HIV-1 transcripts use ires-initiation under conditions where cap-dependent translation is restricted by poliovirus 2A protease

PLoS ONE

Volumn 9, Issue 2, 2014, Pages

  Amorim, Raquel ^a   Costa, Sara Mesquita ^a   Cavaleiro, Nathalia Pereira ^a   Da Silva, Edson Elias ^b   Da Costa, Luciana Jesus ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ENHANCED GREEN FLUORESCENT PROTEIN; HUMAN IMMUNODEFICIENCY VIRUS PROTEIN; LUCIFERASE; POLIOVIRUS 2A PROTEASE; PROTEINASE; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INTERNAL RIBOSOME ENTRY SITE; LYMPHOID CELL LINE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; PROTEINASE INHIBITION; RNA BINDING; RNA CLEAVAGE; RNA INTERFERENCE; RNA STRUCTURE; RNA TRANSLATION; TRANSCRIPTION INITIATION; TRANSLATION INITIATION; TRANSLATION REGULATION; VIRUS INFECTIVITY; VIRUS RELEASE; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

CELL SURVIVAL; CYSTEINE ENDOPEPTIDASES; DNA, INTERGENIC; EUKARYOTIC INITIATION FACTOR-4G; HELA CELLS; HIV-1; HUMANS; LYMPHOCYTES; PLASMIDS; POLYRIBOSOMES; PROTEIN BIOSYNTHESIS; RNA CAPS; RNA, MESSENGER; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84895545277     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0088619     Document Type: Article

References (50)

1. Johannes G, Carter MS, Eisen MB, Brown PO, 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 U S A 96: 13118-13123.
2. Reineke LC, Lloyd RE (2011) Animal virus schemes for translation dominance. Curr Opin Virol 1: 363-372.
3. Walsh D, Mohr I (2011) Viral subversion of the host protein synthesis machinery. Nat Rev Microbiol 9: 860-875.
4. Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136: 731-745.
5. Jang SK, Pestova TV, Hellen CU, Witherell GW, Wimmer E (1990) Cap-independent translation of picornavirus RNAs: structure and function of the internal ribosomal entry site. Enzyme 44: 292-309.
6. Kuyumcu-Martinez NM, Van Eden ME, Younan P, Lloyd RE (2004) Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: a novel mechanism for host translation shutoff. Mol Cell Biol 24: 1779-1790. (Pubitemid 38167098)
7. Gradi A, Svitkin YV, Imataka H, Sonenberg N (1998) Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. Proc Natl Acad Sci U S A 95: 11089-11094. (Pubitemid 28450086)
8. Chase AJ, Semler BL (2012) Viral subversion of host functions for picornavirus translation and RNA replication. Future Virol 7: 179-191.
9. Gingras AC, Raught B, Sonenberg N (2000) eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68: 913-963. (Pubitemid 29449212)
10. Aldabe R, Feduchi E, Novoa I, Carrasco L (1995) Expression of poliovirus 2Apro in mammalian cells: effects on translation. FEBS Lett 377: 1-5.
11. Soto-Rifo R, Rubilar PS, Limousin T, de Breyne S, Decimo D, et al. (2012) DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs. Embo j 31: 3745-3756.
12. 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 40: 2653-2667.
13. Berkhout B, Arts K, Abbink TE (2011) Ribosomal scanning on the 59-untranslated region of the human immunodeficiency virus RNA genome. Nucleic Acids Res 39: 5232-5244.
14. 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. (Pubitemid 30237759)
15. 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. (Pubitemid 36350935)
16. Camerini V, Decimo D, Balvay L, Pistello M, Bendinelli M, et al. (2008) A dormant internal ribosome entry site controls translation of feline immunode-ficiency virus. J Virol. United States. pp. 3574-3583.
17. Adachi A, Gendelman HE, Koenig S, Folks T, Willey R, et al. (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)
18. Schindler M, W̧rfl S, Benaroch P, Greenough TC, Daniels R, et al. (2003) Down-modulation of mature major histocompatibility complex class II and up-regulation of invariant chain cell surface expression are well-conserved functions of human and simian immunodeficiency virus nef alleles. J Virol 77: 10548-10556.
19. Schindler M, Münch J, Kirchhoff F (2005) Human Immunodeficiency Virus Type 1 Inhibits DNA Damage-Triggered Apoptosis by a Nef-Independent Mechanism.
20. Chang LJ, Urlacher V, Iwakuma T, Cui Y, Zucali J (1999) Efficacy and safety analyses of a recombinant human immunodeficiency virus type 1 derived vector system. Gene Ther 6: 715-728. (Pubitemid 29243643)
21. Muramatsu M, Smetana K, Busch H (1963) Quantitative Aspects of Isolation of Nucleoli of the Walker Carcinosarcoma and Liver of the Rat.
22. Hambidge SJ, Sarnow P (1991) Terminal 7-methyl-guanosine cap structure on the normally uncapped 59 noncoding region of poliovirus mRNA inhibits its translation in mammalian cells. J Virol 65: 6312-6315.
23. Ochs K, Zeller A, Saleh L, Bassili G, Song Y, et al. (2003) Impaired binding of standard initiation factors mediates poliovirus translation attenuation. J Virol 77: 115-122. (Pubitemid 36007798)
24. Castello A, Alvarez E, Carrasco L (2011) The multifaceted poliovirus 2A protease: regulation of gene expression by picornavirus proteases. J Biomed Biotechnol 2011: 369648.
25. Leibowitz R, Penman S (1971) Regulation of protein synthesis in HeLa cells. 3. Inhibition during poliovirus infection. J Virol 8: 661-668.
26. Etchison D, Milburn SC, Edery I, Sonenberg N, Hershey JW (1982) Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J Biol Chem 257: 14806-14810. (Pubitemid 13159573)
27. Lloyd RE (2006) Translational control by viral proteinases. Virus Res 119: 76-88.
28. Barco A, Feduchi E, Carrasco L (2000) A stable HeLa cell line that inducibly expresses poliovirus 2A(pro): effects on cellular and viral gene expression. J Virol 74: 2383-2392. (Pubitemid 30091493)
29. Calandria C, Irurzun A, Barco A, Carrasco L (2004) Individual expression of poliovirus 2Apro and 3Cpro induces activation of caspase-3 and PARP cleavage in HeLa cells. . Virus Res. Netherlands. pp. 39-49.
30. Marion RM, Fortes P, Beloso A, Dotti C, Ortin J (1999) A Human Sequence Homologue of Staufen Is an RNA-Binding Protein That Is Associated with Polysomes and Localizes to the Rough Endoplasmic Reticulum. Mol Cell Biol 19: 2212-2219. (Pubitemid 29098279)
31. Kim YK, Furic L, Parisien M, Major F, DesGroseillers L, et al. (2007) Staufen1 regulates diverse classes of mammalian transcripts. Embo j 26: 2670-2681. (Pubitemid 46884281)
32. Buck CB, Shen X, Egan MA, Pierson TC, Walker CM, et al. (2000) The human immunodeficiency virus type 1 gag gene encodes an internal ribosome entry site. J Virol 75: 181-191.
33. Plank TD, Whitehurst JT, Kieft JS (2013) Cell type specificity and structural determinants of IRES activity from the 59 leaders of different HIV-1 transcripts. Nucleic Acids Res 41: 6698-6714.
34. Ricci EP, Soto Rifo R, Herbreteau CH, Decimo D, Ohlmann T (2008) Lentiviral RNAs can use different mechanisms for translation initiation. Biochem Soc Trans. England. pp. 690-693.
35. 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. United States. pp. e35031.
36. Jowett JB, Planelles V, Poon B, Shah NP, Chen ML, et al. (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.
37. 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. England. pp. 6186-6200.
38. Jurgens CK, Barton DJ, Sharma N, Morasco BJ, Ogram SA, et al. (2006) 2Apro is a multifunctional protein that regulates the stability, translation and replication of poliovirus RNA. Virology 345: 346-357. (Pubitemid 43189895)
39. Kempf BJ, Barton DJ (2008) Poliovirus 2A(Pro) increases viral mRNA and polysome stability coordinately in time with cleavage of eIF4G. J Virol. United States. pp. 5847-5859.
40. Svitkin YV, Gradi A, Imataka H, Morino S, Sonenberg N (1999) Eukaryotic initiation factor 4GII (eIF4GII), but not eIF4GI, cleavage correlates with inhibition of host cell protein synthesis after human rhinovirus infection. J Virol 73: 3467-3472. (Pubitemid 29135743)
41. Marissen WE, Lloyd RE (1998) Eukaryotic translation initiation factor 4G is targeted for proteolytic cleavage by caspase 3 during inhibition of translation in apoptotic cells. Mol Cell Biol 18: 7565-7574. (Pubitemid 28533075)
42. Lejeune F, Ranganathan AC, Maquat LE (2004) eIF4G is required for the pioneer round of translation in mammalian cells. Nat Struct Mol Biol. United States. pp. 992-1000.
43. Zhou H, Xu M, Huang Q, Gates AT, Zhang XD, et al. (2008) Genome-scale RNAi screen for host factors required for HIV replication. Cell Host Microbe. United States. pp. 495-504.
44. Chamond N, Locker N, Sargueil B (2010) The different pathways of HIV genomic RNA translation. Biochem Soc Trans. England. pp. 1548-1552.
45. de Breyne S, Chamond N, Decimo D, Trabaud MA, Andre P, et al. (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.
46. Goh WC, Rogel ME, Kinsey CM, Michael SF, Fultz PN, et al. (1998) HIV-1 Vpr increases viral expression by manipulation of the cell cycle: a mechanism for selection of Vpr in vivo. Nat Med 4: 65-71. (Pubitemid 28133081)
47. 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. United States. pp. 12198-12206.
48. Sharma A, Yilmaz A, Marsh K, Cochrane A, Boris-Lawrie K (2012) Thriving under stress: selective translation of HIV-1 structural protein mRNA during Vpr-mediated impairment of eIF4E translation activity. PLoS Pathog. United States. pp. e1002612.
49. Monette A, Valiente-Echeverria F, Rivero M, Cohen EA, Lopez-Lastra M, et al. (2013) Dual mechanisms of translation initiation of the full-length HIV-1 mRNA contribute to gag synthesis. PLoS One 8: e68108.
50. 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. England. pp. 902-912.