Specific cleavages by RNase H facilitate initiation of plus-strand RNA synthesis by Moloney murine leukemia virus

Journal of Virology

Volumn 77, Issue 9, 2003, Pages 5275-5285

  Schultz, Sharon J ^a   Zhang, Miaohua ^a   Champoux, James J ^a,b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PRIMER DNA; RIBONUCLEASE; RIBONUCLEASE H; RNA DIRECTED DNA POLYMERASE;

3' UNTRANSLATED REGION; ARTICLE; COMPARATIVE STUDY; DATA ANALYSIS; DNA STRAND; DNA SYNTHESIS; DOWNSTREAM PROCESSING; ENZYME BINDING; ENZYME SPECIFICITY; LEUKEMIA VIRUS; MOLONEY LEUKEMIA ONCOVIRUS; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; RNA SYNTHESIS;

ANIMALS; BASE SEQUENCE; DNA, VIRAL; MICE; MOLECULAR SEQUENCE DATA; MOLONEY MURINE LEUKEMIA VIRUS; RIBONUCLEASE H, CALF THYMUS; RNA; RNA, VIRAL; RNA-DIRECTED DNA POLYMERASE; SUBSTRATE SPECIFICITY;

EID: 0037404503     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.9.5275-5285.2003     Document Type: Article

References (51)

1. Amacker, M., M. Hottiger, and U. Hubscher. 1995. Feline immunodeficiency virus reverse transcriptase: expression, functional characterization, and reconstitution of the 66- and 51-kilodalton subunits. J. Virol. 69:6273-6279.
2. Arts, E. J., and S. F. J. LeGrice. 1998. Interaction of retroviral reverse transcriptase with template-primer duplexes during replication. Prog. Nucleic Acid Res. Mol. Biol. 58:339-393.
3. Champoux, J. J. 1993. Roles of ribonuclease H in reverse transcription, p. 103-118. In A. M. Skalka and S. P. Goff (ed.), Reverse transcriptase. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
4. Coffin, J. M., S. H. Hughes, and H. E. Varmus. 1997. Retroviruses. Cold Spring Harbor Laboratory Press, Plainview, N.Y.
5. DeStefano, J. J. 1995. The orientation of binding of human immunodeficiency virus reverse transcriptase on nucleic acid hybrids. Nucleic Acids Res. 23:3901-3908.
6. 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 the reverse transcriptases from avian myeloblastosis, human immunodeficiency, and Moloney murine leukemia viruses are functionally uncoupled. J. Biol. Chem. 266:7423-7431.
7. DeStefano, J. J., J. V. Cristofaro, S. Derebail, W. P. Bohlayer, and M. J. Fitzgerald-Heath. 2001. Physical mapping of HIV reverse transcriptase to the 5′ end of RNA primers. J. Biol. Chem. 276:32515-32521.
8. DeStefano, J. J., L. M. Mallaber, P. J. Fay, and R. A. Bambara. 1993. Determinants of the RNase H cleavage specificity of human immunodeficiency virus reverse transcriptase. Nucleic Acids Res. 21:4330-4338.
9. DeStefano, J. J., L. M. Mallaber, P. J. Fay, and R. A. Bambara. 1994. Quantitative analysis of RNA cleavage during RNA-directed DNA synthesis by human immunodeficiency and avian myeloblastosis virus reverse transcriptases. Nucleic Acids Res. 22:3793-3800.
10. Dudding, L. R., N. C. Nkabinde, and V. Mizrahi. 1991. Analysis of the RNA- and DNA-dependent DNA polymerase activities of point mutants of HIV-1 reverse transcriptase lacking ribonuclease H activity. Biochemistry 30:10498-10506.
11. Fedoroff, O. Y., Y. Ge, and B. R. Reid. 1997. Solution structure of r(gag gaeug):d(CAGTCCTC) hybrid: implications for the initiation of HIV-1 (+)-strand synthesis. J. Mol. Biol. 269:225-239.
12. 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.
13. Fuentes, G. M., P. J. Fay, and R. A. Bambara. 1996. Relationship between plus strand DNA synthesis and removal of downstream segments of RNA by human immunodeficiency virus, murine leukemia virus and avian myeloblastoma virus reverse transcriptases. Nucleic Acids Res. 24:1719-1726.
14. 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.
15. Fuentes, G. M., L. Rodriguez-Rodriguez, C. Palaniappan, P. J. Fay, and R. A. Bambara. 1996. Strand displacement synthesis of the long terminal repeats by HIV reverse transcriptase. J. Biol. Chem. 271:1966-1971.
16. 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.
17. 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.
18. Gotte, M., M. Kameoka, N. McLellan, L. Cellai, and M. A. Wainberg. 2001. Analysis of efficiency and fidelity of HIV-1 (+)-strand DNA synthesis reveals a novel rate-limiting step during retroviral reverse transcription. J. Biol. Chem. 276:6711-6719.
19. Gotte, M., G. Maier, A. M. Onori, L. Cellai, M. A. Wainberg, and H. Heumann. 1999. Temporal coordination between initiation of HIV (+)-strand DNA synthesis and primer removal. J. Biol. Chem. 274:11159-11169.
20. Hottiger, M., V. N. Podust, R. L. Thimmig, C. McHenry, and U. Hubscher. 1994. Strand displacement activity of the human immunodeficiency virus type 1 reverse transcriptase heterodimer and its individual subunits. J. Biol. Chem. 269:986-991.
21. Huber, H. E., J. M. McCoy, J. S. Seehra, and C. C. Richardson. 1989. Human immunodeficiency virus 1 reverse transcriptase. Template binding, processivity, strand displacement synthesis, and template switching. J. Biol. Chem. 264:4669-4678.
22. 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.
23. Isel, C., J. M. Lanchy, S. F. Le Grice, C. Ehresmann, B. Ehresmann, and R. Marquet. 1996. Specific initiation and switch to elongation of human immunodeficiency virus type 1 reverse transcription require the post-transcriptional modifications of primer tRNA3Lys. EMBO J. 15:917-924.
24. Kati, W. M., K. A. Johnson, L. F. Jerva, and K. S. Anderson. 1992. Mechanism and fidelity of HIV reverse transcriptase. J. Biol. Chem. 267:25988-25997.
25. Kelleher, C. D., and J. J. Champoux. 1998. Characterization of RNA strand displacement synthesis by Moloney murine leukemia virus reverse transcriptase. J. Biol. Chem. 273:9976-9986.
26. Kelleher, C. D., and J. J. Champoux. 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.
27. Klarmann, G. J., H. Yu, X. Chen, J. P. Dougherty, and B. D. Preston. 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.
28. Kvaratskhelia, M., S. R. Budihas, and S. F. Le Grice. 2002. Pre-existing distortions in nucleic acid structure aid polypurine tract selection by HIV-1 reverse transcriptase. J. Biol. Chem. 277:16689-16696.
29. Lanchy, J. M., G. Keith, S. F. Le Grice, B. Ehresmann, C. Ehresmann, and R. Marquet. 1998. Contacts between reverse transcriptase and the primer strand govern the transition from initiation to elongation of HIV-1 reverse transcription. J. Biol. Chem. 273:24425-24432.
30. Metzger, W., T. Hermann, O. Schatz, S. F. Le Grice, and H. Heumann. 1993. Hydroxyl radical footprint analysis of human immunodeficiency virus reverse transcriptase-template primer complexes. Proc. Natl. Acad. Sci. USA 90:5909-5913.
31. Palaniappan, C., J. K. Kim, M. Wisniewski, P. J. Fay, and R. A. Bambara. 1998. Control of initiation of viral plus strand DNA synthesis by HIV reverse transcriptase. J. Biol. Chem. 273:3808-3816.
32. Peliska, J. A., and S. J. Benkovic. 1992. Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase. Science 258:1112-1118.
33. Powell, M. D., and J. G. Levin. 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.
34. 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.
35. 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.
36. 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.
37. Schultz, S. J., M. Zhang, C. D. Kelleher, and J. J. Champoux. 2000. Analysis of plus-strand primer selection, removal, and reutilization by retroviral reverse transcriptases. J. Biol. Chem. 275:32299-32309.
38. Schultz, S. J., M. Zhang, C. D. Kelleher, and J. J. Champoux. 1999. Polypurine tract primer generation and utilization by Moloney murine leukemia virus reverse transcriptase. J. Biol. Chem. 274:34547-34555.
39. Shinnick, T. M., R. A. Lerner, and J. G. Sutcliffe. 1981. Nucleotide sequence of Moloney murine leukaemia virus. Nature 293:543-548.
40. Suo, Z., and K. A. Johnson. 1997. Effect of RNA secondary structure on RNA cleavage catalyzed by HIV-1 reverse transcriptase. Biochemistry 36:12468-12476.
41. Suo, Z., and K. A. Johnson. 1997. Effect of RNA secondary structure on the kinetics of DNA synthesis catalyzed by HIV-1 reverse transcriptase. Biochemistry 36:12459-12467.
42. Thrall, S. H., R. Krebs, B. M. Wohrl, L. Cellai, R. S. Goody, and T. Restle. 1998. Pre-steady-state kinetic characterization of RNA-primed initiation of transcription by HIV-1 reverse transcriptase and analysis of the transition to a processive DNA-primed polymerization mode. Biochemistry 37:13349-13358.
43. Whiting, S. H., and J. J. Champoux. 1998. Properties of strand displacement synthesis by Moloney murine leukemia virus reverse transcriptase: mechanistic implications. J. Mol. Biol. 278:559-577.
44. Whiting, S. H., and J. J. Champoux. 1994. Strand displacement synthesis capability of Moloney murine leukemia virus reverse transcriptase. J. Virol. 68:4747-4758.
45. Winshell, J., and J. J. Champoux. 2001. Structural alterations in the DNA ahead of the primer terminus during displacement synthesis by reverse transcriptases. J. Mol. Biol. 306:931-943.
46. Wisniewski, M., M. Balakrishnan, C. Palaniappan, P. J. Fay, and R. A. Bambara. 2000. The sequential mechanism of HIV reverse transcriptase RNase H. J. Biol. Chem. 275:37664-37671.
47. Wisniewski, M., M. Balakrishnan, C. Palaniappan, P. J. Fay, and R. A. Bambara. 1983. 2000. Unique progressive cleavage mechanism of HIV reverse transcriptase RNase H. Proc. Natl. Acad. Sci. USA 97:11978-11983.
48. Wisniewski, M., Y. Chen, M. Balakrishnan, C. Palaniappan, B. P. Roques, P. J. Fay, and R. A. Bambara. 2002. Substrate requirements for secondary cleavage by HIV-1 reverse transcriptase RNase H. J. Biol. Chem. 277:28400-28410.
49. Wohrl, B. M., M. M. Georgiadis, A. Telesnitsky, W. A. Hendrickson, and S. F. Le Grice. 1995. Footprint analysis of replicating murine leukemia virus reverse transcriptase. Science 267:96-99.
50. Wohrl, B. M., C. Tantillo, E. Arnold, and S. F. Le Grice. 1995. An expanded model of replicating human immunodeficiency virus reverse transcriptase. Biochemistry 34:5343-5356.
51. Wu, W., L. E. Henderson, T. D. Copeland, R. J. Gorelick, W. J. Bosche, A. Rein, and J. G. Levin. 1996. Human immunodeficiency virus type 1 nucleocapsid protein reduces reverse transcriptase pausing at a secondary structure near the murine leukemia virus polypurine tract. J. Virol. 70:7132-7142.