Functional and structural analysis of the internal ribosome entry site present in the mrna of natural variants of the hiv-1

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Vallejos, Maricarmen ^a   Carvajal, Felipe ^a   Pino, Karla ^a   Navarrete, Camilo ^b   Ferres, Marcela ^b   Huidobro Toro, Juan Pablo ^b   Sargueil, Bruno ^c   López Lastra, Marcelo ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN A1; MESSENGER RNA; UNCLASSIFIED DRUG; VIRUS RNA;

5' UNTRANSLATED REGION; ALTERNATIVE RNA SPLICING; ANIMAL CELL; ARTICLE; CISTRON; CONTROLLED STUDY; HELA CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; PROMOTER REGION; PROTEIN SECONDARY STRUCTURE; RNA CAPPING; STRUCTURE ANALYSIS; TRANSLATION INITIATION; XENOPUS LAEVIS; BIOLOGICAL MODEL; BLOOD; CONFORMATION; HUMAN; METABOLISM; PROTEIN SYNTHESIS; RIBOSOME;

HUMAN IMMUNODEFICIENCY VIRUS 1; XENOPUS LAEVIS;

5' UNTRANSLATED REGIONS; HELA CELLS; HIV-1; HUMANS; MODELS, BIOLOGICAL; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER; RNA, VIRAL;

EID: 84859337769     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035031     Document Type: Article

References (72)

1. Sonenberg N, Hinnebusch AG, (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
2. Lopez-Lastra M, Ramdohr P, Letelier A, Vallejos M, Vera-Otarola J, et al. (2010) Translation initiation of viral mRNAs. Rev Med Virol 20: 177-195.
3. Jackson RJ, Hellen CU, Pestova TV, (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127.
4. Fitzgerald KD, Semler BL, (2009) Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim Biophys Acta 1789: 518-528.
5. Semler BL, Waterman ML, (2008) IRES-mediated pathways to polysomes: nuclear versus cytoplasmic routes. Trends Microbiol 16: 1-5.
6. Berkhout B, (1996) Structure and function of the human immunodeficiency virus leader RNA. Prog Nucleic Acid Res Mol Biol 54: 1-34.
7. Berkhout B, Arts K, Abbink TE, (2011) Ribosomal scanning on the 5′-untranslated region of the human immunodeficiency virus RNA genome. Nucleic Acids Res 39: 5232-5244.
8. Bolinger C, Sharma A, Singh D, Yu L, Boris-Lawrie K, (2010) RNA helicase A modulates translation of HIV-1 and infectivity of progeny virions. Nucleic Acids Res 38: 1686-1696.
9. Ricci EP, Soto Rifo R, Herbreteau CH, Decimo D, Ohlmann T, (2008) Lentiviral RNAs can use different mechanisms for translation initiation. Biochem Soc Trans 36: 690-693.
10. Brasey A, Lopez-Lastra M, Ohlmann T, Beerens N, Berkhout B, et al. (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.
11. Buck CB, Shen X, Egan MA, Pierson TC, Walker CM, et al. (2001) The human immunodeficiency virus type 1 gag gene encodes an internal ribosome entry site. J Virol 75: 181-191.
12. Weill L, James L, Ulryck N, Chamond N, Herbreteau CH, et al. (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.
13. Chamond N, Locker N, Sargueil B, (2011) The different pathways of HIV genomic RNA translation. Biochem Soc Trans 38: 1548-1552.
14. Gendron K, Ferbeyre G, Heveker N, 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.
15. Locker N, Chamond N, 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.
16. Balvay L, Lopez Lastra M, Sargueil B, Darlix JL, Ohlmann T, (2007) Translational control of retroviruses. Nat Rev Microbiol 5: 128-140.
17. Liu J, Henao-Mejia J, Liu H, Zhao Y, He JJ, (2011) Translational regulation of HIV-1 replication by HIV-1 Rev cellular cofactors Sam68, eIF5A, hRIP, and DDX3. J Neuroimmune Pharmacol 6: 308-321.
18. Monette A, Ajamian L, Lopez-Lastra M, Mouland AJ, (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.
19. Rivas-Aravena A, Ramdohr P, Vallejos M, Valiente-Echeverria F, Dormoy-Raclet V, et al. (2009) The Elav-like protein HuR exerts translational control of viral internal ribosome entry sites. Virology 392: 178-185.
20. Vallejos M, Deforges J, Plank TD, Letelier A, Ramdohr P, et al. (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.
21. Baird SD, Turcotte M, Korneluk RG, Holcik M, (2006) Searching for IRES. RNA 12: 1755-1785.
22. Jackson RJ, Hunt SL, Reynolds JE, Kaminski A, (1995) Cap-dependent and cap-independent translation: operational distinctions and mechanistic interpretations. Curr Top Microbiol Immunol 203: 1-29.
23. Vallejos M, Ramdohr P, Valiente-Echeverria F, Tapia K, Rodriguez FE, et al. (2010) The 5'-untranslated region of the mouse mammary tumor virus mRNA exhibits cap-independent translation initiation. Nucleic Acids Res 38: 618-632.
24. Barria MI, Gonzalez A, Vera-Otarola J, Leon U, Vollrath V, et al. (2009) Analysis of natural variants of the hepatitis C virus internal ribosome entry site reveals that primary sequence plays a key role in cap-independent translation. Nucleic Acids Res 37: 957-971.
25. Wilson JE, Powell MJ, Hoover SE, Sarnow P, (2000) Naturally occurring dicistronic cricket paralysis virus RNA is regulated by two internal ribosome entry sites. Mol Cell Biol 20: 4990-4999.
26. Attal J, Theron MC, Taboit F, Cajero-Juarez M, Kann G, et al. (1996) The RU5 ('R') region from human leukaemia viruses (HTLV-1) contains an internal ribosome entry site (IRES)-like sequence. FEBS Lett 392: 220-224.
27. Berlioz C, Darlix JL, (1995) An internal ribosomal entry mechanism promotes translation of murine leukemia virus gag polyprotein precursors. J Virol 69: 2214-2222.
28. Berlioz C, Torrent C, Darlix JL, (1995) An internal ribosomal entry signal in the rat VL30 region of the Harvey murine sarcoma virus leader and its use in dicistronic retroviral vectors. J Virol 69: 6400-6407.
29. Camerini V, Decimo D, Balvay L, Pistello M, Bendinelli M, et al. (2008) A dormant internal ribosome entry site controls translation of feline immunodeficiency virus. J Virol 82: 3574-3583.
30. Charnay N, Ivanyi-Nagy R, Soto-Rifo R, Ohlmann T, Lopez-Lastra M, et al. (2009) Mechanism of HIV-1 Tat RNA translation and its activation by the Tat protein. Retrovirology 6: 74.
31. Deffaud C, Darlix JL, (2000) Rous sarcoma virus translation revisited: characterization of an internal ribosome entry segment in the 5' leader of the genomic RNA. J Virol 74: 11581-11588.
32. Meignin C, Bailly JL, Arnaud F, Dastugue B, Vaury C, (2003) The 5′ untranslated region and gag product of Idefix, a long terminal repeat-retrotransposon from Drosophila melanogaster, act together to initiate a switch between translated and untranslated states of the genomic mRNA. Molecular and Cellular Biology 23: 8246-8254.
33. Vagner S, Waysbort A, Marenda M, Gensac MC, Amalric F, et al. (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.
34. Ronfort C, De Breyne S, Sandrin V, Darlix JL, Ohlmann T, (2004) Characterization of two distinct RNA domains that regulate translation of the Drosophila gypsy retroelement. RNA 10: 504-515.
35. Lopez-Lastra M, Gabus C, Darlix JL, (1997) Characterization of an internal ribosomal entry segment within the 5′ leader of avian reticuloendotheliosis virus type A RNA and development of novel MLV-REV-based retroviral vectors. Hum Gene Ther 8: 1855-1865.
36. Lopez-Lastra M, Ulrici S, Gabus C, Darlix JL, (1999) Identification of an internal ribosome entry segment in the 5′ region of the mouse VL30 retrotransposon and its use in the development of retroviral vectors. J Virol 73: 8393-8402.
37. Ohlmann T, Lopez-Lastra M, Darlix JL, (2000) An internal ribosome entry segment promotes translation of the simian immunodeficiency virus genomic RNA. J Biol Chem 275: 11899-11906.
38. Han B, Zhang JT, (2002) Regulation of gene expression by internal ribosome entry sites or cryptic promoters: the eIF4G story. Mol Cell Biol 22: 7372-7384.
39. Kozak M, (2003) Alternative ways to think about mRNA sequences and proteins that appear to promote internal initiation of translation. Gene 318: 1-23.
40. Herbreteau CH, Weill L, Decimo D, Prevot D, Darlix JL, et al. (2005) HIV-2 genomic RNA contains a novel type of IRES located downstream of its initiation codon. Nat Struct Mol Biol 12: 1001-1007.
41. Kazadi K, Loeuillet C, Deutsch S, Ciuffi A, Munoz M, et al. (2008) Genomic determinants of the efficiency of internal ribosomal entry sites of viral and cellular origin. Nucleic Acids Res 36: 6918-6925.
42. Silvera D, Arju R, Darvishian F, Levine PH, Zolfaghari L, et al. (2009) Essential role for eIF4GI overexpression in the pathogenesis of inflammatory breast cancer. Nat Cell Biol 11: 903-908.
43. Gamarnik AV, Andino R, (1996) Replication of poliovirus in Xenopus oocytes requires two human factors. Embo J 15: 5988-5998.
44. Keiper BD, Rhoads RE, (1997) Cap-independent translation initiation in Xenopus oocytes. Nucleic Acids Res 25: 395-402.
45. Vopalensky V, Masek T, Horvath O, Vicenova B, Mokrejs M, et al. (2008) Firefly luciferase gene contains a cryptic promoter. RNA 14: 1720-1729.
46. Kieft JS, (2008) Viral IRES RNA structures and ribosome interactions. Trends Biochem Sci 33: 274-283.
47. Pfingsten JS, Costantino DA, Kieft JS, (2006) Structural basis for ribosome recruitment and manipulation by a viral IRES RNA. Science 314: 1450-1454.
48. James L, Sargueil B, (2008) RNA secondary structure of the feline immunodeficiency virus 5′UTR and Gag coding region. Nucleic Acids Res 36: 4653-4666.
49. Damgaard CK, Andersen ES, Knudsen B, Gorodkin J, Kjems J, (2004) RNA interactions in the 5′ region of the HIV-1 genome. J Mol Biol 336: 369-379.
50. Paillart JC, Dettenhofer M, Yu XF, Ehresmann C, Ehresmann B, et al. (2004) First snapshots of the HIV-1 RNA structure in infected cells and in virions. J Biol Chem 279: 48397-48403.
51. Wilkinson KA, Gorelick RJ, Vasa SM, Guex N, Rein A, et al. (2008) High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states. PLoS Biol 6: e96.
52. Cochrane A, (2009) How does the journey affect the message(RNA)? RNA Biol 6: 169-170.
53. Cochrane AW, McNally MT, Mouland AJ, (2006) The retrovirus RNA trafficking granule: from birth to maturity. Retrovirology 3: 18.
54. Ooms M, Huthoff H, Russell R, Liang C, Berkhout B, (2004) A riboswitch regulates RNA dimerization and packaging in human immunodeficiency virus type 1 virions. J Virol 78: 10814-10819.
55. Lopez-Lastra M, Rivas A, Barria MI, (2005) Protein synthesis in eukaryotes: the growing biological relevance of cap-independent translation initiation. Biol Res 38: 121-146.
56. Belsham GJ, Sonenberg N, (2000) Picornavirus RNA translation: roles for cellular proteins. Trends Microbiol 8: 330-335.
57. Berkhout B, Arts K, Abbink TE, (2011) Ribosomal scanning on the 5′-untranslated region of the human immunodeficiency virus RNA genome. Nucleic Acids Res In Press.
58. Yedavalli VS, Jeang KT, (2010) Trimethylguanosine capping selectively promotes expression of Rev-dependent HIV-1 RNAs. Proc Natl Acad Sci U S A 107: 14787-14792.
59. Darzynkiewicz E, Stepinski J, Ekiel I, Jin Y, Haber D, et al. (1988) Beta-globin mRNAs capped with m7G, m2.7(2)G or m2.2.7(3)G differ in intrinsic translation efficiency. Nucleic Acids Res 16: 8953-8962.
60. Cai A, Jankowska-Anyszka M, Centers A, Chlebicka L, Stepinski J, et al. (1999) Quantitative assessment of mRNA cap analogues as inhibitors of in vitro translation. Biochemistry 38: 8538-8547.
61. Carberry SE, Darzynkiewicz E, Stepinski J, Tahara SM, Rhoads RE, et al. (1990) A spectroscopic study of the binding of N-7-substituted cap analogues to human protein synthesis initiation factor 4E. Biochemistry 29: 3337-3341.
62. Carberry SE, Rhoads RE, Goss DJ, (1989) A spectroscopic study of the binding of m7GTP and m7GpppG to human protein synthesis initiation factor 4E. Biochemistry 28: 8078-8083.
63. Rutkowska-Wlodarczyk I, Stepinski J, Dadlez M, Darzynkiewicz E, Stolarski R, et al. (2008) Structural changes of eIF4E upon binding to the mRNA 5′ monomethylguanosine and trimethylguanosine Cap. Biochemistry 47: 2710-2720.
64. Ventoso I, Blanco R, Perales C, Carrasco L, (2001) HIV-1 protease cleaves eukaryotic initiation factor 4G and inhibits cap-dependent translation. Proc Natl Acad Sci U S A 98: 12966-12971.
65. Ohlmann T, Prevot D, Decimo D, Roux F, Garin J, et al. (2002) In vitro cleavage of eIF4GI but not eIF4GII by HIV-1 protease and its effects on translation in the rabbit reticulocyte lysate system. J Mol Biol 318: 9-20.
66. Perales C, Carrasco L, Ventoso I, (2003) Cleavage of eIF4G by HIV-1 protease: effects on translation. FEBS Lett 533: 89-94.
67. Thierry S, Marechal V, Rosenzwajg M, Sabbah M, Redeuilh G, et al. (2004) Cell cycle arrest in G2 induces human immunodeficiency virus type 1 transcriptional activation through histone acetylation and recruitment of CBP, NF-kappaB, and c-Jun to the long terminal repeat promoter. J Virol 78: 12198-12206.
68. Alvarez E, Castello A, Menendez-Arias L, Carrasco L, (2006) HIV protease cleaves poly(A)-binding protein. Biochem J 396: 219-226.
69. Castello A, Franco D, Moral-Lopez P, Berlanga JJ, Alvarez E, et al. (2009) HIV- 1 protease inhibits Cap- and poly(A)-dependent translation upon eIF4GI and PABP cleavage. PLoS One 4: e7997.
70. Acuna-Castillo C, Villalobos C, Moya PR, Saez P, Cassels BK, et al. (2002) Differences in potency and efficacy of a series of phenylisopropylamine/phenylethylamine pairs at 5-HT(2A) and 5-HT(2C) receptors. Br J Pharmacol 136: 510-519.
71. Altafaj X, Joux N, Ronjat M, De Waard M, (2006) Oocyte expression with injection of purified T7 RNA polymerase. Methods Mol Biol 322: 55-67.
72. Gamarnik AV, Andino R, (2006) Exploring RNA virus replication in Xenopus oocytes. Methods Mol Biol 322: 367-378.