Targeting frameshifting in the human immunodeficiency virus

Expert Opinion on Therapeutic Targets

Volumn 16, Issue 3, 2012, Pages 249-258

  Brakier Gingras, Léa ^a   Charbonneau, Johanie ^a   Butcher, Samuel E ^b  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

1 ribosomal frameshift; Antiframeshift agents; Gag Pol:Gag ratio; HIV 1

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; ANTIVIRUS AGENT; CHEMICAL COMPOUND; DOXORUBICIN; NEOMYCIN; VIRUS ENZYME;

BINDING AFFINITY; CHEMICAL MODIFICATION; CISTRON; ENZYME SYNTHESIS; GENE STRUCTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; REVIEW; RIBOSOMAL FRAMESHIFTING; RNA TRANSLATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

FRAMESHIFTING, RIBOSOMAL; HIV INFECTIONS; HIV-1; HUMANS;

EID: 84858173140     PISSN: 14728222     EISSN: 17447631     Source Type: Journal    
DOI: 10.1517/14728222.2012.665879     Document Type: Review

References (64)

1. Nekhai S, Jeang KT. Transcriptional and post-transcriptional regulation of HIV-1 gene expression: role of cellular factors for Tat and Rev. Future Microbiol 2006;1:417-26
2. Jacks T, Power MD, Masiarz FR, et al. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 1988;331:280-3 (Pubitemid 18040598)
3. Dulude D, Baril M, Brakier-Gingras L. Characterization of the frameshift stimulatory signal controlling a programmed-1 ribosomal frameshift in the human immunodeficiency virus type 1. Nucleic Acids Res 2002;30:5094-102 (Pubitemid 36033026)
4. Gaudin C, Mazauric MH, Traikia M, et al. Structure of the RNA signal essential for translational frameshifting in HIV-1. J Mol Biol 2005;349:1024-35 (Pubitemid 40779623)
5. Staple DW, Butcher SE. Solution structure and thermodynamic investigation of the HIV-1 frameshift inducing element. J Mol Biol 2005;349:1011-23 (Pubitemid 40779622)
6. Yang SJ, Lopez LA, Exline CM, et al. Lack of adaptation to human tetherin in HIV-1 Group O and P. Retrovirology 2011;8:78
7. HIV Databases. Los Alamos, New Mexico: Los Alamos National Laboratory, 2005-2006. Available from: http://www.hiv.lanl.gov/content/index
8. Baril M, Dulude D, Gendron K, et al. Efficiency of a programmed-1 ribosomal frameshift in the different subtypes of the human immunodeficiency virus type 1 group M. RNA 2003;9:1246-53 (Pubitemid 37151678)
9. Mazauric MH, Seol Y, Yoshizawa S, et al. Interaction of the HIV-1 frameshift signal with the ribosome. Nucleic Acids Res 2009;37:7654-64
10. Fu J, Munro JB, Blanchard SC, Frank J. Cryoelectron microscopy structures of the ribosome complex in intermediate states during tRNA translocation. Proc Natl Acad Sci USA 2011;108:4817-21
11. Fischer N, Konevega AL, Wintermeyer W, et al. Ribosome dynamics and tRNA movement by time-resolved electron cryomicroscopy. Nature 2010;466:329-33
12. Dulude D, Berchiche YA, Gendron K, et al. Decreasing the frameshift efficiency translates into an equivalent reduction of the replication of the human immunodeficiency virus type 1. Virology 2006;345:127-36 (Pubitemid 43107578)
13. Leger M, Dulude D, Steinberg SV, Brakier-Gingras L. The three transfer RNAs occupying the A, P and E sites on the ribosome are involved in viral programmed-1 ribosomal frameshift. Nucleic Acids Res 2007;35:5581-92 (Pubitemid 47423929)
14. Brakier-Gingras L, Dulude D. Programmed-1 ribosomal frameshift in the human immunodeficiency virus of type 1. In: Atkins JF, Gesteland RF, editors. Recoding: Expansion of Decoding Rules Enriches Gene Expression. Springer; New York, NY: 2010. p. 175-92
15. Liao PY, Choi YS, Dinman JD, Lee KH. The many paths to frameshifting: kinetic modelling and analysis of the effects of different elongation steps on programmed-1 ribosomal frameshifting. Nucleic Acids Res 2011;39:300-12
16. Weiss RB, Dunn DM, Shuh M, et al. E. coli ribosomes re-phase on retroviral frameshift signals at rates ranging from 2 to 50 percent. New Biol 1989;1:159-69
17. Frank J, Gonzalez RL Jr. Structure and dynamics of a processive Brownian motor: the translating ribosome. Annu Rev Biochem 2010;79:381-412
18. Gilbert WV. Functional specialization of ribosomes? Trends Biochem Sci 2011;36:127-32
19. Plant EP, Dinman JD. Comparative study of the effects of heptameric slippery site composition on-1 frameshifting among different eukaryotic systems. RNA 2006;12:666-73
20. Houck-Loomis B, Durney MA, Salguero C, et al. An equilibrium-dependent retroviral mRNA switch regulates translational recoding. Nature 2011;480:561-4
21. Gendron K, Charbonneau J, Dulude D, et al. The presence of the TAR RNA structure alters the programmed-1 ribosomal frameshift efficiency of the human immunodeficiency virus type 1 (HIV-1) by modifying the rate of translation initiation. Nucleic Acids Res 2008;36:30-40
22. Charbonneau J, Gendron K, Ferbeyre G, Brakier-Gingras L. The 5UTR of HIV-1 full-length mRNA and the Tat viral protein modulate the programmed-1 ribosomal frameshift that generates HIV-1 enzymes. RNA 2012;18:519-29
23. Kobayashi Y, Zhuang J, Peltz S, Dougherty J. Identification of a cellular factor that modulates HIV-1 programmed ribosomal frameshifting. J Biol Chem 2010;285:19776-84
24. Clark MB, Janicke M, Gottesbuhren U, et al. Mammalian gene PEG10 expresses two reading frames by high efficiency-1 frameshifting in embryonic-associated tissues. J Biol Chem 2007;282:37359-69
25. Lux H, Flammann H, Hafner M, Lux A. Genetic and molecular analyses of PEG10 reveal new aspects of genomic organization, transcription and translation. PLoS One 2010;5:e8686
26. Wills NM, Moore B, Hammer A, et al. A functional-1 ribosomal frameshift signal in the human paraneoplastic Ma3 gene. J Biol Chem 2006;281:7082-8 (Pubitemid 43847472)
27. Baranov PV, Wills NM, Barriscale KA, et al. Programmed ribosomal frameshifting in the expression of the regulator of intestinal stem cell proliferation, adenomatous polyposis coli (APC). RNA Biol 2011;8:637-47
28. Plant EP, Wang P, Jacobs JL, Dinman JD. A programmed-1 ribosomal frameshift signal can function as a cis-acting mRNA destabilizing element. Nucleic Acids Res 2004;32:784-90 (Pubitemid 38263071)
29. Belew AT, Advani VM, Dinman JD. Endogenous ribosomal frameshift signals operate as mRNA destabilizing elements through at least two molecular pathways in yeast. Nucleic Acids Res 2011;39:2799-808
30. Carlson TL, Green KA, Green WR. Alternative translational reading frames as a novel source of epitopes for an expanded CD8 T-cell repertoire: use of a retroviral system to assess the translational requirements for CTL recognition and lysis. Viral Immunol 2010;23:577-83
31. Dinman JD, Wickner RB. Ribosomal frameshifting efficiency and gag/gag-pol ratio are critical for yeast M1 double-stranded RNA virus propagation. J Virol 1992;66:3669-76
32. Telenti A, Martinez R, Munoz M, et al. Analysis of natural variants of the human immunodeficiency virus type 1 gag-pol frameshift stem-loop structure. J Virol 2002;76:7868-73 (Pubitemid 34761010)
33. Miyauchi K, Komano J, Myint L, et al. Rapid propagation of low-fitness drug-resistant mutants of human immunodeficiency virus type 1 by a streptococcal metabolite sparsomycin. Antivir Chem Chemother 2006;17:167-74 (Pubitemid 46395544)
34. Shehu-Xhilaga M, Crowe SM, Mak J. Maintenance of the Gag/Gag-Pol ratio is important for human immunodeficiency virus type 1 RNA dimerization and viral infectivity. J Virol 2001;75:1834-41 (Pubitemid 32110173)
35. Bidou L, Stahl G, Grima B, et al. In vivo HIV-1 frameshifting efficiency is directly related to the stability of the stem-loop stimulatory signal. RNA 1997;3:1153-8 (Pubitemid 27424282)
36. Tholstrup J, Oddershede LB, Sørensen MA. mRNA pseudoknot structures can act as ribosomal roadblocks. Nucleic Acids Res 2012;40:303-13
37. Stahl G, Bidou L, Rousset J, Cassan M. Versatile vectors to study recoding: conservation of rules between yeast and mammalian cells. Nucleic Acids Res 1995;23:1557-60
38. Leger M, Sidani S, Brakier-Gingras L. A reassessment of the response of the bacterial ribosome to the frameshift stimulatory signal of the human immunodeficiency virus type 1. RNA 2004;10:1225-35 (Pubitemid 38989008)
39. Dinman JD, Ruiz-Echevarria MJ, Peltz SW. Translating old drugs into new treatments: ribosomal frameshifting as a target for antiviral agents. Trends Biotechnol 1998;16:190-6 (Pubitemid 128712952)
40. Hung M, Patel P, Davis S, Green SR. Importance of ribosomal frameshifting for human immunodeficiency virus type 1 particle assembly and replication. J Virol 1998;72:4819-24 (Pubitemid 28215658)
41. Marcheschi RJ, Tonelli M, Kumar A, Butcher SE. Structure of the HIV-1 frameshift site RNA bound to a small molecule inhibitor of viral replication. ACS Chem Biol 2011;6:857-64
42. Brierley I, Dos Ramos FJ. Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV. Virus Res 2006;119:29-42 (Pubitemid 43765977)
43. Grentzmann G, Ingram JA, Kelly PJ, et al. A dual-luciferase reporter system for studying recoding signals. RNA 1998;4:479-86 (Pubitemid 28160788)
44. Harger JW, Dinman JD. An in vivo dual-luciferase assay system for studying translational recoding in the yeast Saccharomyces cerevisiae. RNA 2003;9:1019-24 (Pubitemid 36899244)
45. Dulude D, Theberge-Julien G, Brakier-Gingras L, Heveker N. Selection of peptides interfering with a ribosomal frameshift in the human immunodeficiency virus type 1. RNA 2008;14:981-91 (Pubitemid 351574919)
46. Cardno TS, Poole ES, Mathew SF, et al. A homogeneous cell-based bicistronic fluorescence assay for high-throughput identification of drugs that perturb viral gene recoding and read-through of nonsense stop codons. RNA 2009;15:1614-21
47. Rakauskaite R, Liao PY, Rhodin MH, et al. A rapid, inexpensive yeast-based dual-fluorescence assay of programmed-1 ribosomal frameshifting for high-throughput screening. Nucleic Acids Res 2011;39:e97
48. Staple DW, Venditti V, Niccolai N, et al. Guanidinoneomycin B recognition of an HIV-1 RNA helix. Chem Bio Chem 2008;9:93-102
49. Marcheschi RJ, Mouzakis KD, Butcher SE. Selection and characterization of small molecules that bind the HIV-1 frameshift site RNA. ACS Chem Biol 2009;4:844-54
50. McNaughton BR, Gareiss PC, Miller BL. Identification of a selective small-molecule ligand for HIV-1 frameshift-inducing stem-loop RNA from an 11,325 member resin bound dynamic combinatorial library. J Am Chem Soc 2007;129:11306-7 (Pubitemid 47555529)
51. Palde PB, Ofori LO, Gareiss PC, et al. Strategies for recognition of stem-loop RNA structures by synthetic ligands: application to the HIV-1 frameshift stimulatory sequence. J Med Chem 2010;53:6018-27
52. Howard MT, Gesteland RF, Atkins JF. Efficient stimulation of site-specific ribosome frameshifting by antisense oligonucleotides. RNA 2004;10:1653-61 (Pubitemid 39288198)
53. Olsthoorn RC, Laurs M, Sohet F, et al. Novel application of sRNA: stimulation of ribosomal frameshifting. RNA 2004;10:1702-3 (Pubitemid 39426369)
54. Yu CH, Noteborn MH, Olsthoorn RC. Stimulation of ribosomal frameshifting by antisense LNA. Nucleic Acids Res 2010;38:8277-83
55. Ahn DG, Lee W, Choi JK, et al. Interference of ribosomal frameshifting by antisense peptide nucleic acids suppresses SARS coronavirus replication. Antiviral Res 2011;91:1-10
56. Aupeix-Scheidler K, Chabas S, Bidou L, et al. Inhibition of in vitro and ex vivo translation by a transplatin-modified oligo(2¢-O- methylribonucleotide) directed against the HIV-1 gag-pol frameshift signal. Nucleic Acids Res 2000;28:438-45 (Pubitemid 30057982)
57. Agrawal S, Kandimalla ER. Role of Toll-like receptors in antisense and siRNA corrected. Nat Biotechnol 2004; 22: 1533-1537 (Pubitemid 40039455)
58. Flexner C. HIV drug development: the next 25 years. Nat Rev Drug Discov 2007;6:959-66 (Pubitemid 350201786)
59. Tsygankov AY. Current developments in anti-HIV/AIDS gene therapy. Curr Opin Investig Drugs 2009;10:137-49
60. Gareiss PC, Miller BL. Ribosomal frameshifting: an emerging drug target for HIV. Curr Opin Investig Drugs 2009;10:121-8
61. Hajduk PJ, Greer J. A decade of fragment-based drug design: strategic advances and lessons learned. Nat Rev Drug Discov 2007;6:211-19 (Pubitemid 46344625)
62. Girnary R, King L, Robinson L, et al. Structure-function analysis of the ribosomal frameshifting signal of two human immunodeficiency virus type 1 isolates with increased resistance to viral protease inhibitors. J Gen Virol 2007;88:226-35 (Pubitemid 46085133)
63. Nijhuis M, van Maarseveen NM, Lastere S, et al. A novel substrate-based HIV-1 protease inhibitor drug resistance mechanism. PLoS Med 2007;4:e36
64. Knops E, Brakier-Gingras L, Schulter E, et al. Mutational patterns in the frameshift-regulating site of HIV-1 selected by protease inhibitors. Med Microbiol Immunol 2012;published online 27 December 2011; doi: 10.1007/s00430-011-0224-z