A reassessment of the response of the bacterial ribosome to the frameshift stimulatory signal of the human immunodeficiency virus type 1

RNA

Volumn 10, Issue 8, 2004, Pages 1225-1235

  Léger, Mélissa ^a   Sidani, Sacha ^a   Brakier Gingras, Léa ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Bacterial ribosome; HIV 1 programmed 1 ribosomal frameshift; Ribosomal RNA mutagenesis

Indexed keywords

LUCIFERASE;

ARTICLE; DEACYLATION; ENZYME SPECIFICITY; GENE DISRUPTION; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RECEPTOR OCCUPANCY; RIBOSOMAL FRAMESHIFTING; RISK ASSESSMENT; RNA TRANSLATION; STIMULUS RESPONSE; STOP CODON; WILD TYPE;

CODON, TERMINATOR; ESCHERICHIA COLI; GENES, REPORTER; HIV-1; MUTATION; NUCLEIC ACID CONFORMATION; RIBOSOMES; RNA, RIBOSOMAL, 16S; RNA, VIRAL;

BACTERIA (MICROORGANISMS); EUKARYOTA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 3342905119     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1261/rna.7670704     Document Type: Article

References (55)

1. Atkins, J.F., Baranov, P.V., Fayet, O., Herr, A.J., Howard, M.T., Ivanov, I.P., Matsufuji, S., Miller, W.A., Moore, B., Prère, M.F., et al. 2001. Overriding standard decoding: Implications of recoding for ribosome function and enrichment of gene expression. Cold Spring Harbor Symp. Quant. Biol. 66: 217-232.
2. Ban, N., Nissen, P., Hansen, J., Moore, P.B., and Steitz, T.A. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289: 905-920.
3. Baranov, P.V., Gesteland, R.F., and Atkins, J.F. 2002. Recoding: Translational bifurcations in gene expression. Gene 286: 187-201.
4. -. 2004. P-site tRNA is a crucial initiator of ribosomal frameshifting. RNA 10: 221-230.
5. Baril, M., Dulude, D., Gendron, K., Lemay, G., and Brakier-Gingras, L. 2003. Efficiency of a programmed -1 ribosomal frameshift in the different subtypes of the human immunodeficiency virus type 1 group M. RNA 9: 1246-1253.
6. Bélanger, F., Léger, M., Saraiya, A.A., Cunningham, P.R., and Brakier-Gingras, L. 2002. Functional studies of the 900 tetraloop capping helix 27 of 16S ribosomal RNA. J. Mol. Biol. 320: 979-989.
7. Bélanger, F., Gagnon, M.G., Steinberg, S.V., Cunningham, P.R., and Brakier-Gingras, L. 2004. Study of the functional interaction of the 900 tetraloop of 16S ribosomal RNA with helix 24 within the bacterial ribosome. J. Mol. Biol. 338: 683-693.
8. Bertrand, C., Prère, M.F., Gesteland, R.F., Atkins, I.F., and Fayet, O. 2002. Influence of the stacking potential of the base 3′ of tandem shift codons on -1 ribosomal frameshifting used for gene expression. RNA 8: 16-28.
9. Brakier-Gingras, L., Bélanger, F., and O'Connor, M. 2003. Probing the role of ribosomal RNA in protein synthesis through mutagenesis. In Translation mechanisms (eds. J. Lapointe and L. Brakier-Gingras), pp. 247-263. Landes Bioscience, Georgetown, TX, and Kluwer Academic/Plenum Publishers, New York.
10. Brierley, I. and Pennell, S. 2001. Structure and function of the stimulatory RNAs involved in programmed eukaryotic -1 ribosomal frameshifting. Cold Spring Harbor Symp. Quant. Biol. 66: 233-248.
11. Brierley, I., Jenner, A.J., and Inglis, S.C. 1992. Mutational analysis of the "slippery-sequence" component of a coronavirus ribosomal frameshifting signal. J. Mol. Biol. 227: 463-479.
12. Brunelle, M.N., Payant, C., Lemay, G., and Brakier-Gingras, L. 1999. Expression of the human immunodeficiency virus frameshift signal in a bacterial cell-free system: Influence of an interaction between the ribosome and a stem-loop structure downstream from the slippery site. Nucleic Acids Res. 27: 4783-4791.
13. Cassan, M., Delaunay, N., Vaquero, C., and Rousset, J.P. 1994. Translational frameshifting at the gag-pol junction of human immunodeficiency virus type 1 is not increased in infected T-lymphoid cells. J. Virol. 68: 1501-1508.
14. Dinman, J.D. and Kinzy, T.G. 1997. Translational misreading: Mutations in translation elongation factor 1α differentially affect programmed ribosomal frameshifting and drug sensitivity. RNA 3: 870-881.
15. Dinman, J.D., Icho, T., and Wickner, R.B. 1991. A -1 ribosomal frameshift in a double-stranded RNA virus of yeast forms a gag-pol fusion protein. Proc. Natl. Acad. Sci. 88: 174-178.
16. Dinman, J.D., Ruiz-Echevarria, M.J., Czaplinski, K., and Peltz, S.W. 1997. Peptidyl-transferase inhibitors have antiviral properties by altering programmed -1 ribosomal frameshifting efficiencies: Development of model systems. Proc. Natl. Acad. Sci. 94: 6606-6611.
17. Dulude, D., Baril, M., and Brakier-Gingras, L. 2002. Characterization of the frameshift stimulatory signal controlling a programmed -1 ribosomal frameshift in the human immunodeficiency virus type 1. Nucleic Acids Res. 30: 5094-5102.
18. Farabaugh, P.J. 1997a. Programmed -1 frameshift sites in prokaryotes. In Programmed alternative reading of the genetic code, pp. 103-134. Landes Bioscience, Austin, Texas and Springer-Verlag, Heidelberg, Germany.
19. -. 1997b. Programmed -1 frameshifting in eukaryotes. In Programmed alternative reading of the genetic code, pp. 69-102. Landes Bioscience, Austin, TX, and Springer-Verlag, Heidelberg, Germany.
20. Gromadski, K.B. and Rodnina, M.V. 2004. Kinetic determinants of high-fidelity tRNA discrimination on the ribosome. Mol. Cell 13: 191-200.
21. Harger, J.W., Meskauskas, A., and Dinman, J.D. 2002. An "integrated model" of programmed ribosomal frameshifting. Trends Biochem. Sci. 27: 448-454.
22. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
23. Horsfield, J.A., Wilson, D.N., Mannering, S.A., Adamski, F.M., and Tate, W.P. 1995. Prokaryotic ribosomes recode the HIV-1 gag-pol -1 frameshift sequence by an E/P site post-translocation simultaneous slippage mechanism. Nucleic Acids Res. 23: 1487-1494.
24. Jacks, T., Power, M.D., Masiarz, F.R., Luciw, P.A., Barr, P.J., and Varmus, H.E. 1988a. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 331: 280-283.
25. Jacks, T., Madhani, H.D., Masiarz, F.R., and Varmus, H.E. 1988b. Signals for ribosomal frameshifting in the Rous sarcoma virus gagpol region. Cell 55: 447-458.
26. Kang, H. 1998. Direct structural evidence for formation of a stem-loop structure involved in ribosomal frameshifting in human immunodeficiency virus type 1. Biochim. Biophys. Acta 1397: 73-78.
27. Kontos, H., Napthine, S., and Brierley, I. 2001. Ribosomal pausing at a frameshifter RNA pseudoknot is sensitive to reading phase but shows little correlation with frameshift efficiency. Mol. Cell. Biol. 21: 8657-8670.
28. Leclerc, D., Melançon, P., and Brakier-Gingras, L. 1991. Mutations in the 915 region of Escherichia coli 16S ribosomal RNA reduce the binding of streptomycin to the ribosome. Nucleic Acids Res. 19: 3973-3977.
29. Lee, K., Varma, S., SantaLucia Jr., J., and Cunningham, P.R. 1997. In vivo determination of RNA structure-function relationships: analysis of the 790 loop in ribosomal RNA. J. Mol. Biol. 269: 732-743.
30. Lopinski, J.D., Dinman, J.D., and Bruenn, J.A. 2000. Kinetics of ribosomal pausing during programmed -1 translational frameshifting. Mol. Cell. Biol. 20: 1095-1103.
31. Meskauskas, A., Harger, J.W., Jacobs, K.L., and Dinman, J.D. 2003. Decreased peptidyltransferase activity correlates with increased programmed -1 ribosomal frameshifting and viral maintenance defects in the yeast Saccharomyces cerevisiae. RNA 9: 982-992.
32. Morosyuk, S.V., Lee, K., SantaLucia Jr., J., and Cunningham, P.R. 2000. Structure and function of the conserved 690 hairpin in Escherichia coli 16S ribosomal RNA: Analysis of the stem nucleotides. J. Mol. Biol. 300: 113-126.
33. Morosyuk, S.V., SantaLucia Jr., J., and Cunningham, P.R. 2001. Structure and function of the conserved 690 hairpin in Escherichia coli 16S ribosomal RNA. III. Functional analysis of the 690 loop. J. Mol. Biol. 307: 213-228.
34. Napthine, S., Vidakovic, M., Girnary, R., Namy, O., and Brierley, I. 2003. Prokaryotic-style frameshifting in a plant translation system: Conservation of an unusual single-tRNA slippage event. EMBO J. 22: 3941-3950.
35. Noller, H.F., Yusupov, M.M., Yusupova, G.Z., Baucom, A., and Cate, J.H. 2002. Translocation of tRNA during protein synthesis. FEBS Lett. 514: 11-16.
36. Ogle, J.M., Brodersen, D.E., Clemons Jr., W.M., Tarry, M.J., Carter, A.P., and Ramakrishnan, V. 2001. Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292: 897-902.
37. Ogle, J.M., Murphy, F.V., Tarry, M.J., and Ramakrishnan, V. 2002. Selection of tRNA by the ribosome requires a transition from an open to a closed form. Cell 111: 721-732.
38. Ogle, J.M., Carter, A.P., and Ramakrishnan, V. 2003. Insights into the decoding mechanism from recent ribosome structures. Trends Biochem. Sci. 28: 259-266.
39. Pape, T., Wintermeyer, W., and Rodnina, M.V. 1998. Complete kinetic mechanism of elongation factor Tu-dependent binding of aminoacyl-tRNA to the A site of the E. coli ribosome. EMBO J. 17: 7490-7497.
40. Parkin, N.T., Chamorro, M., and Varmus, H.E. 1992. Human immunodeficiency virus type 1 gag-pol frameshifting is dependent on downstream mRNA secondary structure: Demonstration by expression in vivo. J. Virol. 66: 5147-5151.
41. Plant, E.P., Jacobs, K.L., Harger, J.W., Meskauskas, A., Jacobs, J.L., Baxter, J.L., Petrov, A.N., and Dinman, J.D. 2003. The 9-Å solution: How mRNA pseudoknots promote efficient programmed -1 ribosomal frameshifting. RNA 9: 168-174.
42. Ramakrishnan, V. 2002. Ribosome structure and the mechanism of translation. Cell 108: 557-572.
43. Reil, H., Kollmus, H., Weidle, U.H., and Hauser, H. 1993. A hepta-nucleotide sequence mediates ribosomal frameshifting in mammalian cells. J. Virol. 67: 5579-5584.
44. Rodnina, M.V. and Wintermeyer, W. 2001. Fidelity of aminoacyl-tRNA selection on the ribosome: Kinetic and structural mechanisms. Annu. Rev. Biochem. 70: 415-435.
45. Schluenzen, F., Tocilj, A., Zarivach, R., Harms, J., Gluehmann, M., Janell, D., Bashan, A., Bartels, H., Agmon, I., Franceschi, F., et al. 2000. Structure of functionally activated small ribosomal subunit at 3.3 Å resolution. Cell 102: 615-623.
46. Somogyi, P., Jenner, A.J., Brierley, I., and Inglis, S.C. 1993. Ribosomal pausing during translation of an RNA pseudoknot. Mol. Cell. Biol. 13: 6931-6940.
47. Stark, H., Rodnina, M.V., Wieden, H.J., Zemlin, F., Wintermeyer, W., and van Heel, M. 2002. Ribosome interactions of aminoacyl-tRNA and elongation factor Tu in the codon-recognition complex. Nat. Struct. Biol. 9: 849-854.
48. Tu, C., Tzeng, T.H., and Bruenn, J.A. 1992. Ribosomal movement impeded at a pseudoknot required for frameshifting. Proc. Natl. Acad. Sci. 89: 8636-8640.
49. Tumer, N.E., Parikh, B.A., Li, P., and Dinman, J.D. 1998. The pokeweed antiviral protein specifically inhibits Tyl-directed +1 ribosomal frameshifting and retrotransposition in Saccharomyces cerevisiae. J. Virol. 72: 1036-1042.
50. Valle, M., Zavialov, A., Li, W., Stagg, S.M., Sengupta, J., Nielsen, R.C., Nissen, P., Harvey, S.C., Ehrenberg, M., and Frank, J. 2003. Incorporation of aminoacyl-tRNA into the ribosome as seen by cryoelectron microscopy. Nat. Struct. Biol. 10: 899-906.
51. Weiss, R.B., Dunn, D.M., Shuh, M., Atkins, J.F., and Gesteland, R.F. 1989. E. coli ribosomes re-phase on retroviral frameshift signals at rates ranging from 2 to 50 percent. New Biol. 1: 159-169.
52. Wimberly, B.T., Brodersen, D.E., Clemons Jr., W.M., Morgan-Warren, R.J., Carter, A.P., Vonrhein, C., Hartsch, T., and Ramakrishnan, V. 2000. Structure of the 30S ribosomal subunit. Nature 407: 327-339.
53. Yelverton, E., Lindsley, D., Yamauchi, P., and Gallant, J.A. 1994. The function of a ribosomal frameshifting signal from human immunodeficiency virus -1 in Escherichia coli. Mol. Microbiol. 11: 303-313.
54. Yusupov, M.M., Yusupova, G.Z., Baucom, A., Lieberman, K., Earnest, T.N., Cate, J.H., and Noller, H.F. 2001. Crystal structure of the ribosome at 5.5 Å resolution. Science 292: 883-896.
55. Yusupova, G.Z., Yusupov, M.M., Cate, J.H., and Noller, H.F. 2001. The path of messenger RNA through the ribosome. Cell 106: 233-241.