Connection between stop codon reassignment and frequent use of shifty stop frameshifting

RNA

Volumn 15, Issue 5, 2009, Pages 889-897

  Vallabhaneni, Haritha ^a   Fan Minogue, Hua ^b   Bedwell, David M ^b   Farabaugh, Philip J ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

Codon reassignment; Euplotes octocarinatus; Programmed frameshifting; Saccharomyces cerevisiae; Tetrahymena thermophila; Translation termination

Indexed keywords

GLUTAMINE; PROTEIN ERF1; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; FRAMESHIFT MUTATION; MOLECULAR RECOGNITION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN STRUCTURE; STOP CODON;

ANIMALS; CODON, TERMINATOR; EUPLOTES; FRAMESHIFTING, RIBOSOMAL; GENETIC CODE; HUMANS; MODELS, MOLECULAR; PEPTIDE TERMINATION FACTORS; TETRAHYMENA THERMOPHILA;

EUPLOTES; EUPLOTES OCTOCARINATUS; MYXOZOA; SACCHAROMYCES CEREVISIAE; TETRAHYMENA THERMOPHILA;

EID: 65249136560     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1508109     Document Type: Article

References (76)

1. Lys anticodon explains tRNA's role in bacterial and mammalian ribosomal frameshifting and primer selection by HIV-1. RNA 3: 420-428.
2. Alkalaeva, E.Z., Pisarev, A.V., Frolova, L.Y., Kisselev, L.L., and Pestova, T.V. 2006. In vitro reconstitution of eukaryotic translation reveals cooperativity between release factors eRF1 and eRF3. Cell 125: 1125-1136.
3. Arkov, A.L., Korolev, S.V., and Kisselev, L.L. 1993. Termination of translation in bacteria may be modulated via specific interaction between peptide chain release factor 2 and the last peptidyl-tRNASer/Phe. Nucleic Acids Res. 21: 2891-2897.
4. Asakura, T., Sasaki, T., Nagano, F., Satoh, A., Obaishi, H., Nishioka, H., Imamura, H., Hotta, K., Tanaka, K., Nakanishi, H., et al. 1998. Isolation and characterization of a novel actin filament-binding protein from Saccharomyces cerevisiae. Oncogene 16: 121-130.
5. Belcourt, M.F. and Farabaugh, P.J. 1990. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell 62: 339-352.
6. Bertram, G., Bell, H.A., Ritchie, D.W., Fullerton, G., and Stansfield, I. 2000. Terminating eukaryote translation: Domain 1 of release factor eRF1 functions in stop codon recognition. RNA 6: 1236-1247.
7. Bidou, L., Stahl, G., Hatin, I., Namy, O., Rousset, J.P., and Farabaugh, P.J. 2000. Nonsense-mediated decay mutants do not affect programmed -1 frameshifting. RNA 6: 952-961.
8. Bonetti, B., Fu, L., Moon, J., and Bedwell, D.M. 1995. The efficiency of translation termination is determined by a synergistic interplay between upstream and downstream sequences in Saccharomyces cerevisiae. J. Mol. Biol. 251: 334-345.
9. Brierley, I., Meredith, M.R., Bloys, A.J., and Hagervall, T.G. 1997. Expression of a coronavirus ribosomal frameshift signal in Escherichia coli: Influence of tRNA anticodon modification on frameshifting. J. Mol. Biol. 270: 360-373.
10. Brown, C.M., Stockwell, P.A., Trotman, C.N.A., and Tate, W.P. 1990a. Sequence analysis suggests that tetra-nucleotides signal the termination of protein synthesis in eukaryotes. Nucleic Acids Res. 18: 6339-6345.
11. Brown, C.M., Stockwell, P.A., Trotman, C.N.A., and Tate, W.P. 1990b. The signal for the termination of protein synthesis in procaryotes. Nucleic Acids Res. 18: 2079-2086.
12. Carlson, B.A., Kwon, S.Y., Chamorro, M., Oroszlan, S., Hatfield, D.L., and Lee, B.J. 1999. Transfer RNA modification status influences retroviral ribosomal frameshifting. Virology 255: 2-8.
13. Chavatte, L., Seit-Nebi, A., Dubovaya, V., and Favre, A. 2002. The invariant uridine ofstop codons contacts the conserved NIKSR loop of human eRF1 in the ribosome. EMBO J. 21: 5302-5311.
14. Crick, F.H. 1968. The origin of the genetic code. J. Mol. Biol. 38: 367-379.
15. Ebihara, K. and Nakamura, Y. 1999. C-terminal interaction of translational release factors eRF1 and eRF3 of fission yeast: G-domain uncoupled binding and the role of conserved amino acids. RNA 5: 739-750.
16. Eisen, J.A., Coyne, R.S., Wu, M., Wu, D., Thiagarajan, M., Wortman, J.R., Badger, J.H., Ren, Q., Amedeo, P., Jones, K.M., et al. 2006. Macronuclear genome sequence of the ciliate Tetrahy- mena thermophila, a model eukaryote. PLoS Biol. 4: e286.
17. Eurwilaichitr, L., Graves, F.M., Stansfield, I., and Tuite, M.F. 1999. The C-terminus of eRF1 defines a functionally important domain for translation termination in Saccharomyces cerevisiae. Mol. Microbiol. 32: 485-496.
18. Fan-Minogue, H., Du, M., Pisarev, A.V., Kallmeyer, A.K., Salas- Marco, J., Keeling, K.M., Thompson, S.R., Pestova, T.V., and Bedwell, D.M. 2008. Distinct eRF3 requirements suggest alternate eRF1 conformations mediate peptide release during eukaryotic translation termination. Mol. Cell 30: 599-609.
19. Farabaugh, P.J. 1996. Programmed translational frameshifting. Microbiol. Rev. 60: 103-134.
20. Farabaugh, P., Liao, X.-B., Belcourt, M., Zhao, H., Kapakos, J., and Clare, J. 1989. Enhancer and silencerlike sites within the transcribed portion of a Ty2 transposable element of Saccharomyces cerevisiae. Mol. Cell. Biol. 9: 4824-834.
21. Frolova, L.Y., Simonsen, J.L., Merkulova, T.I., Litvinov, D.Y., Martensen, P.M., Rechinsky, V.O., Camonis, J.H., Kisselev, L.L., and Justesen, J. 1998. Functional expression of eukaryotic poly- peptide chain release factors 1 and 3 by means of baculovirus/ insect cells and complex formation between the factors. Eur. J. Biochem. 256: 36-44.
22. Frolova, L.Y., Tsivkovskii, R.Y., Sivolobova, G.F., Oparina, N.Y., Serpinsky, O.I., Blinov, V.M., Tatkov, S.I., and Kisselev, L.L. 1999. Mutations in the highly conserved GGQ motif of class 1 polypeptide release factors abolish abilityofhuman eRF1 to trigger peptidyl-tRNA hydrolysis. RNA 5: 1014-1020.
23. Frolova, L.Y., Merkulova, T.I., and Kisselev, L.L. 2000. Translation termination in eukaryotes: Polypeptide release factor eRF1 is composed of functionally and structurally distinct domains. RNA 6: 381-390.
24. Goldstein, J., Milman, G., Scolnick, E., and Caskey, T. 1970. Peptide chain termination. VI. Purification and site of action of S. Proc. Natl. Acad. Sci. 65: 430-437.
25. Hagervall, T., Tuohy, T., Atkins, J., and Bjork, G. 1993. Deficiency of 1-methylguanosine in tRNA from Salmonella typhimurium induces frameshifting by quadruplet translocation. J. Mol. Biol. 232: 756-765.
26. Hanyu, N., Kuchino, Y., Nishimura, S., and Beier, H. 1986. Dramatic events in ciliate evolution: Alteration of UAA and UAG termination codons to glutamine codons due to anticodon mutations in two Tetrahymena tRNAs. EMBO J. 5: 1307-1311.
27. Heurgue-Hamard, V., Champ, S., Mora, L., Merkoulova-Rainon, T., Kisselev, L.L., and Buckingham, R.H. 2005. The glutamine residue of the conserved GGQ motif in Saccharomyces cerevisiae release factor eRF1 is methylated by the product of the YDR140w gene. J. Biol. Chem. 280: 2439-2445.
28. Horowitz, S. and Gorovsky, M.A. 1985. An unusual genetic code in nuclear genes of Tetrahymena. Proc. Natl. Acad. Sci. 82: 2452-2455.
29. Inagaki, Y., Blouin, C., Doolittle, W.F., and Roger, A.J. 2002. Convergence and constraint in eukaryotic release factor 1 (eRF1) domain 1: The evolution of stop codon specificity. Nucleic Acids Res. 30: 532-544.
30. Ito, K., Ebihara, K., and Nakamura, Y. 1998. The stretch of C-terminal acidic amino acids of translational release factor eRF1 is a primary binding site for eRF3 of fission yeast. RNA 4: 958-972.
31. Ito, K., Frolova, L., Seit-Nebi, A., Karamyshev, A., Kisselev, L., and Nakamura, Y. 2002. Omnipotent decoding potential resides in eukaryotic translation termination factor eRF1 of variant-code organisms and is modulated by the interactions of amino acid sequences within domain 1. Proc. Natl. Acad. Sci. 99: 8494-8499.
32. Kervestin, S., Frolova, L., Kisselev, L., and Jean-Jean, O. 2001. Stop codon recognition in ciliates: Euplotes release factor does not respond to reassigned UGA codon. EMBO Rep. 2: 680-684.
33. Kim, O.T., Yura, K., Go, N., and Harumoto, T. 2005. Newly sequenced eRF1s from ciliates: The diversity of stop codon usage and the molecular surfaces that are important for stop codon interactions. Gene 346: 277-286.
34. Klobutcher, L.A. 2005. Sequencing of random Euplotes crassus macronuclear genes supports a high frequency of +1 translational frameshifting. Eukaryot. Cell 4: 2098-2105.
35. Klobutcher, L.A. and Farabaugh, P.J. 2002. Shifty ciliates. Frequent programmed translational frameshifting in euplotids. Cell 111: 763-766.
36. Knight, R.D. and Landweber, L.F. 2000. The early evolution of the genetic code. Cell 101: 569-572.
37. Knight, R.D., Freeland, S.J., and Landweber, L.F. 2001. Rewiring the keyboard: Evolvabilityofthe genetic code. Nat. Rev. Genet. 2: 49-58.
38. Kolosov, P., Frolova, L., Seit-Nebi, A., Dubovaya, V., Kononenko, A.,Oparina, N., Justesen, J., Efimov, A., and Kisselev, L. 2005. Invariant amino acids essential for decoding function of polypeptide release factor eRF1. Nucleic Acids Res. 33: 6418-6425.
39. Kuchino, Y., Hanyu, N., Tashiro, F., and Nishimura, S. 1985. Tetrahymena thermophila glutamine tRNA and its gene that corresponds to UAA termination codon. Proc. Natl. Acad. Sci. 82: 4758-4762.
40. 5Arg triggers the wild-type peptidyl-tRNA to frameshift. RNA 11: 796-807.
41. Lozupone, C.A., Knight, R.D., and Landweber, L.F. 2001. The molecular basis of nuclear genetic code change in ciliates. Curr. Biol. 11: 65-74.
42. Martin, R., Hearn, M., Jenny, P., and Gallant, J. 1988. Release factor competition is equivalent at strong and weakly suppressed nonsense codons. Mol. Gen. Genet. 213: 144-149.
43. Merkulova, T.I., Frolova, L.Y., Lazar, M., Camonis, J., and Kisselev, L.L. 1999. C-terminal domains of human translation termination factors eRF1 and eRF3 mediate their in vivo interaction. FEBS Lett. 443: 41-47.
44. Meyer, F., Schmidt, H.J., Plumper, E., Hasilik, A., Mersmann, G., Meyer, H.E., Engstrom, A., and Heckmann, K. 1991. UGA is translated as cysteine in pheromone 3 of Euplotes octocarinatus. Proc. Natl. Acad. Sci. 88: 3758-3761.
45. Morris, D.K. and Lundblad, V. 1997. Programmed translational frameshifting in a gene required for yeast telomere replication. Curr. Biol. 7: 969-976.
46. Mottagui-Tabar, S. and Isaksson, L.A. 1997. Only the last amino acids in the nascent peptide influence translation termination in Escherichia coli genes. FEBS Lett. 414: 165-170.
47. Oba, T., Andachi, Y., Muto, A., and Osawa, S. 1991. CGG: An unassigned or nonsense codon in Mycoplasma capricolum. Proc. Natl. Acad. Sci. 88: 921-925.
48. Osawa, S. and Jukes, T.H. 1989. Codon reassignment (codon capture) in evolution. J. Mol. Evol. 28: 271-278.
49. Osawa, S., Jukes, T., Watanabe, K., and Muto, A. 1992. Recent evidence for evolution of the genetic code. Microbiol. Rev. 56: 229-264.
50. Palanimurugan, R., Scheel, H., Hofmann, K., and Dohmen, R.J. 2004. Polyamines regulate their synthesis by inducing expression and blocking degradation of ODC antizyme. EMBO J. 23: 4857-4867.
51. Pande, S., Vimaladithan, A., Zhao, H., and Farabaugh, P.J. 1995. Pulling the ribosome out of frame +1 at a programmed frameshift site by cognate binding of aminoacyl-tRNA. Mol. Cell. Biol. 15: 298-304.
52. Plant, E.P., Wang, P., Jacobs, J.L., and Dinman, J.D. 2004. A programmed -1 ribosomal frameshift signal can function as a cis-acting mRNA destabilizing element. Nucleic Acids Res. 32: 784-790.
53. Poole, E.S., Brown, C.M., and Tate, W.P. 1995. The identity of the base following the stop codon determines the efficiency of in vivo translational termination in Escherichia coli. EMBO J. 14: 151-158.
54. Salas-Marco, J. and Bedwell, D.M. 2004. GTP hydrolysis by eRF3 facilitates stop codon decoding during eukaryotic translation termination. Mol. Cell. Biol. 24: 7769-7778.
55. Salas-Marco, J., Fan-Minogue, H., Kallmeyer, A.K., Klobutcher, L.A., Farabaugh, P.J., and Bedwell, D.M. 2006. Distinct paths to stop codon reassignment by the variant-code organisms Tetrahymena and Euplotes. Mol. Cell. Biol. 26: 438-447.
56. Santos, M.A., Cheesman, C., Costa, V., Moradas-Ferreira, P., and Tuite, M.F. 1999. Selective advantages created by codon ambiguity allowed for the evolution of an alternative genetic code in Candida spp. Mol. Microbiol. 31: 937-947.
57. Santos, M.A., Moura, G., Massey, S.E., and Tuite, M.F. 2004. Driving change: The evolution of alternative genetic codes. Trends Genet. 20: 95-102.
58. Gln isoaccep- tors as tools for studying unorthodox codon recognition and codon context effects during protein synthesis in vitro. Nucleic Acids Res. 22: 1974-1980.
59. Schultz, D.W. and Yarus, M. 1994. Transfer RNA mutation and the malleability of the genetic code. J. Mol. Biol. 235: 1377-1380.
60. Scolnick, E., Tompkins, R., Caskey, T., and Nirenberg, M. 1968. Release factors differing in specificity for terminator codons. Proc. Natl. Acad. Sci. 61: 768-774.
61. Seit-Nebi, A., Frolova, L., and Kisselev, L. 2002. Conversion of omnipotent translation termination factor eRF1 into ciliate-like UGA-only unipotent eRF1. EMBO Rep. 3: 881-886.
62. Song, H., Mugnier, P., Das, A.K., Webb, H.M., Evans, D.R., Tuite, M.F., Hemmings, B.A., and Barford, D. 2000. The crystal structure of human eukaryotic release factor eRF1-Mechanism of stop codon recognition and peptidyl-tRNA hydrolysis. Cell 100: 311-321.
63. Stahl, G., Bidou, L., Hatin, I., Namy, O., Rousset, J.P., and Farabaugh, P. 2000. The case against the involvement of the NMD proteins in programmed frameshifting. RNA 6: 1687-1688.
64. Stahl, G., Salem, S.N., Chen, L., Zhao, B., and Farabaugh, P.J. 2004. Translational accuracy during exponential, postdiauxic, and stationary growth phases in Saccharomyces cerevisiae. Eukaryot. Cell 3: 331-338.
65. Stansfield, I., Jones, K.M., Kushnirov, V.V., Dagkesamanskaya, A.R., Poznyakovski, A.I., Paushkin, S.V., Nierras, C.R., Cox, B.S., Tervanesyan, M.D., and Tuite, M.F. 1995. The products of the SUP45 (eRF1) and SUP35 genes interact to mediate translation termination in Saccharomyces cerevisiae. EMBO J. 14: 4365-4373.
66. Sundararajan, A., Michaud, W.A., Qian, Q., Stahl, G., and Farabaugh, P.J. 1999. Near-cognate peptidyl-tRNAs promote +1 programmed translational frameshifting in yeast. Mol. Cell 4: 1005-1015.
67. Suzuki, T., Ueda, T., and Watanabe, K. 1997. The "polysemous" codon-A codon with multiple amino acid assignment caused by dual specificity of tRNA identity. EMBO J. 16: 1122-1134.
68. Tate, W.P. and Mannering, S.A. 1996. Three, four or more: The translational stop signal at length. Mol. Microbiol. 21: 213-219.
69. Tourancheau, A.B., Tsao, N., Klobutcher, L.A., Pearlman, R.E., and Adoutte, A. 1995. Genetic code deviations in the ciliates: Evidence for multiple and independent events. EMBO J. 14: 3262-3267.
70. Urbonavicius, J., Qian, Q., Durand, J.M., Hagervall, T.G., and Bjork, G.R. 2001. Improvement of reading frame maintenance is a common function for several tRNA modifications. EMBO J. 20: 4863-4873.
71. Urbonavicius, J., Stahl, G., Durand, J.M., Ben Salem, S.N., Qian, Q., Farabaugh, P.J., and Bjork, G.R. 2003. Transfer RNA modifications that alter +1 frameshifting in general fail to affect -1 frameshift- ing. RNA 9: 760-768.
72. Vestergaard, B., Van, L.B., Andersen, G.R., Nyborg, J., Buckingham, R.H., and Kjeldgaard, M. 2001. Bacterial polypeptide release factor RF2 is structurally distinct from eukaryotic eRF1. Mol. Cell 8: 1375-1382.
73. Vimaladithan, A. and Farabaugh, P.J. 1994. Special peptidyl-tRNA molecules promote translational frameshifting without slippage. Mol. Cell. Biol. 14: 8107-8116.
74. Waas, W.F., Druzina, Z., Hanan, M., and Schimmel, P. 2007. Role ofa tRNA base modification and its precursors in frameshifting in eukaryotes. J. Biol. Chem. 282: 26026-26034. Weiss, R.B., Dunn, D.M., Atkins, J.F., and Gesteland, R.F. 1987.
75. Slippery runs, shifty stops, backward steps, and forward hops: -2, -1, +1, +2, +5, and +6 ribosomal frameshifting. Cold Spring Harb. Symp. Quant. Biol. 52: 687-693.
76. Zhouravleva, G., Frolova, L., Le Goff, X., Le Guellec, R., Inge- Vechtomov, S., Kisselev, L., and Philippe, M. 1995. Termination of translation in eukaryotes is governed by two interacting poly- peptide chain release factors, eRF1 and eRF3. EMBO J. 14: 4065-4072.