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Research Paper

HIV-1 Pr55Gag binds genomic and spliced RNAs with different affinity and stoichiometry

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Pages 90-103 | Received 26 Aug 2016, Accepted 30 Oct 2016, Published online: 18 Dec 2016

References

  • Kuzembayeva M, Dilley K, Sardo L, Hu WS. Life of psi: how full-length HIV-1 RNAs become packaged genomes in the viral particles. Virology 2014; 454–5:362-70; PMID:24530126; http://dx.doi.org/10.1016/j.virol.2014.01.019
  • Berkowitz RD, Luban J, Goff SP. Specific binding of human immunodeficiency virus type 1 gag polyprotein and nucleocapsid protein to viral RNAs detected by RNA mobility shift assays. J Virol 1993; 67:7190-200; PMID:8230441
  • Clever J, Sassetti C, Parslow TG. RNA secondary structure and binding sites for gag gene products in the 5′ packaging signal of human immunodeficiency virus type 1. J Virol 1995; 69:2101-9; PMID:7884856
  • Paillart JC, Shehu-Xhilaga M, Marquet R, Mak J. Dimerization of retroviral RNA genomes: an inseparable pair. Nat Rev Microbiol 2004; 2:461-72; PMID:15152202; http://dx.doi.org/10.1038/nrmicro903
  • D'Souza V, Summers MF. How retroviruses select their genomes. Nat Rev Microbiol 2005; 3:643-55; PMID:16064056; http://dx.doi.org/10.1038/nrmicro1210
  • Lu K, Heng X, Summers MF. Structural determinants and mechanism of HIV-1 genome packaging. J Mol Biol 2011; 410:609-33; PMID:21762803; http://dx.doi.org/10.1016/j.jmb.2011.04.029
  • Rein A, Datta SA, Jones CP, Musier-Forsyth K. Diverse interactions of retroviral Gag proteins with RNAs. Trends Biochem Sci 2011; 36:373-80; PMID:21550256; http://dx.doi.org/10.1016/j.tibs.2011.04.001
  • Berkhout B. Structure and function of the human immunodeficiency virus leader RNA. Prog Nucleic Acid Res Mol Biol 1996; 54:1-34; PMID:8768071; http://dx.doi.org/10.1016/S0079-6603(08)60359-1
  • Russell RS, Hu J, Beriault V, Mouland AJ, Laughrea M, Kleiman L, Wainberg MA, Liang C. Sequences downstream of the 5′ splice donor site are required for both packaging and dimerization of human immunodeficiency virus type 1 RNA. J Virol 2003; 77:84-96; PMID:12477813; http://dx.doi.org/10.1128/JVI.77.1.84-96.2003
  • Lever A, Gottlinger H, Haseltine W, Sodroski J. Identification of a sequence required for efficient packaging of human immunodeficiency virus type 1 RNA into virions. J Virol 1989; 63:4085-7; PMID:2760989
  • Aldovini A, Young RA. Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus. J Virol 1990; 64:1920-6; PMID:2109098
  • Luban J, Goff SP. Mutational analysis of cis-acting packaging signals in human immunodeficiency virus type 1 RNA. J Virol 1994; 68:3784-93; PMID:8189516
  • McBride MS, Panganiban AT. Position dependence of functional hairpins important for human immunodeficiency virus type 1 RNA encapsidation in vivo. J Virol 1997; 71:2050-8; PMID:9032337
  • Abbink TE, Berkhout B. A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the Gag start codon. J Biol Chem 2003; 278:11601-11; PMID:12458192; http://dx.doi.org/10.1074/jbc.M210291200
  • Abbink TE, Ooms M, Haasnoot PC, Berkhout B. The HIV-1 leader RNA conformational switch regulates RNA dimerization but does not regulate mRNA translation. Biochemistry 2005; 44:9058-66; PMID:15966729; http://dx.doi.org/10.1021/bi0502588
  • Damgaard CK, Andersen ES, Knudsen B, Gorodkin J, Kjems J. RNA interactions in the 5′ region of the HIV-1 genome. J Mol Biol 2004; 336:369-79; PMID:14757051; http://dx.doi.org/10.1016/j.jmb.2003.12.010
  • Wilkinson KA, Gorelick RJ, Vasa SM, Guex N, Rein A, Mathews DH, Giddings MC, Weeks KM. High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol 2008; 6:e96; PMID:18447581; http://dx.doi.org/10.1371/journal.pbio.0060096
  • Heng X, Kharytonchyk S, Garcia EL, Lu K, Divakaruni SS, LaCotti C, Edme K, Telesnitsky A, Summers MF. Identification of a minimal region of the HIV-1 5′-leader required for RNA dimerization, NC binding, and packaging. J Mol Biol 2012; 417:224-39; PMID:22306406; http://dx.doi.org/10.1016/j.jmb.2012.01.033
  • Lu K, Heng X, Garyu L, Monti S, Garcia EL, Kharytonchyk S, Dorjsuren B, Kulandaivel G, Jones S, Hiremath A, et al. NMR detection of structures in the HIV-1 5′-leader RNA that regulate genome packaging. Science 2011; 334:242-5; PMID:21998393; http://dx.doi.org/10.1126/science.1210460
  • Clavel F, Orenstein JM. A mutant of human immunodeficiency virus with reduced RNA packaging and abnormal particle morphology. J Virol 1990; 64:5230-4; PMID:2204725
  • Berkhout B, van Wamel JL. Role of the DIS hairpin in replication of human immunodeficiency virus type 1. J Virol 1996; 70:6723-32; PMID:8794309
  • Paillart JC, Berthoux L, Ottmann M, Darlix JL, Marquet R, Ehresmann B, Ehresmann C. A dual role of the putative RNA dimerization initiation site of human immunodeficiency virus type 1 in genomic RNA packaging and proviral DNA synthesis. J Virol 1996; 70:8348-54; PMID:8970954
  • Harrison GP, Miele G, Hunter E, Lever AM. Functional analysis of the core human immunodeficiency virus type 1 packaging signal in a permissive cell line. J Virol 1998; 72:5886-96; PMID:9621050
  • Houzet L, Paillart JC, Smagulova F, Maurel S, Morichaud Z, Marquet R, Mougel M. HIV controls the selective packaging of genomic, spliced viral and cellular RNAs into virions through different mechanisms. Nucleic Acids Res 2007; 35:2695-704; PMID:17426127; http://dx.doi.org/10.1093/nar/gkm153
  • Skripkin E, Paillart JC, Marquet R, Ehresmann B, Ehresmann C. Identification of the primary site of the human immunodeficiency virus type 1 RNA dimerization in vitro. Proc Natl Acad Sci U S A 1994; 91:4945-9; PMID:8197162; http://dx.doi.org/10.1073/pnas.91.11.4945
  • Paillart JC, Marquet R, Skripkin E, Ehresmann B, Ehresmann C. Mutational analysis of the bipartite dimer linkage structure of human immunodeficiency virus type 1 genomic RNA. J Biol Chem 1994; 269:27486-93; PMID:7961663
  • Paillart JC, Skripkin E, Ehresmann B, Ehresmann C, Marquet R. 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 1996; 93:5572-7; PMID:8643617; http://dx.doi.org/10.1073/pnas.93.11.5572
  • Paillart JC, Skripkin E, Ehresmann B, Ehresmann C, Marquet R. The use of chemical modification interference and inverse PCR mutagenesis to identify the dimerization initiation site of HIV-1 genomic RNA. Pharm Acta Helv 1996; 71:21-8; PMID:8786995; http://dx.doi.org/10.1016/0031-6865(95)00048-8
  • Paillart JC, Marquet R, Skripkin E, Ehresmann C, Ehresmann B. Dimerization of retroviral genomic RNAs: structural and functional implications. Biochimie 1996; 78:639-53; PMID:8955907; http://dx.doi.org/10.1016/S0300-9084(96)80010-1
  • 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. J Biol Chem 2002; 277:19967-75; PMID:11896057; http://dx.doi.org/10.1074/jbc.M200950200
  • van Bel N, Das AT, Cornelissen M, Abbink TE, Berkhout B. A short sequence motif in the 5′ leader of the HIV-1 genome modulates extended RNA dimer formation and virus replication. J Biol Chem 2014; 289:35061-74; PMID:25368321; http://dx.doi.org/10.1074/jbc.M114.621425
  • Clever JL, Parslow TG. Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation. J Virol 1997; 71:3407-14; PMID:9094610
  • Laughrea M, Jette L, Mak J, Kleiman L, Liang C, Wainberg MA. Mutations in the kissing-loop hairpin of human immunodeficiency virus type 1 reduce viral infectivity as well as genomic RNA packaging and dimerization. J Virol 1997; 71:3397-406; PMID:9094609
  • Russell RS, Liang C, Wainberg MA. Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably? Retrovirology 2004; 1:23; PMID:15345057; http://dx.doi.org/10.1186/1742-4690-1-23
  • Chen J, Rahman SA, Nikolaitchik OA, Grunwald D, Sardo L, Burdick RC, Plisov S, Liang E, Tai S, Pathak VK, et al. HIV-1 RNA genome dimerizes on the plasma membrane in the presence of Gag protein. Proc Natl Acad Sci U S A 2016; 113:E201-8; PMID:26712001; http://dx.doi.org/10.1073/pnas.1518572113
  • Alfadhli A, McNett H, Tsagli S, Bachinger HP, Peyton DH, Barklis E. HIV-1 matrix protein binding to RNA. J Mol Biol 2011; 410:653-66; PMID:21762806; http://dx.doi.org/10.1016/j.jmb.2011.04.063
  • Ooms M, Huthoff H, Russell R, Liang C, Berkhout B. A riboswitch regulates RNA dimerization and packaging in human immunodeficiency virus type 1 virions. J Virol 2004; 78:10814-9; PMID:15367648; http://dx.doi.org/10.1128/JVI.78.19.10814-10819.2004
  • Aktar SJ, Vivet-Boudou V, Ali LM, Jabeen A, Kalloush RM, Richer D, Mustafa F, Marquet R, Rizvi TA. Structural basis of genomic RNA (gRNA) dimerization and packaging determinants of mouse mammary tumor virus (MMTV). Retrovirology 2014; 11:96; PMID:25394412; http://dx.doi.org/10.1186/s12977-014-0096-6
  • Helga-Maria C, Hammarskjold ML, Rekosh D. An intact TAR element and cytoplasmic localization are necessary for efficient packaging of human immunodeficiency virus type 1 genomic RNA. J Virol 1999; 73:4127-35; PMID:10196309
  • Didierlaurent L, Racine PJ, Houzet L, Chamontin C, Berkhout B, Mougel M. Role of HIV-1 RNA and protein determinants for the selective packaging of spliced and unspliced viral RNA and host U6 and 7SL RNA in virus particles. Nucleic Acids Res 2011; 39:8915-27; PMID:21791531; http://dx.doi.org/10.1093/nar/gkr577
  • Russell RS, Hu J, Laughrea M, Wainberg MA, Liang C. Deficient dimerization of human immunodeficiency virus type 1 RNA caused by mutations of the u5 RNA sequences. Virology 2002; 303:152-63; PMID:12482667; http://dx.doi.org/10.1006/viro.2002.1592
  • Clever JL, Miranda D, Jr., Parslow TG. RNA structure and packaging signals in the 5′ leader region of the human immunodeficiency virus type 1 genome. J Virol 2002; 76:12381-7; PMID:12414982; http://dx.doi.org/10.1128/JVI.76.23.12381-12387.2002
  • Vrolijk MM, Ooms M, Harwig A, Das AT, Berkhout B. Destabilization of the TAR hairpin affects the structure and function of the HIV-1 leader RNA. Nucleic Acids Res 2008; 36:4352-63; PMID:18586822; http://dx.doi.org/10.1093/nar/gkn364
  • Das AT, Vrolijk MM, Harwig A, Berkhout B. Opening of the TAR hairpin in the HIV-1 genome causes aberrant RNA dimerization and packaging. Retrovirology 2012; 9:59; PMID:22828074; http://dx.doi.org/10.1186/1742-4690-9-59
  • Sinck L, Richer D, Howard J, Alexander M, Purcell DF, Marquet R, Paillart JC. In vitro dimerization of human immunodeficiency virus type 1 (HIV-1) spliced RNAs. RNA 2007; 13:2141-50; PMID:17925344; http://dx.doi.org/10.1261/rna.678307
  • Cimarelli A, Sandin S, Hoglund S, Luban J. Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA. J Virol 2000; 74:3046-57; PMID:10708419; http://dx.doi.org/10.1128/JVI.74.7.3046-3057.2000
  • Campbell S, Rein A. In vitro assembly properties of human immunodeficiency virus type 1 Gag protein lacking the p6 domain. J Virol 1999; 73:2270-9; PMID:9971810
  • Zhang Y, Qian H, Love Z, Barklis E. Analysis of the assembly function of the human immunodeficiency virus type 1 gag protein nucleocapsid domain. J Virol 1998; 72:1782-9; PMID:9499028
  • Dannull J, Surovoy A, Jung G, Moelling K. Specific binding of HIV-1 nucleocapsid protein to PSI RNA in vitro requires N-terminal zinc finger and flanking basic amino acid residues. EMBO J 1994; 13:1525-33; PMID:8156990
  • Geigenmuller U, Linial ML. Specific binding of human immunodeficiency virus type 1 (HIV-1) Gag-derived proteins to a 5′ HIV-1 genomic RNA sequence. J Virol 1996; 70:667-71; PMID:8523591
  • Webb JA, Jones CP, Parent LJ, Rouzina I, Musier-Forsyth K. Distinct binding interactions of HIV-1 Gag to Psi and non-Psi RNAs: implications for viral genomic RNA packaging. RNA 2013; 19:1078-88; PMID:23798665; http://dx.doi.org/10.1261/rna.038869.113
  • Amarasinghe GK, De Guzman RN, Turner RB, Summers MF. NMR structure of stem-loop SL2 of the HIV-1 psi RNA packaging signal reveals a novel A-U-A base-triple platform. J Mol Biol 2000; 299:145-56; PMID:10860728; http://dx.doi.org/10.1006/jmbi.2000.3710
  • Amarasinghe GK, Zhou J, Miskimon M, Chancellor KJ, McDonald JA, Matthews AG, Miller RR, Rouse MD, Summers MF. Stem-loop SL4 of the HIV-1 psi RNA packaging signal exhibits weak affinity for the nucleocapsid protein. structural studies and implications for genome recognition. J Mol Biol 2001; 314:961-70; PMID:11743714; http://dx.doi.org/10.1006/jmbi.2000.5182
  • Paoletti AC, Shubsda MF, Hudson BS, Borer PN. Affinities of the nucleocapsid protein for variants of SL3 RNA in HIV-1. Biochemistry 2002; 41:15423-8; PMID:12484783; http://dx.doi.org/10.1021/bi026307n
  • Shubsda MF, Paoletti AC, Hudson BS, Borer PN. Affinities of packaging domain loops in HIV-1 RNA for the nucleocapsid protein. Biochemistry 2002; 41:5276-82; PMID:11955077; http://dx.doi.org/10.1021/bi016045+
  • Athavale SS, Ouyang W, McPike MP, Hudson BS, Borer PN. Effects of the nature and concentration of salt on the interaction of the HIV-1 nucleocapsid protein with SL3 RNA. Biochemistry 2010; 49:3525-33; PMID:20359247; http://dx.doi.org/10.1021/bi901279e
  • Godet J, Boudier C, Humbert N, Ivanyi-Nagy R, Darlix JL, Mely Y. Comparative nucleic acid chaperone properties of the nucleocapsid protein NCp7 and Tat protein of HIV-1. Virus Res 2012; 169:349-60; PMID:22743066; http://dx.doi.org/10.1016/j.virusres.2012.06.021
  • Sleiman D, Goldschmidt V, Barraud P, Marquet R, Paillart JC, Tisne C. Initiation of HIV-1 reverse transcription and functional role of nucleocapsid-mediated tRNA/viral genome interactions. Virus Res 2012; 169:324-39; PMID:22721779; http://dx.doi.org/10.1016/j.virusres.2012.06.006
  • Muriaux D, De Rocquigny H, Roques BP, Paoletti J. NCp7 activates HIV-1Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. J Biol Chem 1996; 271:33686-92; PMID:8969239; http://dx.doi.org/10.1074/jbc.271.52.33686
  • Takahashi K, Baba S, Koyanagi Y, Yamamoto N, Takaku H, Kawai G. Two basic regions of NCp7 are sufficient for conformational conversion of HIV-1 dimerization initiation site from kissing-loop dimer to extended-duplex dimer. J Biol Chem 2001; 276:31274-8; PMID:11418609; http://dx.doi.org/10.1074/jbc.M104577200
  • Kafaie J, Song R, Abrahamyan L, Mouland AJ, Laughrea M. Mapping of nucleocapsid residues important for HIV-1 genomic RNA dimerization and packaging. Virology 2008; 375:592-610; PMID:18343475; http://dx.doi.org/10.1016/j.virol.2008.02.001
  • Jalalirad M, Laughrea M. Formation of immature and mature genomic RNA dimers in wild-type and protease-inactive HIV-1: differential roles of the Gag polyprotein, nucleocapsid proteins NCp15, NCp9, NCp7, and the dimerization initiation site. Virology 2010; 407:225-36; PMID:20828778; http://dx.doi.org/10.1016/j.virol.2010.08.013
  • Cruceanu M, Gorelick RJ, Musier-Forsyth K, Rouzina I, Williams MC. Rapid kinetics of protein-nucleic acid interaction is a major component of HIV-1 nucleocapsid protein's nucleic acid chaperone function. J Mol Biol 2006; 363:867-77; PMID:16997322; http://dx.doi.org/10.1016/j.jmb.2006.08.070
  • Wu T, Datta SA, Mitra M, Gorelick RJ, Rein A, Levin JG. Fundamental differences between the nucleic acid chaperone activities of HIV-1 nucleocapsid protein and Gag or Gag-derived proteins: biological implications. Virology 2010; 405:556-67; PMID:20655566; http://dx.doi.org/10.1016/j.virol.2010.06.042
  • Damgaard CK, 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 Res 1998; 26:3667-76; PMID:9685481; http://dx.doi.org/10.1093/nar/26.16.3667
  • Cruceanu M, Urbaneja MA, Hixson CV, Johnson DG, Datta SA, Fivash MJ, Stephen AG, Fisher RJ, Gorelick RJ, Casas-Finet JR, et al. Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins. Nucleic Acids Res 2006; 34:593-605; PMID:16449201; http://dx.doi.org/10.1093/nar/gkj458
  • Rein A. Nucleic acid chaperone activity of retroviral Gag proteins. RNA Biol 2010; 7:700-5; PMID:21045546; http://dx.doi.org/10.4161/rna.7.6.13685
  • Chukkapalli V, Oh SJ, Ono A. Opposing mechanisms involving RNA and lipids regulate HIV-1 Gag membrane binding through the highly basic region of the matrix domain. Proc Natl Acad Sci U S A 2010; 107:1600-5; PMID:20080620; http://dx.doi.org/10.1073/pnas.0908661107
  • Kutluay SB, Zang T, Blanco-Melo D, Powell C, Jannain D, Errando M, Bieniasz PD. Global changes in the RNA binding specificity of HIV-1 gag regulate virion genesis. Cell 2014; 159:1096-109; PMID:25416948; http://dx.doi.org/10.1016/j.cell.2014.09.057
  • Saad JS, Miller J, Tai J, Kim A, Ghanam RH, Summers MF. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. Proc Natl Acad Sci U S A 2006; 103:11364-9; PMID:16840558; http://dx.doi.org/10.1073/pnas.0602818103
  • Shkriabai N, Datta SA, Zhao Z, Hess S, Rein A, Kvaratskhelia M. Interactions of HIV-1 Gag with assembly cofactors. Biochemistry 2006; 45:4077-83; PMID:16566581; http://dx.doi.org/10.1021/bi052308e
  • Ott DE, Coren LV, Gagliardi TD. Redundant roles for nucleocapsid and matrix RNA-binding sequences in human immunodeficiency virus type 1 assembly. J Virol 2005; 79:13839-47; PMID:16254319; http://dx.doi.org/10.1128/JVI.79.22.13839-13847.2005
  • Levin JG, Guo J, Rouzina I, Musier-Forsyth K. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog Nucleic Acid Res Mol Biol 2005; 80:217-86; PMID:16164976; http://dx.doi.org/10.1016/S0079-6603(05)80006-6
  • Rye-McCurdy TD, Nadaraia-Hoke S, Gudleski-O'Regan N, Flanagan JM, Parent LJ, Musier-Forsyth K. Mechanistic differences between nucleic acid chaperone activities of the Gag proteins of Rous sarcoma virus and human immunodeficiency virus type 1 are attributed to the MA domain. J Virol 2014; 88:7852-61; PMID:24789780; http://dx.doi.org/10.1128/JVI.00736-14
  • Jones CP, Datta SA, Rein A, Rouzina I, Musier-Forsyth K. Matrix domain modulates HIV-1 Gag's nucleic acid chaperone activity via inositol phosphate binding. J Virol 2011; 85:1594-603; PMID:21123373; http://dx.doi.org/10.1128/JVI.01809-10
  • Munro JB, Nath A, Farber M, Datta SA, Rein A, Rhoades E, Mothes W. A conformational transition observed in single HIV-1 Gag molecules during in vitro assembly of virus-like particles. J Virol 2014; 88:3577-85; PMID:24403576; http://dx.doi.org/10.1128/JVI.03353-13
  • Datta SA, Heinrich F, Raghunandan S, Krueger S, Curtis JE, Rein A, Nanda H. HIV-1 Gag extension: conformational changes require simultaneous interaction with membrane and nucleic acid. J Mol Biol 2011; 406:205-14; PMID:21134384; http://dx.doi.org/10.1016/j.jmb.2010.11.051
  • Datta SA, Curtis JE, Ratcliff W, Clark PK, Crist RM, Lebowitz J, Krueger S, Rein A. Conformation of the HIV-1 Gag protein in solution. J Mol Biol 2007; 365:812-24; PMID:17097677; http://dx.doi.org/10.1016/j.jmb.2006.10.073
  • Kenyon JC, Prestwood LJ, Lever AM. A novel combined RNA-protein interaction analysis distinguishes HIV-1 Gag protein binding sites from structural change in the viral RNA leader. Sci Rep 2015; 5:14369; PMID:26449409; http://dx.doi.org/10.1038/srep14369
  • Datta SA, Zhao Z, Clark PK, Tarasov S, Alexandratos JN, Campbell SJ, Kvaratskhelia M, Lebowitz J, Rein A. Interactions between HIV-1 Gag molecules in solution: an inositol phosphate-mediated switch. J Mol Biol 2007; 365:799-811; PMID:17098251; http://dx.doi.org/10.1016/j.jmb.2006.10.072
  • Feng YX, Copeland TD, Henderson LE, Gorelick RJ, Bosche WJ, Levin JG, Rein A. HIV-1 nucleocapsid protein induces “maturation” of dimeric retroviral RNA in vitro. Proc Natl Acad Sci U S A 1996; 93:7577-81; PMID:8755517; http://dx.doi.org/10.1073/pnas.93.15.7577
  • Levin JG, Mitra M, Mascarenhas A, Musier-Forsyth K. Role of HIV-1 nucleocapsid protein in HIV-1 reverse transcription. RNA Biol 2010; 7:754-74; PMID:21160280; http://dx.doi.org/10.4161/rna.7.6.14115
  • Kempf N, Postupalenko V, Bora S, Didier P, Arntz Y, de Rocquigny H, Mely Y. The HIV-1 nucleocapsid protein recruits negatively charged lipids to ensure its optimal binding to lipid membranes. J Virol 2015; 89:1756-67; PMID:25410868; http://dx.doi.org/10.1128/JVI.02931-14
  • McKinstry WJ, Hijnen M, Tanwar HS, Sparrow LG, Nagarajan S, Pham ST, Mak J. Expression and purification of soluble recombinant full length HIV-1 Pr55(Gag) protein in Escherichia coli. Protein Expr Purif 2014; 100:10-8; PMID:24810910; http://dx.doi.org/10.1016/j.pep.2014.04.013
  • Abd El-Wahab EW, Smyth RP, Mailler E, Bernacchi S, Vivet-Boudou V, Hijnen M, Jossinet F, Mak J, Paillart JC, Marquet R. Specific recognition of the HIV-1 genomic RNA by the Gag precursor. Nat Commun 2014; 5:4304; PMID:24986025; http://dx.doi.org/10.1038/ncomms5304
  • Smyth RP, Despons L, Huili G, Bernacchi S, Hijnen M, Mak J, Jossinet F, Weixi L, Paillart JC, von Kleist M, et al. Mutational interference mapping experiment (MIME) for studying RNA structure and function. Nat Methods 2015; 106(45):19114-9; PMID:19861549; http://dx.doi.org/10.1038/ncomms5304
  • Jouvenet N, Simon SM, Bieniasz PD. Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles. Proc Natl Acad Sci U S A 2009; 106:19114-9; http://dx.doi.org/doi:10.1073/pnas.0907364106
  • Kutluay SB, Bieniasz PD. Analysis of the initiating events in HIV-1 particle assembly and genome packaging. PLoS Pathog 2010; 6:e1001200; PMID:21124996; http://dx.doi.org/10.1371/journal.ppat.1001200
  • Hendrix J, Baumgartel V, Schrimpf W, Ivanchenko S, Digman MA, Gratton E, Krausslich HG, Muller B, Lamb DC. Live-cell observation of cytosolic HIV-1 assembly onset reveals RNA-interacting Gag oligomers. J Cell Biol 2015; 210:629-46; PMID:26283800; http://dx.doi.org/10.1083/jcb.201504006
  • Chen Y, Barkley MD. Toward understanding tryptophan fluorescence in proteins. Biochemistry 1998; 37:9976-82; PMID:9665702; http://dx.doi.org/10.1021/bi980274n
  • Onafuwa-Nuga AA, Telesnitsky A, King SR. 7SL RNA, but not the 54-kd signal recognition particle protein, is an abundant component of both infectious HIV-1 and minimal virus-like particles. RNA 2006; 12:542-6; PMID:16489186; http://dx.doi.org/10.1261/rna.2306306
  • Keene SE, Telesnitsky A. cis-Acting determinants of 7SL RNA packaging by HIV-1. J Virol 2012; 86:7934-42; PMID:22593161; http://dx.doi.org/10.1128/JVI.00856-12
  • Mercenne G, Bernacchi S, Richer D, Bec G, Henriet S, Paillart JC, Marquet R. HIV-1 Vif binds to APOBEC3G mRNA and inhibits its translation. Nucleic Acids Res 2010; 38:633-46; PMID:19910370; http://dx.doi.org/10.1093/nar/gkp1009
  • Alexandrova J, Paulus C, Rudinger-Thirion J, Jossinet F, Frugier M. Elaborate uORF/IRES features control expression and localization of human glycyl-tRNA synthetase. RNA Biol 2015; 12:1301-13; PMID:26327585; http://dx.doi.org/10.1080/15476286.2015.1086866
  • Wurth L, Gribling-Burrer AS, Verheggen C, Leichter M, Takeuchi A, Baudrey S, Martin F, Krol A, Bertrand E, Allmang C. Hypermethylated-capped selenoprotein mRNAs in mammals. Nucleic Acids Res 2014; 42:8663-77; PMID:25013170; http://dx.doi.org/10.1093/nar/gku580
  • Martin F, Barends S, Jaeger S, Schaeffer L, Prongidi-Fix L, Eriani G. Cap-assisted internal initiation of translation of histone H4. Mol Cell 2011; 41:197-209; PMID:21255730; http://dx.doi.org/10.1016/j.molcel.2010.12.019
  • Martin F, Menetret JF, Simonetti A, Myasnikov AG, Vicens Q, Prongidi-Fix L, Natchiar SK, Klaholz BP, Eriani G. Ribosomal 18S rRNA base pairs with mRNA during eukaryotic translation initiation. Nat Commun 2016; 7:12622; PMID:27554013; http://dx.doi.org/10.1038/ncomms12622
  • Bewley MC, Reinhart L, Stake MS, Nadaraia-Hoke S, Parent LJ, Flanagan JM. A non-cleavable hexahistidine affinity tag at the carboxyl-terminus of the Pr55Gag polyprotein alters nucleic acid binding properties. Protein Expr Purif 2016; 130:137-145; PMID:27721079; http://dx.doi.org/10.1016/j.pep.2016.10.001
  • Majerfeld I, Puthenvedu D, Yarus M. RNA affinity for molecular L-histidine; genetic code origins. J Mol Evol 2005; 61:226-35; PMID:15999244; http://dx.doi.org/10.1007/s00239-004-0360-9
  • Jouvenet N, Bieniasz PD, Simon SM. Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 2008; 454:236-40; PMID:18500329; http://dx.doi.org/10.1038/nature06998
  • Liang C, Rong L, Laughrea M, Kleiman L, Wainberg MA. Compensatory point mutations in the human immunodeficiency virus type 1 Gag region that are distal from deletion mutations in the dimerization initiation site can restore viral replication. J Virol 1998; 72:6629-36; PMID:9658109
  • Liang C, Rong L, Quan Y, Laughrea M, Kleiman L, Wainberg MA. Mutations within four distinct gag proteins are required to restore replication of human immunodeficiency virus type 1 after deletion mutagenesis within the dimerization initiation site. J Virol 1999; 73:7014-20; PMID:10400801
  • Laughrea M, Shen N, Jette L, Wainberg MA. Variant effects of non-native kissing-loop hairpin palindromes on HIV replication and HIV RNA dimerization: role of stem-loop B in HIV replication and HIV RNA dimerization. Biochemistry 1999; 38:226-34; PMID:9890902; http://dx.doi.org/10.1021/bi981728j
  • Shen N, Jette L, Liang C, Wainberg MA, Laughrea M. Impact of human immunodeficiency virus type 1 RNA dimerization on viral infectivity and of stem-loop B on RNA dimerization and reverse transcription and dissociation of dimerization from packaging. J Virol 2000; 74:5729-35; PMID:10823883; http://dx.doi.org/10.1128/JVI.74.12.5729-5735.2000
  • Shen N, Jette L, Wainberg MA, Laughrea M. Role of stem B, loop B, and nucleotides next to the primer binding site and the kissing-loop domain in human immunodeficiency virus type 1 replication and genomic-RNA dimerization. J Virol 2001; 75:10543-9; PMID:11581429; http://dx.doi.org/10.1128/JVI.75.21.10543-10549.2001
  • Keane SC, Heng X, Lu K, Kharytonchyk S, Ramakrishnan V, Carter G, Barton S, Hosic A, Florwick A, Santos J, et al. RNA structure. Structure of the HIV-1 RNA packaging signal. Science 2015; 348:917-21; PMID:25999508; http://dx.doi.org/10.1126/science.aaa9266
  • Paillart JC, Skripkin E, Ehresmann B, Ehresmann C, Marquet R. In vitro evidence for a long range pseudoknot in the 5′-untranslated and matrix coding regions of HIV-1 genomic RNA. J Biol Chem 2002; 277:5995-6004; PMID:11744696; http://dx.doi.org/10.1074/jbc.M108972200
  • Sakuragi J, Ode H, Sakuragi S, Shioda T, Sato H. A proposal for a new HIV-1 DLS structural model. Nucleic Acids Res 2012; 40:5012-22; PMID:22328732; http://dx.doi.org/10.1093/nar/gks156
  • Lodmell JS, Paillart JC, Mignot D, Ehresmann B, Ehresmann C, Marquet R. Oligonucleotide-mediated inhibition of genomic RNA dimerization of HIV-1 strains MAL and LAI: a comparative analysis. Antisense Nucleic Acid Drug Dev 1998; 8:517-29; PMID:9918116; http://dx.doi.org/10.1089/oli.1.1998.8.517
  • Marquet R, Baudin F, Gabus C, Darlix JL, Mougel M, Ehresmann C, Ehresmann B. Dimerization of human immunodeficiency virus (type 1) RNA: stimulation by cations and possible mechanism. Nucleic Acids Res 1991; 19:2349-57; PMID:1645868; http://dx.doi.org/10.1093/nar/19.9.2349
  • Scatchard G. The attractions of proteins fo small molecules and ions. Ann NY Acad Sci 1949; 51:660-72; http://dx.doi.org/10.1111/j.1749-6632.1949.t00027297.x
  • Bernacchi S, Henriet S, Dumas P, Paillart JC, Marquet R. RNA and DNA binding properties of HIV-1 Vif protein: a fluorescence study. J Biol Chem 2007; 282:26361-8; PMID:17609216; http://dx.doi.org/10.1074/jbc.M703122200

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