Changed in translation: MRNA recoding by -1 programmed ribosomal frameshifting

Trends in Biochemical Sciences

Volumn 40, Issue 5, 2015, Pages 265-274

  Caliskan, Neva ^a   Peske, Frank ^a   Rodnina, Marina V ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

Decoding; Gene expression; MRNA reading frame maintenance; Protein synthesis; Ribosome; Translation

Indexed keywords

CIS ACTING ELEMENT; CYTOKINE RECEPTOR; MESSENGER RNA; PROTEIN 1PRF; PROTEOME; TRANS ACTING FACTOR; UNCLASSIFIED DRUG;

CELL FUNCTION; CODON; EUKARYOTE; HUMAN; MOLECULAR BIOLOGY; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY SEQUENCE; REVIEW; RIBOSOMAL FRAMESHIFTING; RNA CONFORMATION; RNA STABILITY; RNA SYNTHESIS; RNA TRANSLATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN SYNTHESIS; RIBOSOME;

EUKARYOTA;

FRAMESHIFTING, RIBOSOMAL; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, MESSENGER;

EID: 84927912034     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2015.03.006     Document Type: Review

References (85)

1. Drummond D.A., Wilke C.O. The evolutionary consequences of erroneous protein synthesis. Nat. Rev. Genet. 2009, 10:715-724.
2. Baranov P.V., et al. Recoding in bacteriophages and bacterial IS elements. Trends Genet. 2006, 22:174-181.
3. Baranov P.V., et al. Recoding: translational bifurcations in gene expression. Gene 2002, 286:187-201.
4. Gesteland R.F., Atkins J.F. Recoding: dynamic reprogramming of translation. Annu. Rev. Biochem. 1996, 65:741-768.
5. Fayet O., Prere M.F. Programmed ribosomal-1 frameshifting as a tradition: the bacterial transposable elements of the IS3 family. Recoding: Expansion of Decoding Rules Enriches Gene Expression 2010, 259-280. Springer. J.F. Atkins, R.F. Gesteland (Eds.).
6. Recoding: Expansion of Decoding Rules Enriches Gene Expression 2010, Springer. J.F. Atkins, R.F. Gesteland (Eds.).
7. Chandler M., Fayet O. Translational frameshifting in the control of transposition in bacteria. Mol. Microbiol. 1993, 7:497-503.
8. Brierley I., Dos Ramos F.J. Programmed ribosomal frameshifting in HIV-1 and the SARS-CoV. Virus Res. 2006, 119:29-42.
9. Brakier-Gingras L., et al. Targeting frameshifting in the human immunodeficiency virus. Expert Opin. Ther. Targets 2012, 16:249-258.
10. Dulude D., et al. Decreasing the frameshift efficiency translates into an equivalent reduction of the replication of the human immunodeficiency virus type 1. Virology 2006, 345:127-136.
11. Hung M., et al. Importance of ribosomal frameshifting for human immunodeficiency virus type 1 particle assembly and replication. J. Virol. 1998, 72:4819-4824.
12. Belew A.T., et al. PRFdb: a database of computationally predicted eukaryotic programmed -1 ribosomal frameshift signals. BMC Genomics 2008, 9:339.
13. Advani V.M., et al. Yeast telomere maintenance is globally controlled by programmed ribosomal frameshifting and the nonsense-mediated mRNA decay pathway. Translation 2013, 1:e24418.
14. Belew A.T., et al. Ribosomal frameshifting in the CCR5 mRNA is regulated by miRNAs and the NMD pathway. Nature 2014, 512:265-269.
15. Belew A.T., Dinman J.D. Cell cycle control (and more) by programmed -1 ribosomal frameshifting: implications for disease and therapeutics. Cell Cycle 2015, 14:172-178.
16. Manktelow E., et al. Characterization of the frameshift signal of Edr, a mammalian example of programmed -1 ribosomal frameshifting. Nucleic Acids Res. 2005, 33:1553-1563.
17. Shigemoto K., et al. Identification and characterisation of a developmentally regulated mammalian gene that utilises -1 programmed ribosomal frameshifting. Nucleic Acids Res. 2001, 29:4079-4088.
18. Michel A.M., et al. Observation of dually decoded regions of the human genome using ribosome profiling data. Genome Res. 2012, 22:2219-2229.
19. Brierley I., et al. Pseudoknot-dependent programmed -1 ribosomal frameshifting: structures, mechanisms and models. Recoding: Expansion of Decoding Rules Enriches Gene Expression 2010, 149-174. Springer. J.F. Atkins, R.F. Gesteland (Eds.).
20. Howard M.T., et al. Efficient stimulation of site-specific ribosome frameshifting by antisense oligonucleotides. RNA 2004, 10:1653-1661.
21. Yu C.H., et al. Stimulation of ribosomal frameshifting by RNA G-quadruplex structures. Nucleic Acids Res. 2014, 42:1887-1892.
22. Larsen B., et al. rRNA-mRNA base pairing stimulates a programmed -1 ribosomal frameshift. J. Bacteriol. 1994, 176:6842-6851.
23. Miller W.A., Giedroc D.P. Ribosomal frameshifting in decoding plant viral RNAs. Recoding: Expansion of Decoding Rules Enriches Gene Expression 2010, 193-220. Springer. J.F. Atkins, R.F. Gesteland (Eds.).
24. Somogyi P., et al. Ribosomal pausing during translation of an RNA pseudoknot. Mol. Cell. Biol. 1993, 13:6931-6940.
25. Lopinski J.D., et al. Kinetics of ribosomal pausing during programmed -1 translational frameshifting. Mol. Cell. Biol. 2000, 20:1095-1103.
26. Tu C., et al. Ribosomal movement impeded at a pseudoknot required for frameshifting. Proc. Natl. Acad. Sci. U.S.A. 1992, 89:8636-8640.
27. Caliskan N., et al. Programmed -1 frameshifting by kinetic partitioning during impeded translocation. Cell 2014, 157:1619-1631.
28. Yan S., et al. Ribosome excursions during mRNA translocation mediate broad branching of frameshift pathways. Cell 2015, 160:870-881.
29. Liao P.Y., et al. 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, 39:300-312.
30. Yelverton E., et al. The function of a ribosomal frameshifting signal from human immunodeficiency virus-1 in Escherichia coli. Mol. Microbiol. 1994, 11:303-313.
31. Fang Y., et al. Efficient -2 frameshifting by mammalian ribosomes to synthesize an additional arterivirus protein. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:E2920-E2928.
32. Dayhuff T.J., et al. Characterization of ribosomal frameshift events by protein sequence analysis. J. Biol. Chem. 1986, 261:7491-7500.
33. Jiang H., et al. Orsay virus utilizes ribosomal frameshifting to express a novel protein that is incorporated into virions. Virology 2014, 450-451:213-221.
34. Chen C., et al. Dynamics of translation by single ribosomes through mRNA secondary structures. Nat. Struct. Mol. Biol. 2013, 20:582-588.
35. Chen J., et al. Dynamic pathways of -1 translational frameshifting. Nature 2014, 512:328-332.
36. Kim H.K., et al. A frameshifting stimulatory stem loop destabilizes the hybrid state and impedes ribosomal translocation. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:5538-5543.
37. Brierley I., et al. Expression of a coronavirus ribosomal frameshift signal in Escherichia coli: influence of tRNA anticodon modification on frameshifting. J. Mol. Biol. 1997, 270:360-373.
38. Takyar S., et al. mRNA helicase activity of the ribosome. Cell 2005, 120:49-58.
39. Qin P., et al. Structured mRNA induces the ribosome into a hyper-rotated state. EMBO Rep. 2014, 15:185-190.
40. Fredrick K., Noller H.F. Accurate translocation of mRNA by the ribosome requires a peptidyl group or its analog on the tRNA moving into the 30S P site. Mol. Cell 2002, 9:1125-1131.
41. Qu X., et al. The ribosome uses two active mechanisms to unwind messenger RNA during translation. Nature 2011, 475:118-121.
42. Wen J.D., et al. Following translation by single ribosomes one codon at a time. Nature 2008, 452:598-603.
43. Yusupova G., et al. Structural basis for messenger RNA movement on the ribosome. Nature 2006, 444:391-394.
44. Mouzakis K.D., et al. HIV-1 frameshift efficiency is primarily determined by the stability of base pairs positioned at the mRNA entrance channel of the ribosome. Nucleic Acids Res. 2013, 41:1901-1913.
45. Houck-Loomis B., et al. An equilibrium-dependent retroviral mRNA switch regulates translational recoding. Nature 2011, 480:561-564.
46. Ritchie D.B., et al. Programmed -1 frameshifting efficiency correlates with RNA pseudoknot conformational plasticity, not resistance to mechanical unfolding. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:16167-16172.
47. Theis C., et al. KnotInFrame: prediction of -1 ribosomal frameshift events. Nucleic Acids Res. 2008, 36:6013-6020.
48. Harger J.W., et al. An 'integrated model' of programmed ribosomal frameshifting. Trends Biochem. Sci. 2002, 27:448-454.
49. Gupta P., et al. Regulation of gene expression by macrolide-induced ribosomal frameshifting. Mol. Cell 2013, 52:629-642.
50. Brierley I. Macrolide-induced ribosomal frameshifting: a new route to antibiotic resistance. Mol. Cell 2013, 52:613-615.
51. Beura L.K., et al. Cellular poly(C) binding proteins 1 and 2 interact with porcine reproductive and respiratory syndrome virus nonstructural protein 1β and support viral replication. J. Virol. 2011, 85:12939-12949.
52. Kwak H., et al. Annexin A2 binds RNA and reduces the frameshifting efficiency of infectious bronchitis virus. PLoS ONE 2011, 6:e24067.
53. Charbonneau J., et al. The 5' UTR of HIV-1 full-length mRNA and the Tat viral protein modulate the programmed -1 ribosomal frameshift that generates HIV-1 enzymes. RNA 2012, 18:519-529.
54. Gendron K., 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.
55. Kobayashi Y., et al. Identification of a cellular factor that modulates HIV-1 programmed ribosomal frameshifting. J. Biol. Chem. 2010, 285:19776-19784.
56. +]. FEBS Lett. 2009, 583:665-669.
57. Parker J. Errors and alternatives in reading the universal genetic code. Microbiol. Rev. 1989, 53:273-298.
58. Manickam N., et al. Studies of translational misreading in vivo show that the ribosome very efficiently discriminates against most potential errors. RNA 2014, 20:9-15.
59. Kramer E.B., Farabaugh P.J. The frequency of translational misreading errors in E. coli is largely determined by tRNA competition. RNA 2007, 13:87-96.
60. Kurland C.G. Translational accuracy and the fitness of bacteria. Annu. Rev. Genet. 1992, 26:29-50.
61. Tsuchihashi Z., Kornberg A. Translational frameshifting generates the gamma subunit of DNA polymerase III holoenzyme. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:2516-2520.
62. Huang W.M., et al. A persistent untranslated sequence within bacteriophage T4 DNA topoisomerase gene 60. Science 1988, 239:1005-1012.
63. Loughran G., et al. Evidence of efficient stop codon readthrough in four mammalian genes. Nucleic Acids Res. 2014, 42:8928-8938.
64. Lang B.F., et al. Massive programmed translational jumping in mitochondria. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:5926-5931.
65. Samatova E., et al. High-efficiency translational bypassing of non-coding nucleotides specified by mRNA structure and nascent peptide. Nat. Commun. 2014, 5:4459.
66. Mikuni O., et al. Sequence and functional analysis of mutations in the gene encoding peptide-chain-release factor 2 of Escherichia coli. Biochimie 1991, 73:1509-1516.
67. Matsufuji S., et al. Autoregulatory frameshifting in decoding mammalian ornithine decarboxylase antizyme. Cell 1995, 80:51-60.
68. Holtkamp W., et al. Synchronous tRNA movements during translocation on the ribosome are orchestrated by elongation factor G and GTP hydrolysis. Bioessays 2014, 36:908-918.
69. Ermolenko D.N., et al. Observation of intersubunit movement of the ribosome in solution using FRET. J. Mol. Biol. 2007, 370:530-540.
70. Mejlhede N., et al. Ribosomal -1 frameshifting during decoding of Bacillus subtilis cdd occurs at the sequence CGA AAG. J. Bacteriol. 1999, 181:2930-2937.
71. Brierley I., et al. An efficient ribosomal frame-shifting signal in the polymerase-encoding region of the coronavirus IBV. EMBO J. 1987, 6:3779-3785.
72. Bredenbeek P.J., et al. The primary structure and expression of the second open reading frame of the polymerase gene of the coronavirus MHV-A59; a highly conserved polymerase is expressed by an efficient ribosomal frameshifting mechanism. Nucleic Acids Res. 1990, 18:1825-1832.
73. Herold J., Siddell S.G. An 'elaborated' pseudoknot is required for high frequency frameshifting during translation of HCV 229E polymerase mRNA. Nucleic Acids Res. 1993, 21:5838-5842.
74. Su M.C., et al. An atypical RNA pseudoknot stimulator and an upstream attenuation signal for -1 ribosomal frameshifting of SARS coronavirus. Nucleic Acids Res. 2005, 33:4265-4275.
75. Pennell S., et al. The stimulatory RNA of the Visna-Maedi retrovirus ribosomal frameshifting signal is an unusual pseudoknot with an interstem element. RNA 2008, 14:1366-1377.
76. Morikawa S., Bishop D.H. Identification and analysis of the gag-pol ribosomal frameshift site of feline immunodeficiency virus. Virology 1992, 186:389-397.
77. Marcheschi R.J., et al. Programmed ribosomal frameshifting in SIV is induced by a highly structured RNA stem-loop. J. Mol. Biol. 2007, 373:652-663.
78. Jacks T., et al. Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 1988, 331:280-283.
79. Cornish P.V., et al. A loop 2 cytidine-stem 1 minor groove interaction as a positive determinant for pseudoknot-stimulated -1 ribosomal frameshifting. Proc. Natl. Acad. Sci U.S.A. 2005, 102:12694-12699.
80. Nixon P.L., et al. Thermodynamic analysis of conserved loop-stem interactions in P1-P2 frameshifting RNA pseudoknots from plant Luteoviridae. Biochemistry 2002, 41:10665-10674.
81. Dinman J.D., Wickner R.B. Ribosomal frameshifting efficiency and gag/gag-pol ratio are critical for yeast M1 double-stranded RNA virus propagation. J. Virol. 1992, 66:3669-3676.
82. Marczinke B., et al. The human astrovirus RNA-dependent RNA polymerase coding region is expressed by ribosomal frameshifting. J. Virol. 1994, 68:5588-5595.
83. den Boon J.A., et al. Equine arteritis virus is not a togavirus but belongs to the coronaviruslike superfamily. J. Virol. 1991, 65:2910-2920.
84. Snijder E.J., et al. The carboxyl-terminal part of the putative Berne virus polymerase is expressed by ribosomal frameshifting and contains sequence motifs which indicate that toro- and coronaviruses are evolutionarily related. Nucleic Acids Res. 1990, 18:4535-4542.
85. Wills N.M., et al. A functional -1 ribosomal frameshift signal in the human paraneoplastic Ma3 gene. J. Biol. Chem. 2006, 281:7082-7088.