Cell type specificity and structural determinants of IRES activity from the 5′ leaders of different HIV-1 transcripts

Nucleic Acids Research

Volumn 41, Issue 13, 2013, Pages 6698-6714

  Plank, Terra Dawn M ^a   Whitehurst, James T ^a   Kieft, Jeffrey S ^a,b  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA;

ALTERNATIVE RNA SPLICING; ARTICLE; CELL CYCLE G2 PHASE; CELL DIFFERENTIATION; CELL STRAIN HEK293; CELL TYPE; CONTROLLED STUDY; EXON; HELA CELL; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERNAL RIBOSOME ENTRY SITE; LEUKEMIA CELL LINE; MONOCYTE MACROPHAGE PRECURSOR CELL; MUTAGENESIS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RNA SEQUENCE; RNA SPLICING; RNA STRUCTURE; T LYMPHOCYTE; TRANSLATION INITIATION;

5' UNTRANSLATED REGIONS; ALTERNATIVE SPLICING; CELL LINE; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; HUMANS; JURKAT CELLS; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; RNA SPLICE SITES; RNA, MESSENGER; RNA, VIRAL;

EID: 84879804212     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt358     Document Type: Article

References (55)

1. 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)
2. Berkhout, B. (1996) Structure and function of the human immunodeficiency virus leader RNA. Prog. Nucleic Acid. Res. Mol. Biol., 54, 1-34.
3. Parkin, N.T., Cohen, E.A., Darveau, A., Rosen, C., Haseltine, W. and Sonenberg, N. (1988) Mutational analysis of the 5' non-coding region of human immunodeficiency virus type 1: effects of secondary structure on translation. EMBO J., 7, 2831-2837.
4. Jowett, J.B., Planelles, V., Poon, B., Shah, N.P., Chen, M.L. and Chen, I.S. (1995) The human immunodeficiency virus type 1 vpr gene arrests infected T cells in the G2 + M phase of the cell cycle. J. Virol., 69, 6304-6313.
5. 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.
6. 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.
7. Jackson, R.J. (2005) Alternative mechanisms of initiating translation of mammalian mRNAs. Biochem. Soc. Trans., 33, 1231-1241. (Pubitemid 41779656)
8. Komar, A.A. and Hatzoglou, M. (2011) Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle, 10, 229-240.
9. de Breyne, S., Soto-Rifo, R., Lopez-Lastra, M. and Ohlmann, T. (2013) Translation initiation is driven by different mechanisms on the HIV-1 and HIV-2 genomic RNAs. Virus Res., 171, 366-381.
10. Miele, G., Mouland, A., Harrison, G.P., Cohen, E. and Lever, A.M. (1996) The human immunodeficiency virus type 1 5' packaging signal structure affects translation but does not function as an internal ribosome entry site structure. J. Virol., 70, 944-951.
11. Berkhout, B., Arts, K. and Abbink, T.E. (2011) Ribosomal scanning on the 5'-untranslated region of the human immunodeficiency virus RNA genome. Nucleic Acids Res., 39, 5232-5244.
12. Soto-Rifo, R., Rubilar, P.S., Limousin, T., de Breyne, S., Decimo, D. and Ohlmann, T. (2012) DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs. EMBO J., 31, 3745-3756.
13. Soto-Rifo, R., Limousin, T., Rubilar, P.S., Ricci, E.P., Decimo, D., Moncorge, O., Trabaud, M.A., Andre, P., Cimarelli, A. and Ohlmann, T. (2012) Different effects of the TAR structure on HIV-1 and HIV-2 genomic RNA translation. Nucleic Acids Res., 40, 2653-2667.
14. 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)
15. Vallejos, M., Deforges, J., Plank, T.D., Letelier, A., Ramdohr, P., Abraham, C.G., Valiente-Echeverria, F., Kieft, J.S., Sargueil, B. and Lopez-Lastra, M. (2011) Activity of the human immunodeficiency virus type 1 cell cycle-dependent internal ribosomal entry site is modulated by IRES trans-acting factors. Nucleic Acids Res., 39, 6186-6200.
16. 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.
17. 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.
18. 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.
19. Purcell, D.F. and Martin, M.A. (1993) Alternative splicing of human immunodeficiency virus type 1 mRNA modulates viral protein expression, replication, and infectivity. J. Virol., 67, 6365-6378. (Pubitemid 23309100)
20. 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.
21. Stoneley, M., Paulin, F.E., Le Quesne, J.P., Chappell, S.A. and Willis, A.E. (1998) C-Myc 5' untranslated region contains an internal ribosome entry segment. Oncogene, 16, 423-428. (Pubitemid 28052297)
22. Filbin, M.E. and Kieft, J.S. (2011) HCV IRES domain IIb affects the configuration of coding RNA in the 40S subunit's decoding groove. RNA, 17, 1258-1273.
23. Kieft, J.S., Zhou, K., Jubin, R., Murray, M.G., Lau, J.Y. and Doudna, J.A. (1999) The hepatitis C virus internal ribosome entry site adopts an ion-dependent tertiary fold. J. Mol. Biol., 292, 513-529. (Pubitemid 29457315)
24. Kieft, J.S., Costantino, D.A., Filbin, M.E., Hammond, J. and Pfingsten, J.S. (2007) Structural methods for studying IRES function. Methods Enzymol., 430, 333-371.
25. 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.
26. Veo, B.L. and Krushel, L.A. (2009) Translation initiation of the human tau mRNA through an internal ribosomal entry site. J. Alzheimers Dis., 16, 271-275.
27. Johannes, G., Carter, M.S., Eisen, M.B., Brown, P.O. and Sarnow, P. (1999) Identification of eukaryotic mRNAs that are translated at reduced cap binding complex eIF4F concentrations using a cDNA microarray. Proc. Natl Acad. Sci. USA, 96, 13118-13123.
28. Chen, C.Y. and Sarnow, P. (1995) Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science, 268, 415-417.
29. Lu, K., Heng, X., Garyu, L., Monti, S., Garcia, E.L., Kharytonchyk, S., Dorjsuren, B., Kulandaivel, G., Jones, S., Hiremath, A. et al. (2011) NMR detection of structures in the HIV-1 5'-leader RNA that regulate genome packaging. Science, 334, 242-245.
30. 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.
31. de Breyne, S., Chamond, N., Decimo, D., Trabaud, M.A., Andre, P., Sargueil, B. and Ohlmann, T. (2012) In vitro studies reveal that different modes of initiation on HIV-1 mRNA have different levels of requirement for eukaryotic initiation factor 4F. FEBS J., 279, 3098-3111.
32. Valiente-Echeverria, F., Vallejos, M., Monette, A., Pino, K., Letelier, A., Huidobro-Toro, J.P., Mouland, A.J. and Lopez-Lastra, M. (2013) A cis-acting element present within the Gag open reading frame negatively impacts on the activity of the HIV-1 IRES. PLoS One, 8, e56962.
33. Kieft, J.S., Zhou, K., Jubin, R. and Doudna, J.A. (2001) Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA, 7, 194-206. (Pubitemid 33590503)
34. Kolupaeva, V.G., Pestova, T.V. and Hellen, C.U. (2000) An enzymatic footprinting analysis of the interaction of 40S ribosomal subunits with the internal ribosomal entry site of hepatitis C virus. J. Virol., 74, 6242-6250. (Pubitemid 30429788)
35. Jan, E. and Sarnow, P. (2002) Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J. Mol. Biol., 324, 889-902. (Pubitemid 41782981)
36. Nishiyama, T., Yamamoto, H., Shibuya, N., Hatakeyama, Y., Hachimori, A., Uchiumi, T. and Nakashima, N. (2003) Structural elements in the internal ribosome entry site of Plautia stali intestine virus responsible for binding with ribosomes. Nucleic Acids Res., 31, 2434-2442. (Pubitemid 37442112)
37. Lu, K., Heng, X. and Summers, M.F. (2011) Structural determinants and mechanism of HIV-1 genome packaging. J. Mol. Biol., 410, 609-633.
38. Cheong, C., Varani, G. and Tinoco, I. Jr (1990) Solution structure of an unusually stable RNA hairpin, 5'GGAC(UUCG)GUCC. Nature, 346, 680-682.
39. Tuerk, C., Gauss, P., Thermes, C., Groebe, D.R., Gayle, M., Guild, N., Stormo, G., d'Aubenton-Carafa, Y., Uhlenbeck, O.C., Tinoco, I. Jr et al. (1988) CUUCGG hairpins: extraordinarily stable RNA secondary structures associated with various biochemical processes. Proc. Natl Acad. Sci. USA, 85, 1364-1368.
40. Jubin, R., Vantuno, N.E., Kieft, J.S., Murray, M.G., Doudna, J.A., Lau, J.Y. and Baroudy, B.M. (2000) Hepatitis C virus internal ribosome entry site (IRES) stem loop IIId contains a phylogenetically conserved GGG triplet essential for translation and IRES folding. J. Virol., 74, 10430-10437.
41. Kieft, J.S., Zhou, K., Jubin, R., Murray, M.G., Lau, J.Y. and Doudna, J.A. (1999) The hepatitis C virus internal ribosome entry site adopts an ion-dependent tertiary fold. J. Mol. Biol., 292, 513-529. (Pubitemid 29457315)
42. Filbin, M.E. and Kieft, J.S. (2009) Toward a structural understanding of IRES RNA function. Curr. Opin. Struct. Biol., 19, 267-276.
43. Plank, T.D. and Kieft, J.S. (2012) The structures of nonprotein-coding RNAs that drive internal ribosome entry site function. Wiley Interdiscip. Rev. RNA, 3, 195-212.
44. Pickering, B.M., Mitchell, S.A., Spriggs, K.A., Stoneley, M. and Willis, A.E. (2004) Bag-1 internal ribosome entry segment activity is promoted by structural changes mediated by poly(rC) binding protein 1 and recruitment of polypyrimidine tract binding protein 1. Mol. Cell Biol., 24, 5595-5605. (Pubitemid 38738189)
45. Mitchell, S.A., Spriggs, K.A., Coldwell, M.J., Jackson, R.J. and Willis, A.E. (2003) The Apaf-1 internal ribosome entry segment attains the correct structural conformation for function via interactions with PTB and unr. Mol. Cell, 11, 757-771. (Pubitemid 36385128)
46. Kafasla, P., Morgner, N., Poyry, T.A., Curry, S., Robinson, C.V. and Jackson, R.J. (2009) Polypyrimidine tract binding protein stabilizes the encephalomyocarditis virus IRES structure via binding multiple sites in a unique orientation. Mol. Cell, 34, 556-568.
47. Konig, R., Zhou, Y., Elleder, D., Diamond, T.L., Bonamy, G.M., Irelan, J.T., Chiang, C.Y., Tu, B.P., De Jesus, P.D., Lilley, C.E. et al. (2008) Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell, 135, 49-60.
48. Yeung, M.L., Houzet, L., Yedavalli, V.S. and Jeang, K.T. (2009) A genome-wide short hairpin RNA screening of jurkat T-cells for human proteins contributing to productive HIV-1 replication. J. Biol. Chem., 284, 19463-19473.
49. Zhou, H., Xu, M., Huang, Q., Gates, A.T., Zhang, X.D., Castle, J.C., Stec, E., Ferrer, M., Strulovici, B., Hazuda, D.J. et al. (2008) Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe., 4, 495-504.
50. Brass, A.L., Dykxhoorn, D.M., Benita, Y., Yan, N., Engelman, A., Xavier, R.J., Lieberman, J. and Elledge, S.J. (2008) Identification of host proteins required for HIV infection through a functional genomic screen. Science, 319, 921-926. (Pubitemid 351263756)
51. Jager, S., Cimermancic, P., Gulbahce, N., Johnson, J.R., McGovern, K.E., Clarke, S.C., Shales, M., Mercenne, G., Pache, L., Li, K. et al. (2012) Global landscape of HIV-human protein complexes. Nature, 481, 365-370.
52. Stoneley, M., Subkhankulova, T., Le Quesne, J.P., Coldwell, M.J., Jopling, C.L., Belsham, G.J. and Willis, A.E. (2000) Analysis of the c-myc IRES; a potential role for cell-type specific trans-acting factors and the nuclear compartment. Nucleic Acids Res., 28, 687-694. (Pubitemid 30068251)
53. Jopling, C.L. and Willis, A.E. (2001) N-myc translation is initiated via an internal ribosome entry segment that displays enhanced activity in neuronal cells. Oncogene, 20, 2664-2670. (Pubitemid 32525297)
54. Timmerman, S.L., Pfingsten, J.S., Kieft, J.S. and Krushel, L.A. (2008) The 5' leader of the mRNA encoding the mouse neurotrophin receptor TrkB contains two internal ribosomal entry sites that are differentially regulated. PLoS One, 3, e3242.
55. Yu, Y., Abaeva, I.S., Marintchev, A., Pestova, T.V. and Hellen, C.U. (2011) Common conformational changes induced in type 2 picornavirus IRESs by cognate trans-acting factors. Nucleic Acids Res., 39, 4851-4865.