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Science 13 November 1992:
Vol. 258. no. 5085, pp. 1112 - 1118
DOI: 10.1126/science.1279806
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Articles

Science, Vol 258, Issue 5085, 1112-1118
Copyright © 1992 by American Association for the Advancement of Science

articles

Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase

JA Peliska and SJ Benkovic

Department of Chemistry, Pennsylvania State University, University Park 16802.

Two DNA strand transfer reactions occur during retroviral reverse transcription. The mechanism of the first, minus strand strong-stop DNA, transfer has been studied in vitro with human immunodeficiency virus 1 reverse transcriptase (HIV-1 RT) and a model template-primer system derived from the HIV-1 genome. The results reveal that HIV-1 RT alone can catalyze DNA strand transfer reactions. Two kinetically distinct ribonuclease (RNase) H activities associated with HIV-1 RT are required for removal of RNA fragments annealed to the nascent DNA strand. Examination of the binding of DNA.RNA duplex and single-stranded RNA to HIV-1 RT during strand transfer supports a model where the enzyme accommodates both the acceptor RNA template and the nascent DNA strand before the transfer event is completed. The polymerase activity incorporated additional bases beyond the 5' end of the RNA template, resulting in a base misincorporation upon DNA strand transfer. Such a process occurring in vivo during retroviral homologous recombination could contribute to the hypermutability of the HIV-1 genome.


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Polypurine Tract Primer Generation and Utilization by Moloney Murine Leukemia Virus Reverse Transcriptase.
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J. Biol. Chem. 274, 34547-34555
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   Abstract »    Full Text »    PDF »
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Role of Post-transcriptional Modifications of Primer tRNALys,3 in the Fidelity and Efficacy of Plus Strand DNA Transfer during HIV-1 Reverse Transcription.
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J. Biol. Chem. 273, 32568-32575
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The Nature of Human Immunodeficiency Virus Type 1 Strand Transfers.
H. Yu, A. E. Jetzt, Y. Ron, B. D. Preston, and J. P. Dougherty (1998)
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   Abstract »    Full Text »    PDF »
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J. Virol. 72, 6967-6978
   Abstract »    Full Text »    PDF »
In Vivo Ty1 Reverse Transcription Can Generate Replication Intermediates with Untidy Ends.
E. H. Mules, O. Uzun, and A. Gabriel (1998)
J. Virol. 72, 6490-6503
   Abstract »    Full Text »    PDF »
Localization of the Active Site of HIV-1 Reverse Transcriptase-associated RNase H Domain on a DNA Template Using Site-specific Generated Hydroxyl Radicals.
M. Gotte, G. Maier, H. J. Gross, and H. Heumann (1998)
J. Biol. Chem. 273, 10139-10146
   Abstract »    Full Text »    PDF »
Extended Minus-Strand DNA as Template for R-U5-Mediated Second-Strand Transfer in Recombinational Rescue of Primer Binding Site-Modified Retroviral Vectors.
J. G. Mikkelsen, A. H. Lund, K. Dybkar, M. Duch, and F. S. Pedersen (1998)
J. Virol. 72, 2519-2525
   Abstract »    Full Text »    PDF »
Replication Errors during In Vivo Ty1 Transposition Are Linked to Heterogeneous RNase H Cleavage Sites.
E. H. Mules, O. Uzun, and A. Gabriel (1998)
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J. Biol. Chem. 273, 1483-1489
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Binding of RNA template to a complex of HIV-1 reverse transcriptase/primer/template.
B. Canard, R. Sarfati, and C. C. Richardson (1997)
PNAS 94, 11279-11284
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Posttranscriptional modification of retroviral primers is required for late stages of DNA replication.
B. P. Burnett and C. S. McHenry (1997)
PNAS 94, 7210-7215
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Mutations in HIV reverse transcriptase which alter RNase H activity and decrease strand transfer efficiency are suppressed by HIV nucleocapsid protein.
C. E. Cameron, M. Ghosh, S. F. J. Le Grice, and S. J. Benkovic (1997)
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Mutations within the Primer Grip Region of HIV-1 Reverse Transcriptase Result in Loss of RNase H Function.
C. Palaniappan, M. Wisniewski, P. S. Jacques, S. F.J. Le Grice, P. J. Fay, and R. A. Bambara (1997)
J. Biol. Chem. 272, 11157-11164
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Substituting a Conserved Residue of the Ribonuclease H Domain Alters Substrate Hydrolysis by Retroviral Reverse Transcriptase.
J. W. Rausch and S. F.J. Le Grice (1997)
J. Biol. Chem. 272, 8602-8610
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Strand Displacement Synthesis in the Central Polypurine Tract Region of HIV-1 Promotes DNA to DNA Strand Transfer Recombination.
G. M. Fuentes, C. Palaniappan, P. J. Fay, and R. A. Bambara (1996)
J. Biol. Chem. 271, 29605-29611
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Synthesis of Full-length Viral DNA in CD4-positive Membrane Vesicles Exposed to HIV-1. A MODEL FOR STUDIES OF EARLY STAGES OF THE HIV-1 LIFE CYCLE.
M. Simm, O. Pekarskaya, and D. J. Volsky (1996)
J. Biol. Chem. 271, 28266-28270
   Abstract »    Full Text »    PDF »
Misincorporation by HIV-1 Reverse Transcriptase Promotes Recombination via Strand Transfer Synthesis.
C. Palaniappan, M. Wisniewski, W. Wu, P. J. Fay, and R. A. Bambara (1996)
J. Biol. Chem. 271, 22331-22338
   Abstract »    Full Text »    PDF »
Interaction of Human Immunodeficiency Virus Nucleocapsid Protein with a Structure Mimicking a Replication Intermediate. EFFECTS ON STABILITY, REVERSE TRANSCRIPTASE BINDING, AND STRAND TRANSFER.
J. J. DeStefano and J. J. DeStefano (1996)
J. Biol. Chem. 271, 16350-16356
   Abstract »    Full Text »    PDF »
Helix Structure and Ends of RNA/DNA Hybrids Direct the Cleavage Specificity of HIV-1 Reverse Transcriptase RNase H.
C. Palaniappan, G. M. Fuentes, L. Rodríguez-Rodríguez, P. J. Fay, and R. A. Bambara (1996)
J. Biol. Chem. 271, 2063-2070
   Abstract »    Full Text »    PDF »
Cleavage Specificities of Moloney Murine Leukemia Virus RNase H Implicated in the Second Strand Transfer During Reverse Transcription.
S. J. Schultz, S. H. Whiting, and J. J. Champoux (1995)
J. Biol. Chem. 270, 24135-24145
   Abstract »    Full Text »    PDF »
Influence of Human Immunodeficiency Virus Nucleocapsid Protein on Synthesis and Strand Transfer by the Reverse Transcriptase in Vitro.
L. Rodrguez-Rodrguez, Z. Tsuchihashi, G. M. Fuentes, R. A. Bambara, and P. J. Fay (1995)
J. Biol. Chem. 270, 15005-15011
   Abstract »    Full Text »    PDF »
Truncating alpha-Helix E` of p66 Human Immunodeficiency Virus Reverse Transcriptase Modulates RNase H Function and Impairs DNA Strand Transfer.
M. Ghosh, K. J. Howard, C. E. Cameron, S. J. Benkovic, S. H. Hughes, and S. F. J. Le Grice (1995)
J. Biol. Chem. 270, 7068-7076
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Nevirapine Alters the Cleavage Specificity of Ribonuclease H of Human Immunodeficiency Virus 1 Reverse Transcriptase.
C. Palaniappan, P. J. Fay, and R. A. Bambara (1995)
J. Biol. Chem. 270, 4861-4869
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Strand Transfer Mediated by Human Immunodeficiency Virus Reverse Transcriptase in Vitro Is Promoted by Pausing and Results in Misincorporation.
W. Wu, B. M. Blumberg, P. J. Fay, and R. A. Bambara (1995)
J. Biol. Chem. 270, 325-332
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Structures of ternary complexes of rat DNA polymerase beta, a DNA template-primer, and ddCTP.
H Pelletier, M. Sawaya, A Kumar, S. Wilson, and J Kraut (1994)
Science 264, 1891-1903
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Analysis of Plus-strand Primer Selection, Removal, and Reutilization by Retroviral Reverse Transcriptases.
S. J. Schultz, M. Zhang, C. D. Kelleher, and J. J. Champoux (2000)
J. Biol. Chem. 275, 32299-32309
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The Sequential Mechanism of HIV Reverse Transcriptase RNase H.
M. Wisniewski, M. Balakrishnan, C. Palaniappan, P. J. Fay, and R. A. Bambara (2000)
J. Biol. Chem. 275, 37664-37671
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Analysis of Efficiency and Fidelity of HIV-1 (+)-Strand DNA Synthesis Reveals a Novel Rate-limiting Step during Retroviral Reverse Transcription.
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C. K. Hwang, E. S. Svarovskaia, and V. K. Pathak (2001)
PNAS 98, 12209-12214
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Science. ISSN 0036-8075 (print), 1095-9203 (online)