Retroviral mRNA nuclear export elements regulate protein function and virion assembly

EMBO Journal

Volumn 23, Issue 13, 2004, Pages 2632-2640

  Swanson, Chad M ^a,b   Puffer, Bridget A ^a   Ahmad, K Muneer ^b   Doms, Robert W ^a   Malim, Michael H ^a,b,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c GUY S HOSPITAL   (United Kingdom)

Author keywords

HIV 1 assembly; mRNA export; Species barrier

Indexed keywords

GAG PROTEIN; MESSENGER RNA; POL PROTEIN; PROTEIN; VIRUS RNA;

ANIMAL CELL; ARTICLE; CELL STRAIN 3T3; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; RNA METABOLISM; VIRUS ASSEMBLY; VIRUS CAPSID; VIRUS CELL INTERACTION;

3T3 CELLS; ANIMALS; CELL NUCLEUS; CYTOPLASM; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; FLUORESCENT DYES; GENE PRODUCTS, REV; GENES, GAG; GENES, POL; HELA CELLS; HUMANS; INDOLES; MICE; MICROSCOPY, CONFOCAL; PROTEINS; RETROVIRIDAE; RHODAMINES; RNA, MESSENGER; RNA, VIRAL; VACCINIA; VIRION;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; MURINAE; RODENTIA;

EID: 3342929537     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600270     Document Type: Article

References (73)

1. Atchison RE, Gosling J, Monteclaro FS, Franci C, Digilio L, Charo IF, Goldsmith MA (1996) Multiple extracellular elements of CCR5 and HIV-1 entry: dissociation from response to chemokines. Science 274: 1924-1926
2. Basyuk E, Galli T, Mougel M, Blanchard JM, Sitbon M, Bertrand E (2003) Retroviral genomic RNAs are transported to the plasma membrane by endosomal vesicles. Dev Cell 5: 161-174
3. Bieniasz PD, Cullen BR (2000) Multiple blocks to human immunodeficiency virus type 1 replication in rodent cells. J Virol 74: 9868-9877
4. Bijlmakers MJ, Marsh M (2000) Hsp90 is essential for the synthesis and subsequent membrane association, but not the maintenance, of the Src-kinase p56(lck). Mol Biol Cell 11: 1585-1595
5. Boris-Lawrie K, Roberts TM, Hull S (2001) Retroviral RNA elements integrate components of post-transcriptional gene expression. Life Sci 69: 2697-2709
6. Bray M, Prasad S, Dubay JW, Hunter E, Jeang KT, Rekosh D, Hammarskjold ML (1994) A small element from the Mason-Pfizer monkey virus genome makes human immunodeficiency virus type 1 expression and replication Rev-independent. Proc Natl Acad Sci USA 91: 1256-1260
7. Chen BK, Rousso I, Shim S, Kim PS (2001) Efficient assembly of an HIV-1/MLV Gag-chimeric virus in murine cells. Proc Natl Acad Sci USA 98: 15239-15244
8. Choi G, Park S, Choi B, Hong S, Lee J, Hunter E, Rhee SS (1999) Identification of a cytoplasmic targeting/retention signal in a retroviral Gag polyprotein. J Virol 73: 5431-5437
9. Cullen BR (2003) Nuclear RNA export. J Cell Sci 116: 587-597
10. Daneholt B (2001) Assembly and transport of a premessenger RNP particle. Proc Natl Acad Sci USA 98: 7012-7017
11. Dreyfuss G, Kim VN, Kataoka N (2002) Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3: 195-205
12. Egger D, Wolk B, Gosert R, Bianchi L, Blum HE, Moradpour D, Bienz K (2002) Expression of hepatitis C virus proteins induces distinct membrane alterations including a candidate viral replication complex. J Virol 76: 5974-5984
13. Feng Y, Broder CC, Kennedy PE, Berger EA (1996) HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272: 872-877
14. Freed EO (1998) HIV-1 gag proteins: diverse functions in the virus life cycle. Virology 251: 1-15
15. 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
16. Gallouzi IE, Steitz JA (2001) Delineation of mRNA export pathways by the use of cell-permeable peptides. Science 294: 1895-1901
17. Garber ME, Wei P, KewalRamani VN, Mayall TP, Herrmann CH, Rice AP, Littman DR, Jones KA (1998) The interaction between HIV-1 Tat and human cyclin T1 requires zinc and a critical cysteine residue that is not conserved in the murine CycT1 protein. Genes Dev 12: 3512-3527
18. Garrus JE, von Schwedler UK, Pornillos OW, Morham SG, Zavitz KH, Wang HE, Wettstein DA, Stray KM, Cote M, Rich RL, Myszka DG, Sundquist WI (2001) Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107: 55-65
19. Goff A, Ehrlich LS, Cohen SN, Carter CA (2003) Tsg101 control of human immunodeficiency virus type 1 Gag trafficking and release. J Virol 77: 9173-9182
20. Gruter P, Tabernero C, von Kobbe C, Schmitt C, Saavedra C, Bachi A, Wilm M, Felber BK, Izaurralde E (1998) TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol Cell 1: 649-659
21. Gurer C, Cimarelli A, Luban J (2002) Specific incorporation of heat shock protein 70 family members into primate lentiviral virions. J Virol 76: 4666-4670
22. Hachet O, Ephrussi A (2004) Splicing of oskar RNA in the nucleus is coupled to its cytoplasmic localization. Nature 428: 959-963
23. Heath CM, Windsor M, Wileman T (2001) Aggresomes resemble sites specialized for virus assembly. J Cell Biol 153: 449-455
24. Herold A, Klymenko T, Izaurralde E (2001) NXF1/p15 heterodimers are essential for mRNA nuclear export in Drosophila. RNA 7: 1768-1780
25. Herold A, Teixeira L, Izaurralde E (2003) Genome-wide analysis of nuclear mRNA export pathways in Drosophila. EMBO J 22: 2472-2483
26. Hieronymus H, Silver PA (2003) Genome-wide analysis of RNA-protein interactions illustrates specificity of the mRNA export machinery. Nat Genet 33: 155-161
27. Hong S, Choi G, Park S, Chung AS, Hunter E, Rhee SS (2001) Type D retrovirus Gag polyprotein interacts with the cytosolic chaperonin TRiC. J Virol 75: 2526-2534
28. Jansen RP (1999) RNA-cytoskeletal associations. FASEB J 13: 455-466
29. Kloc M, Zearfoss NR, Etkin LD (2002) Mechanisms of subcellular mRNA localization. Cell 108: 533-544
30. Koito A, Shigekane H, Matsushita S (2003) Ability of small animal cells to support the postintegration phase of human immunodeficiency virus type-1 replication. Virology 305: 181-191
31. Kotsopoulou E, Kim VN, Kingsman AJ, Kingsman SM, Mitrophanous KA (2000) A Rev-independent human immunodeficiency virus type 1 (HIV-1)-based vector that exploits a codon-optimized HIV-1 gag-pol gene. J Virol 74: 4839-4852
32. Lei EP, Silver PA (2002) Protein and RNA export from the nucleus. Dev Cell 2: 261-272
33. Maddon PJ, Dalgleish AG, McDougal JS, Clapham PR, Weiss RA, Axel R (1986) The T4 gene encodes the AIDS virus receptor and is expressed in the immune system and the brain. Cell 47: 333-348
34. Malim MH, McCarn DF, Tiley LS, Cullen BR (1991) Mutational definition of the human immunodeficiency virus type 1 Rev activation domain. J Virol 65: 4248-4254
35. Maquat LE (2004) Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat Rev Mol Cell Biol 5: 89-99
36. Mariani R, Rasala BA, Rutter G, Wiegers K, Brandt SM, Krausslich HG, Landau NR (2001) Mouse-human heterokaryons support efficient human immunodeficiency virus type 1 assembly. J Virol 75: 3141-3151
37. Mariani R, Rutter G, Harris ME, Hope TJ, Krausslich HG, Landau NR (2000) A block to human immunodeficiency virus type 1 assembly in murine cells. J Virol 74: 3859-3870
38. Martin-Serrano J, Yarovoy A, Perez-Caballero D, Bieniasz PD (2003) Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins. Proc Natl Acad Sci USA 100: 12414-12419
39. Moss B (2001) Poxviridae: the viruses and their replication. In Fields Virology, Knipe DH, PM (ed) Vol. 2, pp 2849-2884. Philadelphia: Lippincott Williams & Wilkins
40. Nasioulas G, Hughes SH, Felber BK, Whitcomb JM (1995) Production of avian leukosis virus particles in mammalian cells can be mediated by the interaction of the human immunodeficiency virus protein Rev and the Rev-responsive element. Proc Natl Acad Sci USA 92: 11940-11944
41. Nott A, Le Hir H, Moore MJ (2004) Splicing enhances translation in mammalian cells: an additional function of the exon junction complex. Genes Dev 18: 210-222
42. Nydegger S, Foti M, Derdowski A, Spearman P, Thali M (2003) HIV-1 egress is gated through late endosomal membranes. Traffic 4: 902-910
43. Ogert RA, Lee LH, Beemon KL (1996) Avian retroviral RNA element promotes unspliced RNA accumulation in the cytoplasm. J Virol 70: 3834-3843
44. Ohno M, Segref A, Kuersten S, Mattaj IW (2002) Identity elements used in export of mRNAs. Mol Cell 9: 659-671
45. Ono A, Freed EO (1999) Binding of human immunodeficiency virus type 1 Gag to membrane: role of the matrix amino terminus. J Virol 73: 4136-4144
46. Ono A, Freed EO (2004) Cell-type-dependent targeting of human immunodeficiency virus type 1 assembly to the plasma membrane and the multivesicular body. J Virol 78: 1552-1563
47. Palacios IM, Gatfield D, St Johnston D, Izaurralde E (2004) An eIF4AIII-containing complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427: 753-757
48. Palacios IM, Johnston DS (2001) Getting the message across: the intracellular localization of mRNAs in higher eukaryotes. Annu Rev Cell Dev Biol 17: 569-614
49. Pelchen-Matthews A, Kramer B, Marsh M (2003) Infectious HIV-1 assembles in late endosomes in primary macrophages. J Cell Biol 162: 443-455
50. Pollard VW, Malim MH (1998) The HIV-1 Rev protein. Annu Rev Microbiol 52: 491-532
51. Reed M, Mariani R, Sheppard L, Pekrun K, Landau NR, Soong NW (2002) Chimeric human immunodeficiency virus type 1 containing murine leukemia virus matrix assembles in murine cells. J Virol 76: 436-443
52. Reed R, Hurt E (2002) A conserved mRNA export machinery coupled to pre-mRNA splicing. Cell 108: 523-531
53. Rhee SS, Hunter E (1990) A single amino acid substitution within the matrix protein of a type D retrovirus converts its morphogenesis to that of a type C retrovirus. Cell 63: 77-86
54. Sanchez V, Greis KD, Sztul E, Britt WJ (2000) Accumulation of virion tegument and envelope proteins in a stable cytoplasmic compartment during human cytomegalovirus replication: characterization of a potential site of virus assembly. J Virol 74: 975-986
55. Segref A, Sharma K, Doye V, Hellwig A, Huber J, Luhrmann R, Hurt E (1997) Mex67p, a novel factor for nuclear mRNA export, binds to both poly (A) + RNA and nuclear pores. EMBO J 16: 3256-3271
56. Sfakianos JN, Hunter E (2003) M-PMV capsid transport is mediated by Env/Gag interactions at the pericentriolar recycling endosome. Traffic 4: 671-680
57. Sfakianos JN, LaCasse RA, Hunter E (2003) The M-PMV cytoplasmic targeting-retention signal directs nascent Gag polypeptides to a pericentriolar region of the cell. Traffic 4: 660-670
58. 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
59. Sherer NM, Lehmann MJ, Jimenez-Soto LF, Ingmundson A, Horner SM, Cicchetti G, Allen PG, Pypaert M, Cunningham JM, Mothes W (2003) Visualization of retroviral replication in living cells reveals budding into multivesicular bodies. Traffic 4: 785-801
60. Shi ST, Lee KJ, Aizaki H, Hwang SB, Lai MM (2003) Hepatitis C virus RNA replication occurs on a detergent-resistant membrane that cofractionates with caveolin-2. J Virol 77: 4160-4168
61. Simon JH, Fouchier RA, Southerling TE, Guerra CB, Grant CK, Malim MH (1997) The Vif and Gag proteins of human immunodeficiency virus type 1 colocalize in infected human T cells. J Virol 71: 5259-5267
62. Strack B, Calistri A, Craig S, Popova E, Gottlinger HG (2003) AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding. Cell 114: 689-699
63. Stutz F, Izaurralde E (2003) The interplay of nuclear mRNP assembly, mRNA surveillance and export. Trends Cell Biol 13: 319-327
64. Tan W, Zolotukhin AS, Bear J, Patenaude DJ, Felber BK (2000) The mRNA export in Caenorhabditis elegans is mediated by Ce-NXF-1, an ortholog of human TAP/NXF and Saccharomyces cerevisiae Mex67p. RNA 6: 1762-1772
65. Tang C, Loeliger E, Luncsford P, Kinde I, Beckett D, Summers MF (2004) Entropic switch regulates myristate exposure in the HIV-1 matrix protein. Proc Natl Acad Sci USA 101: 517-522
66. Trono D, Baltimore D (1990) A human cell factor is essential for HIV-1 Rev action. EMBO J 9: 4155-4160
67. VerPlank L, Bouamr F, LaGrassa TJ, Agresta B, Kikonyogo A, Leis J, Carter CA (2001) Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag). Proc Natl Acad Sci USA 98: 7724-7729
68. von Schwedler UK, Stuchell M, Muller B, Ward DM, Chung HY, Morita E, Wang HE, Davis T, He GP, Cimbora DM, Scott A, Krausslich HG, Kaplan J, Morham SG, Sundquist WI (2003) The protein network of HIV budding. Cell 114: 701-713
69. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA (1998) A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell 92: 451-462
70. Wilkie GS, Zimyanin V, Kirby R, Korey C, Francis-Lang H, Van Vactor D, Davis I (2001) Small bristles, the Drosophila ortholog of NXF-1, is essential for mRNA export throughout development. RNA 7: 1781-1792
71. Wodrich H, Schambach A, Krausslich HG (2000) Multiple copies of the Mason-Pfizer monkey virus constitutive RNA transport element lead to enhanced HIV-1 Gag expression in a context-dependent manner. Nucleic Acids Res 28: 901-910
72. Zheng YH, Yu HF, Peterlin BM (2003) Human p32 protein relieves a post-transcriptional block to HIV replication in murine cells. Nat Cell Biol 5: 611-618
73. Zimmerman C, Klein KC, Kiser PK, Singh AR, Firestein BL, Riba SC, Lingappa JR (2002) Identification of a host protein essential for assembly of immature HIV-1 capsids. Nature 415: 88-92