los Alamos National Laboratory, Los Alamos, N. Mex.
38. Oyama, F., R. Kikuchi, R. J. Crouch, and T. Uchida. 1989. Intrinsic properties of reverse transcriptase in reverse transcription. Associated RNase H is essentially regarded as an endonuclease. J. Biol. Chem. 264:18808-18817.
39. Panganiban, A. T., and D. Fiore. 1988. Ordered interstrand and intrastrand DNA transfer during reverse transcription. Science 241:1064-1069.
40. Peliska, J. A., and S. J. Benkovic. 1992. Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase. Science 258:1112-1118.
41. Peters, G. G., and J. Hu. 1980. Reverse transcriptase as the major determinant for selective packaging of tRNA's into avian sarcoma virus particles. J. Virol. 36:692-700.
42. Post, K., J. Guo, E. Kalman, T. Uchida, R. J. Crouch, and J. G. Levin. 1993. A large deletion in the connection subdomain of murine leukemia virus reverse transcriptase or replacement of the RNase H domain with Escherichia coli RNase H results in altered polymerase and RNase H activities. Biochemistry 32:5508-5517.
43. Pullen, K. A., and J. J. Champoux. 1990. Plus-strand origin for human immunodeficiency virus type 1: implications for integration. J. Virol. 64: 6274-6277.
44. Pullen, K. A., A. J. Rattray, and J. J. Champoux. 1993. The sequence features important for plus strand priming by human immunodeficiency virus type 1 reverse transcriptase. J. Biol. Chem. 268:6221-6227.
45. Randolph, C. A., and J. J. Champoux. 1994. The use of DNA and RNA oligonucleotides in hybrid structures with longer polynucleotide chains to probe the structural requirements for Moloney murine leukemia virus plus strand priming. J. Biol. Chem. 269:19207-19215.
46. Ratmeyer, L., R. Vinayak, Y. Y. Zhong, G. Zon, and W. D. Wilson. 1994. Sequence specific thermodynamic and structural properties for DNA · RNA duplexes. Biochemistry 33:5298-5304.
47. Ratner, L., W. Haseltine, R. Patarca, K. J. Livak, B. Starcich, S. F. Josephs, E. R. Doran, J. A. Rafalski, E. A. Whitehorn, K. Baumeister, L. Ivanoff, S. R. Petteway, Jr., M. L. Pearson, J. A. Lautenberger, T. S. Papas, J. Ghrayeb, N. T. Chang, R. C. Gallo, and F. Wong-Staal. 1985. Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature (London) 313:277-284.
48. Rattray, A. J., and J. J. Champoux. 1987. The role of Moloney murine leukemia virus RNase H activity in the formation of plus-strand primers. J. Virol. 61:2843-2851.
49. Rattray, A. J., and J. J. Champoux. 1989. Plus-strand priming by Moloney murine leukemia virus. The sequence features important for cleavage by RNase H. J. Mol. Biol. 208:445-456.
50. Resnick, R., C. A. Omer, and A, J. Faras. 1984. Involvement of retrovirus reverse transcriptase-associated RNase H in the initiation of strong-stop (+) DNA synthesis and the generation of the long terminal repeat. J. Virol. 51:813-821.
51. Sanchez-Pescador, R., M. D. Power, P. J. Barr, K. S. Sleimer, M. M. Stempien, S. L. Brown-Shimer, W. W. Gee, A. Renard, A. Randolph, J. A. Levy, D. Dina, and P. A. Luciw. 1985. Nucleotide sequence and expression of an AIDS-associated retrovirus (ARV-2). Science 227:484-492.
52. Sawyer, R. C., and H. Hanafusa. 1979. Comparison of the small RNAs of polymerase-deficient and polymerase-positive Rous sarcoma virus and another species of avian retrovirus. J. Virol. 29:863-871.
53. Schatz, O., J. Mous, and S. F. J. Le Grice. 1990. HIV-1 RT-associated ribonuclease H displays both endonuclease and 3′→5′ exonuclease activity. EMBO J. 9:1171-1176.
54. Shinnick, T. M., R. A. Lerner, and J. G. Sutcliffe. 1981. Nucleotide sequence of Moloney murine leukaemia virus. Nature (London) 293:543-548.
55. Smith, J. K., A. Cywinski, and J. M. Taylor. 1984 Specificity of initiation of plus-strand DNA by Rous sarcoma virus. J. Virol. 52:314-319.
56. Sonigo, P., M. Alizon, K. Staskus, D. Klatzmann, S. Cole, O. Danos, E. Retzel, P. Tiollais, A. Haase, and S. Wain-Hobson. 1985. Nucleotide sequence of the visna lentivirus: relationship to the AIDS virus. Cell 42:369-382.
57. 3 region of the Rous sarcoma virus genome provides a ris-acting function. J. Virol. 43:482-488.
58. Tanese, N., A. Telesnitsky, and S. P. Goff. 1991. Abortive reverse transcription by mutants of Moloney murine leukemia virus deficient in the reverse transcriptase-associated RNase H function. J. Virol. 65:4387-4397.
59. Telesnitsky, A., and S. P. Goff. 1993. Strong-stop strand transfer during reverse transcription, p. 49-83. In A. M. Skalka and S. P. Goff (ed.), Reverse transcriptase. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
60. Varmus, H., and P. Brown. 1989. Retroviruses, p. 53-108. In D. E. Berg and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
61. Varmus, H., and R. Swanstrom. 1984. Replication of retroviruses, p. 369-512. In R. Weiss, N. Teich, H. Varmus, and J. Coffin (ed.), Molecular biology of tumor viruses, RNA tumor viruses, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
62. Wain-Hobson, S., P. Sonigo, O. Danos, S. Cole, and M. Alizon. 1985. Nucleotide sequence of the AIDS virus, LAV. Cell 40:9-17.
63. Wilson, S. H., and J. Abbotts. 1992. tRNA in the molecular biology of retroviruses, p. 1-21. In D. L. Hatfield, B. J. Lee, and R. M. Pirtle (ed.), Transfer RNA in protein synthesis. CRC Press, Inc., Boca Raton, Fla.
64. Wöhrl, B. M., and K. Moelling. 1990. Interaction of HIV-1 ribonuclease H with polypurine tract containing RNA-DNA hybrids. Biochemistry 29:10141-10147.