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Transfer RNA modifications and DNA editing in HIV-1 reverse transcription

Part of the Topics in Current Genetics book series (TCG,volume 12)

Abstract

Reverse transcription is a central step in HIV-1 replication that represents a typical case of interplay between viral and cellular factors. HIV-1 diverts a cellular tRNA, tRNALys3, to prime reverse transcription. The post-transcriptional modifications of tRNALys3 are crucial for completion of reverse transcription. In some HIV-1 isolates, they are required for efficient initiation of (–) strand DNA synthesis, and in all strains, methylation of A58 is required to allow productive strand transfer during (+) strand DNA synthesis. On the other hand, some human cell types have evolved an innate antiretroviral mechanism by promoting extensive deamination of the (–) strand DNA during reverse transcription. In the absence of viral defence, this hyper-editing induces DNA degradation and lethal mutagenesis of the viral DNA. However, Vif, one of the HIV-1 “accessory” proteins, is able to inhibit DNA deamination by preventing incorporation of the editing enzymes APOBEC3G and APOBEC3F into the viral particles.

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References

  • 1. Agris PF (1996) The importance of being modified: roles of modified nucleosides and Mg2+ in RNA structure and function. Prog Nucleic Acid Res Mol Biol 53:79-129

    Google Scholar 

  • 2. Agris PF, Guenther R, Ingram PC, Basti MM, Stuart JW, Sochacka E, Malkiewicz A (1997) Unconventional structure of tRNA(Lys)SUU anticodon explains tRNA’s role in bacterial and mammalian ribosomal frameshifting and primer selection by HIV-1. RNA 3:420-428

    Google Scholar 

  • 3. Alce TM, Popik W (2004) APOBEC3G is incorporated into virus-like particles by a direct interaction with HIV-1 Gag nucleocapsid protein. J Biol Chem 279:34083-34086

    CrossRef  Google Scholar 

  • 4. Alexander L, Aquino-DeJesus MJ, Chan M, Andiman WA (2002) Inhibition of human immunodeficiency virus type 1 (HIV-1) replication by a two-amino-acid insertion in HIV-1 Vif from a nonprogressing mother and child. J Virol 76:10533-10539

    CrossRef  Google Scholar 

  • 5. Arion D, Harada R, Li X, Wainberg MA, Parniak MA (1996) HIV-1 reverse transcriptase shows no specificity for the binding of primer tRNA(Lys3). Biochem Biophys Res Commun 225:839-843

    CrossRef  Google Scholar 

  • 6. Auxilien S, Keith G, Le Grice SF, Darlix JL (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 274:4412-4420

    CrossRef  Google Scholar 

  • 7. Bajji AC, Sundaram M, Myszka DG, Davis DR (2002) An RNA complex of the HIV-1 A-loop and tRNA(Lys,3) is stabilized by nucleoside modifications. J Am Chem Soc 124:14302-14303

    CrossRef  Google Scholar 

  • 8. Barat C, Lullien V, Schatz O, Keith G, Nugeyre MT, Gruninger-Leitch F, Barre-Sinoussi F, LeGrice SF, Darlix JL (1989) HIV-1 reverse transcriptase specifically interacts with the anticodon domain of its cognate primer tRNA. EMBO J 8:3279-3285

    Google Scholar 

  • 9. Bass BL (2002) RNA editing by adenosine deaminases that act on RNA. Annu Rev Biochem 71:817-846

    CrossRef  Google Scholar 

  • 10. Beale RC, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS (2004) Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo. J Mol Biol 337:585-596

    CrossRef  Google Scholar 

  • 11. Beerens N, Berkhout B (2000) In vitro studies on tRNA annealing and reverse transcription with mutant HIV-1 RNA templates. J Biol Chem 275:15474-15481

    CrossRef  Google Scholar 

  • 12. Beerens N, Groot F, Berkhout B (2000a) Stabilization of the U5-leader stem in the HIV-1 RNA genome affects initiation and elongation of reverse transcription. Nucleic Acids Res 28:4130-4137

    CrossRef  Google Scholar 

  • 13. Beerens N, Groot F, Berkhout B (2001) Initiation of HIV-1 reverse transcription is regulated by a primer activation signal. J Biol Chem 276:31247-31256

    CrossRef  Google Scholar 

  • 14. Beerens N, Klaver B, Berkhout B (2000b) A structured RNA motif is involved in correct placement of the tRNA(3)(Lys) primer onto the human immunodeficiency virus genome. J Virol 74:2227-2238

    CrossRef  Google Scholar 

  • 15. Ben-Artzi H, Shemesh J, Zeelon E, Amit B, Kleiman L, Gorecki M, Panet A (1996) Molecular analysis of the second template switch during reverse transcription of the HIV RNA template. Biochemistry 35:10549-10557

    CrossRef  Google Scholar 

  • 16. Benas P, Bec G, Keith G, Marquet R, Ehresmann C, Ehresmann B, Dumas P (2000) The crystal structure of HIV reverse-transcription primer tRNA(Lys,3) shows a canonical anticodon loop. RNA 6:1347-1355

    CrossRef  Google Scholar 

  • 17. Berkhout B, De Ronde A (2004) APOBEC3G versus reverse transcriptase in the generation of HIV-1 drug-resistance mutations. Aids 18:1861-1863

    CrossRef  Google Scholar 

  • 18. Berkhout B, Grigoriev A, Bakker M, Lukashov VV (2002) Codon and amino acid usage in retroviral genomes is consistent with virus-specific nucleotide pressure. AIDS Res Hum Retroviruses 18:133-141

    CrossRef  Google Scholar 

  • 19. Berkhout B, van Hemert FJ (1994) The unusual nucleotide content of the HIV RNA genome results in a biased amino acid composition of HIV proteins. Nucleic Acids Res 22:1705-1711

    Google Scholar 

  • 20. Bishop KN, Holmes RK, Sheehy AM, Davidson NO, Cho SJ, Malim MH (2004) Cytidine deamination of retroviral DNA by diverse APOBEC proteins. Curr Biol 14:1392-1396

    CrossRef  Google Scholar 

  • 21. Bogerd HP, Doehle BP, Wiegand HL, Cullen BR (2004) A single amino acid difference in the host APOBEC3G protein controls the primate species specificity of HIV type 1 virion infectivity factor. Proc Natl Acad Sci USA 101:3770-3774

    CrossRef  Google Scholar 

  • 22. Brule F, Marquet R, Rong L, Wainberg MA, Roques BP, Le Grice SF, Ehresmann B, Ehresmann C (2002) 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 8:8-15

    CrossRef  Google Scholar 

  • 23. Burnett BP, McHenry CS (1997) Posttranscriptional modification of retroviral primers is required for late stages of DNA replication. Proc Natl Acad Sci USA 94:7210-7215

    CrossRef  Google Scholar 

  • 24. Cen S, Guo F, Niu M, Saadatmand J, Deflassieux J, Kleiman L (2004a) The interaction between HIV-1 Gag and APOBEC3G. J Biol Chem 279:33177-33184

    CrossRef  Google Scholar 

  • 25. Cen S, Javanbakht H, Niu M, Kleiman L (2004b) Ability of wild-type and mutant lysyl-tRNA synthetase to facilitate tRNA(Lys) incorporation into human immunodeficiency virus type 1. J Virol 78:1595-1601

    CrossRef  Google Scholar 

  • 26. Conticello SG, Harris RS, Neuberger MS (2003) The Vif protein of HIV triggers degradation of the human antiretroviral DNA deaminase APOBEC3G. Curr Biol 13:2009-2013

    CrossRef  Google Scholar 

  • 27. Das AT, Klaver B, Berkhout B (1995) Reduced replication of human immunodeficiency virus type 1 mutants that use reverse transcription primers other than the natural tRNA(3Lys). J Virol 69:3090-3097

    Google Scholar 

  • 28. Davanloo P, Sprinzl M, Watanabe K, Albani M, Kersten H (1979) Role of ribothymidine in the thermal stability of transfer RNA as monitored by proton magnetic resonance. Nucleic Acids Res 6:1571-1581

    Google Scholar 

  • 29. De Rocquigny H, Gabus C, Vincent A, Fournie-Zaluski MC, Roques B, Darlix JL (1992) Viral RNA annealing activities of human immunodeficiency virus type 1 nucleocapsid protein require only peptide domains outside the zinc fingers. Proc Natl Acad Sci USA 89:6472-6476

    Google Scholar 

  • 30. Derrick WB, Horowitz J (1993) Probing structural differences between native and in vitro transcribed Escherichia coli valine transfer RNA: evidence for stable base modification-dependent conformers. Nucleic Acids Res 21:4948-4953

    Google Scholar 

  • 31. Desrosiers RC, Lifson JD, Gibbs JS, Czajak SC, Howe AY, Arthur LO, Johnson RP (1998) Identification of highly attenuated mutants of simian immunodeficiency virus. J Virol 72:1431-1437

    Google Scholar 

  • 32. Dettenhofer M, Cen S, Carlson BA, Kleiman L, Yu XF (2000) Association of human immunodeficiency virus type 1 Vif with RNA and its role in reverse transcription. J Virol 74:8938-8945

    CrossRef  Google Scholar 

  • 33. Dornadula G, Yang S, Pomerantz RJ, Zhang H (2000) Partial rescue of the Vif-negative phenotype of mutant human immunodeficiency virus type 1 strains from nonpermissive cells by intravirion reverse transcription. J Virol 74:2594-2602

    CrossRef  Google Scholar 

  • 34. Douaisi M, Dussart S, Courcoul M, Bessou G, Vigne R, Decroly E (2004) HIV-1 and MLV Gag proteins are sufficient to recruit APOBEC3G into virus-like particles. Biochem Biophys Res Commun 321:566-573

    CrossRef  Google Scholar 

  • 35. Droogmans L, Roovers M, Bujnicki JM, Tricot C, Hartsh T, Stalon V, Grosjean H (2003) Cloning and characterization of tRNA (m1A58) methyltransferase (TrmI) from Thermus thermophilus HB27, a protein required for cell growth at extreme temperatures. Nucleic Acids Res 31:2148-2156

    CrossRef  Google Scholar 

  • 36. Fitzgibbon JE, Mazar S, Dubin DT (1993) A new type of G$to$A hypermutation affecting human immunodeficiency virus. AIDS Res Hum Retroviruses 9:833-838

    Google Scholar 

  • 37. Fortini P, Pascucci B, Parlanti E, D’Errico M, Simonelli V, Dogliotti E (2003) The base excision repair: mechanisms and its relevance for cancer susceptibility. Biochimie 85:1053-1071

    CrossRef  Google Scholar 

  • 38. Francin M, Kaminska M, Kerjan P, Mirande M (2002) The N-terminal domain of mammalian Lysyl-tRNA synthetase is a functional tRNA-binding domain. J Biol Chem 277:1762-1769

    CrossRef  Google Scholar 

  • 39. Francin M, Mirande M (2003) Functional dissection of the eukaryotic-specific tRNA-interacting factor of lysyl-tRNA synthetase. J Biol Chem 278:1472-1479

    CrossRef  Google Scholar 

  • 40. Gabuzda DH, Lawrence K, Langhoff E, Terwilliger E, Dorfman T, Haseltine WA, Sodroski J (1992) Role of vif in replication of human immunodeficiency virus type 1 in CD4+ T lymphocytes. J Virol 66:6489-6495

    Google Scholar 

  • 41. Gaddis NC, Chertova E, Sheehy AM, Henderson LE, Malim MH (2003) Comprehensive investigation of the molecular defect in vif-deficient human immunodeficiency virus type 1 virions. J Virol 77:5810-5820

    CrossRef  Google Scholar 

  • 42. Gilboa E, Mitra SW, Goff S, Baltimore D (1979) A detailed model of reverse transcription and tests of crucial aspects. Cell 18:93-100

    CrossRef  Google Scholar 

  • 43. Goldschmidt V, Ehresmann C, Ehresmann B, Marquet R (2003) Does the HIV-1 primer activation signal interact with tRNA3(Lys) during the initiation of reverse transcription? Nucleic Acids Res 31:850-859

    CrossRef  Google Scholar 

  • 44. Goldschmidt V, Paillart JC, Rigourd M, Ehresmann B, Aubertin AM, Ehresmann C, Marquet R (2004) Structural variability of the initiation complex of HIV-1 reverse transcription. J Biol Chem 279:35923-35931

    CrossRef  Google Scholar 

  • 45. Grosjean H, Houssier C, Romby P, Marquet R (1998) Modulatory role of modified nucleotides in RNA loop-loop interactions. In: Benne R (ed) Modification and Editing of RNA. ASM Press, Washington, D.C., pp 517-533

    Google Scholar 

  • 46. Gunther S, Sommer G, Plikat U, Iwanska A, Wain-Hobson S, Will H, Meyerhans A (1997) Naturally occurring hepatitis B virus genomes bearing the hallmarks of retroviral G$to$A hypermutation. Virology 235:104-108

    Google Scholar 

  • 47. Guo F, Cen S, Niu M, Javanbakht H, Kleiman L (2003) Specific inhibition of the synthesis of human lysyl-tRNA synthetase results in decreases in tRNA(Lys) incorporation, tRNA(3)(Lys) annealing to viral RNA, and viral infectivity in human immunodeficiency virus type 1. J Virol 77:9817-9822

    CrossRef  Google Scholar 

  • 48. Halwani R, Cen S, Javanbakht H, Saadatmand J, Kim S, Shiba K, Kleiman L (2004) Cellular distribution of Lysyl-tRNA synthetase and its interaction with Gag during human immunodeficiency virus type 1 assembly. J Virol 78:7553-7564

    CrossRef  Google Scholar 

  • 49. Hargittai MR, Gorelick RJ, Rouzina I, Musier-Forsyth K (2004) Mechanistic insights into the kinetics of HIV-1 nucleocapsid protein-facilitated tRNA annealing to the primer binding site. J Mol Biol 337:951-968

    CrossRef  Google Scholar 

  • 50. Hargittai MR, Mangla AT, Gorelick RJ, Musier-Forsyth K (2001) HIV-1 nucleocapsid protein zinc finger structures induce tRNA(Lys,3) structural changes but are not critical for primer/template annealing. J Mol Biol 312:985-997

    CrossRef  Google Scholar 

  • 51. Harmache A, Russo P, Guiguen F, Vitu C, Vignoni M, Bouyac M, Hieblot C, Pepin M, Vigne R, Suzan M (1996) Requirement of caprine arthritis encephalitis virus vif gene for in vivo replication. Virology 224:246-255

    CrossRef  Google Scholar 

  • 52. Harris RS, Bishop KN, Sheehy AM, Craig HM, Petersen-Mahrt SK, Watt IN, Neuberger MS, Malim MH (2003) DNA deamination mediates innate immunity to retroviral infection. Cell 113:803-809

    CrossRef  Google Scholar 

  • 53. Houssier C, Degee P, Nicoghosian K, Grosjean H (1988) Effect of uridine dethiolation in the anticodon triplet of tRNA(Glu) on its association with tRNA(Phe). J Biomol Struct Dyn 5:1259-1266

    Google Scholar 

  • 54. Huang Y, Shalom A, Li Z, Wang J, Mak J, Wainberg MA, Kleiman L (1996) Effects of modifying the tRNA(3Lys) anticodon on the initiation of human immunodeficiency virus type 1 reverse transcription. J Virol 70:4700-4706

    Google Scholar 

  • 55. Huang Y, Wang J, Shalom A, Li Z, Khorchid A, Wainberg MA, Kleiman L (1997) Primer tRNA3Lys on the viral genome exists in unextended and two-base extended forms within mature human immunodeficiency virus type 1. J Virol 71:726-728

    Google Scholar 

  • 56. Inoshima Y, Miyazawa T, Mikami T (1998) In vivo functions of the auxiliary genes and regulatory elements of feline immunodeficiency virus. Vet Microbiol 60:141-153

    CrossRef  Google Scholar 

  • 57. Isel C, Ehresmann C, Keith G, Ehresmann B, Marquet R (1995) Initiation of reverse transcription of HIV-1: secondary structure of the HIV-1 RNA/tRNA(3Lys) (template/primer). J Mol Biol 247:236-250

    CrossRef  Google Scholar 

  • 58. Isel C, Keith G, Ehresmann B, Ehresmann C, Marquet R (1998) Mutational analysis of the tRNA3Lys/HIV-1 RNA (primer/template) complex. Nucleic Acids Res 26:1198-1204

    CrossRef  Google Scholar 

  • 59. Isel C, Lanchy JM, Le Grice SF, Ehresmann C, Ehresmann B, Marquet R (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

    Google Scholar 

  • 60. Isel C, Marquet R, Keith G, Ehresmann C, Ehresmann B (1993) Modified nucleotides of tRNA(3Lys) modulate primer/template loop-loop interaction in the initiation complex of HIV-1 reverse transcription. J Biol Chem 268:25269-25272

    Google Scholar 

  • 61. Isel C, Westhof E, Massire C, Le Grice SF, Ehresmann B, Ehresmann C, Marquet R (1999) Structural basis for the specificity of the initiation of HIV-1 reverse transcription. EMBO J 18:1038-1048

    CrossRef  Google Scholar 

  • 62. Janini M, Rogers M, Birx DR, McCutchan FE (2001) Human immunodeficiency virus type 1 DNA sequences genetically damaged by hypermutation are often abundant in patient peripheral blood mononuclear cells and may be generated during near-simultaneous infection and activation of CD4(+) T cells. J Virol 75:7973-7986

    CrossRef  Google Scholar 

  • 63. Jarmuz A, Chester A, Bayliss J, Gisbourne J, Dunham I, Scott J, Navaratnam N (2002) An anthropoid-specific locus of orphan C to U RNA-editing enzymes on chromosome 22. Genomics 79:285-296

    CrossRef  Google Scholar 

  • 64. Javanbakht H, Halwani R, Cen S, Saadatmand J, Musier-Forsyth K, Gottlinger H, Kleiman L (2003) The interaction between HIV-1 Gag and human lysyl-tRNA synthetase during viral assembly. J Biol Chem 278:27644-27651

    CrossRef  Google Scholar 

  • 65. Johnson PR, Hamm TE, Goldstein S, Kitov S, Hirsch VM (1991) The genetic fate of molecularly cloned simian immunodeficiency virus in experimentally infected macaques. Virology 185:217-228

    Google Scholar 

  • 66. Kang SM, Morrow CD (1999) Genetic analysis of a unique human immunodeficiency virus type 1 (HIV-1) with a primer binding site complementary to tRNAMet supports a role for U5-PBS stem-loop RNA structures in initiation of HIV-1 reverse transcription. J Virol 73:1818-1827

    Google Scholar 

  • 67. Kang SM, Wakefield JK, Morrow CD (1996) Mutations in both the U5 region and the primer-binding site influence the selection of the tRNA used for the initiation of HIV-1 reverse transcription. Virology 222:401-414

    Google Scholar 

  • 68. Kang SM, Zhang Z, Morrow CD (1999) Identification of a human immunodeficiency virus type 1 that stably uses tRNALys1,2 rather than tRNALys,3 for initiation of reverse transcription. Virology 257:95-105

    CrossRef  Google Scholar 

  • 69. Kao S, Khan MA, Miyagi E, Plishka R, Buckler-White A, Strebel K (2003) The human immunodeficiency virus type 1 Vif protein reduces intracellular expression and inhibits packaging of APOBEC3G (CEM15), a cellular inhibitor of virus infectivity. J Virol 77:11398-11407

    CrossRef  Google Scholar 

  • 70. Kintanar A, Yue D, Horowitz J (1994) Effect of nucleoside modifications on the structure and thermal stability of Escherichia coli valine tRNA. Biochimie 76:1192-1204

    CrossRef  Google Scholar 

  • 71. Klarmann GJ, Chen X, North TW, Preston BD (2003) Incorporation of uracil into minus strand DNA affects the specificity of plus strand synthesis initiation during lentiviral reverse transcription. J Biol Chem 278:7902-7909

    CrossRef  Google Scholar 

  • 72. Kleiman L, Halwani R, Javanbakht H (2004) The selective packaging and annealing of primer tRNALys3 in HIV-1. Curr HIV Res 2:163-175

    Google Scholar 

  • 73. Lanchy JM, Ehresmann C, Le Grice SF, Ehresmann B, Marquet R (1996) Binding and kinetic properties of HIV-1 reverse transcriptase markedly differ during initiation and elongation of reverse transcription. EMBO J 15:7178-7187

    Google Scholar 

  • 74. Le Grice SF (2003) ”In the beginning”: initiation of minus strand DNA synthesis in retroviruses and LTR-containing retrotransposons. Biochemistry 42:14349-14355

    CrossRef  Google Scholar 

  • 75. Lecossier D, Bouchonnet F, Clavel F, Hance AJ (2003) Hypermutation of HIV-1 DNA in the absence of the Vif protein. Science 300:1112

    CrossRef  Google Scholar 

  • 76. Li J, Potash MJ, Volsky DJ (2004) Functional domains of APOBEC3G required for antiviral activity. J Cell Biochem 92:560-572

    CrossRef  Google Scholar 

  • 77. Li X, Mak J, Arts EJ, Gu Z, Kleiman L, Wainberg MA, Parniak MA (1994) Effects of alterations of primer-binding site sequences on human immunodeficiency virus type 1 replication. J Virol 68:6198-6206

    Google Scholar 

  • 78. Liang C, Li X, Rong L, Inouye P, Quan Y, Kleiman L, Wainberg MA (1997) The importance of the A-rich loop in human immunodeficiency virus type 1 reverse transcription and infectivity. J Virol 71:5750-5757

    Google Scholar 

  • 79. Liddament MT, Brown WL, Schumacher AJ, Harris RS (2004) APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo. Curr Biol 14:1385-1391

    CrossRef  Google Scholar 

  • 80. Liu B, Yu X, Luo K, Yu Y, Yu XF (2004) Influence of primate lentiviral Vif and proteasome inhibitors on human immunodeficiency virus type 1 virion packaging of APOBEC3G. J Virol 78:2072-2081

    CrossRef  Google Scholar 

  • 81. Madani N, Kabat D (1998) An endogenous inhibitor of human immunodeficiency virus in human lymphocytes is overcome by the viral Vif protein. J Virol 72:10251-10255

    Google Scholar 

  • 82. Maglott EJ, Deo SS, Przykorska A, Glick GD (1998) Conformational transitions of an unmodified tRNA: implications for RNA folding. Biochemistry 37:16349-16359

    CrossRef  Google Scholar 

  • 83. Mak J, Jiang M, Wainberg MA, Hammarskjold ML, Rekosh D, Kleiman L (1994) Role of Pr160gag-pol in mediating the selective incorporation of tRNA(Lys) into human immunodeficiency virus type 1 particles. J Virol 68:2065-2072

    Google Scholar 

  • 84. Mak J, Khorchid A, Cao Q, Huang Y, Lowy I, Parniak MA, Prasad VR, Wainberg MA, Kleiman L (1997) Effects of mutations in Pr160gag-pol upon tRNA(Lys3) and Pr160gag-plo incorporation into HIV-1. J Mol Biol 265:419-431

    CrossRef  Google Scholar 

  • 85. Mangeat B, Turelli P, Caron G, Friedli M, Perrin L, Trono D (2003) Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts. Nature 424:99-103

    Google Scholar 

  • 86. Mangeat B, Turelli P, Liao S, Trono D (2004) A single amino acid determinant governs the species-specific sensitivity of APOBEC3G to Vif action. J Biol Chem 279:14481-14483

    CrossRef  Google Scholar 

  • 87. Mansky LM (2000) In vivo analysis of human T-cell leukemia virus type 1 reverse transcription accuracy. J Virol 74:9525-9531

    CrossRef  Google Scholar 

  • 88. Mariani R, Chen D, Schrofelbauer B, Navarro F, Konig R, Bollman B, Munk C, Nymark-McMahon H, Landau NR (2003) Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114:21-31

    CrossRef  Google Scholar 

  • 89. Marin M, Rose KM, Kozak SL, Kabat D (2003) HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat Med 9:1398-1403

    CrossRef  Google Scholar 

  • 90. Marquet R (1998) Importance of Modified Nucleotides in Replication of Retroviruses, Plant Pararetroviruses, and Retrotransposons. In: Benne R (ed) Modification and Editing of RNA. ASM Press, Washington, D.C., pp 517-533

    Google Scholar 

  • 91. Marquet R, Isel C, Ehresmann C, Ehresmann B (1995) tRNAs as primer of reverse transcriptases. Biochimie 77:113-124

    CrossRef  Google Scholar 

  • 92. Mehle A, Strack B, Ancuta P, Zhang C, McPike M, Gabuzda D (2004) Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway. J Biol Chem 279:7792-7798

    CrossRef  Google Scholar 

  • 93. Miller JT, Khvorova A, Scaringe SA, Le Grice SF (2004) Synthetic tRNALys,3 as the replication primer for the HIV-1HXB2 and HIV-1Mal genomes. Nucleic Acids Res 32:4687-4695

    CrossRef  Google Scholar 

  • 94. Paillart JC, Shehu-Xhilaga M, Marquet R, Mak J (2004) Dimerization of retroviral RNA genomes: an inseparable pair. Nat Rev Microbiol 2:461-472

    CrossRef  Google Scholar 

  • 95. Pathak VK, Temin HM (1990) Broad spectrum of in vivo forward mutations, hypermutations, and mutational hotspots in a retroviral shuttle vector after a single replication cycle: substitutions, frameshifts, and hypermutations. Proc Natl Acad Sci USA 87:6019-6023

    Google Scholar 

  • 96. Perret V, Garcia A, Puglisi J, Grosjean H, Ebel JP, Florentz C, Giege R (1990) Conformation in solution of yeast tRNA(Asp) transcripts deprived of modified nucleotides. Biochimie 72:735-743

    CrossRef  Google Scholar 

  • 97. Priet S, Navarro JM, Gros N, Querat G, Sire J (2003a) Differential incorporation of uracil DNA glycosylase UNG2 into HIV-1, HIV-2, and SIV(MAC) viral particles. Virology 307:283-289

    CrossRef  Google Scholar 

  • 98. Priet S, Navarro JM, Gros N, Querat G, Sire J (2003b) Functional role of HIV-1 virion-associated uracil DNA glycosylase 2 in the correction of G:U mispairs to G:C pairs. J Biol Chem 278:4566-4571

    CrossRef  Google Scholar 

  • 99. Raba M, Limburg K, Burghagen M, Katze JR, Simsek M, Heckman JE, Rajbhandary UL, Gross HJ (1979) Nucleotide sequence of three isoaccepting lysine tRNAs from rabbit liver and SV40-transformed mouse fibroblasts. Eur J Biochem 97:305-318

    Google Scholar 

  • 100. Rein A, Henderson LE, Levin JG (1998) Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem Sci 23:297-301

    CrossRef  Google Scholar 

  • 101. Renda MJ, Rosenblatt JD, Klimatcheva E, Demeter LM, Bambara RA, Planelles V (2001) Mutation of the methylated tRNA(Lys)(3) residue A58 disrupts reverse transcription and inhibits replication of human immunodeficiency virus type 1. J Virol 75:9671-9678

    CrossRef  Google Scholar 

  • 102. Rigourd M, Goldschmidt V, Brule F, Morrow CD, Ehresmann B, Ehresmann C, Marquet R (2003) Structure-function relationships of the initiation complex of HIV-1 reverse transcription: the case of mutant viruses using tRNA(His) as primer. Nucleic Acids Res 31:5764-5775

    CrossRef  Google Scholar 

  • 103. Rosler C, Kock J, Malim MH, Blum HE, von Weizsacker F (2004) Comment on ”Inhibition of hepatitis B virus replication by APOBEC3G”. Science 305:1403; author reply 1403

    CrossRef  Google Scholar 

  • 104. Sallafranque-Andreola ML, Robert D, Barr PJ, Fournier M, Litvak S, Sarih-Cottin L, Tarrago-Litvak L (1989) Human immunodeficiency virus reverse transcriptase expressed in transformed yeast cells. Biochemical properties and interactions with bovine tRNALys. Eur J Biochem 184:367-374

    Google Scholar 

  • 105. Sampson JR, Uhlenbeck OC (1988) Biochemical and physical characterization of an unmodified yeast phenylalanine transfer RNA transcribed in vitro. Proc Natl Acad Sci USA 85:1033-1037

    Google Scholar 

  • 106. Sawyer SL, Emerman M, Malik HS (2004) Ancient adaptive evolution of the primate antiviral DNA-editing enzyme APOBEC3G. PLoS Biol 2:E275

    CrossRef  Google Scholar 

  • 107. Schrofelbauer B, Chen D, Landau NR (2004) A single amino acid of APOBEC3G controls its species-specific interaction with virion infectivity factor (Vif). Proc Natl Acad Sci USA 101:3927-3932

    CrossRef  Google Scholar 

  • 108. Sheehy AM, Gaddis NC, Choi JD, Malim MH (2002) Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418:646-650

    Google Scholar 

  • 109. Sheehy AM, Gaddis NC, Malim MH (2003) The antiretroviral enzyme APOBEC3G is degraded by the proteasome in response to HIV-1 Vif. Nat Med 9:1404-1407

    CrossRef  Google Scholar 

  • 110. Shindo K, Takaori-Kondo A, Kobayashi M, Abudu A, Fukunaga K, Uchiyama T (2003) The enzymatic activity of CEM15/Apobec-3G is essential for the regulation of the infectivity of HIV-1 virion but not a sole determinant of its antiviral activity. J Biol Chem 278:44412-44416

    CrossRef  Google Scholar 

  • 111. Simon JH, Gaddis NC, Fouchier RA, Malim MH (1998a) Evidence for a newly discovered cellular anti-HIV-1 phenotype. Nat Med 4:1397-1400

    CrossRef  Google Scholar 

  • 112. Simon JH, Miller DL, Fouchier RA, Soares MA, Peden KW, Malim MH (1998b) The regulation of primate immunodeficiency virus infectivity by Vif is cell species restricted: a role for Vif in determining virus host range and cross-species transmission. EMBO J 17:1259-1267

    CrossRef  Google Scholar 

  • 113. Simon JH, Southerling TE, Peterson JC, Meyer BE, Malim MH (1995) Complementation of vif-defective human immunodeficiency virus type 1 by primate, but not nonprimate, lentivirus vif genes. J Virol 69:4166-4172

    Google Scholar 

  • 114. Stopak K, de Noronha C, Yonemoto W, Greene WC (2003) HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability. Mol Cell 12:591-601

    CrossRef  Google Scholar 

  • 115. Strebel K, Daugherty D, Clouse K, Cohen D, Folks T, Martin MA (1987) The HIV ‘A’ (sor) gene product is essential for virus infectivity. Nature 328:728-730

    Google Scholar 

  • 116. Sundaram M, Durant PC, Davis DR (2000) Hypermodified nucleosides in the anticodon of tRNALys stabilize a canonical U-turn structure. Biochemistry 39:12575-12584

    CrossRef  Google Scholar 

  • 117. Suspene R, Sommer P, Henry M, Ferris S, Guetard D, Pochet S, Chester A, Navaratnam N, Wain-Hobson S, Vartanian JP (2004) APOBEC3G is a single-stranded DNA cytidine deaminase and functions independently of HIV reverse transcriptase. Nucleic Acids Res 32:2421-2429

    CrossRef  Google Scholar 

  • 118. Svarovskaia ES, Xu H, Mbisa JL, Barr R, Gorelick RJ, Ono A, Freed EO, Hu WS, Pathak VK (2004) Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs. J Biol Chem 279:35822-35828

    CrossRef  Google Scholar 

  • 119. Tisne C, Rigourd M, Marquet R, Ehresmann C, Dardel F (2000) 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 6:1403-1412

    CrossRef  Google Scholar 

  • 120. Tisne C, Roques BP, Dardel F (2004) The annealing mechanism of HIV-1 reverse transcription primer onto the viral genome. J Biol Chem 279:3588-3595

    CrossRef  Google Scholar 

  • 121. Turelli P, Mangeat B, Jost S, Vianin S, Trono D (2004a) Inhibition of hepatitis B virus replication by APOBEC3G. Science 303:1829

    CrossRef  Google Scholar 

  • 122. Turelli P, Vianin S, Trono D (2004b) The innate antiretroviral factor APOBEC3G does not affect human LINE-1 retrotransposition in a cell culture assay. J Biol Chem

    Google Scholar 

  • 123. Vartanian JP, Henry M, Wain-Hobson S (2002) Sustained G$to$A hypermutation during reverse transcription of an entire human immunodeficiency virus type 1 strain Vau group O genome. J Gen Virol 83:801-805

    Google Scholar 

  • 124. Vartanian JP, Meyerhans A, Sala M, Wain-Hobson S (1994) G$to$A hypermutation of the human immunodeficiency virus type 1 genome: evidence for dCTP pool imbalance during reverse transcription. Proc Natl Acad Sci USA 91:3092-3096

    Google Scholar 

  • 125. von Schwedler U, Song J, Aiken C, Trono D (1993) Vif is crucial for human immunodeficiency virus type 1 proviral DNA synthesis in infected cells. J Virol 67:4945-4955

    Google Scholar 

  • 126. Wain-Hobson S, Sonigo P, Guyader M, Gazit A, Henry M (1995) Erratic G$to$A hypermutation within a complete caprine arthritis-encephalitis virus (CAEV) provirus. Virology 209:297-303

    Google Scholar 

  • 127. Wakefield JK, Kang SM, Morrow CD (1996) Construction of a type 1 human immunodeficiency virus that maintains a primer binding site complementary to tRNA(His). J Virol 70:966-975

    Google Scholar 

  • 128. Wakefield JK, Wolf AG, Morrow CD (1995) 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). J Virol 69:6021-6029

    Google Scholar 

  • 129. Wei X, Gotte M, Wainberg MA (2000) Human immunodeficiency virus type-1 reverse transcription can be inhibited in vitro by oligonucleotides that target both natural and synthetic tRNA primers. Nucleic Acids Res 28:3065-3074

    CrossRef  Google Scholar 

  • 130. Weiss S, Konig B, Muller HJ, Seidel H, Goody RS (1992) Synthetic human tRNA(UUULys3) and natural bovine tRNA(UUULys3) interact with HIV-1 reverse transcriptase and serve as specific primers for retroviral cDNA synthesis. Gene 111:183-197

    CrossRef  Google Scholar 

  • 131. Weissenbach J, Grosjean H (1981) Effect of threonylcarbamoyl modification (t6A) in yeast tRNA Arg III on codon-anticodon and anticodon-anticodon interactions. A thermodynamic and kinetic evaluation. Eur J Biochem 116:207-213

    Google Scholar 

  • 132. Wiegand HL, Doehle BP, Bogerd HP, Cullen BR (2004) A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins. EMBO J 23:2451-2458

    CrossRef  Google Scholar 

  • 133. Willetts KE, Rey F, Agostini I, Navarro JM, Baudat Y, Vigne R, Sire J (1999) DNA repair enzyme uracil DNA glycosylase is specifically incorporated into human immunodeficiency virus type 1 viral particles through a Vpr-independent mechanism. J Virol 73:1682-1688

    Google Scholar 

  • 134. Wu T, Guo J, Bess J, Henderson LE, Levin JG (1999) Molecular requirements for human immunodeficiency virus type 1 plus-strand transfer: analysis in reconstituted and endogenous reverse transcription systems. J Virol 73:4794-4805

    Google Scholar 

  • 135. Xu H, Svarovskaia ES, Barr R, Zhang Y, Khan MA, Strebel K, Pathak VK (2004) A single amino acid substitution in human APOBEC3G antiretroviral enzyme confers resistance to HIV-1 virion infectivity factor-induced depletion. Proc Natl Acad Sci USA 101:5652-5657

    CrossRef  Google Scholar 

  • 136. Yu Q, Konig R, Pillai S, Chiles K, Kearney M, Palmer S, Richman D, Coffin JM, Landau NR (2004) Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome. Nat Struct Mol Biol 11:435-442

    Google Scholar 

  • 137. Yu X, Yu Y, Liu B, Luo K, Kong W, Mao P, Yu XF (2003) Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302:1056-1060

    CrossRef  Google Scholar 

  • 138. Zhang H, Yang B, Pomerantz RJ, Zhang C, Arunachalam SC, Gao L (2003) The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA. Nature 424:94-98

    Google Scholar 

  • 139. Zhang Z, Kang SM, LeBlanc A, Hajduk SL, Morrow CD (1996) 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 226:306-317

    Google Scholar 

  • 140. Zheng YH, Irwin D, Kurosu T, Tokunaga K, Sata T, Peterlin BM (2004) Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication. J Virol 78:6073-6076

    CrossRef  Google Scholar 

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Marquet, R., Dardel, F. Transfer RNA modifications and DNA editing in HIV-1 reverse transcription. In: Grosjean, H. (eds) Fine-Tuning of RNA Functions by Modification and Editing. Topics in Current Genetics, vol 12. Springer, Berlin, Heidelberg. https://doi.org/10.1007/b106366

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