Initiation complex dynamics direct the transitions between distinct phases of early HIV reverse transcription

Nature Structural and Molecular Biology

Volumn 17, Issue 12, 2010, Pages 1453-1460

  Liu, Shixin ^a   Harada, Bryan T ^b   Miller, Jennifer T ^c   Le Grice, Stuart F J ^c   Zhuang, Xiaowei ^a,d,e  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD UNIVERSITY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d HARVARD UNIVERSITY   (United States)

^e HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA DIRECTED DNA POLYMERASE; TRANSFER RNA; VIRUS RNA;

ARTICLE; DNA RNA HYBRIDIZATION; ENZYME BINDING; GENE DISRUPTION; HUMAN IMMUNODEFICIENCY VIRUS; NONHUMAN; PRIORITY JOURNAL; REVERSE TRANSCRIPTION; RNA STRUCTURE; RNA TRANSLATION;

DNA; FLUORESCENCE RESONANCE ENERGY TRANSFER; HIV-1; MODELS, GENETIC; NUCLEIC ACID CONFORMATION; REVERSE TRANSCRIPTION; RNA, VIRAL; RNA-DIRECTED DNA POLYMERASE; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS;

EID: 78649866357     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1937     Document Type: Article

References (55)

1. Telesnitsky, A. & Goff, S.P. Reverse transcriptase and the generation of retroviral DNA. in Retroviruses (eds. Coffn, J.M., Hughes, S.H. & Varmus, H.E.) 121-160 (Cold Spring Harbor Laboratory Press, 1997).
2. Marquet, R., Isel, C., Ehresmann, C. & Ehresmann, B. tRNAs as primer of reverse transcriptases. Biochimie 77, 113-124 (1995).
3. Cobrinik, D., Soskey, L. & Leis, J. A retroviral RNA secondary structure required for effcient initiation of reverse transcription. J. Virol. 62, 3622-3630 (1988).
4. Trp as primer for RNA-directed DNA polymerase: structural determinants of function. J. Biol. Chem. 254, 1866-1874 (1979).
5. Harrich, D. & Hooker, B. Mechanistic aspects of HIV-1 reverse transcription initiation. Rev. Med. Virol. 12, 31-45 (2002).
6. Götte, M., Li, X. & Wainberg, M.A. HIV-1 reverse transcription: a brief overview focused on structure-function relationships among molecules involved in initiation of the reaction. Arch. Biochem. Biophys. 365, 199-210 (1999).
7. Le Grice, S.F. "In the beginning": initiation of minus strand DNA synthesis in retroviruses and LTR-containing retrotransposons. Biochemistry 42, 14349-14355 (2003).
8. 3Lys to the HIV-1 viral RNA. Curr. HIV Res. 3, 147-156 (2005).
9. Abbink, T.E. & Berkhout, B. HIV-1 reverse transcription initiation: a potential target for novel antivirals? Virus Res. 134, 4-18 (2008).
10. Isel, C., Ehresmann, C. & Marquet, R. Initiation of HIV reverse transcription. Viruses 2, 213-243 (2010).
11. Lys. EMBO J. 15, 917-924 (1996).
12. Lanchy, J.M., Ehresmann, C., Le Grice, S.F., Ehresmann, B. & Marquet, R. Binding and kinetic properties of HIV-1 reverse transcriptase markedly differ during initiation and elongation of reverse transcription. EMBO J. 15, 7178-7187 (1996).
13. Lanchy, J.M. et al. 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 (1998).
14. Goldschmidt, V. et al. Structural variability of the initiation complex of HIV-1 reverse transcription. J. Biol. Chem. 279, 35923-35931 (2004).
15. Wilkinson, K.A. et al. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol. 6, e96 (2008).
16. Liang, C. et al. Mechanistic studies of early pausing events during initiation of HIV-1 reverse transcription. J. Biol. Chem. 273, 21309-21315 (1998).
17. Thrall, S.H. et al. 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 (1998).
18. Lanchy, J.M. et al. Dynamics of the HIV-1 reverse transcription complex during initiation of DNA synthesis. J. Biol. Chem. 275, 12306-12312 (2000).
19. Lys.3 and viral RNA template play different roles during initiation of (-) strand DNA reverse transcription. J. Biol. Chem. 276, 47725-47732 (2001).
20. Abbondanzieri, E.A. et al. Dynamic binding orientations direct activity of HIV reverse transcriptase. Nature 453, 184-189 (2008).
21. Liu, S., Abbondanzieri, E.A., Rausch, J.W., Le Grice, S.F. & Zhuang, X. Slide into action: dynamic shuttling of HIV reverse transcriptase on nucleic acid substrates. Science 322, 1092-1097 (2008).
22. DeStefano, J.J., Mallaber, L.M., Fay, P.J. & Bambara, R.A. Determinants of the RNase H cleavage specifcity of human immunodefciency virus reverse transcriptase. Nucleic Acids Res. 21, 4330-4338 (1993).
23. Stryer, L. & Haugland, R.P. Energy transfer: a spectroscopic ruler. Proc. Natl. Acad. Sci. USA 58, 719-726 (1967).
24. Ha, T. et al. Probing the interaction between two single molecules: fuorescence resonance energy transfer between a single donor and a single acceptor. Proc. Natl. Acad. Sci. USA 93, 6264-6268 (1996).
25. Iwatani, Y., Rosen, A.E., Guo, J., Musier-Forsyth, K. & Levin, J.G. Effcient initiation of HIV-1 reverse transcription in vitro. Requirement for RNA sequences downstream of the primer binding site abrogated by nucleocapsid protein-dependent primer-template interactions. J. Biol. Chem. 278, 14185-14195 (2003).
26. Huang, H., Chopra, R., Verdine, G.L. & Harrison, S.C. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282, 1669-1675 (1998).
27. Sarafanos, S.G. et al. Crystal structure of HIV-1 reverse transcriptase in complex with a polypurine tract RNA:DNA. EMBO J. 20, 1449-1461 (2001).
28. Isel, C. et al. Structural basis for the specifcity of the initiation of HIV-1 reverse transcription. EMBO J. 18, 1038-1048 (1999).
29. Paillart, J.C. et al. First snapshots of the HIV-1 RNA structure in infected cells and in virions. J. Biol. Chem. 279, 48397-48403 (2004).
30. Suo, Z. & Johnson, K.A. Effect of RNA secondary structure on the kinetics of DNA synthesis catalyzed by HIV-1 reverse transcriptase. Biochemistry 36, 12459-12467 (1997). (Pubitemid 27446669)
31. Thomas, J.A. & Gorelick, R.J. Nucleocapsid protein function in early infection processes. Virus Res. 134, 39-63 (2008).
32. Rein, A., Henderson, L.E. & Levin, J.G. Nucleic-acid-chaperon activity of retroviral nucleocapsid proteins: signifcance for viral replication. Trends Biochem. Sci. 23, 297-301 (1998).
33. Herschlag, D. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270, 20871-20874 (1995).
34. Rodríguez-Rodríguez, L., Tsuchihashi, Z., Fuentes, G.M., Bambara, R.A. & Fay, P.J. Infuence of human immunodefciency virus nucleocapsid protein on synthesis and strand transfer by the reverse transcriptase in vitro. J. Biol. Chem. 270, 15005-15011 (1995).
35. Wu, W. et al. Human immunodefciency 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 (1996).
36. Ji, X., Klarmann, G.J. & Preston, B.D. Effect of human immunodefciency virus type 1 (HIV-1) nucleocapsid protein on HIV-1 reverse transcriptase activity in vitro. Biochemistry 35, 132-143 (1996).
37. Grohmann, D., Godet, J., Mely, Y., Darlix, J.L. & Restle, T. HIV-1 nucleocapsid traps reverse transcriptase on nucleic acid substrates. Biochemistry 47, 12230-12240 (2008).
38. Tanchou, V., Gabus, C., Rogemond, V. & Darlix, J.L. Formation of stable and functional HIV-1 nucleocapsid complexes in vitro. J. Mol. Biol. 252, 563-571 (1995).
39. Lori, F. et al. Viral DNA carried by human immunodefciency virus type 1 virions. J. Virol. 66, 5067-5074 (1992).
40. Trono, D. Partial reverse transcripts in virions from human immunodefciency and murine leukemia viruses. J. Virol. 66, 4893-4900 (1992).
41. Zhang, H., Dornadula, G., Orenstein, J. & Pomerantz, R.J. Morphologic changes in human immunodefciency virus type 1 virions secondary to intravirion reverse transcription: evidence indicating that reverse transcription may not take place within the intact viral core. J. Hum. Virol. 3, 165-172 (2000).
42. Houzet, L. et al. Nucleocapsid mutations turn HIV-1 into a DNA-containing virus. Nucleic Acids Res. 36, 2311-2319 (2008).
43. Thomas, J.A., Bosche, W.J., Shatzer, T.L., Johnson, D.G. & Gorelick, R.J. Mutations in human immunodefciency virus type 1 nucleocapsid protein zinc fngers cause premature reverse transcription. J. Virol. 82, 9318-9328 (2008).
44. Beerens, N., Groot, F. & Berkhout, B. Initiation of HIV-1 reverse transcription is regulated by a primer activation signal. J. Biol. Chem. 276, 31247-31256 (2001).
45. Wu, T. et al. Fundamental differences between the nucleic acid chaperone activities of HIV-1 nucleocapsid protein and Gag or Gag-derived proteins: biological implications. Virology 405, 556-567 (2010).
46. Hooker, C.W., Lott, W.B. & Harrich, D. Inhibitors of human immunodefciency virus type 1 reverse transcriptase target distinct phases of early reverse transcription. J. Virol. 75, 3095-3104 (2001).
47. Rigourd, M. et al. Inhibition of the initiation of HIV-1 reverse transcription by 3′-azido-3′-deoxythymidine. Comparison with elongation. J. Biol. Chem. 275, 26944-26951 (2000).
48. Le Grice, S.F.J., Cameron, C.E. & Benkovic, S.J. Purifcation and characterization of human immunodefciency virus type 1 reverse transcriptase. Methods Enzymol. 262, 130-144 (1995).
49. Rausch, J.W., Sathyanarayana, B.K., Bona, M.K. & Le Grice, S.F. Probing contacts between the ribonuclease H domain of HIV-1 reverse transcriptase and nucleic acid by site-specifc photocross-linking. J. Biol. Chem. 275, 16015-16022 (2000).
50. Lapham, J. & Crothers, D.M. RNase H cleavage for processing of in vitro transcribed RNA for NMR studies and RNA ligation. RNA 2, 289-296 (1996).
51. Rasnik, I., McKinney, S.A. & Ha, T. Nonblinking and long-lasting single-molecule fuorescence imaging. Nat. Methods 3, 891-893 (2006).
52. Venezia, C.F., Howard, K.J., Ignatov, M.E., Holladay, L.A. & Barkley, M.D. Effects of efavirenz binding on the subunit equilibria of HIV-1 reverse transcriptase. Biochemistry 45, 2779-2789 (2006).
53. Kapanidis, A.N. et al. Fluorescence-aided molecule sorting: analysis of structure and interactions by alternating-laser excitation of single molecules. Proc. Natl. Acad. Sci. USA 101, 8936-8941 (2004).
54. Thompson, R.E., Larson, D.R. & Webb, W.W. Precise nanometer localization analysis for individual fuorescent probes. Biophys. J. 82, 2775-2783 (2002).
55. Yildiz, A. et al. Myosin V walks hand-over-hand: single fuorophore imaging with 1.5-nm localization. Science 300, 2061-2065 (2003).