Advertisement

Role of Nonsense, Frameshift, and Missense Suppressor tRNAs in Mammalian Cells

  • D. Hatfield
  • B. J. Lee
  • D. W. E. Smith
  • S. Oroszlan
Chapter
Part of the Progress in Molecular and Subcellular Biology book series (PMSB, volume 11)

Abstract

Three classes of point mutations occur in nature: (1) missense; (2) nonsense; and (3) frameshift. Aminoacyl-tRNAs, which suppress mutations within each class, have been characterized in microorganisms; excellent reviews covering these studies have been published (Eggertsson and Sö11 1988; Hill 1975; Körner et al. 1978; Murgola 1985, 1989; Sherman 1982; Smith 1979; Steege and Söll 1979). The aminoacyl-tRNAs involved in suppression of point mutations are called missense, nonsense, and frameshift suppressors. Nonsense suppressors are further classified as amber, ochre, and opal when they suppress UAG, UAA, and UGA codons, respectively. Even though our understanding of the occurrence, structure, and function of suppressor tRNAs in mammalian cells is largely just beginning to emerge, it would seem that our interpretation of the role of suppressor tRNAs in mammalian cells may have to be altered from the classical viewpoint. That is, in microorganisms, suppressor tRNAs have largely been thought of as providing a mechanism of correcting or reversing deleterious mutations. It appears that suppressor tRNAs, when they occur in mammalian cells, have specialized functions and are not present in order to reverse the effect of deleterious mutations.

Keywords

Termination Codon Equine Infectious Anemia Virus Beet Necrotic Yellow Vein Virus Anticodon Loop Nonsense Suppression 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Barbacid M (1987) Ras genes. Annu Rev Biochem 56:779–827PubMedCrossRefGoogle Scholar
  2. Barciszewski J, Barciszewski M, Suter B, Kubli E (1985) Plant tRNA suppressors: in vivo readthrough properties and nucleotide sequence of yellow lupin seeds tRNAtYr. Plant Sci 40: 193–196CrossRefGoogle Scholar
  3. Baserga SJ, Benz EJ Jr (1988) Nonsense mutations in the human beta-globin gene affect mRNA metabolism. Proc Natl Acad Sci USA 85: 2056–2060PubMedCrossRefGoogle Scholar
  4. Beier H, Barciszewski M, Krupp G, Mitnacht R, Gross HJ (1984a) UAG readthrough during TMV RNA translation: isolation and sequence of two tRNAstY with suppressor activity from tobacco plants. EMBO J 3: 351–356PubMedGoogle Scholar
  5. Beier H, Barciszewski M, Sickinger H-D (1984b) The molecular basis for the differential translation of TMV RNA in tobacco protoplasts and wheat germ extracts. EMBO J 3: 1091–1096PubMedGoogle Scholar
  6. Bienz M, Kubli E (1981) Wild-type tRNATY/G reads the TMV RNA stop codon, but Q base-modified tRNATYr/Q does not. Nature 294: 188–190CrossRefGoogle Scholar
  7. Bienz M, Kubli E, Kohli J, de Henau S, Grosjean H (1980) Nonsense suppression in eukaryotes: the use of the Xenopus oocyte as an in vivo assay system. Nucleic Acids Research 8: 5169–5178Google Scholar
  8. Bienz M, Kubli E, Kohli J, de Henau S, Huez G, Marbaix G, Grosjean H (1981) Usage of three termination codons in a single eukaryotic cell, the Xenopus oocyte, Nucleic Acids Research 9: 3835–3850Google Scholar
  9. Björk GR, Erickson JU, Gustafsson CED, Hagervall TG, Jönsson YH, Wilkström PM (1987) Transfer RNA Modification. Annu Rev Biochem 56: 263–287PubMedCrossRefGoogle Scholar
  10. Böck A, Stadtman TC (1988) Selenocysteine, a highly specific component of certain enzymes, is incorporated by a UGA-directed co-translational mechanism. Biofactors 1: 245–250PubMedGoogle Scholar
  11. Bossi L (1983) Context effects: translation of UAG codon by suppressor tRNA is affected by the sequence following UAG in the message. J Mol Biol 164: 73–87PubMedCrossRefGoogle Scholar
  12. Brierly I, Boursnell ME, Binns MM, Bilimoria B, Block VC, Brown TDK, Inglis SC (1987) An efficient ribosomal frameshifting signal in the polymerase-encoding region of the corona-virus IBV. EMBO J 6: 3779–3785Google Scholar
  13. Bunn HF, Forget BG (1986) Hemoglobin: molecular, genetics and clinical aspects. Sanders, Philadelphia USAGoogle Scholar
  14. Capecchi MR, Vonder Haar RA, Capecchi NE, Sveda MM (1977) The isolation of a suppressible nonsense mutant in mammalian cells. Cell 12: 371–381PubMedCrossRefGoogle Scholar
  15. Role of Nonsense, Frameshift, and Missense Suppressor tRNAs in Mammalian Cells 139Google Scholar
  16. Capone JP, Sharp PA, RajBhandary UL (1985) Amber, ochre and opal suppressor tRNA genes derived from a human serine tRNA gene. EMBO J 4: 213–221PubMedGoogle Scholar
  17. Capone JP, Sedivy JM, Sharp PA, RajBhandary UL (1986) Introduction of UAG, UAA, and UGA nonsense mutations at a specific site in the Escherichia colt chloramphenicol acetyltransferase gene: use in measurement of amber, ochre, and opal suppression in mammalian cells. Mol Cell Biol 6: 3059–3067PubMedGoogle Scholar
  18. Celis JE, Piper PW (1981) Nonsense suppressors in eukaryotes. Trends Biochem Sci 6: 177–179CrossRefGoogle Scholar
  19. Chakrabarti L, Guyader M, Alizon M, Daniel MD, Desrosiers RC, Tiollais P, Sonigo P (1987) Sequence of simian immunodeficiency virus from macaque and its relationship to other human and simian retroviruses. Nature 328: 543–547PubMedCrossRefGoogle Scholar
  20. Chambers I, Harrison PR (1987) A new puzzle in selenoprotein biosynthesis: selenocysteine seems to be encoded by the ‘stop’ codon, UGA. Trends Biochem Sci 12: 255–256CrossRefGoogle Scholar
  21. Chambers I, Frampton J, Goldfarb P, Affara N, McBain W, Harrison PR (1986) The structure of the mouse gluthione peroxidase gene: the selenocysteine in the active site is encoded by the `termination’ codon, TGA. EMBO J 5: 1221–1227Google Scholar
  22. Chen S-H, Habib G, Yang C-Y, Gu Z-W, Lee BR, Weng S-A, Silberman SS, Cai S-J, Deslypere JP, Rosseneu M, Gotto AM Jr, Li W-H, Chan L (1987) Apolipoprotein B-48 is the product of a messenger RNA with an organ-specific in-frame stop codon. Science 238: 363–366PubMedCrossRefGoogle Scholar
  23. Craigan WJ, Caskey CT (1987) Translational frameshifting: where will it stop? Cell 50: 1–2CrossRefGoogle Scholar
  24. Cremer KJ, Bodemer M, Summers WP, Summers WC, Gesteland RF (1979) In vitro suppression of UAG and UGA mutants in the thymidine kinase gene of Herpes simplex virus. Proc Natl Acad Sci USA 76: 430–434PubMedCrossRefGoogle Scholar
  25. Crick FHA (1966) Codon-anticodon pairing: the wobble hypothesis. J Mol Biol 19: 548–555PubMedCrossRefGoogle Scholar
  26. Davidson NO, Powell LM, Wallis SC, Scott J (1988) Thyroid hormone modulates the introduction of a stop codon in rat liver apolipoprotein B messenger RNA. J Biol Chem 263: 13482–13485PubMedGoogle Scholar
  27. Dayhuff TJ, Atkins JF, Gesteland RF (1986) Characterization of ribosomal frameshift events by protein sequence analysis. J Biol Chem 261: 7491–7500PubMedGoogle Scholar
  28. Diamond A, Dudock B, Hatfield D (1981) Structure and properties of a bovine liver UGA suppressor serine tRNA with a tryptophan anticodon. Cell 25: 497–506PubMedCrossRefGoogle Scholar
  29. Efstratiadis A, Kafatos F, Maniatis T (1977) The primary structure of rabbit ß-globin mRNA as determined from cloned DNA. Cell 10: 571–585PubMedCrossRefGoogle Scholar
  30. Eggertsson G, Söll D, (1988) Transfer ribonucleic acid-mediated suppression of termination codons. Microbiol Rev 52: 354–374PubMedGoogle Scholar
  31. Engelberg-Kulka H, Schoulaker-Schwarz R (1988a) Stop is not the end: physiological implications of translational readthrough. J Theor Biol 131: 477–485PubMedCrossRefGoogle Scholar
  32. Engelberg-Kulka H, Schoulaker-Schwarz R (1988b) A flexible genetic code, or why does selenocysteine have no unique codon? Trends Biochem Sci 13: 419–421PubMedCrossRefGoogle Scholar
  33. Feng Y-X, Dong L, Zhang Y (1986) Homogeneous sequence in the anticodon of natural UAG suppressor tRNATYr. Acta Biochim Biophys Sinica 18: 90–95Google Scholar
  34. Feng Y-X, Hatfield D, Rein A, Levin JG (1989a) Translational readthrough of the murine leukemia virus gag gene amber codon does not require virus-induced alteration of tRNA. J Virol 63: 2405–2410PubMedGoogle Scholar
  35. Feng Y-X, Levin J, Hatfield D, Schaefer T, Gorelick R, Rein A (1989b) Suppression of UAA and UGA termination codons in mutant murine leukemia virus. J Virol 63: 2870–2873PubMedGoogle Scholar
  36. Franchini G, Gurgo C, Guo H-G, Gallo RC, Collalti E, Fragnoli KA, Hall LF, Wong-Stahl F, Reitz MS (1987) Sequence of simian immunodeficiency virus and its relationship to the human immunodeficiency viruses. Nature 328: 539–543PubMedCrossRefGoogle Scholar
  37. Geller AI, Rich A (1980) UGA termination suppression tRNAT`P active in rabbit reticulocytes. Nature 283: 41–46PubMedCrossRefGoogle Scholar
  38. Gesteland R, Wills N (1979) Use of yeast suppressors for identification of adenovirus nonsense mutants. In: Celis JE, Smith JD (eds) Nonsense mutations and tRNA suppressors. Academic Press, London, pp 277–284Google Scholar
  39. Gesteland RF, Wills N, Lewis JB, Grodzicker T (1977) Identification of amber and ochre mutants of the human virus Ad2 + ND1. Proc Natl Acad Sci USA 74: 4567–4571PubMedCrossRefGoogle Scholar
  40. Guyader M, Emerman M, Sonigo P, Clavel F, Montagnier L, Alizon M (1987) Genome organization and transactivation of the human immunodeficiency virus type 2. Nature 326: 662–669PubMedCrossRefGoogle Scholar
  41. Hardman DA, Protter AA, Schilling JW, Kane JP (1987) Carboxyl terminal analysis of human B-48 protein confirms the novel mechanism proposed for chain termination. Biochem Biophys Res Commun 149: 1214–1219PubMedCrossRefGoogle Scholar
  42. Harley CB, Pollard JW, Stanners CP, Goldstein S (1981) Model for messenger RNA translation during amino acid starvation applied to the calculation of protein synthetic error rates. J Biol Chem 156: 10786–10794Google Scholar
  43. Hatfield D (1972) Recognition of nonsense codons in mammalian cells. Proc Natl Acad Sci USA 69: 3014–3018PubMedCrossRefGoogle Scholar
  44. Hatfield D (1985) Suppression of termination codons in higher eukaryotes. Trends Biochem Sci 10: 201–204CrossRefGoogle Scholar
  45. Hatfield D, Nirenberg M (1971) Binding of radioactive oligonucleotides to ribosomes Biochemistry 10: 4318–4323Google Scholar
  46. Hatfield D, Portugal FH (1970) Seryl-tRNA in mammalian tissues: chromatographic differences in brain and liver and a specific response to the codon UGA. Proc Natl Acad Sci USA 67: 1200–1206PubMedCrossRefGoogle Scholar
  47. Hatfield D, Rice M (1986) Aminoacyl-tRNA (anticodon): codon adaptation in human and rabbit reticulocytes. Biochem Int 13: 835–842PubMedGoogle Scholar
  48. Hatfield D, Matthews CR, Rice M (1979) Aminoacyl-transfer RNA populations in mammalian cells: chromatographic profiles and patterns of codon recognition. Biochim Biophys Acta 564: 414–423PubMedGoogle Scholar
  49. Hatfield D, Diamond A, Dudock B (1982a) Opal suppressor serine tRNAs from bovine liver form phosphoseryl-tRNA. Proc Natl Acad USA 79: 6215–6219CrossRefGoogle Scholar
  50. Hatfield D, Varricchio F, Rice M, Forget BG (1982b) The aminoacyl-tRNA population of human reticulocytes. J Biol Chem 257: 3183–3188PubMedGoogle Scholar
  51. Hatfield D, Dudock BS, Eden FC (1983) Characterization and nucleotide sequence of a chicken gene encoding an opal suppressor tRNA and its flanking DNA segments. Proc Natl Acad Sci USA 80: 4940–4944PubMedCrossRefGoogle Scholar
  52. Hatfield D, Thorgeirsson SS, Copeland TD, Oroszlan S, Bustin M (1988) Immunopurification of the suppressor tRNA dependent rabbit beta-globin readthrough protein. Biochemistry 27: 1179–1183PubMedCrossRefGoogle Scholar
  53. Hatfield D, Feng Y-X, Lee BJ, Rein A, Levin JG, Oroszlan S (1989) Chromatographic analysis of aminoacyl-tRNAs which are required for translation of codons at and around the ribosomal frameshift sites in HIV, HTLV-I, and BLV. Virology 173: 736–742Google Scholar
  54. Hatfield D, Smith DWE, Lee BJ, Worland PJ, Oroszlan S (1989) Structure and function of suppressor tRNAs in higher eukaryotes. CRC critical reviews in biochemistry. CRC PressGoogle Scholar
  55. Herr W (1984) Nucleotide sequence of AKV murine leukemia virus. J Virol 49: 471–478PubMedGoogle Scholar
  56. Higuchi K, Hospattankar AV, Law SW, Meglin N, Cortright J, Brewer HB Jr (1988) Human apolipoprotein B (apoB) mRNA: identification of two distinct apoB mRNAs, an mRNA with the apo-B-100 sequence and an apoB mRNA containing a premature in-frame translational stop codon, in both liver and intestine. Proc Natl Acad Sci USA 85: 1772–1776PubMedCrossRefGoogle Scholar
  57. Hill CW (1975) Informational suppression of missense mutations. Cell 6: 419–427CrossRefGoogle Scholar
  58. Hiramatsu K, Nishida J, Naito A, Yoshikura H (1987) Molecular cloning of the closed circular provirus of human T cell leukemia virus type I: a new open reading frame in the gag-pol region. J Gen Virol 68: 213–218PubMedCrossRefGoogle Scholar
  59. Hizi A, Henderson LE, Copeland TD, Sowder RC, Hixson CV, Oroszlan S (1987) Characterization of mouse tumor virus gag-pol gene products and the ribosomal frameshift site by protein sequencing. Proc Natl Acad Sci USA 84: 7041–7045PubMedCrossRefGoogle Scholar
  60. Ho Y-S, Kan YW (1987) In vivo aminoacylation of human and Xenopus suppressor tRNAs constructed by site-specific mutagenesis. Proc Natl Acad Sci USA 84: 2185–2188PubMedCrossRefGoogle Scholar
  61. Ho Y-S, Norton GP, Palese P, Dozy AM, Kan YW (1986) Expression and function of suppressor tRNA genes in mammalian cells. Cold Spring Harbor Symposium on Quantitative Biology vol 51, Cold Spring Harbor, New York, pp 1033–1040Google Scholar
  62. Hudziak RM, Laski FA, RajBhandary UL, Sharp PA, Capecchi MR (1982) Establishment of Role of Nonsense, Frameshift, and Missense Suppressor tRNAs in Mammalian Cells 141 mammalian cell lines containing multiple nonsense mutations and functional suppressor tRNA genes. Cell 31: 137–146PubMedCrossRefGoogle Scholar
  63. Inoue J-I, Watanabe T, Sato M, Oda A, Toyoshima K, Yoshida M, Seiki M (1986) Nucleotide sequence of the protease-coding region in an infectious DNA of simian retrovirus (STLV) of the HTLV-1 family. Virology 150: 187–195PubMedCrossRefGoogle Scholar
  64. Ishikawa M, Meshi T, Motoyoshi F, Takamatsu N, Okada Y (1986) In vitro mutagenesis of the putative replicase genes of tobacco mosaic virus. Nucleic Acids Res 14: 8291–8305PubMedCrossRefGoogle Scholar
  65. Jacks T, Varmus HE (1985) Expression of the Rous sarcoma virus pol gene by ribosomal frameshifting. Science 230: 1237–1242PubMedCrossRefGoogle Scholar
  66. Jacks T, Townsley K, Varmus HE, Majors J (1987) Two efficient ribosomal frameshifting events are required for synthesis of mouse mammary tumor virus gag-related polyproteins. Proc Natl Acad Sci USA 84: 4298–4302PubMedCrossRefGoogle Scholar
  67. Jacks T, Madhani HD, Masiraz FR, Varmus HE (1988a) Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell 55: 447–458PubMedCrossRefGoogle Scholar
  68. Jacks T, Power MD, Masiarz FR, Luciw PA, Barr PJ, Varmus H (1988b) Characterization of ribosomal frameshifting in HIV-1 gag-pol expression. Nature 331: 280–283PubMedCrossRefGoogle Scholar
  69. Jackson RJ, Hunt T (1983) Preparation and use of nuclease-treated rabbit reticulocyte lysates for the translation of eukaryotic messenger RNA. Methods Enzymol 96: 50–74PubMedCrossRefGoogle Scholar
  70. Jank P, Shindo-Okada N, Nishimura S, Gross HJ (1977) Rabbit liver tRNA: primary structure and unusual codon recognition. Nucletic Acids Res 4: 1999–2008CrossRefGoogle Scholar
  71. Johnson PF, Abelson J (1983) The yeast tRNATY gene intron is essential for correct modification of its tRNA product. Nature 302: 681–687PubMedCrossRefGoogle Scholar
  72. Kato N, Hoshino H, Harada F (1983) Minor serine tRNA containing anticodon NCA(C4 RNA) from human and mouse cells. Biochem Int 7: 635–645PubMedGoogle Scholar
  73. Kawakami T, Sherman L, Dahlberg J, Gazit A, Yaniv A, Tronick SR, Aaronson SA (1987) Nucleotide sequence analysis of equine infectious anemia virus proviral DNA. Virology 158: 300–312PubMedCrossRefGoogle Scholar
  74. Kohli J, Grosjean H (1981) Usage of the three termination codons: compilation and analysis of known eukaryotic and prokaryotic translation termination sequences. Mol Gen Genet 182: 430–439PubMedCrossRefGoogle Scholar
  75. Kohli J, Kwong T, Altruda F, Söll D (1979) Characterization of a UGA-suppressing serine tRNA from Schizosaccharomyces pombe with the help of a new in vitro assay system for eukaryotic suppressor tRNAs. J Biol Chem 254: 1546–1551PubMedGoogle Scholar
  76. Körner AM, Freinstein SI, Altman S (1978) Transfer RNA-mediated suppression. In: Altman S (ed) Transfer RNA. MIT Press, Cambridge, pp 105–135Google Scholar
  77. Kubli E, Schmidt T, Martin PF, Sofer W (1982) In vitro suppression of a nonsense mutant of Drosophila melanogaster. Nucleic Acids Res 10: 7145–7152PubMedCrossRefGoogle Scholar
  78. Kuchino Y, Borek E, Grunberger D, Mushinski J, Nishimura S (1982) Changes of post-transcriptional modification of Wye base in tumor-specific tRNAPh`. Nucleic Acids Res 10: 6421–6432PubMedCrossRefGoogle Scholar
  79. Kuchino Y, Beier H, Akita N, Nishimura S (1987) Natural UAG suppressor glutamine tRNA is elevated in mouse cells infected with Moloney murine leukemia virus. Proc Natl Acad Sci USA 84: 2668–2672PubMedCrossRefGoogle Scholar
  80. Kuchino Y, Nishimura S, Schröder HC, Rottmann M, Müller WEG (1988) Selective inhibition of formation of suppressor glutamine tRNA in Moloney murine leukemia virus-infected NIH-3T3 cells by Avarol. Virology 165: 518–526PubMedCrossRefGoogle Scholar
  81. Laski FA, Belagaje R, RajBhandary UL, Sharp PA (1982) An amber suppressor tRNA gene derived by site-specific mutagenesis: cloning and function in mammalian cells. Proc Natl Acad Sci USA 79: 5813–5817PubMedCrossRefGoogle Scholar
  82. Laski FA, Belagaje R, Hudziak RM, Capecchi MR, Norton GP, Palese P, RajBhandary UL, Sharp PA (1984) Synthesis of an ochre suppressor tRNA gene and expression in mammalian cells. EMBO J 3: 2445–2452PubMedGoogle Scholar
  83. Lee BJ, Kang SG, Hatfield D (1989a) Transcription of Xenopus selenocysteyl-tRNAs (formerly designated opal suppressor phosphoserine tRNA) is directed by mutiple 5’ extra-genic regulatory elements. J Biol Chem 264: 9696–9702Google Scholar
  84. Lee BJ, de la Peria P, Tobian JA, Zasloff M, Hatfield D (1987) Unique pathway of expression of an opal suppressor phosphoserine tRNA. Proc Natl Acad Sci USA 84: 6384–6388PubMedCrossRefGoogle Scholar
  85. Lee BJ, Worland PJ, Davis J, Stadium TC, Hatfield D (1989b) Identification of a selenocysteyl-tRNAser in mammalian cells which recognizes the nonsense codon, UGA. J Biol Chem 264: 9724–9727Google Scholar
  86. Lehrman MA, Goldstein JL, Brown MS, Russell DW, Schneider WJ (1985) Internalization-defective LDL receptors produced by genes with nonsense and frameshift mutations that truncate the cytoplasmic domain. Cell 41: 735–743PubMedCrossRefGoogle Scholar
  87. Leinfelder W, Zehelein E, Mandrand-Berthelot M-A, Böck A (1988) Gene for a novel tRNA species that accepts L-serine and cotranslationally inserts selenocysteine. Nature 331: 723–725PubMedCrossRefGoogle Scholar
  88. Leinfelder W, Stadtman TC, Böck A (1989) Occurrence in vivo of selenocysteyl-tRNASe’ in Escherichia coli: effect of sel mutants. J Biol Chem 264: 9720–9723PubMedGoogle Scholar
  89. Li G, Rice CM (1989) Mutagenesis of the in-frame opal termination codon preceeding nsP4 of Sindbis virus: studies of translational readthrough and its effect on virus replication. J Virol 63: 1326–1337PubMedGoogle Scholar
  90. Lin JP, Aker M, Sitney KC, Mortimer RL (1986) First position wobble in codon-anticodon pairing: amber suppression by a yeast glutamine tRNA. Gene 49: 383–388PubMedCrossRefGoogle Scholar
  91. Mäenpää PH (1972) Seryl transfer RNA alterations during estrogen-induced phosvitin synthesis: quantitative assay of the hormone-responding species by ribosomal binding. Biochem Biophys Res Commun 47: 971–974PubMedCrossRefGoogle Scholar
  92. Mäenpää PH, Bernfield MR (1970) A specific hepatic transfer RNA for phosphoserine. Proc Natl Acad Sci USA 67: 688–695PubMedCrossRefGoogle Scholar
  93. Marlor RL, Parkhurst SM, Corces VG (1986) The Drosophila melanogaster gypsy transposable elements encodes putative gene products homologous to retroviral proteins. Mol Cell Biol 6: 1129–1134PubMedGoogle Scholar
  94. Marotta C, Wilson J, Forget BG, Weissman S (1977) Human globin messenger RNA: nucleotide sequences derived from complementary DNA. J Biol Chem 252: 5040–5053PubMedGoogle Scholar
  95. McAdam RA, Goundis D, Reid KBM (1988) A homozygous point mutation results in a stop codon in the CIgB-chain of a Clq-deficient individual Immunogenetics 27: 259–264Google Scholar
  96. McBride OW, Rajagopalan M, Hatfield D (1987) Opal suppressor phosphoserine tRNA gene and pseudogene are located on human chromosomes 19 and 22, respectively. J Biol Chem 262: 11163–11166PubMedGoogle Scholar
  97. McBride OW, Mitchell A, Lee BJ, Mullenbach G, Hatfield D (1988) Gene for selenium-dependent glutathione peroxidase maps to human chromosomes 3, 21, and X. BioFactors 1: 285–292Google Scholar
  98. Meier F, Suter B, Grosjean H, Keith G, Kubli E (1985) Queuosine modification of the wobble base in tRNA’s influences in vivo decoding properties. EMBO J 4: 823–827PubMedGoogle Scholar
  99. Mietz JA, Grossman Z, Lueders KK, Kuff EL (1987) Nucleotide sequence of a complete mouse intracisternal A-particle genome: relationship to known aspects of particle assembly and function. J Virol 61: 3020–3029PubMedGoogle Scholar
  100. Miller JH, Albertini AM (1983) Effects of surrounding sequence on the suppression of nonsense codons. J Mol Biol 164: 59–71PubMedCrossRefGoogle Scholar
  101. Mizutani T, Hashimoto A (1984) Purification and properties of suppressor seryl-tRNA: ATP phosphotransferase from bovine liver. FEBS Lett 169: 319–322PubMedCrossRefGoogle Scholar
  102. Mizutani T, Hitaka T (1988) Stronger affinity of reticulocyte release factor than natural suppressor tRNAse’ for the opal termination codon. FEBS Lett 226: 227–231PubMedCrossRefGoogle Scholar
  103. Mizutani T, Tachibana Y (1986) Possible incorporation of phosphoserine into globin readthrough protein via bovine opal suppressor phosphoseryl-tRNA. FEBS Lett 207: 162–166PubMedCrossRefGoogle Scholar
  104. Mizutani T, Narihara T, Hashimoto A (1984) Purification and properties of bovine liver seryltRNA synthetase. Eur J Biochem 143: 9–13PubMedCrossRefGoogle Scholar
  105. Mizutani T, Kanbe K, Kimura Y, Tachibana Y, Hitaka T (1988) Non-partition of opal suppressor phosphoseryl-transfer ribonucleic acid (tRNA) in phosphoserine aminotransferase catalysis. Chem Pharm Bull 36: 824–827PubMedGoogle Scholar
  106. Moore R, Dixon M, Smith R, Peters G, Dickson C (1987) Complete nucleotide sequence of a milk-transmitted mouse mammary tumor virus: two frameshift suppression events are required for translation of gag and pol. J Virol 61: 480–490PubMedGoogle Scholar
  107. Role of Nonsense, Frameshift, and Missense Suppressor tRNAs in Mammalian Cells 143Google Scholar
  108. Mullenback GT, Tabrizi A, Irvine BD, Bell GI, Hallewell RA (1987) Sequence of a cDNA coding for human glutathione peroxidase confirms TGA encodes active site selenocysteine. Nucleic Acids Res 15: 5484CrossRefGoogle Scholar
  109. Mullenback GT, Tabrizi A, Irvine BD, Bell GI, Tainer JA, Hallewell RA (1988) Selenocysteine’s mechanism of incorporation and evolution revealed in cDNAs of three glutathione peroxidases. Protein Engineer 2: 239–246CrossRefGoogle Scholar
  110. Müller WEG, Schröder HC, Reuter P, Sarin PS, Hess G, Meyer zum Büschenfelde K-H, Kuchino Y, Nishimura S (1988) Inhibition of expression of natural UAG suppressor glutamine tRNA in HIV-infected human H9 cells in vitro by Avarol. AIDS Res Human Retrovir 4: 279–286CrossRefGoogle Scholar
  111. Murgola EJ (1985) tRNA, suppression, and the code. Annu Rev Genet 19:57–80PubMedCrossRefGoogle Scholar
  112. Murgola EJ (1989) Mutant glycine tRNAs and other wonders of translation suppression. In: Cherayil JD (ed) Transfer RNAs and other soluble RNAs. CRC Press, Boca RatonGoogle Scholar
  113. Murphy EC Jr, Wills N, Arlinghaus RB (1980) Suppression of murine retrovirus polypeptide termination: effect of amber suppressor tRNA on the cell-free translation of Rauscher murine leukemia virus, Moleney murine leukemia virus, and Moloney murine sarcoma virus 124 RNA. J Virol 34: 464–473PubMedGoogle Scholar
  114. Nam SH, Kidokoro M, Shida H, Hatanka M (1988) Processing of gag precursor polyprotein of human T-cell leukemia virus type I by virus-encoded protease. J Virol 62: 3718–3728PubMedGoogle Scholar
  115. Nirenberg M, Leder P (1964) RNA codewords and protein synthesis: the effect of trinculeotides upon the binding of sRNA to ribosomes. Science 145: 1399–1407PubMedCrossRefGoogle Scholar
  116. O’Neill VA, Eden FC, Pratt K, Hatfield D (1985) A human opal suppressor tRNA gene and pseudogene. J Biol Chem 260: 2501–2508PubMedGoogle Scholar
  117. Panganiban AT (1988) Retroviral gag gene amber codon suppression is caused by an intrinsic cis-acting component of the viral mRNA. J Virol 62: 3574–3580PubMedGoogle Scholar
  118. Parker J, Pollard JW, Friesen JD, Stanners CP (1978) Stuttering: high-level mistranslation in animal and bacterial cells. Proc Natl Acad Sci USA 75: 1091–1095PubMedCrossRefGoogle Scholar
  119. Pelham HRB (1978) Leaky UAG termination codon in tobacco mosaic virus RNA. Nature 272: 469–471PubMedCrossRefGoogle Scholar
  120. Philipson L, Andersson P, Olshevsky U, Weinberg R, Baltimore D (1978) Translation of MuLV and MSV RNAs in nuclease-treated reticulocyte extracts: enhancement of the gag-pol polypeptide with yeast suppressor tRNA. Cell 13: 189–199PubMedCrossRefGoogle Scholar
  121. Pollard J, Harley CB, Chamberlin JW, Goldstein S, Stanners CP (1982) Is transformation associated with an increased error frequency in mammalian cells? J Biol Chem 257: 5977–5979PubMedGoogle Scholar
  122. Powell LM, Wallis SC, Pease RJ, Edwards YH, Knott TJ, Scott J (1987) A novel form of tissue- specific RNA processing produces apolipoprotein-B48 in intestine. Cell 50: 831–840PubMedCrossRefGoogle Scholar
  123. Power MD, Marx PA, Bryant ML, Gardner MB, Barr PJ, Luciw PA (1986) Nucleotide sequence of SRV-1, a type D simian acquired immune deficiency syndrome retrovirus. Science 231: 1567–1572PubMedCrossRefGoogle Scholar
  124. Pratt K, Eden FC, You KH, O’Neill VA, Hatfield D (1985) Conserved sequences in both coding and 5’ flanking regions of mammalian opal suppressor tRNA genes. Nucleic Acids Res 13: 4765–4775PubMedCrossRefGoogle Scholar
  125. Pure GA, Robinson GW, Naumovski L, Friedberg EC (1985) Partial suppression of an ochre mutation in Saccharomyces cerevisiae by multicopy plasmids containing a normal yeast tRNAG’ gene. J Mol Biol 183: 31–42PubMedCrossRefGoogle Scholar
  126. Raba M, Limberg K, Burghagen M, Katze JR, Simsek M, Heckman JE, RajBhandary UL, Gross HJ (1979) Nucleotide sequence of three isoaccepting lysine tRNAs from rabbit liver and SV40-transformed mouse fibroblast. Eur J Biochem 97: 305–318PubMedCrossRefGoogle Scholar
  127. Ratner L, Haseltine W, Patarca R, Livak KJ, Starcich B, Josephs SF, Doran ER, Rafalski JA, Whitehorn EA, Baumeister K, Ivanoff J, Petteway SR, Pearson ML, Lautenberger JA, Papas TS, Ghrayeb J, Chang NT, Gallo RC, Wong-Staal F (1985) Complete nucleotide sequence of the AIDS virus, HTLV-III. Nature 313: 277–284Google Scholar
  128. Reddy AP, Hsu BL, Reddy PS, Li N-Q, Thyagaraju K, Reddy CC, Tam MF, Tu C-PD (1988) Expression of glutathione peroxidase I gene in selenium-deficient rats. Nucleic Acids Res 16: 5557–5568PubMedCrossRefGoogle Scholar
  129. Rice N R, Stephens R, Burny A, Gilden R (1985) The gag and pol genes of bovine leukemia virus: nucleotide sequence and analysis. Virology 142: 357–377PubMedCrossRefGoogle Scholar
  130. Roberts BE, Paterson BM (1973) Efficient translation of tobacco mosaic virus RNA and rabbit globin 9S RNA in a cell-free system from commercial wheat germ. Proc Natl Acad Sci USA 70: 2330–2334PubMedCrossRefGoogle Scholar
  131. Romeo G. Hassan HJ, Staempfli S, Roncuzzi L, Cianetti L, Leonardi A, Vicente V, Mannucci PM, Bertina R, Peschle C, Cortese R (1987) Hereditary thrombophilia: identification of nonsense and missense mutations in the protein C gene. Proc Natl Acad Sci USA 84: 2829–2832PubMedCrossRefGoogle Scholar
  132. Sagata N, Yasunaga T, Tsuzuku-Kawamura J, Ohishi K, Ogawa Y, Ikawa Y (1985) Complete nucleotide sequence of the genome of bovine leukemia virus: its evolutionary relationship to other retroviruses. Proc Natl Acad Sci USA 82: 677–681PubMedCrossRefGoogle Scholar
  133. Saigo K, Kugiyama W, Matsuo Y, Inouye S, Yoshioka K, Yuki S (1984) Identification of the coding sequence for a reverse transcriptase-like enzyme in a transposable genetic element in Drosophila melanogaster. Nature 312: 659–663PubMedCrossRefGoogle Scholar
  134. Sanchez-Pescador R, Power MD, Barr PJ, Steimer KS, Stempien MM, Brown-Shimer SL, Gee WW, Renard A, Randolph A, Levy JA, Dina D, Luciw PA (1985) Nucleotide sequence and expression of AIDS-associated retrovirus (ARV-2). Science 227: 484–492PubMedCrossRefGoogle Scholar
  135. Satoh K, Nukiwa T, Brantly M, Garver RI Jr, Hofker M, Courtney M, Crystal RG (1988) Emphysema associated with complete absence of al-antitrypsin of a stop codon in an alantitrypsin-coding exon. Am J Human Genet 42: 77–83Google Scholar
  136. Schwartz DE, Tizard R, Gilbert W (1983) Nucleotide sequence of Rous sarcoma virus. Cell 32: 853–869PubMedCrossRefGoogle Scholar
  137. Sedivy JM, Capone JP, RajBhandary UL, Sharp PA (1987) An inducible mammalian amber suppressor: propagation of a poliovirus mutant. Cell 50: 379–389PubMedCrossRefGoogle Scholar
  138. Seiki M, Hattori S, Hirayama Y, Yoshida M (1983) Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci USA 80: 3618–3622PubMedCrossRefGoogle Scholar
  139. Sharp SJ, Stewart TS (1977) The characterization of phosphoseryl tRNA from lactating bovine mammary gland. Nucleic Acids Res 4: 2123–2136PubMedCrossRefGoogle Scholar
  140. Sherman F (1982) Suppression in yeast Saccharomyces cerevisiae. In: Strathern JN, Jones EW, Broach JR (eds) Molecular biology of the yeast Saccharomyces; metabolism and gene expression. Cold Spring Harbor Laboratories, New York, pp 463–486Google Scholar
  141. Shimotohno K, Takahashi Y, Shimizu N, Gojobori T, Golde DW, Chen IS, Miwa M, Sugimura T (1985) Complete nucleotide sequence of an infectious clone of human T-cell leukemia virus type II: an open reading frame for the protease gene. Proc Natl Acad Sci USA 82: 3101–3105PubMedCrossRefGoogle Scholar
  142. Shindo-Okada N, Akimoto H, Nomura H, Nishmura S (1985) Recognition of UAG termination codon by mammalian tyrosine tRNA containing 6-thioqueuine in the first position of the anticodon. Proc Jpn Acad 61: 94–98CrossRefGoogle Scholar
  143. Shinnick TM, Lerner RA, Sutclife JG (1981) Nucleotide sequence of Moloney murine leukemia virus. Nature 293: 543–548PubMedCrossRefGoogle Scholar
  144. Smith DWE, Hatfield D (1986) Effects of post-translational base modifications on the site- specific function of transfer RNA in eukaryote translation. J Mol Biol 189: 663–671PubMedCrossRefGoogle Scholar
  145. Smith DWE, McNamara AL (1982) The effect of the Q base modification on the usage of tRNAH’s in globin synthesis. Biochem Biophys Res Commun 104: 1459–1463PubMedCrossRefGoogle Scholar
  146. Smith DWE, McNamara A, Rice M, Hatfield D (1981) The effects of a post-transcriptional modification on the function of tRNA isoaccepting species in translation. J Biol Chem 256: 10033–10036PubMedGoogle Scholar
  147. Smith DWE, McNamara AL, Mushinski JF, Hatfield DL (1985) Tumor-specific, hypomodified phenylalanyl-tRNA is utilized in translation in preference to the fully modified isoacceptor of normal cells. J Biol Chem 260: 147–151PubMedGoogle Scholar
  148. Smith JD (1979) Suppressor tRNAs in prokaryotes. In: Celis JE, Smith JD (eds) Nonsense mutations and tRNA suppressors. Academic Press, London pp 109–125Google Scholar
  149. Sonigo P, Alizon M, Staskus K, Klatzmann D, Cole S, Danos O, Retzel E, Tiollais O, Haase A, Wain-Hobson S (1985) Nucleotide sequence of the visna lentivirus: relationship to the AIDS virus. Cell 42: 369–382PubMedCrossRefGoogle Scholar
  150. Role of Nonsense, Frameshift, and Missense Suppressor tRNAs in Mammalian Cells 145Google Scholar
  151. Sonigo P, Barker C, Hunter E, Wain-Hobson S (1986) Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus. Cell 45: 375–385PubMedCrossRefGoogle Scholar
  152. Sprinzl M, Hartmann T, Meissner F, Moll J, Vorderwülbecke T (1987) Compilation of tRNA sequences and tRNA genes. Nucleic Acids Res (Sequences supplement) 15: 53–188Google Scholar
  153. Steege DA, Söll DG (1979) Suppression. In: Goldberger RF (ed) Biological Regulation and Development (vol 1 ). Plenum, New York, pp 433–485Google Scholar
  154. Stephens RM, Casey JW, Rice NR (1986) Equine infectious anemia virus gag and pot genes: relatedness to visna and AIDS virus. Science 231: 589–594PubMedCrossRefGoogle Scholar
  155. Stewart T, Sharp S (1984) Characterizing the function of Ofi-phosphoseryl-tRNA. Methods Enzymol 106: 157–161PubMedCrossRefGoogle Scholar
  156. Strauss EG, Rice CM, Strauss JH (1983) Sequence coding for the alphavirus nonstructural proteins is interrupted by an opal termination codon. Proc Natl Acad Sci USA 80: 5271–5275PubMedCrossRefGoogle Scholar
  157. Strauss EG, Rice CM, Strauss JH (1984) Complete nucleotide sequence of the genomic RNA of Sindbis virus. Virology 133: 92–110PubMedCrossRefGoogle Scholar
  158. Sukenaga Y, Ishida K, Takeda T, Takagi K (1987) cDNA sequence coding for human glutathione peroxidase. Nucleic Acids Res 15: 71–78CrossRefGoogle Scholar
  159. Summers WP, Summers WC, Laski FA, RajBhandary UL, Sharp PA (1983) Functional suppression in mammalian cells of nonsense mutations in the Herpes simplex virus thymidine kinase gene by suppressor tRNA genes. J Virol 47: 376–379PubMedGoogle Scholar
  160. Sundee RA, Evenson JK (1987) Serine incorporation into the selenocysteine moiety of glutathione peroxidase. J Biol Chem 262: 933–937Google Scholar
  161. Suter B, Altwegg M, Choffat Y, Kubli E (1986) The nucleotide sequence of two homogeneic Drosophila melanogaster tRNATY isoacceptors: application of a rapid tRNA anticodon sequencing method using S-1 nuclease. Arch Biochem Biophys 247: 233–237PubMedCrossRefGoogle Scholar
  162. Temple GF, Dozy AM, Roy KL, Kan YW (1982) Construction of a functional human suppressor tRNA gene: an approach to gene therapy for beta-thalassaemia. Nature 296: 537–540PubMedCrossRefGoogle Scholar
  163. Thayer RM, Power MD, Bryant ML, Gardner MB, Barr PJ, Luciw PA (1987) Sequence relationships of type D retroviruses which cause simian acquired immunodeficiency syndrome. Virology 157: 317–329PubMedCrossRefGoogle Scholar
  164. Topai MD, Fresco JR (1976) Complementary base pairing and the origin of substitution mutations. Nature 263: 285–289CrossRefGoogle Scholar
  165. Tukalo MA, Vlasov V, Vasil’chenko I, Matsuka G, Knorre D (1980) Dokl Akad Nauk SSSR 253: 253–256Google Scholar
  166. Valle RPC, Morch M-D (1988) Stop making sense or regulation at the level of termination in eukaryotic protein synthesis. FEBS Lett 235: 1–15PubMedCrossRefGoogle Scholar
  167. Valle RPC, Morch M-D, Haenni A-L (1987) Novel amber suppressor tRNAs of mammalian origin. EMBO J 6: 3049–3055PubMedGoogle Scholar
  168. Vasil’ieva IG, Tukalo MA, Krikliviy IA, Matduka GCH (1984) Mol Biol Akad Nauk SSSR 18: 1321–1325Google Scholar
  169. Wain-Hobson S, Sonigo P, Danos O, Cole S, Alizon M (1985) Nucleotide sequence of the AIDS virus, LAV. Cell 40: 9–17CrossRefGoogle Scholar
  170. Ward DC, Reich E (1968) Conformational properties of polyformycin: a polyribonucleotide with individual residues in the syn conformation. Proc Natl Acad Sci USA 61: 1494–1501PubMedCrossRefGoogle Scholar
  171. Weiss WA, Friedberg EC (1986) Normal yeast tRNAG’n/CAG can suppress amber codons and is encoded by an essential gene. J Mol Biol 192: 725–735PubMedCrossRefGoogle Scholar
  172. Weiss RB, Dunn JF, Atkins JF, Gesteland RF (1987a) Slippery runs, shifty stops, backward steps, and forward hops:–2,–1, + 1, + 2, + 5, and + 6 ribosomal frameshifting. Cold Spring Harbor Symposia on Quantitative Biology vol II, Gold Spring Harbor, New York, pp 687–696Google Scholar
  173. Weiss WA, Edelman I, Culbertson MR, Friedberg EC (1987b) Physiological levels of normal tRNA/CAG can effect partial suppression of amber mutations in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci USA 84: 8031–8034PubMedCrossRefGoogle Scholar
  174. Weiss R, Lindsley D, Falahee B, Gallant J (1988) On the mechanism of ribosomal frameshifting at hungry codons. J Mol Biol 203: 403–410PubMedCrossRefGoogle Scholar
  175. Wilson W, Braddock M, Adams S, Rathjen P, Kingsman S, Kingsman A (1988) HIV expression strategies: ribosomal frameshifting is directed by a short sequence in both mammalian and yeast systems. Cell 55: 1159–1169PubMedCrossRefGoogle Scholar
  176. Yoshinaka Y, Katosh I, Copeland TD, Oroszlan S (1985a) Murine leukemia virus protease is encoded by the gag-pol gene and is synthesized through suppression of an amber termination codon. Proc Natl Acad Sci USA 82: 1618–1622CrossRefGoogle Scholar
  177. Yoshinaka Y, Katoh I, Copeland TD, Oroszlan S (1985b) Translational readthrough of an amber termination codon during synthesis of feline leukemia virus protease. J Virol 55: 870–873Google Scholar
  178. Young JF, Capecchi M, Laski FA, RajBhandary UL, Sharp PA, Palese P (1983) Measurement of suppressor transfer RNA activity. Science 221: 873–875PubMedCrossRefGoogle Scholar
  179. Ziegler V, Richards K, Guilley H, Jonard T, Putz C (1985) Cell-free translation of beet necrotic yellow vein virus: readthrough of the coat protein cistron. J Gen Virol 66: 2079–2087CrossRefGoogle Scholar
  180. Zinoni F, Birkmann A, Leinfelder E, Böck A (1987) Cotranslational insertion of selenocysteine into formate dehydrogenase from Escherichia coli directed by a UGA codon. Proc Natl Acad Sci USA 84: 3156–3160PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1990

Authors and Affiliations

  • D. Hatfield
    • 1
  • B. J. Lee
    • 1
  • D. W. E. Smith
    • 2
  • S. Oroszlan
    • 3
  1. 1.Laboratory of Experimental Carcinogenesis, National Cancer InstituteNational Institutes of HealthBethesdaUSA
  2. 2.Department of PathologyNorthwestern University Medical SchoolChicagoUSA
  3. 3.Laboratory of Molecular Virology and Carcinogenesis, Bionetics Research Inc., Basic Research ProgramNational Cancer Institute-Frederick Center Research FacilityFrederickUSA

Personalised recommendations