3,290
Views
86
CrossRef citations to date
0
Altmetric
Review

Properties and functions of the nucleocapsid protein in virus assembly

&
Pages 744-753 | Published online: 01 Nov 2010

References

  • Baltimore D. RNA-dependent DNA polymerase in virions of RNA tumour viruses. Nature 1970; 226:1209 - 1211
  • Gilboa E, Mitra SW, Goff S, Baltimore D. A detailed model of reverse transcription and tests of crucial aspects. Cell 1979; 18:93 - 100
  • Coffin JM. Fields BN, Knipe DM, et al. Virology 1990; 2:New York Raven Press Ltd. 1437 - 500
  • Mougel M, Houzet L, Darlix JL. When is it time for reverse transcription to start and go?. Retrovirology 2009; 6:24
  • Temin HM, Mizutani S. RNA-dependent DNA polymerase in virions of Rous sarcoma virus. Nature 1970; 226:1211 - 1213
  • Mizutani S, Boettiger D, Temin HM. A DNAdependent DNA polymerase and a DNA endonuclease in virions of Rous sarcoma virus. Nature 1970; 228:424 - 427
  • Delelis O, Carayon K, Saib A, Deprez E, Mouscadet JF. Integrase and integration: biochemical activities of HIV-1 integrase. Retrovirology 2008; 5:114
  • Lewinski MK, Bushman FD. Retroviral DNA integration—mechanism and consequences. Adv Genet 2005; 55:147 - 181
  • Coffin J, Hughes S, Varmus H. Retroviruses 1997; Cold Spring Harbor, New York Cold Spring Harbor laboratory Press
  • Ganser-Pornillos BK, Yeager M, Sundquist WI. The structural biology of HIV assembly. Curr Opin Struct Biol 2008; 18:203 - 217
  • Mateu MG. The capsid protein of human immunodeficiency virus: intersubunit interactions during virus assembly. FEBS J 2009; 276:6098 - 6109
  • Pornillos O, Ganser-Pornillos BK, Kelly BN, Hua Y, Whitby FG, Stout CD, et al. X-ray structures of the hexameric building block of the HIV capsid. Cell 2009; 137:1282 - 1292
  • Vogt VM, Simon MN. Mass determination of rous sarcoma virus virions by scanning transmission electron microscopy. J Virol 1999; 73:7050 - 7055
  • Chen J, Nikolaitchik O, Singh J, Wright A, Bencsics CE, Coffin JM, et al. High efficiency of HIV-1 genomic RNA packaging and heterozygote formation revealed by single virion analysis. Proc Natl Acad Sci USA 2009; 106:13535 - 13540
  • Chertova E, Chertov O, Coren LV, Roser JD, Trubey CM, Bess JWJ, et al. Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J Virol 2006; 80:9039 - 9052
  • Darlix JL, Garrido JL, Morellet N, Mély Y, de Rocquigny H. Properties, functions and drug targeting of the multifunctional nucleocapsid protein of the human immunodeficiency virus. Adv Pharmacol 2007; 55:299 - 346
  • Darlix JL, Lapadat-Tapolsky M, de Rocquigny H, Roques BP. First glimpses at structure-function relationships of the nucleocapsid protein of retroviruses. J Mol Biol 1995; 254:523 - 537
  • Rein A, Henderson LE, Levin JG. Nucleic-acid-chaperone activity of retroviral nucleocapsid proteins: significance for viral replication. Trends Biochem Sci 1998; 23:297 - 301
  • Cimarelli A, Darlix JL. Assembling the human immunodeficiency virus type 1. Cell Mol Life Sci 2002; 59:1166 - 1184
  • Muriaux D, Darlix JL, Cimarelli A. Targeting the assembly of the human immunodeficiency virus type 1. Curr Pharm Des 2004; 10:3725 - 3739
  • Morellet N, de Rocquigny H, Mely Y, Jullian N, Déméné H, Ottmann M, et al. Conformational behaviour of the active and inactive forms of the nucleocapsid NCp7 of HIV-1 studied by 1H NMR. J Mol Biol 1994; 235:287 - 301
  • Morellet N, Jullian N, De Rocquigny H, Maigret B, Darlix JL, Roques BP. Determination of the structure of the nucleocapsid protein NCp7 from the human immunodeficiency virus type 1 by 1H NMR. EMBO J 1992; 11:3059 - 3065
  • Summers MF, Henderson LE, Chance MR, Bess JWJ, South TL, Blake PR, 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 Sci 1992; 1:563 - 574
  • Lee BM, De Guzman RN, Turner BG, Tjandra N, Summers MF. Dynamical behavior of the HIV-1 nucleocapsid protein. J Mol Biol 1998; 279:633 - 649
  • Mely Y, Jullian N, Morellet N, et al. Spatial proximity of the HIV-1 nucleocapsid protein zinc fingers investigated by time-resolved fluorescence and fluorescence resonance energy transfer. Biochemistry 1994; 33:12085 - 12091
  • Ramboarina S, Srividya N, Atkinson RA, et al. Effects of temperature on the dynamic behaviour of the HIV-1 nucleocapsid NCp7 and its DNA complex. J Mol Biol 2002; 316:611 - 627
  • Bourbigot S, Ramalanjaona N, Boudier C, et al. How the HIV-1 nucleocapsid protein binds and destabilises the (-) primer binding site during reverse transcription. J Mol Biol 2008; 383:1112 - 1128
  • Spriggs S, Garyu L, Connor R, Summers MF. Potential intra- and intermolecular interactions involving the unique-5′ region of the HIV-1 5′-UTR. Biochemistry 2008; 47:13064 - 13073
  • Amarasinghe GK, De Guzman RN, Turner RB, et al. NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the psi-RNA packaging signal. Implications for genome recognition. J Mol Biol 2000; 301:491 - 511
  • De Guzman RN, Wu ZR, Stalling CC, et al. Structure of the HIV-1 nucleocapsid protein bound to the SL3 psi-RNA recognition element. Science 1998; 279:384 - 388
  • Morellet N, Demene H, Teilleux V, et al. Structure of the complex between the HIV-1 nucleocapsid protein NCp7 and the single-stranded pentanucleotide d(ACG CC). J Mol Biol 1998; 283:419 - 434
  • Bombarda E, Ababou A, Vuilleumier C, et al. Time-resolved fluorescence investigation of the human immunodeficiency virus type 1 nucleocapsid protein: influence of the binding of nucleic acids. Biophys J 1999; 76:1561 - 1570
  • 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 - 1926
  • Demene H, Dong CZ, Ottmann M, et al. 1H NMR structure and biological studies of the His23→Cys mutant nucleocapsid protein of HIV-1 indicate that the conformation of the first zinc finger is critical for virus infectivity. Biochemistry 1994; 33:11707 - 11716
  • Dorfman T, Luban J, Goff SP, Haseltine WA, Gottlinger HG. Mapping of functionally important residues of a cysteine-histidine box in the human immunodeficiency virus type 1 nucleocapsid protein. J Virol 1993; 67:6159 - 6169
  • Gorelick RJ, Nigida SM Jr, Bess JW Jr, et al. Noninfectious human immunodeficiency virus type 1 mutants deficient in genomic RNA. J Virol 1990; 64:3207 - 3211
  • Ottmann M, Gabus C, Darlix JL. The central globular domain of the nucleocapsid protein of human immunodeficiency virus type 1 is critical for virion structure and infectivity. J Virol 1995; 69:1778 - 1784
  • Gorelick RJ, Gagliardi TD, Bosche WJ, et al. Strict conservation of the retroviral nucleocapsid protein zinc finger is strongly influenced by its role in viral infection processes: characterization of HIV-1 particles containing mutant nucleocapsid zinc-coordinating sequences. Virology 1999; 256:92 - 104
  • Tanchou V, Decimo D, Pechoux C, et al. Role of the N-terminal zinc finger of human immunodeficiency virus type 1 nucleocapsid protein in virus structure and replication. J Virol 1998; 72:4442 - 4447
  • Thomas JA, Gorelick RJ. Nucleocapsid protein function in early infection processes. Virus Res 2008; 134:39 - 63
  • Gabus C, Auxilien S, Péchoux C, Dormont D, Swietnicki W, Morillas M, et al. The prion protein has DNA strand transfer properties similar to retroviral nucleocapsid protein. J Mol Biol 2001; 307:1011 - 1021
  • Krishnamoorthy G, Roques B, Darlix JL, Mely Y. DNA condensation by the nucleocapsid protein of HIV-1: a mechanism ensuring DNA protection. Nucleic Acids Res 2003; 31:5425 - 5432
  • Lapadat-Tapolsky M, De Rocquigny H, Van Gent D, et al. Interactions between HIV-1 nucleocapsid protein and viral DNA may have important functions in the viral life cycle. Nucleic Acids Res 1993; 21:831 - 839
  • Muriaux D, Mirro J, Harvin D, Rein A. RNA is a structural element in retrovirus particles. Proc Natl Acad Sci USA 2001; 98:5246 - 5251
  • Mark-Danieli M, Laham N, Kenan-Eichler M, Castiel A, Melamed D, Landau M, et al. Single point mutations in the zinc finger motifs of the human immunodeficiency virus type 1 nucleocapsid alter RNA binding specificities of the gag protein and enhance packaging and infectivity. J Virol 2005; 79:7756 - 7767
  • 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 USA 2009; 106:19114 - 19119
  • Ivanyi-Nagy R, Davidovic L, Khandjian EW, Darlix JL. Disordered RNA chaperone proteins: from functions to diseases. Cell Mol Life Sci 2005; 62:1409 - 1417
  • Tompa P, Csermely P. The role of structural disorder in the function of RNA and protein chaperones. FASEB J 2004; 18:1169 - 1175
  • 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 - 286
  • Cristofari G, Darlix JL. The ubiquitous nature of RNA chaperone proteins. Prog Nucleic Acid Res Mol Biol 2002; 72:223 - 268
  • Cruceanu M, Urbaneja MA, Hixson CV, Johnson DG, Datta SA, Fivash MJ, et al. Nucleic acid binding and chaperone properties of HIV-1 Gag and nucleocapsid proteins. Nucleic Acids Res 2006; 34:593 - 605
  • Williams MC, Rouzina I, Wenner JR, Gorelick RJ, Musier-Forsyth K, Bloomfield VA. Mechanism for nucleic acid chaperone activity of HIV-1 nucleocapsid protein revealed by single molecule stretching. Proc Natl Acad Sci USA 2001; 98:6121 - 6126
  • Cruceanu M, Stephen AG, Beuning PJ, Gorelick RJ, Fisher RJ, Williams MC. Single DNA molecule stretching measures the activity of chemicals that target the HIV-1 nucleocapsid protein. Anal Biochem 2006; 358:159 - 170
  • Godet J, de Rocquigny H, Raja C, Glasser N, Ficheux D, Darlix JL, Mély Y. During the early phase of HIV-1 DNA synthesis, nucleocapsid protein directs hybridization of the TAR complementary sequences via the ends of their double-stranded stem. J Mol Biol 2006; 356:1180 - 1192
  • Ramalanjaona N, de Rocquigny H, Millet A, Ficheux D, Darlix JL, Mély Y. Investigating the mechanism of the nucleocapsid protein chaperoning of the second strand transfer during HIV-1 DNA synthesis. J Mol Biol 2007; 374:1041 - 1053
  • Beltz H, Azoulay J, Bernacchi S, Clamme JP, Ficheux D, Roques B, et al. Impact of the terminal bulges of HIV-1 cTAR DNA on its stability and the destabilizing activity of the nucleocapsid protein NCp7. J Mol Biol 2003; 328:95 - 108
  • de Rocquigny H, Shvadchak V, Avilov S, Dong CZ, Dietrich U, Darlix JL, Mély Y. Targeting the viral nucleocapsid protein in anti-HIV-1 therapy. Mini Rev Med Chem 2008; 8:24 - 35
  • Ivanyi-Nagy R, Darlix JL. Intrinsic Disorder In The Core Proteins Of Flaviviruses. Protein Pept Lett 2010; 5 10
  • Gabus C, Derrington E, Leblanc P, Chnaiderman J, Dormont D, Swietnicki W, et al. The prion protein has RNA binding and chaperoning properties characteristic of nucleocapsid protein NCP7 of HIV-1. J Biol Chem 2001; 276:19301 - 19309
  • Marylène Mougel, Andrea Cimarelli, Jean-Luc Darlix. Implications of the Nucleocapsid and the Microenvironment in Retroviral Reverse Transcription. Viruses 2010; 2:939 - 960
  • Demirov DG, Freed EO. Retrovirus budding. Virus Res 2004; 106:87 - 102
  • Klein KC, Reed JC, Lingappa JR. Intracellular destinies: degradation, targeting, assembly and endocytosis of HIV Gag. AIDS Rev 2007; 9:150 - 161
  • Chu H, Wang JJ, Spearman P. Human immunodeficiency virus type-1 Gag and host vesicular trafficking pathways. Curr Top Microbiol Immunol 2009; 339:67 - 84
  • Bieniasz PD. The cell biology of HIV-1 virion genesis. Cell Host Microbe 2009; 5:550 - 558
  • Ono A. HIV-1 Assembly at the Plasma Membrane: Gag Trafficking and Localization. Future Virol 2009; 4:241 - 257
  • Ganser-Pornillos BK, Yeager M, Sundquist WI. The structural biology of HIV assembly. Curr Opin Struct Biol 2008; 18:203 - 217
  • Briggs JA, Riches JD, Glass B, Bartonova V, Zanetti G, Kräusslich HG. Structure and assembly of immature HIV. Proc Natl Acad Sci USA 2009; 106:11090 - 11095
  • Morita E, Sundquist WI. Retrovirus budding. Annu Rev Cell Dev Biol 2004; 20:395 - 425
  • Usami Y, Popov S, Popova E, Inoue M, Weissenhorn W, Göttlinger HG. The ESCRT pathway and HIV-1 budding. Biochem Soc Trans 2009; 37:181 - 184
  • Yuan B, Campbell S, Bacharach E, Rein A, Goff SP. Infectivity of Moloney murine leukemia virus defective in late assembly events is restored by late assembly domains of other retroviruses. J Virol 2000; 74:7250 - 7260
  • Yuan B, Fassati A, Yueh A, Goff SP. Characterization of Moloney murine leukemia virus p12 mutants blocked during early events of infection. J Virol 2002; 76:10801 - 10810
  • Scheifele LZ, Kenney SP, Cairns TM, Craven RC, Parent LJ. Overlapping roles of the Rous sarcoma virus Gag p10 domain in nuclear export and virion core morphology. J Virol 2007; 81:10718 - 10728
  • Phillips JM, Murray PS, Murray D, Vogt VM. A molecular switch required for retrovirus assembly participates in the hexagonal immature lattice. EMBO J 2008; 27:1411 - 1420
  • Burniston MT, Cimarelli A, Colgan J, Curtis SP, Luban J. Human immunodeficiency virus type 1 Gag polyprotein multimerization requires the nucleocapsid domain and RNA and is promoted by the capsid-dimer interface and the basic region of matrix protein. J Virol 1999; 73:8527 - 8540
  • Cimarelli A, Sandin S, Höglund S, Luban J. Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA. J Virol 2000; 74:3046 - 3057
  • Muriaux D, Costes KS, Nagashima J, Mirro E, Cho S, Lockett SJ, Rein A. Role of murine leukemia virus nucleocapsid protein in virus assembly. J Virol 2004; 78:12378 - 12385
  • Lee EG, Linial ML. Basic residues of the retroviral nucleocapsid play different roles in gag-gag and Gag-Psi RNA interactions. J Virol 2004; 78:8486 - 8495
  • Bohmovα K, Hadravovα R, Stokrovα J, Tuma R, Ruml T, Pichovα I, Rumlovα M. Effect of dimerizing domains and basic residues on in vitro and in vivo assembly of Mason-Pfizer monkey virus and human immunodeficiency virus. J Virol 2010; 84:1977 - 1988
  • Wang SW, Aldovini A. RNA incorporation is critical for retroviral particle integrity after cell membrane assembly of Gag complexes. J Virol 2002; 76:11853 - 11865
  • Wang SW, Noonan K, Aldovini A. Nucleocapsid-RNA interactions are essential to structural stability but not to assembly of retroviruses. J Virol 2004; 78:716 - 723
  • Yovandich JL, Chertova EN, Kane BP, Gagliardi TD, Bess JW Jr, Sowder RC 2nd, et al. Alteration of zinc-binding residues of simian immunodeficiency virus p8(NC) results in subtle differences in gag processing and virion maturation associated with degradative loss of mutant NC. J Virol 2001; 75:115 - 124
  • Lee EG, Linial ML. Deletion of a Cys-His motif from the Alpharetrovirus nucleocapsid domain reveals late domain mutant-like budding defects. Virology 2006; 347:226 - 233
  • Grigorov B, Décimo D, Smagulova F, Mougel MD, Muriaux JL, Darlix JL. Intracellular localization of Gag is impaired by mutations in the nucleocapsid zinc fingers. Retrovirology 2007; 4:54
  • Hogue IB, Hoppe A, Ono A. Quantitative fluorescence resonance energy transfer microscopy analysis of the human immunodeficiency virus type 1 Gag-Gag interaction: relative contributions of the CA and NC domains and membrane binding. J Virol 2009; 83:7322 - 7336
  • Ott DE, Coren LV, Shatzer T. The nucleocapsid region of human immunodeficiency virus type 1 Gag assists in the coordination of assembly and Gag processing: role for RNA-Gag binding in the early stages of assembly. J Virol 2009; 83:7718 - 7727
  • Ono A, Waheed AA, Joshi A, Freed EO. Association of human immunodeficiency virus type 1 gag with membrane does not require highly basic sequences in the nucleocapsid: use of a novel Gag multimerization assay. J Virol 2005; 79:14131 - 14140
  • Popov S, Popova E, Inoue M, Göttlinger HG. Divergent Bro1 domains share the capacity to bind human immunodeficiency virus type 1 nucleocapsid and to enhance virus-like particle production. J Virol 2009; 83:7185 - 7193
  • Dussupt V, Javid MP, Abou-Jaoudé G, Jadwin JA, de La Cruz J, Nagashima K, Bouamr F. The nucleocapsid region of HIV-1 Gag cooperates with the PTAP and LYPXnL late domains to recruit the cellular machinery necessary for viral budding. PLoS Pathog 2009; 5:1000339
  • Popova E, Popov S, Göttlinger HG. Human immunodeficiency virus type 1 nucleocapsid p1 confers ESCRT pathway dependence. J Virol 2010; 84:6590 - 6597
  • Resh MD. Intracellular trafficking of HIV-1 Gag: how Gag interacts with cell membranes and makes viral particles. AIDS Rev 2005; 7:84 - 91
  • 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 USA 2006; 103:11364 - 11369
  • Alfadhli A, Dhenub TC, Still A, Barklis E. Analysis of human immunodeficiency virus type 1 Gag dimerization-induced assembly. J Virol 2005; 79:14498 - 14506
  • 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 - 13847
  • Sherer NM, Swanson CM, Papaioannou S, Malim MH. Matrix mediates the functional link between human immunodeficiency virus type 1 RNA nuclear export elements and the assembly competency of Gag in murine cells. J Virol 2009; 83:8525 - 8535
  • Jin J, Sturgeon T, Weisz OA, Mothes W, Montelaro RC. HIV-1 matrix dependent membrane targeting is regulated by Gag mRNA trafficking. PLoS One 2009; 4:655196
  • Muriaux D, Mirro J, Nagashima K, Harvin D, Rein A. Murine leukemia virus nucleocapsid mutant particles lacking viral RNA encapsidate ribosomes. J Virol 2002; 76:11405 - 11413
  • Poon DT, Chertova EN, Ott DE. Human immunodeficiency virus type 1 preferentially encapsidates genomic RNAs that encode Pr55(Gag): functional linkage between translation and RNA packaging. Virology 2002; 293:368 - 378
  • Balvay L, Lopez Lastra M, Sargueil B, Darlix JL, Ohlmann T. Translational control of retroviruses. Nat Rev Microbiol 2007; 5:128 - 140
  • Ono A, Ablan SD, Lockett SJ, Nagashima K, Freed EO. Phosphatidylinositol(4,5)bisphosphate regulates HIV-1 Gag targeting to the plasma membrane. Proc Natl Acad Sci USA 2004; 101:14889 - 14894
  • Freed EO. HIV-1 Gag: flipped out for PI(4,5)P. Proc Natl Acad Sci USA 2006; 103:11101 - 11102
  • Hamard-Péron E, Juillard F, Saad JS, Roy C, Roingeard P, Summers MF, et al. Targeting of MuLV Gag to the plasma membrane is mediated by PIP2/PS and a poly-basic region in the Matrix. J Virol 2010; 84:503 - 515
  • 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 USA 2010; 107:1600 - 1605
  • Camus G, Segura-Morales C, Molle D, Lopez-Vergès S, Begon-Pescia C, Cazevieille C, et al. The clathrin adaptor complex AP-1 binds HIV-1 and MLV Gag and facilitates their budding. Mol Biol Cell 2007; 18:3193 - 3203
  • Batonick M, Favre M, Boge M, Spearman P, Höning S, Thali M. Interaction of HIV-1 Gag with the clathrin-associated adaptor AP-2. Virology 2005; 342:190 - 200
  • Dong X, Li H, Derdowski A, Ding L, Burnett A, Chen X, et al. AP-3 directs the intracellular trafficking of HIV-1 Gag and plays a key role in particle assembly. Cell 2005; 120:663 - 674
  • Joshi A, Garg H, Nagashima K, Bonifacino JS, Freed EO. GGA and Arf proteins modulate retrovirus assembly and release. Mol Cell 2008; 30:227 - 238
  • Grigorov B, Arcanger F, Roingeard P, Darlix JL, Muriaux D. Assembly of infectious HIV-1 in human epithelial and lymphoblastic cell lines. J Mol Biol 2006; 359:848 - 862
  • Molle D, Segura-Morales C, Camus G, Berlioz-Torrent C, Kjems J, Basyuk E, Bertrand E. Endosomal trafficking of HIV-1 gag and genomic RNAs regulates viral egress. J Biol Chem 2009; 284:19727 - 19743
  • Lehmann M, Milev MP, Abrahamyan L, Yao XJ, Pante N, Mouland AJ. Intracellular transport of human immunodeficiency virus type 1 genomic RNA and viral production are dependent on dynein motor function and late endosome positioning. J Biol Chem 2009; 284:14572 - 14585
  • Tritel M, Resh M. Kinetic analysis of HIV-1 assembly reveals the presence of sequential intermediates. J Virol 2000; 74:5845 - 5855
  • Lingappa JR, Thielen BK. Assembly of immature HIV-1 capsids using a cell-free system. Methods Mol Biol 2009; 485:185 - 195
  • Cochrane AW, McNally MT, Mouland AJ. The retrovirus RNA trafficking granule: from birth to maturity. Retrovirology 2006; 3:18
  • Mouland AJ, Mercier J, Luo M, Bernier L, DesGroseillers L, Cohen EA. The double-stranded RNA-binding protein Staufen is incorporated in human immunodeficiency virus type 1: evidence for a role in genomic RNA encapsidation. J Virol 2000; 74:5441 - 5451
  • Chatel-Chaix L, Clément JF, Martel C, Bériault V, Gatignol A, DesGroseillers L, Mouland AJ. Identification of Staufen in the human immunodeficiency virus type 1 Gag ribonucleoprotein complex and a role in generating infectious viral particles. Mol Cell Biol 2004; 24:2637 - 2648
  • Chatel-Chaix L, Boulay K, Mouland AJ, Desgroseillers L. The host protein Staufen1 interacts with the Pr55Gag zinc fingers and regulates HIV-1 assembly via its N-terminus. Retrovirology 2008; 5:41
  • Ueno T, Tokunaga K, Sawa H, Maeda M, Chiba J, Kojima A, et al. Nucleolin and the packaging signal, psi, promote the budding of human immunodeficiency virus type-1 (HIV-1). Microbiol Immunol 2004; 48:111 - 118
  • Bacharach E, Gonsky J, Alin K, Orlova M, Goff SP. The carboxy-terminal fragment of nucleolin interacts with the nucleocapsid domain of retroviral gag proteins and inhibits virion assembly. J Virol 2000; 74:11027 - 11039
  • Zimmerman C, Klein KC, Kiser PK, Singh AR, Firestein BL, Riba SC, Lingappa JR. Identification of a host protein essential for assembly of immature HIV-1 capsids. Nature 2002; 415:88 - 92
  • Lingappa J, Dooher J, Newman M, Kiser P, Klein K. Basic residues in the nucleocapsid domain of Gag are required for interaction of HIV-1 gag with ABCE1 (HP68), a cellular protein important for HIV-1 capsid assembly. J Biol Chem 2006; 281:3773 - 3784
  • Dooher JE, Schneider BL, Reed JC, Lingappa JR. Host ABCE1 is at plasma membrane HIV assembly sites and its dissociation from Gag is linked to subsequent events of virus production. Traffic 2007; 8:195 - 211
  • Ott DE. Cellular proteins detected in HIV-1. Rev Med Virol 2008; 18:159 - 175
  • Lehmann MJ, Sherer NM, Marks CB, Pypaert M, Mothes W. Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J Cell Biol 2005; 170:317 - 325
  • Chen C, Weisz OA, Stolz DB, Watkins SC, Montelaro RC. Differential effects of actin cytoskeleton dynamics on equine infectious anemia virus particle production. J Virol 2004; 78:882 - 891
  • Chen C, Jin J, Rubin M, Huang L, Sturgeon T, Weixel KM, et al. Association of gag multimers with filamentous actin during equine infectious anemia virus assembly. Curr HIV Res 2007; 5:315 - 323
  • Gladnikoff M, Shimoni E, Gov NS, Rousso I. Retroviral assembly and budding occur through an actin-driven mechanism. Biophys J 2009; 97:2419 - 2428
  • Leblanc P, Baas D, Darlix JL. Analysis of the interactions between HIV-1 and the cellular prion protein in a human cell line. J Mol Biol 2004; 337:1035 - 1051
  • Lötscher M, Recher M, Lang KS, Navarini A, Hunziker L, Santimaria R, et al. Induced prion protein controls immune-activated retroviruses in the mouse spleen. PLoS One 2007; 2:1158
  • Perugi F, Muriaux D, Ramirez BC, Chabani S, Decroly E, Darlix JL, et al. Human Discs Large is a new negative regulator of HIV-1 infectivity. Mol Biol Cell 2009; 20:498 - 508
  • Leung K, Kim JO, Ganesh L, Kabat J, Schwartz O, Nabel GJ. HIV-1 assembly: viral glycoproteins segregate quantally to lipid rafts that associate individually with HIV-1 capsids and virions. Cell Host Microbe 2008; 3:285 - 292
  • Henriet S, Mercenne G, Bernacchi S, Paillart JC, Marquet R. Tumultuous relationship between the human immunodeficiency virus type 1 viral infectivity factor (Vif) and the human APOBEC-3G and APOBEC-3F restriction factors. Microbiol Mol Biol Rev 2009; 73:211 - 232
  • Zennou V, Perez-Caballero D, Gottlinger H, Bieniasz PD. APOBEC3G incorporation into human immunodeficiency virus type 1 particles. J Virol 2004; 78:12058 - 12061
  • Burnett A, Spearman P. APOBEC3G multimers are recruited to the plasma membrane for packaging into human immunodeficiency virus type 1 virus-like particles in an RNA-dependent process requiring the NC basic linker. J Virol 2007; 81:5000 - 5013
  • Simon JH, Carpenter EA, Fouchier RA, Malim MH. Vif and the p55Gag polyprotein of human immunodeficiency virus type 1 are present in colocalizing membrane-free cytoplasmic complexes. J Virol 1999; 73:2667 - 2674
  • Zhang H, Pomerantz RJ, Dornadula G, Sun Y. Human immunodeficiency virus type 1 Vif protein is an integral component of an mRNP complex of viral RNA and could be involved in the viral RNA folding and packaging process. J Virol 2000; 74:8252 - 8826
  • Henriet S, Richer D, Bernacchi S, Decroly E, Vigne R, Ehresmann B, et al. Cooperative and specific binding of Vif to the 5′ region of HIV-1 genomic RNA. J Mol Biol 2005; 354:55 - 72
  • Neil SJ, Zang T, Bieniasz PD. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 2008; 451:425 - 430
  • Neil SJ, Eastman SW, Jouvenet N, Bieniasz PD. HIV-1 Vpu promotes release and prevents endocytosis of nascent retrovirus particles from the plasma membrane. PLoS Pathog 2006; 2:39
  • Perez-Caballero D, Zang T, Ebrahimi A, McNatt MW, Gregory DA, Johnson MC, Bieniasz PD. Tetherin inhibits HIV-1 release by directly tethering virions to cells. Cell 2009; 139:499 - 511
  • Perlman M, Resh MD. Identification of an intracellular trafficking and assembly pathway for HIV-1 Gag. Traffic 2006; 7:731 - 745
  • Ehrlich LS, Medina GN, Khan MB, Powell MD, Mikoshiba K, Carter CA. Activation of the inositol (1,4,5)-triphosphate calcium gate receptor is required for HIV-1 Gag release. J Virol 2010; 84:6438 - 6451
  • 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 - 9066
  • Brasey A, Lopez-Lastra M, Ohlmann T, Beerens N, Berkhout B, Darlix JL, Sonenberg N. The leader of human immunodeficiency virus type 1 genomic RNA harbors an internal ribosome entry segment that is active during the G2/M phase of the cell cycle. J Virol 2003; 77:3939 - 3949
  • Larson DR, Johnson MC, Webb WW, Vogt VM. Visualization of retrovirus budding with correlated light and electron microscopy. Proc Natl Acad Sci USA 2005; 102:15453 - 15458
  • Jouvenet N, Bieniasz PD, Simon SM. Imaging the biogenesis of individual HIV-1 virions in live cells. Nature 2008; 454:236 - 240
  • Ivanchenko S, Godinez WJ, Lampe M, Kräusslich HG, Eils R, Rohr K, et al. Dynamics of HIV-1 assembly and release. PLoS Pathog 2009; 5:1000652
  • Gousset K, Ablan SD, Coren LV, Ono A, Soheilian F, Nagashima K, et al. Real-time visualization of HIV-1 Gag trafficking in infected macrophages. PLoS Pathog 2008; 4:1000015
  • Milev MP, Brown CM, Mouland AJ. Live cell visualization of the interactions between HIV-1 Gag and the cellular RNA-binding protein Staufen1. Retrovirology 2010; 7:41
  • Jin J, Sherer NM, Heidecker G, Derse D, Mothes W. Assembly of the murine leukemia virus is directed towards sites of cell-cell contact. PLoS Biol 2009; 7:1000163