Cooperative and specific binding of Vif to the 5′ region of HIV-1 genomic RNA

Journal of Molecular Biology

Volumn 354, Issue 1, 2005, Pages 55-72

  Henriet, Simon ^a   Richer, Delphine ^a   Bernacchi, Serena ^a   Decroly, Etienne ^b,c   Vigne, Robert ^b   Ehresmann, Bernard ^a   Ehresmann, Chantal ^a   Paillart, Jean Christophe ^a   Marquet, Roland ^a  

^a INST DE BIOL MOLEC ET CELLULAIRE   (France)

^b INSERM   (France)

^c Centre National de la Recherche Scientifique   (France)

Author keywords

Cooperativity; HIV 1; RNA interactions; Structure; Vif

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3F; APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3G; ENZYME; GENOMIC RNA; NUCLEOTIDE DERIVATIVE; PROTEIN DERIVATIVE; RECOMBINANT PROTEIN; RIBONUCLEASE T1; UNCLASSIFIED DRUG; VIRAL INFECTIVITY FACTOR PROTEIN; VIRUS PROTEIN; VIRUS RNA;

5' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; CHEMICAL ANALYSIS; DNA PACKAGING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN RNA BINDING; REGULATORY MECHANISM; REVERSE TRANSCRIPTION; STRUCTURAL GENE; VIRUS GENOME; VIRUS REPLICATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 27344451439     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.09.025     Document Type: Article

References (94)

1. R.C. Desrosiers, J.D. Lifson, J.S. Gibbs, S.C. Czajak, A.Y. Howe, L.O. Arthur, and R.P. Johnson Identification of highly attenuated mutants of simian immunodeficiency virus J. Virol. 72 1998 1431 1437
2. K. Strebel, D. Daugherty, K. Clouse, D. Cohen, T. Folks, and M.A. Martin The HIV 'A' (sor) gene product is essential for virus infectivity Nature 328 1987 728 730
3. D.H. Gabuzda, K. Lawrence, E. Langhoff, E. Terwilliger, T. Dorfman, W.A. Haseltine, and J. Sodroski Role of vif in replication of human immunodeficiency virus type 1 in CD4+T lymphocytes J. Virol. 66 1992 6489 6495
4. D.H. Gabuzda, H. Li, K. Lawrence, B.S. Vasir, K. Crawford, and E. Langhoff Essential role of vif in establishing productive HIV-1 infection in peripheral blood T lymphocytes and monocyte/macrophages J. Acquir. Immune Defic. Syndr. 7 1994 908 915
5. U. von Schwedler, J. Song, C. Aiken, and D. Trono Vif is crucial for human immunodeficiency virus type 1 proviral DNA synthesis in infected cells J. Virol. 67 1993 4945 4955
6. J.H. Simon, D.L. Miller, R.A. Fouchier, M.A. Soares, K.W. Peden, and M.H. Malim The regulation of primate immunodeficiency virus infectivity by Vif is cell species restricted: a role for Vif in determining virus host range and cross-species transmission EMBO J. 17 1998 1259 1267
7. P. Sova, and D.J. Volsky Efficiency of viral DNA synthesis during infection of permissive and nonpermissive cells with vif-negative human immunodeficiency virus type 1 J. Virol. 67 1993 6322 6326
8. J.X. Zou, and P.A. Luciw The requirement for Vif of SIVmac is cell-type dependent J. Gen. Virol. 77 1996 427 434
9. N. Madani, and D. Kabat An endogenous inhibitor of human immunodeficiency virus in human lymphocytes is overcome by the viral Vif protein J. Virol. 72 1998 10251 10255
10. J.H. Simon, N.C. Gaddis, R.A. Fouchier, and M.H. Malim Evidence for a newly discovered cellular anti-HIV-1 phenotype Nature Med. 4 1998 1397 1400
11. A.M. Sheehy, N.C. Gaddis, J.D. Choi, and M.H. Malim Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein Nature 418 2002 646 650
12. H. Zhang, B. Yang, R.J. Pomerantz, C. Zhang, S.C. Arunachalam, and L. Gao The cytidine deaminase CEM15 induces hypermutation in newly synthesized HIV-1 DNA Nature 424 2003 94 98
13. D. Lecossier, F. Bouchonnet, F. Clavel, and A.J. Hance Hypermutation of HIV-1 DNA in the absence of the Vif protein Science 300 2003 1112
14. B. Mangeat, P. Turelli, G. Caron, M. Friedli, L. Perrin, and D. Trono Broad antiretroviral defence by human APOBEC3G through lethal editing of nascent reverse transcripts Nature 424 2003 99 103
15. R.S. Harris, K.N. Bishop, A.M. Sheehy, H.M. Craig, S.K. Petersen-Mahrt, and I.N. Watt DNA deamination mediates innate immunity to retroviral infection Cell 113 2003 803 809
16. R. Mariani, D. Chen, B. Schrofelbauer, F. Navarro, R. Konig, B. Bollman, and C. Munk Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif Cell 114 2003 21 31
17. M.T. Liddament, W.L. Brown, A.J. Schumacher, and R.S. Harris APOBEC3F properties and hypermutation preferences indicate activity against HIV-1 in vivo Curr. Biol. 14 2004 1385 1391
18. H.L. Wiegand, B.P. Doehle, H.P. Bogerd, and B.R. Cullen A second human antiretroviral factor, APOBEC3F, is suppressed by the HIV-1 and HIV-2 Vif proteins EMBO J. 23 2004 2451 2458
19. Y.H. Zheng, D. Irwin, T. Kurosu, K. Tokunaga, T. Sata, and B.M. Peterlin Human APOBEC3F is another host factor that blocks human immunodeficiency virus type 1 replication J. Virol. 78 2004 6073 6076
20. T.M. Alce, and W. Popik APOBEC3G is incorporated into virus-like particles by a direct interaction with HIV-1 Gag nucleocapsid protein J. Biol. Chem. 279 2004 34083 34086
21. S. Cen, F. Guo, M. Niu, J. Saadatmand, J. Deflassieux, and L. Kleiman The interaction between HIV-1 Gag and APOBEC3G J. Biol. Chem. 279 2004 33177 33184
22. E.S. Svarovskaia, H. Xu, J.L. Mbisa, R. Barr, R.J. Gorelick, and A. Ono Human apolipoprotein B mRNA-editing enzyme-catalytic polypeptide-like 3G (APOBEC3G) is incorporated into HIV-1 virions through interactions with viral and nonviral RNAs J. Biol. Chem. 279 2004 35822 35828
23. V. Zennou, D. Perez-Caballero, H. Gottlinger, and P.D. Bieniasz APOBEC3G incorporation into human immunodeficiency virus type 1 particles J. Virol. 78 2004 12058 12061
24. M. Douaisi, S. Dussart, M. Courcoul, G. Bessou, R. Vigne, E. Decroly, and L.V. HIV-1 Gag proteins are sufficient to recruit APOBEC3G into virus-like particles Biochem. Biophys. Res. Commun. 321 2004 566 573
25. Q. Yu, R. Konig, S. Pillai, K. Chiles, M. Kearney, and S. Palmer Single-strand specificity of APOBEC3G accounts for minus-strand deamination of the HIV genome Nature Struct. Mol. Biol. 11 2004 435 442
26. M. Marin, K.M. Rose, S.L. Kozak, and D. Kabat HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation Nature Med. 9 2003 1398 1403
27. A. Mehle, J. Goncalves, M. Santa-Marta, M. McPike, and D. Gabuzda Phosphorylation of a novel SOCS-box regulates assembly of the HIV-1 Vif-Cul5 complex that promotes APOBEC3G degradation Genes Dev. 18 2004 2861 2866
28. X. Yu, Y. Yu, B. Liu, K. Luo, W. Kong, P. Mao, and X.F. Yu Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex Science 302 2003 1056 1060
29. Y. Yu, Z. Xiao, E.S. Ehrlich, X. Yu, and X.F. Yu Selective assembly of HIV-1 Vif-Cul5-ElonginB-ElonginC E3 ubiquitin ligase complex through a novel SOCS box and upstream cysteines Genes Dev. 18 2004 2867 2872
30. H. Takeuchi, S. Kao, E. Miyagi, M.A. Khan, A. Buckler-White, R. Plishka, and K. Strebel Production of infectious SIVagm from human cells requires functional inactivation but not viral exclusion of human APOBEC3G J. Biol. Chem. 280 2005 375 382
31. S. Kao, E. Miyagi, M.A. Khan, H. Takeuchi, S. Opi, R. Goila-Gaur, and K. Strebel Production of infectious human immunodeficiency virus type 1 does not require depletion of APOBEC3G from virus-producing cells Retrovirology 1 2004 1 12
32. A. Ohagen, and D. Gabuzda Role of Vif in stability of the human immunodeficiency virus type 1 core J. Virol. 74 2000 11055 11066
33. S. Hoglund, A. Ohagen, K. Lawrence, and D. Gabuzda Role of vif during packing of the core of HIV-1 Virology 201 1994 349 355
34. H. Zhang, R.J. Pomerantz, G. Dornadula, and Y. Sun 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. 74 2000 8252 8261
35. M.K. Karczewski, and K. Strebel Cytoskeleton association and virion incorporation of the human immunodeficiency virus type 1 Vif protein J. Virol. 70 1996 494 507
36. C. Zimmerman, K.C. Klein, P.K. Kiser, A.R. Singh, B.L. Firestein, S.C. Riba, and J.R. Lingappa Identification of a host protein essential for assembly of immature HIV-1 capsids Nature 415 2002 88 92
37. J. Lake, J. Carr, F. Feng, L. Mundy, C. Burrell, and P. Li The role of Vif during HIV-1 infection: interaction with novel host cellular factors J. Clin. Virol. 26 2003 143 152
38. J.E. Dooher, and J.R. Lingappa Conservation of a stepwise, energy-sensitive pathway involving HP68 for assembly of primate lentivirus capsids in cells J. Virol. 78 2004 1645 1656
39. J.H. Simon, R.A. Fouchier, T.E. Southerling, C.B. Guerra, C.K. Grant, and M.H. Malim The Vif and Gag proteins of human immunodeficiency virus type 1 colocalize in infected human T cells J. Virol. 71 1997 5259 5267
40. I. Huvent, S.S. Hong, C. Fournier, B. Gay, J. Tournier, and C. Carriere Interaction and co-encapsidation of human immunodeficiency virus type 1 Gag and Vif recombinant proteins J. Gen. Virol. 79 1998 1069 1081
41. J.H. Simon, E.A. Carpenter, R.A. Fouchier, and M.H. Malim Vif and the p55(Gag) polyprotein of human immunodeficiency virus type 1 are present in colocalizing membrane-free cytoplasmic complexes J. Virol. 73 1999 2667 2674
42. M. Bouyac, M. Courcoul, G. Bertoia, Y. Baudat, D. Gabuzda, and D. Blanc Human immunodeficiency virus type 1 Vif protein binds to the Pr55Gag precursor J. Virol. 71 1997 9358 9365
43. J. Goncalves, B. Shi, X. Yang, and D. Gabuzda Biological activity of human immunodeficiency virus type 1 Vif requires membrane targeting by C-terminal basic domains J. Virol. 69 1995 7196 7204
44. M.A. Khan, H. Akari, S. Kao, C. Aberham, D. Davis, A. Buckler-White, and K. Strebel Intravirion processing of the human immunodeficiency virus type 1 Vif protein by the viral protease may be correlated with Vif function J. Virol. 76 2002 9112 9123
45. H. Akari, M. Fujita, S. Kao, M.A. Khan, M. Shehu-Xhilaga, A. Adachi, and K. Strebel High level expression of human immunodeficiency virus type-1 Vif inhibits viral infectivity by modulating proteolytic processing of the Gag precursor at the p2/nucleocapsid processing site J. Biol. Chem. 279 2004 12355 12362
46. L. Baraz, M. Hutoran, I. Blumenzweig, M. Katzenellenbogen, A. Friedler, and C. Gilon Human immunodeficiency virus type 1 Vif binds the viral protease by interaction with its N-terminal region J. Gen. Virol. 83 2002 2225 2230
47. M. Bardy, B. Gay, S. Pebernard, N. Chazal, M. Courcoul, and R. Vigne Interaction of human immunodeficiency virus type 1 Vif with Gag and Gag-Pol precursors: co-encapsidation and interference with viral protease-mediated Gag processing J. Gen. Virol. 82 2001 2719 2733
48. S. Dussart, M. Courcoul, G. Bessou, M. Douaisi, Y. Duverger, R. Vigne, and E. Decroly The Vif protein of human immunodeficiency virus type 1 is posttranslationally modified by ubiquitin Biochem. Biophys. Res. Commun. 315 2004 66 72
49. H. Liu, X. Wu, M. Newman, G.M. Shaw, B.H. Hahn, and J.C. Kappes The Vif protein of human and simian immunodeficiency viruses is packaged into virions and associates with viral core structures J. Virol. 69 1995 7630 7638
50. S. Kao, H. Akari, M.A. Khan, M. Dettenhofer, X.F. Yu, and K. Strebel Human immunodeficiency virus type 1 Vif is efficiently packaged into virions during productive but not chronic infection J. Virol. 77 2003 1131 1140
51. M.A. Khan, C. Aberham, S. Kao, H. Akari, R. Gorelick, S. Bour, and K. Strebel Human immunodeficiency virus type 1 Vif protein is packaged into the nucleoprotein complex through an interaction with viral genomic RNA J. Virol. 75 2001 7252 7265
52. M. Dettenhofer, S. Cen, B.A. Carlson, L. Kleiman, and X.F. Yu Association of human immunodeficiency virus type 1 Vif with RNA and its role in reverse transcription J. Virol. 74 2000 8938 8945
53. R. Marquet, C. Isel, C. Ehresmann, and B. Ehresmann tRNAs as primer of reverse transcriptases Biochimie 77 1995 113 124
54. B. Berkhout Structure and function of the human immunodeficiency virus leader RNA Prog. Nucl. Acid Res. Mol. Biol. 54 1996 1 34
55. J.-C. Paillart, M. Shehu-Xhilaga, R. Marquet, and J. Mak Dimerization of retroviral RNA genomes: an inseparable pair Nature Rev. Microbiol. 2 2004 461 472
56. J.C. Paillart, M. Dettenhofer, X.F. Yu, C. Ehresmann, B. Ehresmann, and R. Marquet First snapshots of the HIV-1 RNA structure in infected cells and in virions J. Biol. Chem. 279 2004 48397 48403
57. C.K. Damgaard, E.S. Andersen, B. Knudsen, J. Gorodkin, and J. Kjems RNA interactions in the 5′ region of the HIV-1 genome J. Mol. Biol. 336 2004 369 379
58. F. Baudin, R. Marquet, C. Isel, J.-L. Darlix, B. Ehresmann, and C. Ehresmann Functional sites in the 5′ region of human immunodeficiency virus type-1 RNA form defined structural domains J. Mol. Biol. 229 1993 382 397
59. J.C. Paillart, E. Skripkin, B. Ehresmann, C. Ehresmann, and R. Marquet In vitro evidence for a long range pseudoknot in the 5′-untranslated and matrix coding regions of HIV-1 genomic RNA J. Biol. Chem. 277 2002 5995 6004
60. C. Schaeffer, B. Bardoni, J.L. Mandel, B. Ehresmann, C. Ehresmann, and H. Moine The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif EMBO J. 20 2001 4803 4813
61. X. Yang, J. Goncalves, and D. Gabuzda Phosphorylation of Vif and its role in HIV-1 replication J. Biol. Chem. 271 1996 10121 10129
62. X. Yang, and D. Gabuzda Mitogen-activated protein kinase phosphorylates and regulates the HIV-1 Vif protein J. Biol. Chem. 273 1998 29879 29887
63. M. Dettenhofer, and X.F. Yu Highly purified human immunodeficiency virus type 1 reveals a virtual absence of Vif in virions J. Virol. 73 1999 1460 1467
64. D. Camaur, and D. Trono Characterization of human immunodeficiency virus type 1 Vif particle incorporation J. Virol. 70 1996 6106 6211
65. J.H. Simon, D.L. Miller, R.A. Fouchier, and M.H. Malim Virion incorporation of human immunodeficiency virus type-1 Vif is determined by intracellular expression level and may not be necessary for function Virology 248 1998 182 187
66. R.A. Fouchier, J.H. Simon, A.B. Jaffe, and M.H. Malim Human immunodeficiency virus type 1 Vif does not influence expression or virion incorporation of gag-, pol-, and env-encoded proteins J. Virol. 70 1996 8263 8269
67. S. Yang, Y. Sun, and H. Zhang The multimerization of human immunodeficiency virus type I Vif protein: a requirement for Vif function in the viral life cycle J. Biol. Chem. 276 2001 4889 4893
68. J. Clever, C. Sassetti, and T.G. Parslow RNA secondary structure and binding sites for gag gene products in the 5′ packaging signal of human immunodeficiency virus type 1 J. Virol. 69 1995 2101 2109
69. M.F. Shubsda, A.C. Paoletti, B.S. Hudson, and P.N. Borer Affinities of packaging domain loops in HIV-1 RNA for the nucleocapsid protein Biochemistry 41 2002 5276 5282
70. R.D. Berkowitz, A. Ohagen, S. Hoglund, and S.P. Goff Retroviral nucleocapsid domains mediate the specific recognition of genomic viral RNAs by chimeric Gag polyproteins during RNA packaging in vivo J. Virol. 69 1995 6445 6456
71. R.J. Fisher, A. Rein, M. Fivash, M.A. Urbaneja, J.R. Casas-Finet, M. Medaglia, and L.E. Henderson Sequence-specific binding of human immunodeficiency virus type 1 nucleocapsid protein to short oligonucleotides J. Virol. 72 1998 1902 1909
72. C. Vuilleumier, E. Bombarda, N. Morellet, D. Gerard, B.P. Roques, and Y. Mely Nucleic acid sequence discrimination by the HIV-1 nucleocapsid protein NCp7: a fluorescence study Biochemistry 38 1999 16816 16825
73. A.C. Paoletti, M.F. Shubsda, B.S. Hudson, and P.N. Borer Affinities of the nucleocapsid protein for variants of SL3 RNA in HIV-1 Biochemistry 41 2002 15423 15428
74. R. Khan, and D.P. Giedroc Nucleic acid binding properties of recombinant Zn2 HIV-1 nucleocapsid protein are modulated by COOH-terminal processing J. Biol. Chem. 269 1994 22538 22546
75. Y. Mely, H. de Rocquigny, M. Sorinas-Jimeno, G. Keith, B.P. Roques, R. Marquet, and D. Gerard Binding of the HIV-1 nucleocapsid protein to the primer tRNA(3Lys), in vitro, is essentially not specific J. Biol. Chem. 270 1995 1650 1656
76. B.I. Klasens, M. Thiesen, A. Virtanen, and B. Berkhout The ability of the HIV-1 AAUAAA signal to bind polyadenylation factors is controlled by local RNA structure Nucl. Acids Res. 27 1999 446 454
77. B.R. Graveley, E.S. Fleming, and G.M. Gilmartin RNA structure is a critical determinant of poly(A) site recognition by cleavage and polyadenylation specificity factor Mol. Cell. Biol. 16 1996 4942 4951
78. P. Wang, M.C. Rouyez, S. Ducamp, S. Saragosti, and M. Ventura Similarity of the 5′ and 3′-TAR secondary structures in HIV-1 Biochem. Biophys. Res. Commun. 195 1993 565 573
79. J.L. Clever, D. Mirandar Jr, and T.G. Parslow RNA structure and packaging signals in the 5′ leader region of the human immunodeficiency virus type 1 genome J. Virol. 76 2002 12381 12387
80. M.A. Khan, S. Kao, E. Miyagi, H. Takeuchi, R. Goila-Gaur, and S. Opi Viral RNA is required for the association of APOBEC3G with human immunodeficiency virus type 1 nucleoprotein complexes J. Virol. 79 2005 5870 5874
81. M. Nascimbeni, M. Bouyac, F. Rey, B. Spire, and F. Clavel The replicative impairment of Vif-mutants of human immunodeficiency virus type 1 correlates with an overall defect in viral DNA synthesis J. Gen. Virol. 79 1998 1945 1950
82. R. Cancio, S. Spadari, and G. Maga Vif is an auxiliary factor of the HIV-1 reverse transcriptase and facilitates abasic site bypass Biochem. J. 383 2004 475 482
83. B. Berkhout, N.L. Vastenhouw, B.I. Klasens, and H. Huthoff Structural features in the HIV-1 repeat region facilitate strand transfer during reverse transcription RNA 7 2001 1097 1114
84. I. Kanevsky, F. Chaminade, D. Ficheux, A. Moumen, R. Gorelick, and M. Negroni Specific interactions between HIV-1 nucleocapsid protein and the TAR element J. Mol. Biol. 348 2005 1059 1077
85. S. Kao, M.A. Khan, E. Miyagi, R. Plishka, A. Buckler-White, and K. Strebel The human immunodeficiency virus type 1 Vif protein reduces intracellular expression and inhibits packaging of APOBEC3G (CEM15), a cellular inhibitor of virus infectivity J. Virol. 77 2003 11398 113407
86. H. Xu, E.S. Svarovskaia, R. Barr, Y. Zhang, M.A. Khan, K. Strebel, and V.K. Pathak A single amino acid substitution in human APOBEC3G antiretroviral enzyme confers resistance to HIV-1 virion infectivity factor-induced depletion Proc. Natl Acad. Sci. USA 101 2004 5652 5657
87. A. Mehle, B. Strack, P. Ancuta, C. Zhang, M. McPike, and D. Gabuzda Vif overcomes the innate antiviral activity of APOBEC3G by promoting its degradation in the ubiquitin-proteasome pathway J. Biol. Chem. 279 2004 7792 7798
88. K. Stopak, C. de Noronha, W. Yonemoto, and W.C. Greene HIV-1 Vif blocks the antiviral activity of APOBEC3G by impairing both its translation and intracellular stability Mol. Cell. 12 2003 591 601
89. R.C. Beale, S.K. Petersen-Mahrt, I.N. Watt, R.S. Harris, C. Rada, and M.S. Neuberger Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra in vivo J. Mol. Biol. 337 2004 585 596
90. R. Marquet, F. Baudin, C. Gabus, J.L. Darlix, M. Mougel, C. Ehresmann, and B. Ehresmann Dimerization of human immunodeficiency virus (type 1) RNA: stimulation by cations and possible mechanism Nucl. Acids Res. 19 1991 2349 2357
91. F. Jossinet, J.C. Paillart, E. Westhof, T. Hermann, E. Skripkin, and J.S. Lodmell Dimerization of HIV-1 genomic RNA of subtypes A and B: RNA loop structure and magnesium binding RNA 5 1999 1222 1234
92. C.R. Cantor, and P.R. Schimmel Biophysical Chemistry 1980 Freeman W.H. and Co San Francisco, CA
93. J.-C. Paillart, L. Berthoux, M. Ottmann, J.-L. Darlix, R. Marquet, B. Ehresmann, and C. Ehresmann 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. 70 1996 8348 8354
94. M. Zuker Mfold web server for nucleic acid folding and hybridization prediction Nucl. Acids Res. 31 2003 3406 3415