A cis-Acting Element Present within the gag Open Reading Frame Negatively Impacts on the Activity of the HIV-1 IRES

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Valiente Echeverría, Fernando ^a   Vallejos, Maricarmen ^a   Monette, Anne ^b,c   Pino, Karla ^a   Letelier, Alejandro ^a   Huidobro Toro, J Pablo ^d   Mouland, Andrew J ^b,c   López Lastra, Marcelo ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b MCGILL UNIVERSITY   (Canada)

^c MCGILL UNIVERSITY   (Canada)

^d PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; GAG PROTEIN; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MESSENGER RNA; PROTEIN HNRNPA1; PROTEIN INS 1; REV PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IN VITRO STUDY; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; TRANSLATION INITIATION;

GENES, GAG; HELA CELLS; HIV-1; HUMANS; IMMUNOBLOTTING; OPEN READING FRAMES; REGULATORY SEQUENCES, NUCLEIC ACID; REV GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84874518208     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0056962     Document Type: Article

References (64)

1. 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.
2. Sonenberg N, Hinnebusch AG, (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
3. Kieft JS, (2008) Viral IRES RNA structures and ribosome interactions. Trends Biochem Sci 33: 274-283.
4. Balvay L, Lopez Lastra M, Sargueil B, Darlix JL, Ohlmann T, (2007) Translational control of retroviruses. Nat Rev Microbiol 5: 128-140.
5. de Breyne S, Soto-Rifo R, Lopez-Lastra M, Ohlmann T (2012) Translation initiation is driven by different mechanisms on the HIV-1 and HIV-2 genomic RNAs. Virus Res (in press).
6. 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.
7. 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.
8. 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.
9. Holcik M, Sonenberg N, (2005) Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6: 318-327.
10. Monette A, Pante N, Mouland AJ, (2011) HIV-1 remodels the nuclear pore complex. J Cell Biol 193: 619-631.
11. 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.
12. Alvarez E, Castello A, Menendez-Arias L, Carrasco L, (2006) HIV protease cleaves poly(A)-binding protein. Biochem J 396: 219-226.
13. 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.
14. 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.
15. Perales C, Carrasco L, Ventoso I, (2003) Cleavage of eIF4G by HIV-1 protease: effects on translation. FEBS Lett 533: 89-94.
16. 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.
17. 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.
18. 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.
19. Cochrane AW, Jones KS, Beidas S, Dillon PJ, Skalka AM, et al. (1991) Identification and characterization of intragenic sequences which repress human immunodeficiency virus structural gene expression. J Virol 65: 5305-5313.
20. Hadzopoulou-Cladaras M, Felber BK, Cladaras C, Athanassopoulos A, Tse A, et al. (1989) The rev (trs/art) protein of human immunodeficiency virus type 1 affects viral mRNA and protein expression via a cis-acting sequence in the env region. J Virol 63: 1265-1274.
21. Maldarelli F, Martin MA, Strebel K, (1991) Identification of posttranscriptionally active inhibitory sequences in human immunodeficiency virus type 1 RNA: novel level of gene regulation. J Virol 65: 5732-5743.
22. Huffman KM, Arrigo SJ, (1997) Identification of cis-acting repressor activity within human immunodeficiency virus type 1 protease sequences. Virology 234: 253-260.
23. Schwartz S, Felber BK, Pavlakis GN, (1992) Distinct RNA sequences in the gag region of human immunodeficiency virus type 1 decrease RNA stability and inhibit expression in the absence of Rev protein. J Virol 66: 150-159.
24. Wolff H, Brack-Werner R, Neumann M, Werner T, Schneider R, (2003) Integrated functional and bioinformatics approach for the identification and experimental verification of RNA signals: application to HIV-1 INS. Nucleic Acids Res 31: 2839-2851.
25. Afonina E, Neumann M, Pavlakis GN, (1997) Preferential binding of poly(A)-binding protein 1 to an inhibitory RNA element in the human immunodeficiency virus type 1 gag mRNA. J Biol Chem 272: 2307-2311.
26. Black AC, Luo J, Chun S, Bakker A, Fraser JK, et al. (1996) Specific binding of polypyrimidine tract binding protein and hnRNP A1 to HIV-1 CRS elements. Virus Genes 12: 275-285.
27. Olsen HS, Cochrane AW, Rosen C, (1992) Interaction of cellular factors with intragenic cis-acting repressive sequences within the HIV genome. Virology 191: 709-715.
28. Zolotukhin AS, Michalowski D, Bear J, Smulevitch SV, Traish AM, et al. (2003) PSF acts through the human immunodeficiency virus type 1 mRNA instability elements to regulate virus expression. Mol Cell Biol 23: 6618-6630.
29. 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.
30. 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.
31. 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.
32. Schwartz S, Campbell M, Nasioulas G, Harrison J, Felber BK, et al. (1992) Mutational inactivation of an inhibitory sequence in human immunodeficiency virus type 1 results in Rev-independent gag expression. J Virol 66: 7176-7182.
33. Wolff H, Hartl A, Eilken HM, Hadian K, Ziegler M, et al. (2006) Live-cell assay for simultaneous monitoring of expression and interaction of proteins. Biotechniques 41: 688, 690, 692.
34. Vallejos M, Carvajal F, Pino K, Navarrete C, Ferres M, et al. (2012) Functional and Structural Analysis of the Internal Ribosome Entry Site Present in the mRNA of Natural Variants of the HIV-1. PLoS One 7: e35031.
35. Cochrane AW, Chen CH, Rosen CA, (1990) Specific interaction of the human immunodeficiency virus Rev protein with a structured region in the env mRNA. Proc Natl Acad Sci U S A 87: 1198-1202.
36. Fraser CS, Doudna JA, (2007) Structural and mechanistic insights into hepatitis C viral translation initiation. Nat Rev Microbiol 5: 29-38.
37. Malim MH, Tiley LS, McCarn DF, Rusche JR, Hauber J, et al. (1990) HIV-1 structural gene expression requires binding of the Rev trans-activator to its RNA target sequence. Cell 60: 675-683.
38. Cochrane AW, McNally MT, Mouland AJ, (2006) The retrovirus RNA trafficking granule: from birth to maturity. Retrovirology 3: 18.
39. Najera I, Krieg M, Karn J, (1999) Synergistic stimulation of HIV-1 rev-dependent export of unspliced mRNA to the cytoplasm by hnRNP A1. J Mol Biol 285: 1951-1964.
40. Beriault V, Clement JF, Levesque K, Lebel C, Yong X, et al. (2004) A late role for the association of hnRNP A2 with the HIV-1 hnRNP A2 response elements in genomic RNA, Gag, and Vpr localization. J Biol Chem 279: 44141-44153.
41. Nasioulas G, Zolotukhin AS, Tabernero C, Solomin L, Cunningham CP, et al. (1994) Elements distinct from human immunodeficiency virus type 1 splice sites are responsible for the Rev dependence of env mRNA. J Virol 68: 2986-2993.
42. Parkin N, Darveau A, Nicholson R, Sonenberg N, (1988) cis-acting translational effects of the 5′ noncoding region of c-myc mRNA. Mol Cell Biol 8: 2875-2883.
43. Silverman RH, Sengupta DN, (1990) Translational regulation by HIV leader RNA, TAT, and interferon-inducible enzymes. J Exp Pathol 5: 69-77.
44. SenGupta DN, Berkhout B, Gatignol A, Zhou AM, Silverman RH, (1990) Direct evidence for translational regulation by leader RNA and Tat protein of human immunodeficiency virus type 1. Proc Natl Acad Sci U S A 87: 7492-7496.
45. Berkhout B, (1996) Structure and function of the human immunodeficiency virus leader RNA. Prog Nucleic Acid Res Mol Biol 54: 1-34.
46. Geballe AP, Gray MK, (1992) Variable inhibition of cell-free translation by HIV-1 transcript leader sequences. Nucleic Acids Res 20: 4291-4297.
47. Ka WH, Jeong YY, You JC, (2012) Identification of the HIV-1 packaging RNA sequence (Psi) as a major determinant for the translation inhibition conferred by the HIV-1 5′ UTR. Biochem Biophys Res Commun 417: 501-507.
48. Soto-Rifo R, Limousin T, Rubilar PS, Ricci EP, Decimo D, et al. (2012) Different effects of the TAR structure on HIV-1 and HIV-2 genomic RNA translation. Nucleic Acids Res.
49. Anderson EC, Lever AM, (2006) Human immunodeficiency virus type 1 Gag polyprotein modulates its own translation. J Virol 80: 10478-10486.
50. Bolinger C, Boris-Lawrie K, (2009) Mechanisms employed by retroviruses to exploit host factors for translational control of a complicated proteome. Retrovirology 6: 8.
51. Groom HC, Anderson EC, Dangerfield JA, Lever AM, (2009) Rev regulates translation of human immunodeficiency virus type 1 RNAs. J Gen Virol 90: 1141-1147.
52. Dillon PJ, Nelbock P, Perkins A, Rosen CA, (1990) Function of the human immunodeficiency virus types 1 and 2 Rev proteins is dependent on their ability to interact with a structured region present in env gene mRNA. J Virol 64: 4428-4437.
53. Zapp ML, Green MR, (1989) Sequence-specific RNA binding by the HIV-1 Rev protein. Nature 342: 714-716.
54. Gallego J, Greatorex J, Zhang H, Yang B, Arunachalam S, et al. (2003) Rev binds specifically to a purine loop in the SL1 region of the HIV-1 leader RNA. J Biol Chem 278: 40385-40391.
55. Cheunim T, Zhang J, Milligan SG, McPhillips MG, Graham SV, (2008) The alternative splicing factor hnRNP A1 is up-regulated during virus-infected epithelial cell differentiation and binds the human papillomavirus type 16 late regulatory element. Virus Res 131: 189-198.
56. Kim CS, Seol SK, Song OK, Park JH, Jang SK, (2007) An RNA-binding protein, hnRNP A1, and a scaffold protein, septin 6, facilitate hepatitis C virus replication. J Virol 81: 3852-3865.
57. Lin JY, Shih SR, Pan M, Li C, Lue CF, et al. (2009) hnRNP A1 interacts with the 5′ untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication. J Virol 83: 6106-6114.
58. Paranjape SM, Harris E, (2007) Y box-binding protein-1 binds to the dengue virus 3′-untranslated region and mediates antiviral effects. J Biol Chem 282: 30497-30508.
59. Kress E, Baydoun HH, Bex F, Gazzolo L, Duc Dodon M, (2005) Critical role of hnRNP A1 in HTLV-1 replication in human transformed T lymphocytes. Retrovirology 2: 8.
60. 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.
61. Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CU, (1998) A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev 12: 67-83.
62. Kolupaeva VG, Pestova TV, Hellen CU, (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.
63. Kieft JS, Zhou K, Jubin R, Doudna JA, (2001) Mechanism of ribosome recruitment by hepatitis C IRES RNA. Rna 7: 194-206.
64. Otto GA, Puglisi JD, (2004) The pathway of HCV IRES-mediated translation initiation. Cell 119: 369-380.