1932

Abstract

Human immunodeficiency virus type 1 (HIV-1) particle assembly requires several protein:RNA interactions that vary widely in their character, from specific recognition of highly conserved and structured viral RNA elements to less specific interactions with variable RNA sequences. Genetic, biochemical, biophysical, and structural studies have illuminated how virion morphogenesis is accompanied by dramatic changes in the interactions among the protein and RNA virion components. The 5′ leader RNA element drives RNA recognition by Gag upon initiation of HIV-1 assembly and can assume variable conformations that influence translation, dimerization, and Gag recognition. As Gag multimerizes on the plasma membrane, forming immature particles, its RNA binding specificity transiently changes, enabling recognition of the A-rich composition of the viral genome. Initiation of assembly may also be regulated by occlusion of the membrane binding surface of Gag by tRNA. Finally, recent work has suggested that RNA interactions with viral enzymes may activate and ensure the accuracy of virion maturation.

Keyword(s): assemblyGagHIV-1packagingRNA
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2018-09-29
2024-04-26
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Literature Cited

  1. 1.  Gomez CY, Hope TJ 2006. Mobility of human immunodeficiency virus type 1 Pr55Gag in living cells. J. Virol. 80:8796–806
    [Google Scholar]
  2. 2.  Kutluay SB, Bieniasz PD 2010. Analysis of the initiating events in HIV-1 particle assembly and genome packaging. PLOS Pathog 6:e1001200
    [Google Scholar]
  3. 3.  Hendrix J, Baumgartel V, Schrimpf W, Ivanchenko S, Digman MA et al. 2015. Live-cell observation of cytosolic HIV-1 assembly onset reveals RNA-interacting Gag oligomers. J. Cell Biol. 210:629–46
    [Google Scholar]
  4. 4.  Jouvenet N, Simon SM, Bieniasz PD 2009. Imaging the interaction of HIV-1 genomes and Gag during assembly of individual viral particles. PNAS 106:19114–19
    [Google Scholar]
  5. 5.  Huang M, Orenstein JM, Martin MA, Freed EO 1995. p6Gag is required for particle production from full-length human immunodeficiency virus type 1 molecular clones expressing protease. J. Virol. 69:6810–18
    [Google Scholar]
  6. 6.  Schubert U, Ott DE, Chertova EN, Welker R, Tessmer U et al. 2000. Proteasome inhibition interferes with Gag polyprotein processing, release, and maturation of HIV-1 and HIV-2. PNAS 97:13057–62
    [Google Scholar]
  7. 7.  Jouvenet N, Neil SJ, Bess C, Johnson MC, Virgen CA et al. 2006. Plasma membrane is the site of productive HIV-1 particle assembly. PLOS Biol 4:e435
    [Google Scholar]
  8. 8.  Jouvenet N, Bieniasz PD, Simon SM 2008. Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 454:236–40
    [Google Scholar]
  9. 9.  Chen J, Grunwald D, Sardo L, Galli A, Plisov S et al. 2014. Cytoplasmic HIV-1 RNA is mainly transported by diffusion in the presence or absence of Gag protein. PNAS 111:E5205–13
    [Google Scholar]
  10. 10.  Sardo L, Hatch SC, Chen J, Nikolaitchik O, Burdick RC et al. 2015. Dynamics of HIV-1 RNA near the plasma membrane during virus assembly. J. Virol. 89:10832–40
    [Google Scholar]
  11. 11.  Ivanchenko S, Godinez WJ, Lampe M, Krausslich HG, Eils R et al. 2009. Dynamics of HIV-1 assembly and release. PLOS Pathog 5:e1000652
    [Google Scholar]
  12. 12.  Chen J, Rahman SA, Nikolaitchik OA, Grunwald D, Sardo L et al. 2016. HIV-1 RNA genome dimerizes on the plasma membrane in the presence of Gag protein. PNAS 113:E201–8
    [Google Scholar]
  13. 13.  Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH et al. 2001. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107:55–65
    [Google Scholar]
  14. 14.  Jouvenet N, Zhadina M, Bieniasz PD, Simon SM 2011. Dynamics of ESCRT protein recruitment during retroviral assembly. Nat. Cell Biol. 13:394–401
    [Google Scholar]
  15. 15.  Baumgartel V, Ivanchenko S, Dupont A, Sergeev M, Wiseman PW et al. 2011. Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component. Nat. Cell Biol. 13:469–74
    [Google Scholar]
  16. 16.  Sundquist WI, Krausslich HG 2012. HIV-1 assembly, budding, and maturation. Cold Spring Harb. Perspect. Med. 2:a006924
    [Google Scholar]
  17. 17.  Berkowitz R, Fisher J, Goff SP 1996. RNA packaging. Morphog. Matur. Retrovir. 214:177–218
    [Google Scholar]
  18. 18.  Levin JG, Guo J, Rouzina I, Musier-Forsyth K 2005. Nucleic acid chaperone activity of HIV-1 nucleocapsid protein: critical role in reverse transcription and molecular mechanism. Prog. Nucleic Acid Res. Mol. Biol. 80:217–86
    [Google Scholar]
  19. 19.  Johnson SF, Telesnitsky A 2010. Retroviral RNA dimerization and packaging: the what, how, when, where, and why. PLOS Pathog 6:e1001007
    [Google Scholar]
  20. 20.  Fu W, Gorelick RJ, Rein A 1994. Characterization of human immunodeficiency virus type 1 dimeric RNA from wild-type and protease-defective virions. J. Virol. 68:5013–18
    [Google Scholar]
  21. 21.  Keene SE, King SR, Telesnitsky A 2010. 7SL RNA is retained in HIV-1 minimal virus-like particles as an S-domain fragment. J. Virol. 84:9070–77
    [Google Scholar]
  22. 22.  Chen J, Nikolaitchik O, Singh J, Wright A, Bencsics CE et al. 2009. High efficiency of HIV-1 genomic RNA packaging and heterozygote formation revealed by single virion analysis. PNAS 106:13535–40
    [Google Scholar]
  23. 23.  Kulpa DA, Moran JV 2006. cis-preferential LINE-1 reverse transcriptase activity in ribonucleoprotein particles. Nat. Struct. Mol. Biol. 13:655–60
    [Google Scholar]
  24. 24.  Kaye JF, Lever AM 1999. Human immunodeficiency virus types 1 and 2 differ in the predominant mechanism used for selection of genomic RNA for encapsidation. J. Virol. 73:3023–31
    [Google Scholar]
  25. 25.  Heng X, Kharytonchyk S, Garcia EL, Lu K, Divakaruni SS et al. 2012. Identification of a minimal region of the HIV-1 5′-leader required for RNA dimerization, NC binding, and packaging. J. Mol. Biol. 417:224–39
    [Google Scholar]
  26. 26.  Naldini L, Blomer U, Gallay P, Ory D, Mulligan R et al. 1996. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272:263–67
    [Google Scholar]
  27. 27.  Muhlebach MD, Schule S, Gerlach N, Schweizer M, Buchholz CJ et al. 2010. Gammaretroviral and lentiviral vectors for gene delivery. Retroviruses: Molecular Biology, Genomics and Pathogenesis R Kurth, N Bannert 347–70 Poole, UK: Caister Acad.
    [Google Scholar]
  28. 28.  Aldovini A, Young RA 1990. Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus. J. Virol. 64:1920–26
    [Google Scholar]
  29. 29.  Gorelick RJ, Nigida SM Jr., Bess JW Jr., Arthur LO, Henderson LE, Rein A 1990. Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. J. Virol. 64:3207–11
    [Google Scholar]
  30. 30.  Lever A, Gottlinger H, Haseltine W, Sodroski J 1989. Identification of a sequence required for efficient packaging of human immunodeficiency virus type 1 RNA into virions. J. Virol. 63:4085–87
    [Google Scholar]
  31. 31.  Mann R, Mulligan RC, Baltimore D 1983. Construction of a retrovirus packaging mutant and its use to produce helper-free defective retrovirus. Cell 33:153–59
    [Google Scholar]
  32. 32.  Adam MA, Miller AD 1988. Identification of a signal in a murine retrovirus that is sufficient for packaging of nonretroviral RNA into virions. J. Virol. 62:3802–6
    [Google Scholar]
  33. 33.  Clever J, Sassetti C, Parslow TG 1995. RNA secondary structure and binding sites for gag gene products in the 5′ packaging signal of human immunodeficiency virus type 1. J. Virol. 69:2101–9
    [Google Scholar]
  34. 34.  Abd El-Wahab EW, Smyth RP, Mailler E, Bernacchi S, Vivet-Boudou V et al. 2014. Specific recognition of the HIV-1 genomic RNA by the Gag precursor. Nat. Commun. 5:4304
    [Google Scholar]
  35. 35.  Pak AJ, Grime JMA, Sengupta P, Chen AK, Durumeric AEP et al. 2017. Immature HIV-1 lattice assembly dynamics are regulated by scaffolding from nucleic acid and the plasma membrane. PNAS 114:E10056–65
    [Google Scholar]
  36. 36.  Carlson LA, Bai Y, Keane SC, Doudna JA, Hurley JH 2016. Reconstitution of selective HIV-1 RNA packaging in vitro by membrane-bound Gag assemblies. eLife 5:e14663
    [Google Scholar]
  37. 37.  Kung HJ, Bailey JM, Davidson N, Vogt PK, Nicolson MO, McAllister RM 1974. Electron-microscope studies of tumor-virus RNA. Cold Spring Harb. Symp. Quant. Biol. 39:827–34
    [Google Scholar]
  38. 38.  Murti KG, Bondurant M, Tereba A 1981. Secondary structural features in the 70S RNAs of Moloney murine leukemia and Rous sarcoma viruses as observed by electron microscopy. J. Virol. 37:411–19
    [Google Scholar]
  39. 39.  Darlix JL, de Rocquigny H, Mauffret O, Mely Y 2014. Retrospective on the all-in-one retroviral nucleocapsid protein. Virus Res 193:2–15
    [Google Scholar]
  40. 40.  Darlix JL, Spahr PF 1982. Binding sites of viral protein P19 onto Rous sarcoma virus RNA and possible controls of viral functions. J. Mol. Biol. 160:147–61
    [Google Scholar]
  41. 41.  Vuilleumier C, Bombarda E, Morellet N, Gerard D, Roques BP, Mely Y 1999. Nucleic acid sequence discrimination by the HIV-1 nucleocapsid protein NCp7: a fluorescence study. Biochemistry 38:16816–25
    [Google Scholar]
  42. 42.  You JC, McHenry CS 1993. HIV nucleocapsid protein. Expression in Escherichia coli, purification, and characterization. J. Biol. Chem. 268:16519–27
    [Google Scholar]
  43. 43.  Rein A, Datta SA, Jones CP, Musier-Forsyth K 2011. Diverse interactions of retroviral Gag proteins with RNAs. Trends Biochem. Sci. 36:373–80
    [Google Scholar]
  44. 44.  Butler PJ 1984. The current picture of the structure and assembly of tobacco mosaic virus. J. Gen. Virol. 65:Pt. 2253–79
    [Google Scholar]
  45. 45.  Gross I, Hohenberg H, Wilk T, Wiegers K, Grattinger M et al. 2000. A conformational switch controlling HIV-1 morphogenesis. EMBO J 19:103–13
    [Google Scholar]
  46. 46.  Telesnitsky A, Wolin SL 2016. The host RNAs in retroviral particles. Viruses 8:E235
    [Google Scholar]
  47. 47.  Rulli SJ Jr., Hibbert CS, Mirro J, Pederson T, Biswal S, Rein A 2007. Selective and nonselective packaging of cellular RNAs in retrovirus particles. J. Virol. 81:6623–31
    [Google Scholar]
  48. 48.  Ueno T, Tokunaga K, Sawa H, Maeda M, Chiba J et al. 2004. Nucleolin and the packaging signal, ψ, promote the budding of human immunodeficiency virus type-1 (HIV-1). Microbiol. Immunol. 48:111–18
    [Google Scholar]
  49. 49.  Dilley KA, Nikolaitchik OA, Galli A, Burdick RC, Levine L et al. 2017. Interactions between HIV-1 Gag and viral RNA genome enhance virion assembly. J. Virol. 91:e02319–16
    [Google Scholar]
  50. 50.  Tanwar HS, Khoo KK, Garvey M, Waddington L, Leis A et al. 2017. The thermodynamics of Pr55Gag-RNA interaction regulate the assembly of HIV. PLOS Pathog 13:e1006221
    [Google Scholar]
  51. 51.  Wagner JM, Zadrozny KK, Chrustowicz J, Purdy MD, Yeager M et al. 2016. Crystal structure of an HIV assembly and maturation switch. eLife 5:e17063
    [Google Scholar]
  52. 52.  Berkhout B 1996. Structure and function of the human immunodeficiency virus leader RNA. Prog. Nucleic Acid Res. Mol. Biol. 54:1–34
    [Google Scholar]
  53. 53.  Blissenbach M, Grewe B, Hoffmann B, Brandt S, Uberla K 2010. Nuclear RNA export and packaging functions of HIV-1 Rev revisited. J. Virol. 84:6598–604
    [Google Scholar]
  54. 54.  Russell RS, Liang C, Wainberg MA 2004. Is HIV-1 RNA dimerization a prerequisite for packaging? Yes, no, probably?. Retrovirology 1:23
    [Google Scholar]
  55. 55.  Sakuragi J, Shioda T, Panganiban AT 2001. Duplication of the primary encapsidation and dimer linkage region of human immunodeficiency virus type 1 RNA results in the appearance of monomeric RNA in virions. J. Virol. 75:2557–65
    [Google Scholar]
  56. 56.  Shin NH, Hartigan-O'Connor D, Pfeiffer JK, Telesnitsky A 2000. Replication of lengthened Moloney murine leukemia virus genomes is impaired at multiple stages. J. Virol. 74:2694–702
    [Google Scholar]
  57. 57.  Lu K, Heng X, Garyu L, Monti S, Garcia EL et al. 2011. NMR detection of structures in the HIV-1 5′-leader RNA that regulate genome packaging. Science 334:242–45
    [Google Scholar]
  58. 58.  Keane SC, Heng X, Lu K, Kharytonchyk S, Ramakrishnan V et al. 2015. Structure of the HIV-1 RNA packaging signal. Science 348:917–21
    [Google Scholar]
  59. 59.  Onafuwa-Nuga A, Telesnitsky A 2009. The remarkable frequency of human immunodeficiency virus type 1 genetic recombination. Microbiol. Mol. Biol. Rev. 73:451–80
    [Google Scholar]
  60. 60.  King SR, Duggal NK, Ndongmo CB, Pacut C, Telesnitsky A 2008. Pseudodiploid genome organization AIDS full-length human immunodeficiency virus type 1 DNA synthesis. J. Virol. 82:2376–84
    [Google Scholar]
  61. 61.  Lu K, Heng X, Summers MF 2011. Structural determinants and mechanism of HIV-1 genome packaging. J. Mol. Biol. 410:609–33
    [Google Scholar]
  62. 62.  Andersen ES, Contera SA, Knudsen B, Damgaard CK, Besenbacher F, Kjems J 2004. Role of the trans-activation response element in dimerization of HIV-1 RNA. J. Biol. Chem. 279:22243–49
    [Google Scholar]
  63. 63.  Helga-Maria C, Hammarskjold ML, Rekosh D 1999. An intact TAR element and cytoplasmic localization are necessary for efficient packaging of human immunodeficiency virus type 1 genomic RNA. J. Virol. 73:4127–35
    [Google Scholar]
  64. 64.  Russell RS, Hu J, Laughrea M, Wainberg MA, Liang C 2002. Deficient dimerization of human immunodeficiency virus type 1 RNA caused by mutations of the u5 RNA sequences. Virology 303:152–63
    [Google Scholar]
  65. 65.  Clever JL, Miranda D Jr., Parslow TG 2002. RNA structure and packaging signals in the 5′ leader region of the human immunodeficiency virus type 1 genome. J. Virol. 76:12381–87
    [Google Scholar]
  66. 66.  Liu Y, Nikolaitchik OA, Rahman SA, Chen J, Pathak VK, Hu WS 2017. HIV-1 sequence necessary and sufficient to package non-viral RNAs into HIV-1 particles. J. Mol. Biol. 429:2542–55
    [Google Scholar]
  67. 67.  McBride MS, Schwartz MD, Panganiban AT 1997. Efficient encapsidation of human immunodeficiency virus type 1 vectors and further characterization of cis elements required for encapsidation. J. Virol. 71:4544–54
    [Google Scholar]
  68. 68.  Lever AM 2007. HIV-1 RNA packaging. Adv. Pharmacol. 55:1–32
    [Google Scholar]
  69. 69.  Das AT, Klaver B, Klasens BI, van Wamel JL, Berkhout B 1997. A conserved hairpin motif in the R-U5 region of the human immunodeficiency virus type 1 RNA genome is essential for replication. J. Virol. 71:2346–56
    [Google Scholar]
  70. 70.  Vrolijk MM, Ooms M, Harwig A, Das AT, Berkhout B 2008. Destabilization of the TAR hairpin affects the structure and function of the HIV-1 leader RNA. Nucleic Acids Res 36:4352–63
    [Google Scholar]
  71. 71.  Laham-Karam N, Bacharach E 2007. Transduction of human immunodeficiency virus type 1 vectors lacking encapsidation and dimerization signals. J. Virol. 81:10687–98
    [Google Scholar]
  72. 72.  Keane SC, Summers MF 2016. NMR studies of the structure and function of the HIV-1 5′-leader. Viruses 8:338
    [Google Scholar]
  73. 73.  Keane SC, Van V, Frank HM, Sciandra CA, McCowin S et al. 2016. NMR detection of intermolecular interaction sites in the dimeric 5′-leader of the HIV-1 genome. PNAS 113:13033–38
    [Google Scholar]
  74. 74.  Abbink TE, Berkhout B 2003. A novel long distance base-pairing interaction in human immunodeficiency virus type 1 RNA occludes the Gag start codon. J. Biol. Chem. 278:11601–11
    [Google Scholar]
  75. 75.  Kutluay SB, Zang T, Blanco-Melo D, Powell C, Jannain D et al. 2014. Global changes in the RNA binding specificity of HIV-1 Gag regulate virion genesis. Cell 159:1096–109
    [Google Scholar]
  76. 76.  Kharytonchyk S, Monti S, Smaldino PJ, Van V, Bolden NC et al. 2016. Transcriptional start site heterogeneity modulates the structure and function of the HIV-1 genome. PNAS 113:13378–83
    [Google Scholar]
  77. 77.  Muesing MA, Smith DH, Cabradilla CD, Benton CV, Lasky LA, Capon DJ 1985. Nucleic acid structure and expression of the human AIDS/lymphadenopathy retrovirus. Nature 313:450–58
    [Google Scholar]
  78. 78.  Starcich B, Ratner L, Josephs SF, Okamoto T, Gallo RC, Wong-Staal F 1985. Characterization of long terminal repeat sequences of HTLV-III. Science 227:538–40
    [Google Scholar]
  79. 79.  Menees TM, Muller B, Krausslich HG 2007. The major 5′ end of HIV type 1 RNA corresponds to G456. AIDS Res. Hum. Retrovir. 23:1042–48
    [Google Scholar]
  80. 80.  Masuda T, Sato Y, Huang YL, Koi S, Takahata T et al. 2015. Fate of HIV-1 cDNA intermediates during reverse transcription is dictated by transcription initiation site of virus genomic RNA. Sci. Rep. 5:17680
    [Google Scholar]
  81. 81.  Fontana J, Jurado KA, Cheng N, Ly NL, Fuchs JR et al. 2015. Distribution and redistribution of HIV-1 Nucleocapsid protein in immature, mature, and integrase-inhibited virions: a role for integrase in maturation. J. Virol. 89:9765–80
    [Google Scholar]
  82. 82.  Clever JL, Parslow TG 1997. Mutant human immunodeficiency virus type 1 genomes with defects in RNA dimerization or encapsidation. J. Virol. 71:3407–14
    [Google Scholar]
  83. 83.  McBride MS, Panganiban AT 1997. Position dependence of functional hairpins important for human immunodeficiency virus type 1 RNA encapsidation in vivo. J. Virol. 71:2050–58
    [Google Scholar]
  84. 84.  Houzet L, Paillart JC, Smagulova F, Maurel S, Morichaud Z et al. 2007. HIV controls the selective packaging of genomic, spliced viral and cellular RNAs into virions through different mechanisms. Nucleic Acids Res 35:2695–704
    [Google Scholar]
  85. 85.  Berkowitz RD, Hammarskjold ML, Helga-Maria C, Rekosh D, Goff SP 1995. 5′ regions of HIV-1 RNAs are not sufficient for encapsidation: implications for the HIV-1 packaging signal. Virology 212:718–23
    [Google Scholar]
  86. 86.  Chamanian M, Purzycka KJ, Wille PT, Ha JS, McDonald D et al. 2013. A cis-acting element in retroviral genomic RNA links Gag-Pol ribosomal frameshifting to selective viral RNA encapsidation. Cell Host Microbe 13:181–92
    [Google Scholar]
  87. 87.  Richardson JH, Child LA, Lever AM 1993. Packaging of human immunodeficiency virus type 1 RNA requires cis-acting sequences outside the 5′ leader region. J. Virol. 67:3997–4005
    [Google Scholar]
  88. 88.  Kaye JF, Richardson JH, Lever AM 1995. cis-acting sequences involved in human immunodeficiency virus type 1 RNA packaging. J. Virol. 69:6588–92
    [Google Scholar]
  89. 89.  Didierlaurent L, Racine PJ, Houzet L, Chamontin C, Berkhout B, Mougel M 2011. 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 39:8915–27
    [Google Scholar]
  90. 90.  Grewe B, Ehrhardt K, Hoffmann B, Blissenbach M, Brandt S, Uberla K 2012. The HIV-1 Rev protein enhances encapsidation of unspliced and spliced, RRE-containing lentiviral vector RNA. PLOS ONE 7:e48688
    [Google Scholar]
  91. 91.  Nikolaitchik OA, Hu WS 2014. Deciphering the role of the Gag-Pol ribosomal frameshift signal in HIV-1 RNA genome packaging. J. Virol. 88:4040–46
    [Google Scholar]
  92. 92.  South TL, Summers MF 1993. Zinc- and sequence-dependent binding to nucleic acids by the N-terminal zinc finger of the HIV-1 nucleocapsid protein: NMR structure of the complex with the Psi-site analog, dACGCC. Protein Sci 2:3–19
    [Google Scholar]
  93. 93.  De Guzman RN, Wu ZR, Stalling CC, Pappalardo L, Borer PN, Summers MF 1998. Structure of the HIV-1 nucleocapsid protein bound to the SL3 Ψ-RNA recognition element. Science 279:384–88
    [Google Scholar]
  94. 94.  van der Kuyl AC, Berkhout B 2012. The biased nucleotide composition of the HIV genome: a constant factor in a highly variable virus. Retrovirology 9:92
    [Google Scholar]
  95. 95.  Patel N, Dykeman EC, Coutts RH, Lomonossoff GP, Rowlands DJ et al. 2015. Revealing the density of encoded functions in a viral RNA. PNAS 112:2227–32
    [Google Scholar]
  96. 96.  Rolfsson O, Middleton S, Manfield IW, White SJ, Fan B et al. 2016. Direct evidence for packaging signal-mediated assembly of bacteriophage MS2. J. Mol. Biol. 428:431–48
    [Google Scholar]
  97. 97.  Stockley PG, White SJ, Dykeman E, Manfield I, Rolfsson O et al. 2016. Bacteriophage MS2 genomic RNA encodes an assembly instruction manual for its capsid. Bacteriophage 6:e1157666
    [Google Scholar]
  98. 98.  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 418:646–50
    [Google Scholar]
  99. 99.  Takata MA, Goncalves-Carneiro D, Zang TM, Soll SJ, York A et al. 2017. CG dinucleotide suppression enables antiviral defence targeting non-self RNA. Nature 550:124–27
    [Google Scholar]
  100. 100.  van Hemert F, van der Kuyl AC, Berkhout B 2016. Impact of the biased nucleotide composition of viral RNA genomes on RNA structure and codon usage. J. Gen. Virol. 97:2608–19
    [Google Scholar]
  101. 101.  Zhou W, Parent LJ, Wills JW, Resh MD 1994. Identification of a membrane-binding domain within the amino-terminal region of human immunodeficiency virus type 1 Gag protein which interacts with acidic phospholipids. J. Virol. 68:2556–69
    [Google Scholar]
  102. 102.  Chukkapalli V, Oh SJ, Ono A 2010. Opposing mechanisms involving RNA and lipids regulate HIV-1 Gag membrane binding through the highly basic region of the matrix domain. PNAS 107:1600–5
    [Google Scholar]
  103. 103.  Dick RA, Kamynina E, Vogt VM 2013. Effect of multimerization on membrane association of Rous sarcoma virus and HIV-1 matrix domain proteins. J. Virol. 87:13598–608
    [Google Scholar]
  104. 104.  Barros M, Heinrich F, Datta SA, Rein A, Karageorgos I et al. 2016. Membrane binding of HIV-1 matrix protein: dependence on bilayer composition and protein lipidation. J. Virol. 90:4544–55
    [Google Scholar]
  105. 105.  Ono A, Ablan SD, Lockett SJ, Nagashima K, Freed EO 2004. Phosphatidylinositol (4,5) bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. PNAS 101:14889–94
    [Google Scholar]
  106. 106.  Cimarelli A, Luban J 1999. Translation elongation factor 1-alpha interacts specifically with the human immunodeficiency virus type 1 Gag polyprotein. J. Virol. 73:5388–401
    [Google Scholar]
  107. 107.  Ott DE, Coren LV, Gagliardi TD 2005. Redundant roles for nucleocapsid and matrix RNA-binding sequences in human immunodeficiency virus type 1 assembly. J. Virol. 79:13839–47
    [Google Scholar]
  108. 108.  Alfadhli A, Still A, Barklis E 2009. Analysis of human immunodeficiency virus type 1 matrix binding to membranes and nucleic acids. J. Virol. 83:12196–203
    [Google Scholar]
  109. 109.  Ramalingam D, Duclair S, Datta SA, Ellington A, Rein A, Prasad VR 2011. RNA aptamers directed to human immunodeficiency virus type 1 Gag polyprotein bind to the matrix and nucleocapsid domains and inhibit virus production. J. Virol. 85:305–14
    [Google Scholar]
  110. 110.  Chukkapalli V, Inlora J, Todd GC, Ono A 2013. Evidence in support of RNA-mediated inhibition of phosphatidylserine-dependent HIV-1 Gag membrane binding in cells. J. Virol. 87:7155–59
    [Google Scholar]
  111. 111.  Datta SA, Curtis JE, Ratcliff W, Clark PK, Crist RM et al. 2007. Conformation of the HIV-1 Gag protein in solution. J. Mol. Biol. 365:812–24
    [Google Scholar]
  112. 112.  Zhou W, Resh MD 1996. Differential membrane binding of the human immunodeficiency virus type 1 matrix protein. J. Virol. 70:8540–48
    [Google Scholar]
  113. 113.  Tang C, Loeliger E, Luncsford P, Kinde I, Beckett D, Summers MF 2004. Entropic switch regulates myristate exposure in the HIV-1 matrix protein. PNAS 101:517–22
    [Google Scholar]
  114. 114.  Saad JS, Miller J, Tai J, Kim A, Ghanam RH, Summers MF 2006. Structural basis for targeting HIV-1 Gag proteins to the plasma membrane for virus assembly. PNAS 103:11364–69
    [Google Scholar]
  115. 115.  Paillart JC, Gottlinger HG 1999. Opposing effects of human immunodeficiency virus type 1 matrix mutations support a myristyl switch model of Gag membrane targeting. J. Virol. 73:2604–12
    [Google Scholar]
  116. 116.  Reil H, Bukovsky AA, Gelderblom HR, Gottlinger HG 1998. Efficient HIV-1 replication can occur in the absence of the viral matrix protein. EMBO J 17:2699–708
    [Google Scholar]
  117. 117.  Perez-Caballero D, Hatziioannou T, Martin-Serrano J, Bieniasz PD 2004. Human immunodeficiency virus type 1 matrix inhibits and confers cooperativity on Gag precursor-membrane interactions. J. Virol. 78:9560–63
    [Google Scholar]
  118. 118.  Hatziioannou T, Martin-Serrano J, Zang T, Bieniasz PD 2005. Matrix-induced inhibition of membrane binding contributes to human immunodeficiency virus type 1 particle assembly defects in murine cells. J. Virol. 79:15586–89
    [Google Scholar]
  119. 119.  Holmes M, Zhang F, Bieniasz PD 2015. Single-cell and single-cycle analysis of HIV-1 replication. PLOS Pathog 11:e1004961
    [Google Scholar]
  120. 120.  Neil SJ, Zang T, Bieniasz PD 2008. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451:425–30
    [Google Scholar]
  121. 121.  Rosa A, Chande A, Ziglio S, De Sanctis V, Bertorelli R et al. 2015. HIV-1 Nef promotes infection by excluding SERINC5 from virion incorporation. Nature 526:212–17
    [Google Scholar]
  122. 122.  Usami Y, Wu Y, Gottlinger HG 2015. SERINC3 and SERINC5 restrict HIV-1 infectivity and are counteracted by Nef. Nature 526:218–23
    [Google Scholar]
  123. 123.  Mirambeau G, Lyonnais S, Coulaud D, Hameau L, Lafosse S et al. 2007. HIV-1 protease and reverse transcriptase control the architecture of their nucleocapsid partner. PLOS ONE 2:e669
    [Google Scholar]
  124. 124.  Sheng N, Erickson-Viitanen S 1994. Cleavage of p15 protein in vitro by human immunodeficiency virus type 1 protease is RNA dependent. J. Virol. 68:6207–14
    [Google Scholar]
  125. 125.  Sheng N, Pettit SC, Tritch RJ, Ozturk DH, Rayner MM et al. 1997. Determinants of the human immunodeficiency virus type 1 p15NC-RNA interaction that affect enhanced cleavage by the viral protease. J. Virol. 71:5723–32
    [Google Scholar]
  126. 126.  Potempa M, Nalivaika E, Ragland D, Lee SK, Schiffer CA, Swanstrom R 2015. A direct interaction with RNA dramatically enhances the catalytic activity of the HIV-1 protease in vitro. J. Mol. Biol. 427:2360–78
    [Google Scholar]
  127. 127.  Engelman A 1999. In vivo analysis of retroviral integrase structure and function. Adv. Virus Res. 52:411–26
    [Google Scholar]
  128. 128.  Desimmie BA, Schrijvers R, Demeulemeester J, Borrenberghs D, Weydert C et al. 2013. LEDGINs inhibit late stage HIV-1 replication by modulating integrase multimerization in the virions. Retrovirology 10:57
    [Google Scholar]
  129. 129.  Jurado KA, Wang H, Slaughter A, Feng L, Kessl JJ et al. 2013. Allosteric integrase inhibitor potency is determined through the inhibition of HIV-1 particle maturation. PNAS 110:8690–95
    [Google Scholar]
  130. 130.  Madison MK, Lawson DQ, Elliott J, Ozanturk AN, Koneru PC et al. 2017. Allosteric HIV-1 integrase inhibitors lead to premature degradation of the viral RNA genome and integrase in target cells. J. Virol. 91:e00821–17
    [Google Scholar]
  131. 131.  Kessl JJ, Kutluay SB, Townsend D, Rebensburg S, Slaughter A et al. 2016. HIV-1 integrase binds the viral RNA genome and is essential during virion morphogenesis. Cell 166:1257–68
    [Google Scholar]
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