The activity of the HIV-1 IRES is stimulated by oxidative stress and controlled by a negative regulatory element

Nucleic Acids Research

Volumn 39, Issue 3, 2011, Pages 902-912

  Gendron, Karine ^a,b   Ferbeyre, Gerardo ^a   Heveker, Nikolaus ^a,b   Brakier Gingras, Léa ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

FIREFLY LUCIFERASE; RENILLA LUCIFERIN 2 MONOOXYGENASE;

ARTICLE; BINDING SITE; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERNAL RIBOSOME ENTRY SITE; LEUKEMIA CELL LINE; MUTATIONAL ANALYSIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REGULATORY SEQUENCE; RNA CAPPING; RNA TRANSLATION; WILD TYPE;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; HIV-1; HUMANS; JURKAT CELLS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; OXIDATIVE STRESS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA, VIRAL; SEQUENCE DELETION;

HUMAN IMMUNODEFICIENCY VIRUS 1; RENILLA LUCIFERASE;

EID: 79951568140     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq885     Document Type: Article

References (61)

1. Pestova, T.V., Lorsh, J.R. and Hellen, C.U.T. (2007) In Mathews, M.B., Sonenberg, N. and Hershey, J.W.B. (eds), Translational Control in Biology and Medicine. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 87-128.
2. Sonenberg, N. and Hinnebusch, A.G. (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell, 136, 731-745.
3. 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.
4. Lopez-Lastra, M., Rivas, A. and Barria, M.I. (2005) Protein synthesis in eukaryotes: the growing biological relevance of cap-independent translation initiation. Biol. Res., 38, 121-146. (Pubitemid 41535614)
5. Martinez-Salas, E., Pacheco, A., Serrano, P. and Fernandez, N. (2008) New insights into internal ribosome entry site elements relevant for viral gene expression. J. Gen. Virol., 89, 611-626.
6. Jackson, R.J. (2005) Alternative mechanisms of initiating translation of mammalian mRNAs. Biochem. Soc. Trans., 33, 1231-1241. (Pubitemid 41779656)
7. Doudna, J. and Sarnow, P. (2007) Translation initiation by viral internal ribosome entry sites. In Hershey, J.W., Mathews, M.B. and Sonenberg, N. (eds), Translational control in Biology and Medicine. CSH Press, New York, pp. 129-153.
8. Hellen, C.U. (2009) IRES-induced conformational changes in the ribosome and the mechanism of translation initiation by internal ribosomal entry. Biochim. Biophys. Acta, 1789, 558-570.
9. Filbin, M.E. and Kieft, J.S. (2009) Toward a structural understanding of IRES RNA function. Curr. Opin. Struct. Biol., 19, 267-276.
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. Fitzgerald, K.D. and Semler, B.L. (2009) Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim. Biophys. Acta, 1789, 518-528.
12. 0 nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol., 62, 2636-2643.
13. 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.
14. 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.
15. Ohlmann, T., Lopez-Lastra, M. and Darlix, J.L. (2000) An internal ribosome entry segment promotes translation of the simian immunodeficiency virus genomic RNA. J. Biol. Chem., 275, 11899-11906. (Pubitemid 30237759)
16. Nicholson, M.G., Rue, S.M., Clements, J.E. and Barber, S.A. (2006) An internal ribosome entry site promotes translation of a novel SIV Pr55(Gag) isoform. Virology, 349, 325-334. (Pubitemid 43782880)
17. 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.
18. 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)
19. 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.
20. 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.
21. Vagner, S., Waysbort, A., Marenda, M., Gensac, M.C., Amalric, F. and Prats, A.C. (1995) Alternative translation initiation of the Moloney murine leukemia virus mRNA controlled by internal ribosome entry involving the p57/PTB splicing factor. J. Biol. Chem., 270, 20376-20383.
22. Berlioz, C. and Darlix, J.L. (1995) An internal ribosomal entry mechanism promotes translation of murine leukemia virus gag polyprotein precursors. J. Virol., 69, 2214-2222.
23. 0 leader of the genomic RNA. J. Virol., 74, 11581-11588. (Pubitemid 32223517)
24. Camerini, V., Decimo, D., Balvay, L., Pistello, M., Bendinelli, M., Darlix, J.L. and Ohlmann, T. (2008) A dormant internal ribosome entry site controls translation of feline immunodeficiency virus. J. Virol., 82, 3574-3583. (Pubitemid 351429933)
25. Vallejos, M., Ramdohr, P., Valiente-Echeverria, F., Tapia, K., Rodriguez, F.E., Lowy, F., Huidobro-Toro, J.P., Dangerfield, J.A. and Lopez-Lastra, M. (2010) The 5'-untranslated region of the mouse mammary tumor virus mRNA exhibits cap-independent translation initiation. Nucleic Acids Res., 38, 618-632.
26. Brierley, I. and Dos Ramos, F.J. (2006) Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV. Virus Res., 119, 29-42. (Pubitemid 43765977)
27. Brakier-Gingras, L. and Dulude, D. (2010) Programmed -1 ribosomal frameshift in the human immunodeficiency virus of type 1. In Atkins, J. and Gesteland, R. (eds), Recoding: Expansion of Decoding Rules Enriches Gene Expression. Springer, New York, pp. 175-192.
28. Balvay, L., Lopez Lastra, M., Sargueil, B., Darlix, J.L. and Ohlmann, T. (2007) Translational control of retroviruses. Nat. Rev. Microbiol., 5, 128-140. (Pubitemid 46151871)
29. 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.
30. Berkhout, B. (1996) Structure and function of the human immunodeficiency virus leader RNA. Prog. Nucleic Acid Res. Mol. Biol., 54, 1-34.
31. 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.
32. Huthoff, H. and Berkhout, B. (2001) Two alternating structures of the HIV-1 leader RNA. RNA, 7, 143-157. (Pubitemid 32381937)
33. 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.
34. 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)
35. Ricci, E.P., Soto Rifo, R., Herbreteau, C.H., Decimo, D. and Ohlmann, T. (2008) Lentiviral RNAs can use different mechanisms for translation initiation. Biochem. Soc. Trans., 36, 690-693.
36. 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.
37. 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.
38. 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.
39. Waysbort, A., Bonnal, S., Audigier, S., Esteve, J.P. and Prats, A.C. (2001) Pyrimidine tract binding protein and La autoantigen interact differently with the 5' untranslated regions of lentiviruses and oncoretrovirus mRNAs. FEBS Lett., 490, 54-58. (Pubitemid 32126643)
40. Chang, Y.N., Kenan, D.J., Keene, J.D., Gatignol, A. and Jeang, K.T. (1994) Direct interactions between autoantigen La and human immunodeficiency virus leader RNA. J. Virol., 68, 7008-7020. (Pubitemid 24328751)
41. Davy, C. and Doorbar, J. (2007) G2/M cell cycle arrest in the life cycle of viruses. Virology, 368, 219-226. (Pubitemid 350016216)
42. Andersen, J.L. and Planelles, V. (2005) The role of Vpr in HIV-1 pathogenesis. Curr. HIV Res., 3, 43-51. (Pubitemid 40081284)
43. Castello, A., Franco, D., Moral-Lopez, P., Berlanga, J.J., Alvarez, E., Wimmer, E. and Carrasco, L. (2009) HIV- 1 protease inhibits Cap-and poly(A)-dependent translation upon eIF4GI and PABP cleavage. PLoS One, 4, e7997.
44. Pyo, C.W., Lee, S.H. and Choi, S.Y. (2008) Oxidative stress induces PKR-dependent apoptosis via IFN-gamma activation signaling in Jurkat T cells. Biochem. Biophys. Res. Commun., 377, 1001-1006.
45. Deshmane, S.L., Mukerjee, R., Fan, S., Del Valle, L., Michiels, C., Sweet, T., Rom, I., Khalili, K., Rappaport, J., Amini, S. et al. (2009) Activation of the oxidative stress pathway by HIV-1 Vpr leads to induction of hypoxia-inducible factor 1alpha expression. J. Biol. Chem., 284, 11364-11373.
46. Lindl, K.A., Akay, C., Wang, Y., White, M.G. and Jordan-Sciutto, K.L. (2007) Expression of the endoplasmic reticulum stress response marker, BiP, in the central nervous system of HIV-positive individuals. Neuropathol. Appl. Neurobiol., 33, 658-669. (Pubitemid 350076089)
47. Peruzzi, F. (2006) The multiple functions of HIV-1 Tat: proliferation versus apoptosis. Front Biosci., 11, 708-717. (Pubitemid 43258174)
48. Peden, K., Emerman, M. and Montagnier, L. (1991) Changes in growth properties on passage in tissue culture of viruses derived from infectious molecular clones of HIV-1LAI, HIV-1MAL, and HIV-1ELI. Virology, 185, 661-672.
49. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K. and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene, 77, 51-59. (Pubitemid 19125653)
50. Venkatesan, A., Sharma, R. and Dasgupta, A. (2003) Cell cycle regulation of hepatitis C and encephalomyocarditis virus internal ribosome entry site-mediated translation in human embryonic kidney 293 cells. Virus Res., 94, 85-95. (Pubitemid 36930032)
51. Van Eden, M.E., Byrd, M.P., Sherrill, K.W. and Lloyd, R.E. (2004) Demonstrating internal ribosome entry sites in eukaryotic mRNAs using stringent RNA test procedures. RNA, 10, 720-730. (Pubitemid 38405950)
52. Borman, A.M., Le Mercier, P., Girard, M. and Kean, K.M. (1997) Comparison of picornaviral IRES-driven internal initiation of translation in cultured cells of different origins. Nucleic Acids Res., 25, 925-932. (Pubitemid 27298259)
53. Holcik, M. and Sonenberg, N. (2005) Translational control in stress and apoptosis. Nat. Rev. Mol. Cell Biol., 6, 318-327. (Pubitemid 40516898)
54. Loening, A.M., Fenn, T.D., Wu, A.M. and Gambhir, S.S. (2006) Consensus guided mutagenesis of Renilla luciferase yields enhanced stability and light output. Protein Eng. Des. Sel., 19, 391-400. (Pubitemid 44306057)
55. Abbink, T.E., Ooms, M., Haasnoot, P.C. and Berkhout, B. (2005) The HIV-1 leader RNA conformational switch regulates RNA dimerization but does not regulate mRNA translation. Biochemistry, 44, 9058-9066. (Pubitemid 40943220)
56. Martinez-Salas, E., Saiz, J.C., Davila, M., Belsham, G.J. and Domingo, E. (1993) A single nucleotide substitution in the internal ribosome entry site of foot-and-mouth disease virus leads to enhanced cap-independent translation in vivo. J. Virol., 67, 3748-3755. (Pubitemid 23180695)
57. Chappell, S.A., LeQuesne, J.P., Paulin, F.E., deSchoolmeester, M.L., Stoneley, M., Soutar, R.L., Ralston, S.H., Helfrich, M.H. and Willis, A.E. (2000) A mutation in the c-myc-IRES leads to enhanced internal ribosome entry in multiple myeloma: a novel mechanism of oncogene de-regulation. Oncogene, 19, 4437-4440.
58. Baek, D., Villen, J., Shin, C., Camargo, F.D., Gygi, S.P. and Bartel, D.P. (2008) The impact of microRNAs on protein output. Nature, 455, 64-71.
59. Selbach, M., Schwanhausser, B., Thierfelder, N., Fang, Z., Khanin, R. and Rajewsky, N. (2008) Widespread changes in protein synthesis induced by microRNAs. Nature, 455, 58-63.
60. Mathews, D.H., Sabina, J., Zuker, M. and Turner, D.H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol., 288, 911-940. (Pubitemid 29248642)
61. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415. (Pubitemid 37442169)