Initiation of HIV-1 reverse transcription and functional role of nucleocapsid-mediated tRNA/viral genome interactions

Virus Research

Volumn 169, Issue 2, 2012, Pages 324-339

  Sleiman, Dona ^a   Goldschmidt, Valérie ^b   Barraud, Pierre ^a,c   Marquet, Roland ^b   Paillart, Jean Christophe ^b   Tisné, Carine ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b UNIVERSITÉ DE STRASBOURG   (France)

^c ETH ZURICH   (Switzerland)

Author keywords

HIV; Nucleocapsid; Reverse transcription; TRNALys3

Indexed keywords

CHAPERONE; GAG PROTEIN; NUCLEOCAPSID PROTEIN; TRANSFER RNA; VIRUS RNA;

ARTICLE; BINDING SITE; COMPLEX FORMATION; GENE INTERACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS 1; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; REVERSE TRANSCRIPTION; RNA ANALYSIS; RNA STRUCTURE; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS NUCLEOCAPSID;

GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR CHAPERONES; NUCLEIC ACID CONFORMATION; REVERSE TRANSCRIPTION; RNA, TRANSFER, LYS; RNA, VIRAL;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 84868625752     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2012.06.006     Document Type: Article

References (146)

1. Abbink T.E., Beerens N., Berkhout B. Forced selection of a human immunodeficiency virus type 1 variant that uses a non-self tRNA primer for reverse transcription: involvement of viral RNA sequences and the reverse transcriptase enzyme. Journal of Virology 2004, 78(19):10706-10714.
2. Abbink T.E., Berkhout B. A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the Gag start codon. Journal of Biological Chemistry 2003, 278(13):11601-11611.
3. Abbink T.E., Berkhout B. HIV-1 reverse transcription: close encounters between the viral genome and a cellular tRNA. Advances in Pharmacology 2007, 55:99-135.
4. Abbink T.E., Ooms M., Haasnoot P.C., Berkhout B. The HIV-1 leader RNA conformational switch regulates RNA dimerization but does not regulate mRNA translation. Biochemistry 2005, 44(25):9058-9066.
5. Abbondanzieri E.A., Bokinsky G., Rausch J.W., Zhang J.X., Le Grice S.F., Zhuang X. Dynamic binding orientations direct activity of HIV reverse transcriptase. Nature 2008, 453(7192):184-189.
6. Aiken C., Trono D. Nef stimulates human immunodeficiency virus type 1 proviral DNA synthesis. Journal of Virology 1995, 69(8):5048-5056.
7. Aiyar A., Cobrinik D., Ge Z., Kung H.J., Leis J. Interaction between retroviral U5 RNA and the T psi C loop of the tRNA(Trp) primer is required for efficient initiation of reverse transcription. Journal of Virology 1992, 66(4):2464-2472.
8. Amarasinghe G.K., De Guzman R.N., Turner R.B., Chancellor K.J., Wu Z.R., Summers M.F. NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the psi-RNA packaging signal. Implications for genome recognition. Journal of Molecular Biology 2000, 301(2):491-511.
9. Arhel N.J., Souquere-Besse S., Munier S., Souque P., Guadagnini S., Rutherford S., Prevost M.C., Allen T.D., Charneau P. HIV-1 DNA Flap formation promotes uncoating of the pre-integration complex at the nuclear pore. EMBO Journal 2007, 26(12):3025-3037.
10. Arts E.J., Ghosh M., Jacques P.S., Ehresmann B., Le Grice S.F. Restoration of tRNA3Lys-primed(-)-strand DNA synthesis to an HIV-1 reverse transcriptase mutant with extended tRNAs. Implications for retroviral replication. Journal of Biological Chemistry 1996, 271(15):9054-9061.
11. Arts E.J., Le Grice S.F. Interaction of retroviral reverse transcriptase with template-primer duplexes during replication. Progress in Nucleic Acid Research and Molecular Biology 1998, 58:339-393.
12. Barraud P., Dardel F., Tisne C. Optimizing HSQC experiment for the observation of exchange broadened signals in RNAeprotein complexes. Comptes Rendus Chimie 2008, 11:474-479.
13. Barraud P., Gaudin C., Dardel F., Tisne C. New insights into the formation of HIV-1 reverse transcription initiation complex. Biochimie 2007, 89(10):1204-1210.
14. Baudin F., Marquet R., Isel C., Darlix J.L., Ehresmann B., Ehresmann C. Functional sites in the 5' region of human immunodeficiency virus type 1 RNA form defined structural domains. Journal of Molecular Biology 1993, 229(2):382-397.
15. Bazzi A., Zargarian L., Chaminade F., Boudier C., De Rocquigny H., Rene B., Mély Y., Fosse P., Mauffret O. Structural insights into the cTAR DNA recognition by the HIV-1 nucleocapsid protein: role of sugar deoxyriboses in the binding polarity of NC. Nucleic Acids Research 2011, 39(9):3903-3916.
16. Beerens N., Berkhout B. Switching the in vitro tRNA usage of HIV-1 by simultaneous adaptation of the PBS and PAS. RNA 2002, 8(3):357-369.
17. Beerens N., Berkhout B. The tRNA primer activation signal in the human immunodeficiency virus type 1 genome is important for initiation and processive elongation of reverse transcription. Journal of Virology 2002, 76(5):2329-2339.
18. Beerens N., Groot F., Berkhout B. Initiation of HIV-1 reverse transcription is regulated by a primer activation signal. Journal of Biological Chemistry 2001, 276(33):31247-31256.
19. Ben-Artzi H., Shemesh J., Zeelon E., Amit B., Kleiman L., Gorecki M., Panet A. Molecular analysis of the second template switch during reverse transcription of the HIV RNA template. Biochemistry 1996, 35(32):10549-10557.
20. Benas P., Bec G., Keith G., Marquet R., Ehresmann C., Ehresmann B., Dumas P. The crystal structure of HIV reverse-transcription primer tRNA(Lys,3) shows a canonical anticodon loop. RNA 2000, 6(10):1347-1355.
21. Berkhout B. Structure and function of the human immunodeficiency virus leader RNA. Progress in Nucleic Acid Research and Molecular Biology 1996, 54:1-34.
22. Berkhout B., Ooms M., Beerens N., Huthoff H., Southern E., Verhoef K. In vitro evidence that the untranslated leader of the HIV-1 genome is an RNA checkpoint that regulates multiple functions through conformational changes. Journal of Biological Chemistry 2002, 277(22):19967-19975.
23. Berkhout B., Schoneveld I. Secondary structure of the HIV-2 leader RNA comprising the tRNA-primer binding site. Nucleic Acids Research 1993, 21(5):1171-1178.
24. Berkhout B., van Wamel J.L. The leader of the HIV-1 RNA genome forms a compactly folded tertiary structure. RNA 2000, 6(2):282-295.
25. Bourbigot S., Ramalanjaona N., Boudier C., Salgado G.F., Roques B.P., Mély Y., Bouaziz S., Morellet N. How the HIV-1 nucleocapsid protein binds and destabilises the (-)primer binding site during reverse transcription. Journal of Molecular Biology 2008, 383(5):1112-1128.
26. Bowerman B., Brown P.O., Bishop J.M., Varmus H.E. A nucleoprotein complex mediates the integration of retroviral DNA. Genes and Development 1989, 3(4):469-478.
27. Briggs J.A., Simon M.N., Gross I., Krausslich H.G., Fuller S.D., Vogt V.M., Johnson M.C. The stoichiometry of Gag protein in HIV-1. Nature Structural and Molecular Biology 2004, 11(7):672-675.
28. Briggs J.A., Wilk T., Welker R., Krausslich H.G., Fuller S.D. Structural organization of authentic, mature HIV-1 virions and cores. EMBO Journal 2003, 22(7):1707-1715.
29. Brule F., Marquet R., Rong L., Wainberg M.A., Roques B.P., Le Grice S.F., Ehresmann B., Ehresmann C. Structural and functional properties of the HIV-1 RNA-tRNA(Lys)3 primer complex annealed by the nucleocapsid protein: comparison with the heat-annealed complex. RNA 2002, 8(1):8-15.
30. Cen S., Huang Y., Khorchid A., Darlix J.L., Wainberg M.A., Kleiman L. The role of Pr55(gag) in the annealing of tRNA3Lys to human immunodeficiency virus type 1 genomic RNA. Journal of Virology 1999, 73(5):4485-4488.
31. Cherepanov P., Maertens G.N., Hare S. Structural insights into the retroviral DNA integration apparatus. Current Opinion in Structural Biology 2011, 21(2):249-256.
32. Chertova E., Chertov O., Coren L.V., Roser J.D., Trubey C.M., Bess J.W., Sowder R.C., Barsov E., Hood B.L., Fisher R.J., Nagashima K., Conrads T.P., Veenstra T.D., Lifson J.D., Ott D.E. Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. Journal of Virology 2006, 80(18):9039-9052.
33. Clever J.L., Miranda D., Parslow T.G. RNA structure and packaging signals in the 5' leader region of the human immunodeficiency virus type 1 genome. Journal of Virology 2002, 76(23):12381-12387.
34. Cruceanu M., Urbaneja M.A., Hixson C.V., Johnson D.G., Datta S.A., Fivash M.J., Stephen A.G., Fisher R.J., Gorelick R.J., Casas-Finet J.R., Rein A., Rouzina I., Williams M.C. Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins. Nucleic Acids Research 2006, 34(2):593-605.
35. Damgaard C.K., Dyhr-Mikkelsen H., Kjems J. Mapping the RNA binding sites for human immunodeficiency virus type-1 gag and NC proteins within the complete HIV-1 and -2 untranslated leader regions. Nucleic Acids Research 1998, 26(16):3667-3676.
36. Darlix J.L., Gabus C., Nugeyre M.T., Clavel F., Barre-Sinoussi F. Cis elements and trans-acting factors involved in the RNA dimerization of the human immunodeficiency virus HIV-1. Journal of Molecular Biology 1990, 216(3):689-699.
37. Darlix J.L., Godet J., Ivanyi-Nagy R., Fosse P., Mauffret O., Mély Y. Flexible nature and specific functions of the HIV-1 nucleocapsid protein. Journal of Molecular Biology 2011, 410(4):565-581.
38. Das A.T., Klaver B., Berkhout B. Reduced replication of human immunodeficiency virus type 1 mutants that use reverse transcription primers other than the natural tRNA(3Lys). Journal of Virology 1995, 69(5):3090-3097.
39. Das A.T., Vink M., Berkhout B. Alternative tRNA priming of human immunodeficiency virus type 1 reverse transcription explains sequence variation in the primer-binding site that has been attributed to APOBEC3G activity. Journal of Virology 2005, 79(5):3179-3181.
40. De Guzman R.N., Wu Z.R., Stalling C.C., Pappalardo L., Borer P.N., Summers M.F. Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science 1998, 279(5349):384-388.
41. De Rocquigny H., Gabus C., Vincent A., Fournie-Zaluski M.C., Roques B., Darlix J.L. Viral RNA annealing activities of human immunodeficiency virus type 1 nucleocapsid protein require only peptide domains outside the zinc fingers. Proceedings of the National Academy of Sciences of the United States of America 1992, 89(14):6472-6476.
42. Deforges J., Chamond N., Sargueil B. Structural investigation of HIV-1 genomic RNA dimerization process reveals a role for the Major Splice-site Donor stem loop. Biochimie 2012, 94(7):1481-1489.
43. Dupuy L.C., Kelly N.J., Elgavish T.E., Harvey S.C., Morrow C.D. Probing the importance of tRNA anticodon: human immunodeficiency virus type 1 (HIV-1) RNA genome complementarity with an HIV-1 that selects tRNA(Glu) for replication. Journal of Virology 2003, 77(16):8756-8764.
44. Fassati A., Goff S.P. Characterization of intracellular reverse transcription complexes of Moloney murine leukemia virus. Journal of Virology 1999, 73(11):8919-8925.
45. Fassati A., Goff S.P. Characterization of intracellular reverse transcription complexes of human immunodeficiency virus type 1. Journal of Virology 2001, 75(8):3626-3635.
46. Feng Y.X., Campbell S., Harvin D., Ehresmann B., Ehresmann C., Rein A. The human immunodeficiency virus type 1 Gag polyprotein has nucleic acid chaperone activity: possible role in dimerization of genomic RNA and placement of tRNA on the primer binding site. Journal of Virology 1999, 73(5):4251-4256.
47. Fisher R.J., Rein A., Fivash M., Urbaneja M.A., Casas-Finet J.R., Medaglia M., Henderson L.E. Sequence-specific binding of human immunodeficiency virus type 1 nucleocapsid protein to short oligonucleotides. Journal of Virology 1998, 72(3):1902-1909.
48. Frankel A.D., Young J.A. HIV-1: fifteen proteins and an RNA. Annual Review of Biochemistry 1998, 67:1-25.
49. Freund F., Boulme F., Litvak S., Tarrago-Litvak L. Initiation of HIV-2 reverse transcription: a secondary structure model of the RNA-tRNA(Lys3) duplex. Nucleic Acids Research 2001, 29(13):2757-2765.
50. Goldschmidt V., Ehresmann C., Ehresmann B., Marquet R. Does the HIV-1 primer activation signal interact with tRNA3(Lys) during the initiation of reverse transcription?. Nucleic Acids Research 2003, 31(3):850-859.
51. Goldschmidt V., Paillart J.C., Rigourd M., Ehresmann B., Aubertin A.M., Ehresmann C., Marquet R. Structural variability of the initiation complex of HIV-1 reverse transcription. Journal of Biological Chemistry 2004, 279(34):35923-35931.
52. Goncalves J., Korin Y., Zack J., Gabuzda D. Role of Vif in human immunodeficiency virus type 1 reverse transcription. Journal of Virology 1996, 70(12):8701-8709.
53. Gorelick R.J., Chabot D.J., Rein A., Henderson L.E., Arthur L.O. The two zinc fingers in the human immunodeficiency virus type 1 nucleocapsid protein are not functionally equivalent. Journal of Virology 1993, 67(7):4027-4036.
54. Gorelick R.J., Henderson L.E., Hanser J.P., Rein A. Point mutants of Moloney murine leukemia virus that fail to package viral RNA: evidence for specific RNA recognition by a zinc finger-like protein sequence. Proceedings of the National Academy of Sciences of the United States of America 1988, 85(22):8420-8424.
55. Gorelick R.J., Nigida S.M., Bess J.W., Arthur L.O., Henderson L.E., Rein A. Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. Journal of Virology 1990, 64(7):3207-3211.
56. Gotte 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. Archives of Biochemistry and Biophysics 1999, 365(2):199-210.
57. Green L.M., Berg J.M. Retroviral nucleocapsid protein-metal ion interactions: folding and sequence variants. Proceedings of the National Academy of Sciences of the United States of America 1990, 87(16):6403-6407.
58. Guo F., Saadatmand J., Niu M., Kleiman L. Roles of Gag and NCp7 in facilitating tRNA(Lys)(3) annealing to viral RNA in human immunodeficiency virus type 1. Journal of Virology 2009, 83(16):8099-8107.
59. Hargittai M.R., Gorelick R.J., Rouzina I., Musier-Forsyth K. Mechanistic insights into the kinetics of HIV-1 nucleocapsid protein-facilitated tRNA annealing to the primer binding site. Journal of Molecular Biology 2004, 337(4):951-968.
60. Hargittai M.R., Mangla A.T., Gorelick R.J., Musier-Forsyth K. HIV-1 nucleocapsid protein zinc finger structures induce tRNA(Lys,3) structural changes but are not critical for primer/template annealing. Journal of Molecular Biology 2001, 312(5):985-997.
61. Harrich D., Ulich C., Garcia-Martinez L.F., Gaynor R.B. Tat is required for efficient HIV-1 reverse transcription. EMBO Journal 1997, 16(6):1224-1235.
62. Harrison G.P., Lever A.M. The human immunodeficiency virus type 1 packaging signal and major splice donor region have a conserved stable secondary structure. Journal of Virology 1992, 66(7):4144-4153.
63. Henderson L.E., Bowers M.A., Sowder R.C., Serabyn S.A., Johnson D.G., Bess J.W., Arthur L.O., Bryant D.K., Fenselau C. Gag proteins of the highly replicative MN strain of human immunodeficiency virus type 1: posttranslational modifications, proteolytic processings, and complete amino acid sequences. Journal of Virology 1992, 66(4):1856-1865.
64. Heng X., Kharytonchyk S., Garcia E.L., Lu K., Divakaruni S.S., LaCotti C., Edme K., Telesnitsky A., Summers M.F. Identification of a minimal region of the HIV-1 5'-leader required for RNA dimerization, NC binding, and packaging. Journal of Molecular Biology 2012, 417(3):224-239.
65. Herschhorn A., Hizi A. Retroviral reverse transcriptases. Cellular and Molecular Life Sciences 2010, 67(16):2717-2747.
66. Holmes R.K., Koning F.A., Bishop K.N., Malim M.H. APOBEC3F can inhibit the accumulation of HIV-1 reverse transcription products in the absence of hypermutation. Comparisons with APOBEC3G. Journal of Biological Chemistry 2007, 282(4):2587-2595.
67. Hostomsky Z., Hostomska Z., Fu T.B., Taylor J. Reverse transcriptase of human immunodeficiency virus type 1: functionality of subunits of the heterodimer in DNA synthesis. Journal of Virology 1992, 66(5):3179-3182.
68. Huang Y., Shalom A., Li Z., Wang J., Mak J., Wainberg M.A., Kleiman L. Effects of modifying the tRNA(3Lys) anticodon on the initiation of human immunodeficiency virus type 1 reverse transcription. Journal of Virology 1996, 70(7):4700-4706.
69. Huthoff H., Bugala K., Barciszewski J., Berkhout B. On the importance of the primer activation signal for initiation of tRNA(lys3)-primed reverse transcription of the HIV-1 RNA genome. Nucleic Acids Research 2003, 31(17):5186-5194.
70. Isel C., Ehresmann C., Keith G., Ehresmann B., Marquet R. Initiation of reverse transcription of HIV-1: secondary structure of the HIV-1 RNA/tRNA(3Lys) (template/primer). Journal of Molecular Biology 1995, 247(2):236-250.
71. Isel C., Ehresmann C., Marquet R. Initiation of HIV reverse transcription. Viruses 2010, 2(1):213-243.
72. Isel C., Keith G., Ehresmann B., Ehresmann C., Marquet R. Mutational analysis of the tRNA3Lys/HIV-1 RNA (primer/template) complex. Nucleic Acids Research 1998, 26(5):1198-1204.
73. Isel C., Lanchy J.M., Le Grice S.F., Ehresmann C., Ehresmann B., Marquet R. Specific initiation and switch to elongation of human immunodeficiency virus type 1 reverse transcription require the post-transcriptional modifications of primer tRNA3Lys. EMBO Journal 1996, 15(4):917-924.
74. Isel C., Marquet R., Keith G., Ehresmann C., Ehresmann B. Modified nucleotides of tRNA(3Lys) modulate primer/template loop-loop interaction in the initiation complex of HIV-1 reverse transcription. Journal of Biological Chemistry 1993, 268(34):25269-25272.
75. Isel C., Westhof E., Massire C., Le Grice S.F., Ehresmann B., Ehresmann C., Marquet R. Structural basis for the specificity of the initiation of HIV-1 reverse transcription. EMBO Journal 1999, 18(4):1038-1048.
76. Iwatani Y., Rosen A.E., Guo J., Musier-Forsyth K., Levin J.G. Efficient 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. Journal of Biological Chemistry 2003, 278(16):14185-14195.
77. Johnson P.E., Turner R.B., Wu Z.R., Hairston L., Guo J., Levin J.G., Summers M.F. A mechanism for plus-strand transfer enhancement by the HIV-1 nucleocapsid protein during reverse transcription. Biochemistry 2000, 39(31):9084-9091.
78. Kang S.M., Zhang Z., Morrow C.D. Identification of a sequence within U5 required for human immunodeficiency virus type 1 to stably maintain a primer binding site complementary to tRNA(Met). Journal of Virology 1997, 71(1):207-217.
79. 3 for initiation of reverse transcription. Virology 1999, 257(1):95-105.
80. Karpel R.L., Henderson L.E., Oroszlan S. Interactions of retroviral structural proteins with single-stranded nucleic acids. Journal of Biological Chemistry 1987, 262(11):4961-4967.
81. Khan R., Giedroc D.P. Nucleic acid binding properties of recombinant Zn2 HIV-1 nucleocapsid protein are modulated by COOH-terminal processing. Journal of Biological Chemistry 1994, 269(36):22538-22546.
82. Kiernan R.E., Ono A., Englund G., Freed E.O. Role of matrix in an early postentry step in the human immunodeficiency virus type 1 life cycle. Journal of Virology 1998, 72(5):4116-4126.
83. Kohlstaedt L.A., Steitz T.A. Reverse transcriptase of human immunodeficiency virus can use either human tRNA(3Lys) or Escherichia coli tRNA(2Gln) as a primer in an in vitro primer-utilization assay. Proceedings of the National Academy of Sciences of the United States of America 1992, 89(20):9652-9656.
84. Lanchy J.M., Isel C., Ehresmann C., Marquet R., Ehresmann B. Structural and functional evidence that initiation and elongation of HIV-1 reverse transcription are distinct processes. Biochimie 1996, 78(11-12):1087-1096.
85. Lanchy J.M., Keith G., Le Grice S.F., Ehresmann B., Ehresmann C., Marquet R. Contacts between reverse transcriptase and the primer strand govern the transition from initiation to elongation of HIV-1 reverse transcription. Journal of Biological Chemistry 1998, 273(38):24425-24432.
86. Lapadat-Tapolsky M., Pernelle C., Borie C., Darlix J.L. Analysis of the nucleic acid annealing activities of nucleocapsid protein from HIV-1. Nucleic Acids Research 1995, 23(13):2434-2441.
87. Le Grice S.F. In the beginning: initiation of minus strand DNA synthesis in retroviruses and LTR-containing retrotransposons. Biochemistry 2003, 42(49):14349-14355.
88. Lee B.M., De Guzman R.N., Turner B.G., Tjandra N., Summers M.F. Dynamical behavior of the HIV-1 nucleocapsid protein. Journal of Molecular Biology 1998, 279(3):633-649.
89. Lescop E., Schanda P., Brutscher B. A set of BEST triple-resonance experiments for time-optimized protein resonance assignment. Journal of Magnetic Resonance 2007, 187(1):163-169.
90. Levin J.G., Guo J., Rouzina I., Musier-Forsyth K. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Progress in Nucleic Acid Research and Molecular Biology 2005, 80:217-286.
91. Li X., Mak J., Arts E.J., Gu Z., Kleiman L., Wainberg M.A., Parniak M.A. Effects of alterations of primer-binding site sequences on human immunodeficiency virus type 1 replication. Journal of Virology 1994, 68(10):6198-6206.
92. Li X., Quan Y., Arts E.J., Li Z., Preston B.D., de Rocquigny H., Roques B.P., Darlix J.L., Kleiman L., Parniak M.A., Wainberg M.A. Human immunodeficiency virus Type 1 nucleocapsid protein (NCp7) directs specific initiation of minus-strand DNA synthesis primed by human tRNA(Lys3) in vitro: studies of viral RNA molecules mutated in regions that flank the primer binding site. Journal of Virology 1996, 70(8):4996-5004.
93. Liang C., Li X., Rong L., Inouye P., Quan Y., Kleiman L., Wainberg M.A. The importance of the A-rich loop in human immunodeficiency virus type 1 reverse transcription and infectivity. Journal of Virology 1997, 71(8):5750-5757.
94. 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 2008, 322(5904):1092-1097.
95. Liu S., Harada B.T., Miller J.T., Le Grice S.F., Zhuang X. Initiation complex dynamics direct the transitions between distinct phases of early HIV reverse transcription. Nature Structural and Molecular Biology 2010, 17(12):1453-1460.
96. Lu K., Heng X., Garyu L., Monti S., Garcia E.L., Kharytonchyk S., Dorjsuren B., Kulandaivel G., Jones S., Hiremath A., Divakaruni S.S., LaCotti C., Barton S., Tummillo D., Hosic A., Edme K., Albrecht S., Telesnitsky A., Summers M.F. NMR detection of structures in the HIV-1 5'-leader RNA that regulate genome packaging. Science 2011, 334(6053):242-245.
97. Mak J., Jiang M., Wainberg M.A., Hammarskjold M.L., Rekosh D., Kleiman L. Role of Pr160gag-pol in mediating the selective incorporation of tRNA(Lys) into human immunodeficiency virus type 1 particles. Journal of Virology 1994, 68(4):2065-2072.
98. Mak J., Kleiman L. Primer tRNAs for reverse transcription. Journal of Virology 1997, 71(11):8087-8095.
99. McCulley A., Morrow C.D. Nucleotides within the anticodon stem are important for optimal use of tRNA(Lys,3) as the primer for HIV-1 reverse transcription. Virology 2007, 364(1):169-177.
100. Mély Y., de Rocquigny H., Sorinas-Jimeno M., Keith G., Roques B.P., Marquet R., Gerard D. Binding of the HIV-1 nucleocapsid protein to the primer tRNA(3Lys), in vitro, is essentially not specific. Journal of Biological Chemistry 1995, 270(4):1650-1656.
101. Morellet N., Demene H., Teilleux V., Huynh-Dinh T., de Rocquigny H., Fournie-Zaluski M.C., Roques B.P. Structure of the complex between the HIV-1 nucleocapsid protein NCp7 and the single-stranded pentanucleotide d(ACGCC). Journal of Molecular Biology 1998, 283(2):419-434.
102. 1H NMR. EMBO Journal 1992, 11(8):3059-3065.
103. Mougel M., Houzet L., Darlix J.L. When is it time for reverse transcription to start and go?. Retrovirology 2009, 6:24.
104. Muriaux D., De Rocquigny H., Roques B.P., Paoletti J. NCp7 activates HIV-1Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. Journal of Biological Chemistry 1996, 271(52):33686-33692.
105. Newman J.L., Butcher E.W., Patel D.T., Mikhaylenko Y., Summers M.F. Flexibility in the P2 domain of the HIV-1 Gag polyprotein. Protein Science 2004, 13(8):2101-2107.
106. Ooms M., Cupac D., Abbink T.E., Huthoff H., Berkhout B. The availability of the primer activation signal (PAS) affects the efficiency of HIV-1 reverse transcription initiation. Nucleic Acids Research 2007, 35(5):1649-1659.
107. Paillart J.C., Dettenhofer M., Yu X.F., Ehresmann C., Ehresmann B., Marquet R. First snapshots of the HIV-1 RNA structure in infected cells and in virions. Journal of Biological Chemistry 2004, 279(46):48397-48403.
108. Paillart J.C., Marquet R., Skripkin E., Ehresmann B., Ehresmann C. Mutational analysis of the bipartite dimer linkage structure of human immunodeficiency virus type 1 genomic RNA. Journal of Biological Chemistry 1994, 269(44):27486-27493.
109. Paillart J.C., Shehu-Xhilaga M., Marquet R., Mak J. Dimerization of retroviral RNA genomes: an inseparable pair. Nature Reviews Microbiology 2004, 2(6):461-472.
110. Peliska J.A., Balasubramanian S., Giedroc D.P., Benkovic S.J. Recombinant HIV-1 nucleocapsid protein accelerates HIV-1 reverse transcriptase catalyzed DNA strand transfer reactions and modulates RNase H activity. Biochemistry 1994, 33(46):13817-13823.
111. Peterlin B.M., Luciw P.A., Barr P.J., Walker M.D. Elevated levels of mRNA can account for the trans-activation of human immunodeficiency virus. Proceedings of the National Academy of Sciences of the United States of America 1986, 83(24):9734-9738.
112. Puglisi E.V., Puglisi J.D. Secondary structure of the HIV reverse transcription initiation complex by NMR. Journal of Molecular Biology 2011, 410(5):863-874.
113. Rein A., Henderson L.E., Levin J.G. Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends in Biochemical Sciences 1998, 23(8):297-301.
114. Rhim H., Park J., Morrow C.D. Deletions in the tRNA(Lys) primer-binding site of human immunodeficiency virus type 1 identify essential regions for reverse transcription. Journal of Virology 1991, 65(9):4555-4564.
115. Rigourd M., Goldschmidt V., Brule F., Morrow C.D., Ehresmann B., Ehresmann C., Marquet R. Structure-function relationships of the initiation complex of HIV-1 reverse transcription: the case of mutant viruses using tRNA(His) as primer. Nucleic Acids Research 2003, 31(19):5764-5775.
116. Saadatmand J., Niu M., Kleiman L., Guo F. The contribution of the primer activation signal to differences between Gag- and NCp7-facilitated tRNA(Lys3) annealing in HIV-1. Virology 2009, 391(2):334-341.
117. Schanda P., Van Melckebeke H., Brutscher B. Speeding up three-dimensional protein NMR experiments to a few minutes. Journal of the American Chemical Society 2006, 128(28):9042-9043.
118. Schwartz O., Marechal V., Danos O., Heard J.M. Human immunodeficiency virus type 1 Nef increases the efficiency of reverse transcription in the infected cell. Journal of Virology 1995, 69(7):4053-4059.
119. Shubsda M.F., Paoletti A.C., Hudson B.S., Borer P.N. Affinities of packaging domain loops in HIV-1 RNA for the nucleocapsid protein. Biochemistry 2002, 41(16):5276-5282.
120. Skripkin E., Paillart J.C., Marquet R., Ehresmann B., Ehresmann C. Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proceedings of the National Academy of Sciences of the United States of America 1994, 91(11):4945-4949.
121. South T.L., Blake P.R., Hare D.R., Summers M.F. C-terminal retroviral-type zinc finger domain from the HIV-1 nucleocapsid protein is structurally similar to the N-terminal zinc finger domain. Biochemistry 1991, 30(25):6342-6349.
122. Sova P., Volsky D.J. Efficiency of viral DNA synthesis during infection of permissive and nonpermissive cells with vif-negative human immunodeficiency virus type 1. Journal of Virology 1993, 67(10):6322-6326.
123. Stark L.A., Hay R.T. Human immunodeficiency virus type 1 (HIV-1) viral protein R (Vpr) interacts with Lys-tRNA synthetase: implications for priming of HIV-1 reverse transcription. Journal of Virology 1998, 72(4):3037-3044.
124. Summers M.F., Henderson L.E., Chance M.R., Bess J.W., South T.L., Blake P.R., Sagi I., Perez-Alvarado G., Sowder R.C., Hare D.R., et al. Nucleocapsid zinc fingers detected in retroviruses: EXAFS studies of intact viruses and the solution-state structure of the nucleocapsid protein from HIV-1. Protein Science 1992, 1(5):563-574.
125. Takahashi H., Matsuda M., Kojima A., Sata T., Andoh T., Kurata T., Nagashima K., Hall W.W. Human immunodeficiency virus type 1 reverse transcriptase: enhancement of activity by interaction with cellular topoisomerase I. Proceedings of the National Academy of Sciences of the United States of America 1995, 92(12):5694-5698.
126. Thali M., Bukovsky A., Kondo E., Rosenwirth B., Walsh C.T., Sodroski J., Gottlinger H.G. Functional association of cyclophilin A with HIV-1 virions. Nature 1994, 372(6504):363-365.
127. Tisne C. Structural bases of the annealing of primer tRNA(3Lys) to the HIV-1 viral RNA. Current HIV Research 2005, 3(2):147-156.
128. Tisne C., Rigourd M., Marquet R., Ehresmann C., Dardel F. NMR and biochemical characterization of recombinant human tRNA(Lys)3 expressed in Escherichia coli: identification of posttranscriptional nucleotide modifications required for efficient initiation of HIV-1 reverse transcription. RNA 2000, 6(10):1403-1412.
129. Tisne C., Roques B.P., Dardel F. The annealing mechanism of HIV-1 reverse transcription primer onto the viral genome. Journal of Biological Chemistry 2004, 279(5):3588-3595.
130. Tsurutani N., Kubo M., Maeda Y., Ohashi T., Yamamoto N., Kannagi M., Masuda T. Identification of critical amino acid residues in human immunodeficiency virus type 1 IN required for efficient proviral DNA formation at steps prior to integration in dividing and nondividing cells. Journal of Virology 2000, 74(10):4795-4806.
131. Urbaneja M.A., Kane B.P., Johnson D.G., Gorelick R.J., Henderson L.E., Casas-Finet J.R. Binding properties of the human immunodeficiency virus type 1 nucleocapsid protein p7 to a model RNA: elucidation of the structural determinants for function. Journal of Molecular Biology 1999, 287(1):59-75.
132. Vuilleumier C., Bombarda E., Morellet N., Gerard D., Roques B.P., Mély Y. Nucleic acid sequence discrimination by the HIV-1 nucleocapsid protein NCp7: a fluorescence study. Biochemistry 1999, 38(51):16816-16825.
133. Wakefield J.K., Kang S.M., Morrow C.D. Construction of a type 1 human immunodeficiency virus that maintains a primer binding site complementary to tRNA(His). Journal of Virology 1996, 70(2):966-975.
134. Wakefield J.K., Wolf A.G., Morrow C.D. Human immunodeficiency virus type 1 can use different tRNAs as primers for reverse transcription but selectively maintains a primer binding site complementary to tRNA(3Lys). Journal of Virology 1995, 69(10):6021-6029.
135. Watts J.M., Dang K.K., Gorelick R.J., Leonard C.W., Bess J.W., Swanstrom R., Burch C.L., Weeks K.M. Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 2009, 460(7256):711-716.
136. Wilkinson K.A., Gorelick R.J., Vasa S.M., Guex N., Rein A., Mathews D.H., Giddings M.C., Weeks K.M. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biology 2008, 6(4):e96.
137. Wohrl B.M., Krebs R., Goody R.S., Restle T. Refined model for primer/template binding by HIV-1 reverse transcriptase: pre-steady-state kinetic analyses of primer/template binding and nucleotide incorporation events distinguish between different binding modes depending on the nature of the nucleic acid substrate. Journal of Molecular Biology 1999, 292(2):333-344.
138. Wondrak E.M., Louis J.M., de Rocquigny H., Chermann J.C., Roques B.P. The gag precursor contains a specific HIV-1 protease cleavage site between the NC (P7) and P1 proteins. FEBS Letters 1993, 333(1-2):21-24.
139. Wu X., Liu H., Xiao H., Conway J.A., Hehl E., Kalpana G.V., Prasad V., Kappes J.C. Human immunodeficiency virus type 1 integrase protein promotes reverse transcription through specific interactions with the nucleoprotein reverse transcription complex. Journal of Virology 1999, 73(3):2126-2135.
140. Yedavalli V.S., Jeang K.T. Trimethylguanosine capping selectively promotes expression of Rev-dependent HIV-1 RNAs. Proceedings of the National Academy of Sciences of the United States of America 2010, 107(33):14787-14792.
141. You J.C., McHenry C.S. HIV nucleocapsid protein. Expression in Escherichia coli, purification, and characterization. Journal of Biological Chemistry 1993, 268(22):16519-16527.
142. Yusupova G., Lanchy J.M., Yusupov M., Keith G., Le Grice S.F., Ehresmann C., Ehresmann B., Marquet R. Primer selection by HIV-1 reverse transcriptase on RNA-tRNA(3Lys) and DNA-tRNA(3Lys) hybrids. Journal of Molecular Biology 1996, 261(3):315-321.
143. Zhang H., Dornadula G., Orenstein J., Pomerantz R.J. Morphologic changes in human immunodeficiency virus type 1 virions secondary to intravirion reverse transcription: evidence indicating that reverse transcription may not take place within the intact viral core. Journal of Human Virology 2000, 3(3):165-172.
144. Zhang Z., Kang S.M., LeBlanc A., Hajduk S.L., Morrow C.D. Nucleotide sequences within the U5 region of the viral RNA genome are the major determinants for an human immunodeficiency virus type 1 to maintain a primer binding site complementary to tRNA(His). Virology 1996, 226(2):306-317.
145. Zhang Z., Kang S.M., Li Y., Morrow C.D. Genetic analysis of the U5-PBS of a novel HIV-1 reveals multiple interactions between the tRNA and RNA genome required for initiation of reverse transcription. RNA 1998, 4(4):394-406.
146. Zhu K., Dobard C., Chow S.A. Requirement for integrase during reverse transcription of human immunodeficiency virus type 1 and the effect of cysteine mutations of integrase on its interactions with reverse transcriptase. Journal of Virology 2004, 78(10):5045-5055.