Strand transfer events during HIV-1 reverse transcription

Aguiar, 2008, APOBEC proteins and reverse transcription, Virus Res., 134, 74, 10.1016/j.virusres.2007.12.022 Allain, 1994, Transactivation of the minus-strand DNA transfer by nucleocapsid protein during reverse transcription of the retroviral genome, EMBO J., 13, 973, 10.1002/j.1460-2075.1994.tb06342.x Arts, 1998, Interaction of retroviral reverse transcriptase with template-primer duplexes during replication, Prog. Nucleic Acid Res. Mol. Biol., 58, 339, 10.1016/S0079-6603(08)60041-0 Auxilien, 1999, Role of post-transcriptional modifications of primer tRNALys,3 in the fidelity and efficacy of plus strand DNA transfer during HIV-1 reverse transcription, J. Biol. Chem., 274, 4412, 10.1074/jbc.274.7.4412 Balakrishnan, 2001, The kissing hairpin sequence promotes recombination within the HIV-I 5′ leader region, J. Biol. Chem., 276, 36482, 10.1074/jbc.M102860200 Balakrishnan, 2003, Template dimerization promotes an acceptor invasion-induced transfer mechanism during human immunodeficiency virus type 1 minus-strand synthesis, J. Virol., 77, 4710, 10.1128/JVI.77.8.4710-4721.2003 Becker, 1997, Major identity determinants for enzymatic formation of ribothymidine and pseudouridine in the T psi-loop of yeast tRNAs, J. Mol. Biol., 274, 505, 10.1006/jmbi.1997.1417 Beltz, 2004, Role of the structure of the top half of HIV-1 cTAR DNA on the nucleic acid destabilizing activity of the nucleocapsid protein NCp7, J. Mol. Biol., 338, 711, 10.1016/j.jmb.2004.03.019 Ben-Artzi, 1996, Molecular analysis of the second template switch during reverse transcription of the HIV RNA template, Biochemistry, 35, 10549, 10.1021/bi960439x Berkhout, 1995, Requirements for DNA strand transfer during reverse transcription in mutant HIV-1 virions, J. Mol. Biol., 252, 59, 10.1006/jmbi.1994.0475 Berkhout, 2001, Structural features in the HIV-1 repeat region facilitate strand transfer during reverse transcription, RNA, 7, 1097, 10.1017/S1355838201002035 Boone, 1981, Viral DNA synthesized in vitro by avian retrovirus particles permiabilized with melittin. I. Kinetics of synthesis and size of minus- and plus-strand transcripts, J. Virol., 37, 109, 10.1128/JVI.37.1.109-116.1981 Brule, 2000, In vitro evidence for the interaction of tRNA(3)(Lys) with U3 during the first strand transfer of HIV-1 reverse transcription, Nucleic Acids Res., 28, 634, 10.1093/nar/28.2.634 Buiser, 1991, Requirements for the catalysis of strand transfer synthesis by retroviral DNA polymerases, J. Biol. Chem., 266, 13103, 10.1016/S0021-9258(18)98810-1 Burnett, 1997, Posttranscriptional modification of retroviral primers is required for late stages of DNA replication, Proc. Natl. Acad. Sci. U.S.A., 94, 7210, 10.1073/pnas.94.14.7210 Champoux, 1993, Roles of ribonuclease in reverse transcription, 103 Chandra, 1986, Serological relationship between reverse transcriptases from human T-cell lymphotropic viruses defined by monoclonal antibodies. Evidence for two forms of reverse transcriptases in the AIDS-associated virus, HTLV-III/LAV, FEBS Lett., 200, 327, 10.1016/0014-5793(86)81162-0 Charneau, 1992, A second origin of DNA plus-strand synthesis is required for optimal human immunodeficiency virus replication, J. Virol., 66, 2814, 10.1128/JVI.66.5.2814-2820.1992 Charneau, 1994, HIV-1 reverse transcription. A termination step at the center of the genome, J. Mol. Biol., 241, 651, 10.1006/jmbi.1994.1542 Chen, 2003, Steps of the acceptor invasion mechanism for HIV-1 minus strand strong stop transfer, J. Biol. Chem., 278, 38368, 10.1074/jbc.M305700200 Chen, 2003, Mechanism of minus strand strong stop transfer in HIV-1 reverse transcription, J. Biol. Chem., 278, 8006, 10.1074/jbc.M210959200 Chen, 2005, Comparison of the genetic recombination rates of human immunodeficiency virus type 1 in macrophages and T cells, J. Virol., 79, 9337, 10.1128/JVI.79.14.9337-9340.2005 Chen, 2005, Acceptor RNA cleavage profile supports an invasion mechanism for HIV-1 minus strand transfer, J. Biol. Chem., 280, 14443, 10.1074/jbc.M412190200 Coffin, 1979, Structure, replication, and recombination of retrovirus genomes: some unifying hypotheses, J. Gen. Virol., 42, 1, 10.1099/0022-1317-42-1-1 Dang, 2001, Effects of homology length in the repeat region on minus-strand DNA transfer and retroviral replication, J. Virol., 75, 809, 10.1128/JVI.75.2.809-820.2001 Darlix, 1993, Trans-activation of the 5′ to 3′ viral DNA strand transfer by nucleocapsid protein during reverse transcription of HIV1 RNA, C.R. Acad. Sci. III, 316, 763 Davis, 1998, Actinomycin D inhibition of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase and nucleocapsid protein, Biochemistry, 37, 14213, 10.1021/bi9814890 Derebail, 2004, Mechanistic analysis of pause site-dependent and -independent recombinogenic strand transfer from structurally diverse regions of the HIV genome, J. Biol. Chem., 279, 47446, 10.1074/jbc.M408927200 Derebail, 2003, Evidence for the differential effects of nucleocapsid protein on strand transfer in various regions of the HIV genome, J. Biol. Chem., 278, 15702, 10.1074/jbc.M211701200 DeStefano, 1994, Kinetic analysis of the catalysis of strand transfer from internal regions of heteropolymeric RNA templates by human immunodeficiency virus reverse transcriptase, J. Mol. Biol., 243, 558, 10.1016/0022-2836(94)90030-2 DeStefano, 1991, Human immunodeficiency virus reverse transcriptase displays a partially processive 3′ to 5′ endonuclease activity, J. Biol. Chem., 266, 24295, 10.1016/S0021-9258(18)54227-7 DeStefano, 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, 10.1016/S0021-9258(20)89464-2 DeStefano, 1992, Parameters that influence processive synthesis and site-specific termination by human immunodeficiency virus reverse transcriptase on RNA and DNA templates, Biochim. Biophys. Acta, 1131, 270, 10.1016/0167-4781(92)90025-U DeStefano, 1992, Requirements for strand transfer between internal regions of heteropolymer templates by human immunodeficiency virus reverse transcriptase, J. Virol., 66, 6370, 10.1128/JVI.66.11.6370-6378.1992 DeStefano, 1993, Determinants of the RNase H cleavage specificity of human immunodeficiency virus reverse transcriptase, Nucleic Acids Res., 21, 4330, 10.1093/nar/21.18.4330 DeStefano, 1994, The mechanism of human immunodeficiency virus reverse transcriptase-catalyzed strand transfer from internal regions of heteropolymeric RNA templates, J. Biol. Chem., 269, 161, 10.1016/S0021-9258(17)42329-5 DeStefano, 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, 10.1093/nar/22.18.3793 DeStefano, 1994, Characterization of an RNase H deficient mutant of human immunodeficiency virus-1 reverse transcriptase having an aspartate to asparagine change at position 498, Biochim. Biophys. Acta, 1219, 380, 10.1016/0167-4781(94)90062-0 di Marzo Veronese, 1986, Characterization of highly immunogenic p66/p51 as the reverse transcriptase of HTLV-III/LAV, Science, 231, 1289, 10.1126/science.2418504 Dib-Hajj, 1993, Retroviral nucleocapsid proteins possess potent nucleic acid strand renaturation activity, Protein Sci., 2, 231, 10.1002/pro.5560020212 Driscoll, 2000, Human immunodeficiency virus type 1 nucleocapsid protein can prevent self-priming of minus-strand strong stop DNA by promoting the annealing of short oligonucleotides to hairpin sequences, J. Virol., 74, 8785, 10.1128/JVI.74.19.8785-8792.2000 Drummond, 1997, Wild-type and mutant HIV type 1 nucleocapsid proteins increase the proportion of long cDNA transcripts by viral reverse transcriptase, AIDS Res. Hum. Retroviruses, 13, 533, 10.1089/aid.1997.13.533 Dudding, 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, 10.1021/bi00107a019 Egele, 2004, HIV-1 nucleocapsid protein binds to the viral DNA initiation sequences and chaperones their kissing interactions, J. Mol. Biol., 342, 453, 10.1016/j.jmb.2004.07.059 Fu, 1992, When retroviral reverse transcriptases reach the end of their RNA templates, J. Virol., 66, 4271, 10.1128/JVI.66.7.4271-4278.1992 Fuentes, 1996, Strand displacement synthesis in the central polypurine tract region of HIV-1 promotes DNA to DNA strand transfer recombination, J. Biol. Chem., 271, 29605, 10.1074/jbc.271.47.29605 Furfine, 1991, Reverse transcriptase. RNase H from the human immunodeficiency virus. Relationship of the DNA polymerase and RNA hydrolysis activities, J. Biol. Chem., 266, 406, 10.1016/S0021-9258(18)52449-2 Gao, 2007, Insights into the multiple roles of pausing in HIV-1 reverse transcriptase-promoted strand transfers, J. Biol. Chem., 282, 6222, 10.1074/jbc.M610056200 Garcés, 1991, Reverse-transcriptase-associated RNaseH activity mediates template switching during reverse transcription in vitro, Proc. Biol. Sci., 243, 235, 10.1098/rspb.1991.0037 Gilboa, 1979, A detailed model of reverse transcription and tests of crucial aspects, Cell, 18, 93, 10.1016/0092-8674(79)90357-X Goldschmidt, 2004, Structural variability of the initiation complex of HIV-1 reverse transcription, J. Biol. Chem., 279, 35923, 10.1074/jbc.M404473200 Golinelli, 2001, Self-priming of retroviral minus-strand strong-stop DNAs, Virology, 285, 278, 10.1006/viro.2001.0970 Goodenow, 1989, HIV-1 isolates are rapidly evolving quasispecies: evidence for viral mixtures and preferred nucleotide substitutions, J. Acquir. Immune Defic. Syndr., 2, 344 Gopalakrishnan, 1992, Human immunodeficiency virus type 1 reverse transcriptase: spatial and temporal relationship between the polymerase and RNase H activities, Proc. Natl. Acad. Sci. U.S.A., 89, 10763, 10.1073/pnas.89.22.10763 Guo, 1997, Human immunodeficiency virus type 1 nucleocapsid protein promotes efficient strand transfer and specific viral DNA synthesis by inhibiting TAR-dependent self-priming from minus-strand strong-stop DNA, J. Virol., 71, 5178, 10.1128/JVI.71.7.5178-5188.1997 Guo, 1998, Actinomycin D inhibits human immunodeficiency virus type 1 minus-strand transfer in in vitro and endogenous reverse transcriptase assays, J. Virol., 72, 6716, 10.1128/JVI.72.8.6716-6724.1998 Guo, 2000, Zinc finger structures in the human immunodeficiency virus type 1 nucleocapsid protein facilitate efficient minus- and plus-strand transfer, J. Virol., 74, 8980, 10.1128/JVI.74.19.8980-8988.2000 Guo, 2002, Subtle alterations of the native zinc finger structures have dramatic effects on the nucleic acid chaperone activity of human immunodeficiency virus type 1 nucleocapsid protein, J. Virol., 76, 4370, 10.1128/JVI.76.9.4370-4378.2002 Hameau, 2001, Human immunodeficiency virus type 1 central DNA flap: dynamic terminal product of plus-strand displacement dna synthesis catalyzed by reverse transcriptase assisted by nucleocapsid protein, J. Virol., 75, 3301, 10.1128/JVI.75.7.3301-3313.2001 Hansen, 1987, RNase H activity associated with bacterially expressed reverse transcriptase of human T-cell lymphotropic virus III/lymphadenopathy-associated virus, J. Biol. Chem., 262, 12393, 10.1016/S0021-9258(18)45212-X Hanson, 2005, Effects of donor and acceptor RNA structures on the mechanism of strand transfer by HIV-1 reverse transcriptase, J. Mol. Biol., 353, 772, 10.1016/j.jmb.2005.08.065 Hanson, 2006, Evidence that creation of invasion sites determines the rate of strand transfer mediated by HIV-1 reverse transcriptase, J. Mol. Biol., 363, 878, 10.1016/j.jmb.2006.08.068 Harrison, 1998, Pausing of reverse transcriptase on retroviral RNA templates is influenced by secondary structures both 5′ and 3′ of the catalytic site, Nucleic Acids Res., 26, 3433, 10.1093/nar/26.14.3433 Heilman-Miller, 2004, Alteration of nucleic acid structure and stability modulates the efficiency of minus-strand transfer mediated by the HIV-1 nucleocapsid protein, J. Biol. Chem., 279, 44154, 10.1074/jbc.M401646200 Hong, 2003, Nucleic acid conformational changes essential for HIV-1 nucleocapsid protein-mediated inhibition of self-priming in minus-strand transfer, J. Mol. Biol., 325, 1, 10.1016/S0022-2836(02)01177-4 Huang, 1998, Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance, Science, 282, 1669, 10.1126/science.282.5394.1669 Huber, 1989, Human immunodeficiency virus 1 reverse transcriptase. Template binding, processivity, strand displacement synthesis, and template switching, J. Biol. Chem., 264, 4669, 10.1016/S0021-9258(18)83795-4 Hurwitz, 1972, RNA-dependent DNA polymerase activity of RNA tumor viruses. I. Directing influence of DNA in the reaction, J. Virol., 9, 116, 10.1128/JVI.9.1.116-129.1972 Hwang, 2001, Dynamic copy choice: steady state between murine leukemia virus polymerase and polymerase-dependent RNase H activity determines frequency of in vivo template switching, Proc. Natl. Acad. Sci. U.S.A., 98, 12209, 10.1073/pnas.221289898 Jacobo-Molina, 1993, Crystal structure of human immunodeficiency virus type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 A resolution shows bent DNA, Proc. Natl. Acad. Sci. U.S.A., 90, 6320, 10.1073/pnas.90.13.6320 Jetzt, 2000, High rate of recombination throughout the human immunodeficiency virus type 1 genome, J. Virol., 74, 1234, 10.1128/JVI.74.3.1234-1240.2000 Ji, 1992, Fidelity of HIV-1 reverse transcriptase copying RNA in vitro, Biochemistry, 31, 954, 10.1021/bi00119a002 Ji, 1996, Effect of human immunodeficiency virus type 1 (HIV-1) nucleocapsid protein on HIV-1 reverse transcriptase activity in vitro, Biochemistry, 35, 132, 10.1021/bi951707e Johnson, 2000, A mechanism for plus-strand transfer enhancement by the HIV-1 nucleocapsid protein during reverse transcription, Biochemistry, 39, 9084, 10.1021/bi000841i Junghans, 1982, Products of reverse transcription in avian retrovirus analyzed by electron microscopy, J. Virol., 43, 544, 10.1128/JVI.43.2.544-554.1982 Junghans, 1982, Retroviral DNA H structures: displacement-assimilation model of recombination, Cell, 30, 53, 10.1016/0092-8674(82)90011-3 Katayanagi, 1990, Three-dimensional structure of ribonuclease H from E. coli, Nature, 347, 306, 10.1038/347306a0 Kati, 1992, Mechanism and fidelity of HIV reverse transcriptase, J. Biol. Chem., 267, 25988, 10.1016/S0021-9258(18)35706-5 Katz, 1990, Generation of diversity in retroviruses, Annu. Rev. Genet., 24, 409, 10.1146/annurev.ge.24.120190.002205 Kim, 1997, Evidence for a unique mechanism of strand transfer from the transactivation response region of HIV-1, J. Biol. Chem., 272, 16769, 10.1074/jbc.272.27.16769 Klarmann, 1993, Template-directed pausing of DNA synthesis by HIV-1 reverse transcriptase during polymerization of HIV-1 sequences in vitro, J. Biol. Chem., 268, 9793, 10.1016/S0021-9258(18)98417-6 Klasens, 1999, The effect of template RNA structure on elongation by HIV-1 reverse transcriptase, Biochim. Biophys. Acta, 1444, 355, 10.1016/S0167-4781(99)00011-1 Kohlstaedt, 1992, Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor, Science, 256, 1783, 10.1126/science.1377403 Lanciault, 2006, Pausing during reverse transcription increases the rate of retroviral recombination, J. Virol., 80, 2483, 10.1128/JVI.80.5.2483-2494.2006 Lapadat-Tapolsky, 1993, Interactions between HIV-1 nucleocapsid protein and viral DNA may have important functions in the viral life cycle, Nucleic Acids Res., 21, 831, 10.1093/nar/21.4.831 Lapadat-Tapolsky, 1995, Analysis of the nucleic acid annealing activities of nucleocapsid protein from HIV-1, Nucleic Acids Res., 23, 2434, 10.1093/nar/23.13.2434 Lapadat-Tapolsky, 1997, Possible roles of HIV-1 nucleocapsid protein in the specificity of proviral DNA synthesis and in its variability, J. Mol. Biol., 268, 250, 10.1006/jmbi.1997.0978 Laughrea, 1996, HIV-1 genome dimerization: formation kinetics and thermal stability of dimeric HIV-1Lai RNAs are not improved by the 1–232 and 296–790 regions flanking the kissing-loop domain, Biochemistry, 35, 9366, 10.1021/bi960395s Laughrea, 1996, Kissing-loop model of HIV-1 genome dimerization: HIV-1 RNAs can assume alternative dimeric forms, and all sequences upstream or downstream of hairpin 248–271 are dispensable for dimer formation, Biochemistry, 35, 1589, 10.1021/bi951838f Leis, 1972, RNA-dependent DNA polymerase activity of RNA tumor viruses. II. Directing influence of RNA in the reaction, J. Virol., 9, 130, 10.1128/JVI.9.1.130-142.1972 Levin, 2005, Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism, Prog. Nucleic Acid Res. Mol. Biol., 80, 217, 10.1016/S0079-6603(05)80006-6 Levy, 2004, Dynamics of HIV-1 recombination in its natural target cells, Proc. Natl. Acad. Sci. U.S.A., 101, 4204, 10.1073/pnas.0306764101 Lightfoote, 1986, Structural characterization of reverse transcriptase and endonuclease polypeptides of the acquired immunodeficiency syndrome retrovirus, J. Virol., 60, 771, 10.1128/JVI.60.2.771-775.1986 Lobel, 1985, Reverse transcription of retroviral genomes: mutations in the terminal repeat sequences, J. Virol., 53, 447, 10.1128/JVI.53.2.447-455.1985 Luo, 1990, Template switching by reverse transcriptase during DNA synthesis, J. Virol., 64, 4321, 10.1128/JVI.64.9.4321-4328.1990 Magiorkinis, 2003, In vivo characteristics of human immunodeficiency virus type 1 intersubtype recombination: determination of hot spots and correlation with sequence similarity, J. Gen. Virol., 84, 2715, 10.1099/vir.0.19180-0 Mak, 1997, Primer tRNAs for reverse transcription, J. Virol., 71, 8087, 10.1128/JVI.71.11.8087-8095.1997 Marquet, 1998, Importance of modified nucleotides in replication of retroviruses, plant pararetroviruses, and retrotranspons, 517 Marquet, 1995, tRNAs as primer of reverse transcriptases, Biochimie, 77, 113, 10.1016/0300-9084(96)88114-4 Mizrahi, 1989, Analysis of the ribonuclease H activity of HIV-1 reverse transcriptase using RNA:DNA hybrid substrates derived from the gag region of HIV-1, Biochemistry, 28, 9088, 10.1021/bi00449a020 Moelling, 1971, Association of viral reverse transcriptase with an enzyme degrading the RNA moiety of RNA–DNA hybrids, Nat. New Biol., 234, 240, 10.1038/newbio234240a0 Muthuswami, 2002, The HIV plus-strand transfer reaction: determination of replication-competent intermediates and identification of a novel lentiviral element, the primer over-extension sequence, J. Mol. Biol., 315, 311, 10.1006/jmbi.2001.5205 Negroni, 1999, Recombination during reverse transcription: an evaluation of the role of the nucleocapsid protein, J. Mol. Biol., 286, 15, 10.1006/jmbi.1998.2460 Negroni, 2000, Copy-choice recombination by reverse transcriptases: reshuffling of genetic markers mediated by RNA chaperones, Proc. Natl. Acad. Sci. U.S.A., 97, 6385, 10.1073/pnas.120520497 Negroni, 2001, Mechanisms of retroviral recombination, Annu. Rev. Genet., 35, 275, 10.1146/annurev.genet.35.102401.090551 Negroni, 1995, Homologous recombination promoted by reverse transcriptase during copying of two distinct RNA templates, Proc. Natl. Acad. Sci. U.S.A., 92, 6971, 10.1073/pnas.92.15.6971 Nikolenko, 2004, Antiretroviral drug resistance mutations in human immunodeficiency virus type 1 reverse transcriptase increase template-switching frequency, J. Virol., 78, 8761, 10.1128/JVI.78.16.8761-8770.2004 Ohi, 2000, Sequences in the 5′ and 3′ R elements of human immunodeficiency virus type 1 critical for efficient reverse transcription, J. Virol., 74, 8324, 10.1128/JVI.74.18.8324-8334.2000 Onafuwa, 2003, Human immunodeficiency virus type 1 genetic recombination is more frequent than that of Moloney murine leukemia virus despite similar template switching rates, J. Virol., 77, 4577, 10.1128/JVI.77.8.4577-4587.2003 Operario, 2006, Reduced dNTP interaction of human immunodeficiency virus type 1 reverse transcriptase promotes strand transfer, J. Biol. Chem., 281, 32113, 10.1074/jbc.M604665200 Paillart, 1996, A loop-loop “kissing” complex is the essential part of the dimer linkage of genomic HIV-1 RNA, Proc. Natl. Acad. Sci. U.S.A., 93, 5572, 10.1073/pnas.93.11.5572 Palaniappan, 1996, Helix structure and ends of RNA/DNA hybrids direct the cleavage specificity of HIV-1 reverse transcriptase RNase H, J. Biol. Chem., 271, 2063, 10.1074/jbc.271.4.2063 Peliska, 1992, Mechanism of DNA strand transfer reactions catalyzed by HIV-1 reverse transcriptase, Science, 258, 1112, 10.1126/science.1279806 Peliska, 1994, Recombinant HIV-1 nucleocapsid protein accelerates HIV-1 reverse transcriptase catalyzed DNA strand transfer reactions and modulates RNase H activity, Biochemistry, 33, 13817, 10.1021/bi00250a036 Pfeiffer, 2001, Effects of limiting homology at the site of intermolecular recombinogenic template switching during Moloney murine leukemia virus replication, J. Virol., 75, 11263, 10.1128/JVI.75.23.11263-11274.2001 Post, 2003, Human immunodeficiency virus type 2 reverse transcriptase activity in model systems that mimic steps in reverse transcription, J. Virol., 77, 7623, 10.1128/JVI.77.13.7623-7634.2003 Preston, 1988, Fidelity of HIV-1 reverse transcriptase, Science, 242, 1168, 10.1126/science.2460924 Pullen, 1992, Incomplete removal of the RNA primer for minus-strand DNA synthesis by human immunodeficiency virus type 1 reverse transcriptase, J. Virol., 66, 367, 10.1128/JVI.66.1.367-373.1992 Purohit, 2005, Evidence that HIV-1 reverse transcriptase employs the DNA 3′ end-directed primary/secondary RNase H cleavage mechanism during synthesis and strand transfer, J. Biol. Chem., 280, 40534, 10.1074/jbc.M507839200 Purohit, 2007, Mechanisms that prevent template inactivation by HIV-1 reverse transcriptase RNase H cleavages, J. Biol. Chem., 282, 12598, 10.1074/jbc.M700043200 Rein, 1998, Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication, Trends Biochem. Sci., 23, 297, 10.1016/S0968-0004(98)01256-0 Renda, 2001, Mutation of the methylated tRNA(Lys)(3) residue A58 disrupts reverse transcription and inhibits replication of human immunodeficiency virus type 1, J. Virol., 75, 9671, 10.1128/JVI.75.20.9671-9678.2001 Repaske, 1989, Inhibition of RNase H activity and viral replication by single mutations in the 3′ region of Moloney murine leukemia virus reverse transcriptase, J. Virol., 63, 1460, 10.1128/JVI.63.3.1460-1464.1989 Reynolds, 1994, Triple-strand-forming methylphosphonate oligodeoxynucleotides targeted to mRNA efficiently block protein synthesis, Proc. Natl. Acad. Sci. U.S.A., 91, 12433, 10.1073/pnas.91.26.12433 Roda, 2002, Strand transfer occurs in retroviruses by a pause-initiated two-step mechanism, J. Biol. Chem., 277, 46900, 10.1074/jbc.M208638200 Roda, 2003, Role of the reverse transcriptase, nucleocapsid protein, and template structure in the two-step transfer mechanism in retroviral recombination, J. Biol. Chem., 278, 31536, 10.1074/jbc.M304608200 Rodriguez-Rodriguez, 1995, Influence of human immunodeficiency virus nucleocapsid protein on synthesis and strand transfer by the reverse transcriptase in vitro, J. Biol. Chem., 270, 15005, 10.1074/jbc.270.25.15005 Roth, 1989, Structure of the termini of DNA intermediates in the integration of retroviral DNA: dependence on IN function and terminal DNA sequence, Cell, 58, 47, 10.1016/0092-8674(89)90401-7 Schultz, 2004, Recognition of internal cleavage sites by retroviral RNases H, J. Mol. Biol., 344, 635, 10.1016/j.jmb.2004.09.081 Schultz, 2006, Sequence, distance, and accessibility are determinants of 5′-end-directed cleavages by retroviral RNases H, J. Biol. Chem., 281, 1943, 10.1074/jbc.M510504200 Skripkin, 1994, Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro, Proc. Natl. Acad. Sci. U.S.A., 91, 4945, 10.1073/pnas.91.11.4945 Smith, 1999, RNase H requirements for the second strand transfer reaction of human immunodeficiency virus type 1 reverse transcription, J. Virol., 73, 6573, 10.1128/JVI.73.8.6573-6581.1999 Snyder, 2000, Comparison of second-strand transfer requirements and RNase H cleavages catalyzed by human immunodeficiency virus type 1 reverse transcriptase (RT) and E478Q RT, J. Virol., 74, 9668, 10.1128/JVI.74.20.9668-9679.2000 Song, 2006, Stimulation of HIV-1 minus strand strong stop DNA transfer by genomic sequences 3′ of the primer binding site, J. Biol. Chem., 281, 24227, 10.1074/jbc.M603097200 Starnes, 1989, Human immunodeficiency virus reverse transcriptase-associated RNase H activity, J. Biol. Chem., 264, 7073, 10.1016/S0021-9258(18)83542-6 Suo, 1997, Effect of RNA secondary structure on RNA cleavage catalyzed by HIV-1 reverse transcriptase, Biochemistry, 36, 12468, 10.1021/bi971218+ Suo, 1997, Effect of RNA secondary structure on the kinetics of DNA synthesis catalyzed by HIV-1 reverse transcriptase, Biochemistry, 36, 12459, 10.1021/bi971217h Svarovskaia, 2000, Structural determinants of murine leukemia virus reverse transcriptase that affect the frequency of template switching, J. Virol., 74, 7171, 10.1128/JVI.74.15.7171-7178.2000 Tanchou, 1995, Formation of stable and functional HIV-1 nucleoprotein complexes in vitro, J. Mol. Biol., 252, 563, 10.1006/jmbi.1995.0520 Tanese, 1991, Abortive reverse transcription by mutants of Moloney murine leukemia virus deficient in the reverse transcriptase-associated RNase H function, J. Virol., 65, 4387, 10.1128/JVI.65.8.4387-4397.1991 Telesnitsky, 1993, Strong-stop strand transfer during reverse transcription, 49 Telesnitsky, 1993, Two defective forms of reverse transcriptase can complement to restore retroviral infectivity, EMBO J., 12, 4433, 10.1002/j.1460-2075.1993.tb06128.x Telesnitsky, 1997, Reverse transcriptase and the generation of retroviral DNA, 121 Temin, 1991, Sex and recombination in retroviruses, Trends Genet., 7, 71, 10.1016/0168-9525(91)90048-U Tisdale, 1991, Mutations within the RNase H domain of human immunodeficiency virus type 1 reverse transcriptase abolish virus infectivity, J. Gen. Virol., 72, 59, 10.1099/0022-1317-72-1-59 Tsuchihashi, 1994, DNA strand exchange and selective DNA annealing promoted by the human immunodeficiency virus type 1 nucleocapsid protein, J. Virol., 68, 5863, 10.1128/JVI.68.9.5863-5870.1994 Urbaneja, 2002, HIV-1 nucleocapsid protein as a nucleic acid chaperone: spectroscopic study of its helix-destabilizing properties, structural binding specificity, and annealing activity, J. Mol. Biol., 318, 749, 10.1016/S0022-2836(02)00043-8 van Wamel, 1998, The first strand transfer during HIV-1 reverse transcription can occur either intramolecularly or intermolecularly, Virology, 244, 245, 10.1006/viro.1998.9096 Varmus, 1978, Kinetics of synthesis, structure and purification of avian sarcoma virus-specific DNA made in the cytoplasm of acutely infected cells, J. Mol. Biol., 120, 55, 10.1016/0022-2836(78)90295-4 Vo, 2006, Mechanistic studies of mini-TAR RNA/DNA annealing in the absence and presence of HIV-1 nucleocapsid protein, J. Mol. Biol., 363, 244, 10.1016/j.jmb.2006.08.039 Wang, 1994, Structural basis of asymmetry in the human immunodeficiency virus type 1 reverse transcriptase heterodimer, Proc. Natl. Acad. Sci. U.S.A., 91, 7242, 10.1073/pnas.91.15.7242 Whitcomb, 1990, Sequence of the circle junction of human immunodeficiency virus type 1: implications for reverse transcription and integration, J. Virol., 64, 4903, 10.1128/JVI.64.10.4903-4906.1990 Williams, 2001, Mechanism for nucleic acid chaperone activity of HIV-1 nucleocapsid protein revealed by single molecule stretching, Proc. Natl. Acad. Sci. U.S.A., 98, 6121, 10.1073/pnas.101033198 Wisniewski, 2000, The sequential mechanism of HIV reverse transcriptase RNase H, J. Biol. Chem., 275, 37664, 10.1074/jbc.M007381200 Wisniewski, 2000, Unique progressive cleavage mechanism of HIV reverse transcriptase RNase H, Proc. Natl. Acad. Sci. U.S.A., 97, 11978, 10.1073/pnas.210392297 Wondrak, 1986, Functional purification and enzymic characterization of the RNA-dependent DNA polymerase of human immunodeficiency virus, J. Gen. Virol., 67, 2791, 10.1099/0022-1317-67-12-2791 Wu, 1995, Strand transfer mediated by human immunodeficiency virus reverse transcriptase in vitro is promoted by pausing and results in misincorporation, J. Biol. Chem., 270, 325, 10.1074/jbc.270.1.325 Wu, 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, 10.1128/JVI.70.10.7132-7142.1996 Wu, 1999, Molecular requirements for human immunodeficiency virus type 1 plus-strand transfer: analysis in reconstituted and endogenous reverse transcription systems, J. Virol., 73, 4794, 10.1128/JVI.73.6.4794-4805.1999 Wu, 2007, Effects of nucleic acid local structure and magnesium ions on minus-strand transfer mediated by the nucleic acid chaperone activity of HIV-1 nucleocapsid protein, Nucleic Acids Res., 35, 3974, 10.1093/nar/gkm375 Yang, 1990, Structure of ribonuclease H phased at 2 A resolution by MAD analysis of the selenomethionyl protein, Science, 249, 1398, 10.1126/science.2169648 You, 1993, HIV nucleocapsid protein. Expression in Escherichia coli, purification, and characterization, J. Biol. Chem., 268, 16519, 10.1016/S0021-9258(19)85450-9 You, 1994, Human immunodeficiency virus nucleocapsid protein accelerates strand transfer of the terminally redundant sequences involved in reverse transcription, J. Biol. Chem., 269, 31491, 10.1016/S0021-9258(18)31721-6 Yu, 1998, The nature of human immunodeficiency virus type 1 strand transfers, J. Biol. Chem., 273, 28384, 10.1074/jbc.273.43.28384 Zhang, 1993, Rate and mechanism of nonhomologous recombination during a single cycle of retroviral replication, Science, 259, 234, 10.1126/science.8421784 Zhang, 2000, Most retroviral recombinations occur during minus-strand DNA synthesis, J. Virol., 74, 2313, 10.1128/JVI.74.5.2313-2322.2000 Zhang, 2002, Zinc finger domain of murine leukemia virus nucleocapsid protein enhances the rate of viral DNA synthesis in vivo, J. Virol., 76, 7473, 10.1128/JVI.76.15.7473-7484.2002 Zhuang, 2002, Human immunodeficiency virus type 1 recombination: rate, fidelity, and putative hot spots, J. Virol., 76, 11273, 10.1128/JVI.76.22.11273-11282.2002