Different effects of the TAR structure on HIV-1 and HIV-2 genomic RNA translation

Nucleic Acids Research

Volumn 40, Issue 6, 2012, Pages 2653-2667

  Soto Rifo, Ricardo ^a,b   Limousin, Taran ^a,b   Rubilar, Paulina S ^a,b   Ricci, Emiliano P ^a,b   Décimo, Didier ^a,b   Moncorgé, Olivier ^a,b   Trabaud, Mary Anne ^c,d   André, Patrice ^c,d   Cimarelli, Andrea ^a,b   Ohlmann, Théophile ^a,b,d  

^a CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^b UNIVERSITÉ DE LYON   (France)

^c University Lyon i   (France)

^d HOSPICES CIVILS DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GENOMIC RNA; MESSENGER RNA; VIRUS PROTEIN;

5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2; NONHUMAN; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN SYNTHESIS; RNA STABILITY; RNA STRUCTURE; RNA TRANSLATION; VIRUS GENOME;

5' UNTRANSLATED REGIONS; ANIMALS; CELL LINE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; GENOME, VIRAL; HIV LONG TERMINAL REPEAT; HIV-1; HIV-2; HUMANS; PROTEIN BIOSYNTHESIS; PROVIRUSES; RIBOSOMES; RNA, VIRAL;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 2;

EID: 84859368195     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1093     Document Type: Article

References (75)

1. Shatkin, A.J. (1976) Capping of eucaryotic mRNAs. Cell, 9, 645-653
2. Jackson, R.J., Hellen, C.U. and Pestova, T.V. (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol., 11, 113-127
3. Kozak, M. (1989) The scanning model for translation: an update. J. Cell Biol., 108, 229-241 (Pubitemid 19065830)
4. Prevot, D., Darlix, J.L. and Ohlmann, T. (2003) Conducting the initiation of protein synthesis: the role of eIF4G. Biol. Cell, 95, 141-156 (Pubitemid 36889217)
5. Abaeva, I.S., Marintchev, A., Pisareva, V.P., Hellen, C.U. and Pestova, T.V. (2011) Bypassing of stems versus linear base-by-base inspection of mammalian mRNAs during ribosomal scanning. EMBO J., 30, 115-129
6. Gebauer, F. and Hentze, M.W. (2004) Molecular mechanisms of translational control. Nat. Rev. Mol. Cell. Biol., 5, 827-835 (Pubitemid 39336276)
7. Sonenberg, N. and Hinnebusch, A.G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell, 136, 731-745
8. Jang, S.K., Krausslich, H.G., Nicklin, M.J., Duke, G.M., Palmenberg, A.C. and Wimmer, E. (1988) A segment of the 50 nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol., 62, 2636-2643
9. Pelletier, J. and Sonenberg, N. (1988) Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature, 334, 320-325
10. Balvay, L., Soto Rifo, R., Ricci, E.P., Decimo, D. and Ohlmann, T. (2009) Structural and functional diversity of viral IRESes. Biochim. Biophys. Acta, 1789, 542-557
11. Holcik, M. and Sonenberg, N. (2005) Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol., 6, 318-327 (Pubitemid 40516898)
12. Butsch, M. and Boris-Lawrie, K. (2002) Destiny of unspliced retroviral RNA: ribosome and/or virion? J. Virol., 76, 3089-3094 (Pubitemid 34224510)
13. Berkhout, B. (1996) Structure and function of the human immunodeficiency virus leader RNA. Prog. Nucleic Acid Res. Mol. Biol., 54, 1-34
14. Damgaard, C.K., Dyhr-Mikkelsen, H. and Kjems, J. (1998) 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., 26, 3667-3676 (Pubitemid 28367971)
15. McCann, E.M. and Lever, A.M. (1997) Location of cis-acting signals important for RNA encapsidation in the leader sequence of human immunodeficiency virus type 2. J. Virol., 71, 4133-4137 (Pubitemid 27172434)
16. Paillart, J.C., Dettenhofer, M., Yu, X.F., Ehresmann, C., Ehresmann, B. and Marquet, R. (2004) First snapshots of the HIV-1 RNA structure in infected cells and in virions. J. Biol. Chem., 279, 48397-48403 (Pubitemid 39540996)
17. Dirac, A.M., Huthoff, H., Kjems, J. and Berkhout, B. (2002) Regulated HIV-2 RNA dimerization by means of alternative RNA conformations. Nucleic Acids Res., 30, 2647-2655 (Pubitemid 34679770)
18. Pachulska-Wieczorek, K., Purzycka, K.J. and Adamiak, R.W. (2006) New, extended hairpin form of the TAR-2 RNA domain points to the structural polymorphism at the 50 end of the HIV-2 leader RNA. Nucleic Acids Res., 34, 2984-2997 (Pubitemid 44540426)
19. Purzycka, K.J., Pachulska-Wieczorek, K. and Adamiak, R.W. (2011) The in vitro loose dimer structure and rearrangements of the HIV-2 leader RNA. Nucleic Acids Res., 39, 7234-7248
20. Watts, J.M., Dang, K.K., Gorelick, R.J., Leonard, C.W., Bess, J.W. Jr, Swanstrom, R., Burch, C.L. and Weeks, K.M. (2009) Architecture and secondary structure of an entire HIV-1 RNA genome. Nature, 460, 711-716
21. Wilkinson, K.A., Gorelick, R.J., Vasa, S.M., Guex, N., Rein, A., Mathews, D.H., Giddings, M.C. and Weeks, K.M. (2008) High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol., 6, e96
22. Berkhout, B. (1992) Structural features in TAR RNA of human and simian immunodeficiency viruses: a phylogenetic analysis. Nucleic Acids Res., 20, 27-31
23. Berkhout, B. and Schoneveld, I. (1993) Secondary structure of the HIV-2 leader RNA comprising the tRNA-primer binding site. Nucleic Acids Res., 21, 1171-1178 (Pubitemid 23155612)
24. SenGupta, D.N., Berkhout, B., Gatignol, A., Zhou, A.M. and Silverman, R.H. (1990) Direct evidence for translational regulation by leader RNA and Tat protein of human immunodeficiency virus type 1. Proc. Natl Acad. Sci. USA, 87, 7492-7496 (Pubitemid 20341742)
25. Berkhout, B., Arts, K. and Abbink, T.E. (2011) Ribosomal scanning on the 50-untranslated region of the human immunodeficiency virus RNA genome. Nucleic Acids Res., 39, 5232-5244
26. Geballe, A.P. and Gray, M.K. (1992) Variable inhibition of cell-free translation by HIV-1 transcript leader sequences. Nucleic Acids Res., 20, 4291-4297
27. Parkin, N.T., Cohen, E.A., Darveau, A., Rosen, C., Haseltine, W. and Sonenberg, N. (1988) Mutational analysis of the 50 non-coding region of human immunodeficiency virus type 1: effects of secondary structure on translation. EMBO J., 7, 2831-2837
28. Brasey, A., Lopez-Lastra, M., Ohlmann, T., Beerens, N., Berkhout, B., Darlix, J.L. and Sonenberg, N. (2003) 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., 77, 3939-3949 (Pubitemid 36350935)
29. Gendron, K., Ferbeyre, G., Heveker, N. and Brakier-Gingras, L. (2011) The activity of the HIV-1 IRES is stimulated by oxidative stress and controlled by a negative regulatory element. Nucleic Acids Res., 39, 902-912
30. Monette, A., Ajamian, L., Lopez-Lastra, M. and Mouland, A.J. (2009) Human immunodeficiency virus type 1 (HIV-1) induces the cytoplasmic retention of heterogeneous nuclear ribonucleoprotein A1 by disrupting nuclear import: implications for HIV-1 gene expression. J. Biol. Chem., 284, 31350-31362
31. Buck, C.B., Shen, X., Egan, M.A., Pierson, T.C., Walker, C.M. and Siliciano, R.F. (2001) The human immunodeficiency virus type 1 gag gene encodes an internal ribosome entry site. J. Virol., 75, 181-191
32. Herbreteau, C.H., Weill, L., Decimo, D., Prevot, D., Darlix, J.L., Sargueil, B. and Ohlmann, T. (2005) HIV-2 genomic RNA contains a novel type of IRES located downstream of its initiation codon. Nat. Struct. Mol. Biol., 12, 1001-1007
33. Ricci, E.P., Herbreteau, C.H., Decimo, D., Schaupp, A., Datta, S.A., Rein, A., Darlix, J.L. and Ohlmann, T. (2008) In vitro expression of the HIV-2 genomic RNA is controlled by three distinct internal ribosome entry segments that are regulated by the HIV protease and the Gag polyprotein. RNA, 14, 1443-1455 (Pubitemid 351872200)
34. Weill, L., James, L., Ulryck, N., Chamond, N., Herbreteau, C.H., Ohlmann, T. and Sargueil, B. (2010) A new type of IRES within gag coding region recruits three initiation complexes on HIV-2 genomic RNA. Nucleic Acids Res., 38, 1367-1381
35. Locker, N., Chamond, N. and Sargueil, B. (2011) A conserved structure within the HIV gag open reading frame that controls translation initiation directly recruits the 40S subunit and eIF3. Nucleic Acids Res., 39, 2367-2377
36. Adachi, A., Gendelman, H.E., Koenig, S., Folks, T., Willey, R., Rabson, A. and Martin, M.A. (1986) Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J. Virol., 59, 284-291 (Pubitemid 16013975)
37. Clavel, F., Guyader, M., Guetard, D., Salle, M., Montagnier, L. and Alizon, M. (1986) Molecular cloning and polymorphism of the human immune deficiency virus type 2. Nature, 324, 691-695 (Pubitemid 17206364)
38. Ricci, E.P., Limousin, T., Soto-Rifo, R., Allison, R., Poyry, T., Decimo, D., Jackson, R.J. and Ohlmann, T. (2011) Activation of a microRNA response in trans reveals a new role for poly(A) in translational repression. Nucleic Acids Res., 39, 5215-5231
39. Dieterich, K., Soto Rifo, R., Faure, A.K., Hennebicq, S., Ben Amar, B., Zahi, M., Perrin, J., Martinez, D., Sele, B., Jouk, P.S. et al. (2007) Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility. Nat. Genet., 39, 661-665 (Pubitemid 46676111)
40. Soto Rifo, R., Ricci, E.P., Decimo, D., Moncorge, O. and Ohlmann, T. (2007) Back to basics: the untreated rabbit reticulocyte lysate as a competitive system to recapitulate cap/poly(A) synergy and the selective advantage of IRES-driven translation. Nucleic Acids Res., 35, e121
41. Jarrosson-Wuilleme, L., Goujon, C., Bernaud, J., Rigal, D., Darlix, J.L. and Cimarelli, A. (2006) Transduction of nondividing human macrophages with gammaretrovirus-derived vectors. J. Virol., 80, 1152-1159 (Pubitemid 43134072)
42. Cimarelli, A., Sandin, S., Hoglund, S. and Luban, J. (2000) Basic residues in human immunodeficiency virus type 1 nucleocapsid promote virion assembly via interaction with RNA. J. Virol., 74, 3046-3057 (Pubitemid 30143727)
43. Kent, K.A., Gritz, L., Stallard, G., Cranage, M.P., Collignon, C., Thiriart, C., Corcoran, T., Silvera, P. and Stott, E.J. (1991) Production and of monoclonal antibodies to simian immunodeficiency virus envelope glycoproteins. AIDS, 5, 829-836
44. Ricci, E.P., Mure, F., Gruffat, H., Decimo, D., Medina-Palazon, C., Ohlmann, T. and Manet, E. (2009) Translation of intronless RNAs is strongly stimulated by the Epstein-Barr virus mRNA export factor EB2. Nucleic Acids Res., 37, 4932-4943
45. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415 (Pubitemid 37442169)
46. Briggs, J.A., Simon, M.N., Gross, I., Krausslich, H.G., Fuller, S.D., Vogt, V.M. and Johnson, M.C. (2004) The stoichiometry of Gag protein in HIV-1. Nat. Struct. Mol. Biol., 11, 672-675 (Pubitemid 38823535)
47. Tritel, M. and Resh, M.D. (2000) Kinetic analysis of human immunodeficiency virus type 1 assembly reveals the presence of sequential intermediates. J. Virol., 74, 5845-5855 (Pubitemid 30412952)
48. Blaak, H., van der Ende, M.E., Boers, P.H., Schuitemaker, H. and Osterhaus, A.D. (2006) In vitro replication capacity of HIV-2 variants from long-term aviremic individuals. Virology, 353, 144-154 (Pubitemid 44291787)
49. MacNeil, A., Sarr, A.D., Sankale, J.L., Meloni, S.T., Mboup, S. and Kanki, P. (2007) Direct evidence of lower viral replication rates in vivo in human immunodeficiency virus type 2 (HIV-2) infection than in HIV-1 infection. J. Virol., 81, 5325-5330 (Pubitemid 46744441)
50. Hizi, A., Tal, R., Shaharabany, M. and Loya, S. (1991) Catalytic properties of the reverse transcriptases of human immunodeficiency viruses type 1 and type 2. J. Biol. Chem., 266, 6230-6239 (Pubitemid 21906208)
51. Bolinger, C. and Boris-Lawrie, K. (2009) Mechanisms employed by retroviruses to exploit host factors for translational control of a complicated proteome. Retrovirology, 6, 8
52. Dorman, N. and Lever, A. (2000) Comparison of viral genomic RNA sorting mechanisms in human immunodeficiency virus type 1 (HIV-1), HIV-2, and Moloney murine leukemia virus. J. Virol., 74, 11413-11417 (Pubitemid 32224013)
53. Ueno, F., Shiota, H., Miyaura, M., Yoshida, A., Sakurai, A., Tatsuki, J., Koyama, A.H., Akari, H., Adachi, A. and Fujita, M. (2003) Vpx and Vpr proteins of HIV-2 up-regulate the viral infectivity by a distinct mechanism in lymphocytic cells. Microb. Infect., 5, 387-395 (Pubitemid 36549180)
54. Owen, S.M., Ellenberger, D., Rayfield, M., Wiktor, S., Michel, P., Grieco, M.H., Gao, F., Hahn, B.H. and Lal, R.B. (1998) Genetically divergent strains of human immunodeficiency virus type 2 use multiple coreceptors for viral entry. J. Virol., 72, 5425-5432 (Pubitemid 28283323)
55. Babendure, J.R., Babendure, J.L., Ding, J.H. and Tsien, R.Y. (2006) Control of mammalian translation by mRNA structure near caps. RNA, 12, 851-861
56. Kozak, M. (1986) Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc. Natl Acad. Sci. USA, 83, 2850-2854 (Pubitemid 16041760)
57. Kozak, M. (1989) Circumstances and mechanisms of inhibition of translation by secondary structure in eucaryotic mRNAs. Mol. Cell. Biol., 9, 5134-5142 (Pubitemid 19275984)
58. Muesing, M.A., Smith, D.H. and Capon, D.J. (1987) Regulation of mRNA accumulation by a human immunodeficiency virus trans-activator protein. Cell, 48, 691-701 (Pubitemid 18096946)
59. Biegalke, B.J. and Geballe, A.P. (1991) Sequence requirements for activation of the HIV-1 LTR by human cytomegalovirus. Virology, 183, 381-385
60. Chin, D.J., Selby, M.J. and Peterlin, B.M. (1991) Human immunodeficiency virus type 1 Tat does not transactivate mature trans-acting responsive region RNA species in the nucleus or cytoplasm of primate cells. J. Virol., 65, 1758-1764
61. Dorin, D., Bonnet, M.C., Bannwarth, S., Gatignol, A., Meurs, E.F. and Vaquero, C. (2003) The TAR RNA-binding protein, TRBP, stimulates the expression of TAR-containing RNAs in vitro and in vivo independently of its ability to inhibit the dsRNA-dependent kinase PKR. J. Biol. Chem., 278, 4440-4448 (Pubitemid 36800938)
62. Dugre-Brisson, S., Elvira, G., Boulay, K., Chatel-Chaix, L., Mouland, A.J. and DesGroseillers, L. (2005) Interaction of Staufen1 with the 50 end of mRNA facilitates translation of these RNAs. Nucleic Acids Res., 33, 4797-4812 (Pubitemid 41418880)
63. Svitkin, Y.V., Pause, A. and Sonenberg, N. (1994) La autoantigen alleviates translational repression by the 50 leader sequence of the human immunodeficiency virus type 1 mRNA. J. Virol., 68, 7001-7007
64. SenGupta, D.N. and Silverman, R.H. (1989) Activation of interferon-regulated, dsRNA-dependent enzymes by human immunodeficiency virus-1 leader RNA. Nucleic Acids Res., 17, 969-978 (Pubitemid 19062884)
65. Maitra, R.K., McMillan, N.A., Desai, S., McSwiggen, J., Hovanessian, A.G., Sen, G., Williams, B.R. and Silverman, R.H. (1994) HIV-1 TAR RNA has an intrinsic ability to activate interferon-inducible enzymes. Virology, 204, 823-827 (Pubitemid 24330891)
66. Chatterjee, P., Garzino-Demo, A., Swinney, P. and Arya, S.K. (1993) Human immunodeficiency virus type 2 multiply spliced transcripts. AIDS Res. Hum. Retroviruses, 9, 331-335 (Pubitemid 23144056)
67. Strong, C.L., Lanchy, J.M., Dieng-Sarr, A., Kanki, P.J. and Lodmell, J.S. (2009) A 50UTR-spliced mRNA isoform is specialized for enhanced HIV-2 gag translation. J. Mol. Biol., 391, 426-437
68. Yilmaz, A., Bolinger, C. and Boris-Lawrie, K. (2006) Retrovirus translation initiation: Issues and hypotheses derived from study of HIV-1. Curr. HIV Res., 4, 131-139
69. Miele, G., Mouland, A., Harrison, G.P., Cohen, E. and Lever, A.M. (1996) The human immunodeficiency virus type 1 50 packaging signal structure affects translation but does not function as an internal ribosome entry site structure. J. Virol., 70, 944-951
70. Schwartz, S., Felber, B.K. and Pavlakis, G.N. (1992) Mechanism of translation of monocistronic and multicistronic human immunodeficiency virus type 1 mRNAs. Mol. Cell Biol., 12, 207-219
71. Charnay, N., Ivanyi-Nagy, R., Soto-Rifo, R., Ohlmann, T., Lopez-Lastra, M. and Darlix, J.L. (2009) Mechanism of HIV-1 Tat RNA translation and its activation by the Tat protein. Retrovirology, 6, 74
72. Rivas-Aravena, A., Ramdohr, P., Vallejos, M., Valiente-Echeverria, F., Dormoy-Raclet, V., Rodriguez, F., Pino, K., Holzmann, C., Huidobro-Toro, J.P., Gallouzi, I.E. et al. (2009) The Elav-like protein HuR exerts translational control of viral internal ribosome entry sites. Virology, 392, 178-185
73. Griffin, S.D., Allen, J.F. and Lever, A.M. (2001) The major human immunodeficiency virus type 2 (HIV-2) packaging signal is present on all HIV-2 RNA species: cotranslational RNA encapsidation and limitation of Gag protein confer specificity. J. Virol., 75, 12058-12069 (Pubitemid 33115878)
74. Kaye, J.F. and Lever, A.M. (1999) Human immunodeficiency virus types 1 and 2 differ in the predominant mechanism used for selection of genomic RNA for encapsidation. J. Virol., 73, 3023-3031 (Pubitemid 29135691)
75. Centlivre, M., Klaver, B., Berkhout, B. and Das, A.T. (2008) Functional analysis of the complex trans-activating response element RNA structure in simian immunodeficiency virus. J. Virol., 82, 9171-9178.