Advertisement

Editing and Modification of Messenger RNA

  • J. Scott
Part of the Nucleic Acids and Molecular Biology book series (NUCLEIC, volume 4)

Abstract

The discovery of messenger RNA (mRNA) more than 30 years ago led to the proposition of the central dogma of molecular biology that DNA makes RNA, and that RNA makes protein. Research has since shown that mRNA takes part in various complex reactions and is subject to a variety of co- and post-transcriptional modifications. RNA can be faithfully copied by reverse transcriptase, edited by the splicing out of intervening sequences, modified by capping and polyadenylation, and can itself catalyze transesterification reactions. None of these discoveries seriously challenges the central dogma of molecular biology. It came therefore as a considerable surprise to find that genetic information not found in the genomic template can be transferred into the mRNA after transcription. Thus, certain trypanosome mitochondrial mRNAs, which are unable to be translated for lack of AUG initiation codons or because of the presence of frameshifts in the coding sequence, are rendered translatable by the introduction or deletion of U residues that are not encoded in the mitochondrial or nuclear genome (Benne et al. 1986; Feagin et al. 1987, 1988; Abraham et al. 1988). Other modifications that alter the coding ability of mRNAs have since been discovered. These include the modification of apolipoprotein (apo)-B mRNA (Chen et al. 1987; Powell et al. 1987) and of plant mitochondrial mRNAs (Covello and Gray 1989; Gualberto et al. 1989; Hiesel et al., in press), in which C to U substitution occurs, and the addition of a nontemplated G residues, which shift the reading frame of paramyxovirus mRNAs (Thomas et al. 1988; Cattaneo et al. 1989; Paterson et al. 1989).

Keywords

Measle Virus Editing Site Versus Protein mRNA Editing Adenylic Deaminase 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Abraham JM, Feagin JE, Stuart K (1988) Characterization of cytochrome C oxidase III transcripts that are edited only in the 3′ region. Cell 55: 267–272PubMedCrossRefGoogle Scholar
  2. Adams JM, Cory S (1975) Modified nucleosides and bizarre 5′-termini in mouse myeloma mRNA. Nature 255: 28–33PubMedCrossRefGoogle Scholar
  3. Attardi G, Schatz G (1989) Biogenesis of mitochondria. Ann Rev Cell Biol 4: 289–333CrossRefGoogle Scholar
  4. Bass BL, Weintraub H (1987) A developmentally regulated activity that unwinds RNA duplexes. Cell 48: 607–613PubMedCrossRefGoogle Scholar
  5. Bass BL, Weintraub H (1988) An unwinding activity that covalently modifies its double-stranded RNA substrate. Cell 55: 1089–1098PubMedCrossRefGoogle Scholar
  6. Bass BL, Weintraub H, Cattaneo R, Billeter MA (1989) Biased hypermutation of viral RNA genomes could be due to unwinding/modifying activity of double-stranded RNA. Cell 56: 331PubMedCrossRefGoogle Scholar
  7. Benne R (1989) RNA-editing in trypanosome mitochondria. Biochem Biophys Acta 1007: 131–139PubMedGoogle Scholar
  8. Benne R, Van den Burg J, Brakenhoff JPJ, Sloof P, Van Boom JH, Tromp MC (1986) Major transcript of the frameshifted CoxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46: 819–826PubMedCrossRefGoogle Scholar
  9. Bestor TH, Ingram VM (1983) Two DNA methyl transferases from murine erythroleukemia cells: purification, sequence specificity, and mode of interaction with DNA. Proc Natl Acad Sci USA 80: 5559–5563PubMedCrossRefGoogle Scholar
  10. Beutler E, Gelbart T, Han J, Koziol JA, Beutler B (1989) Evolution of the genome and genetic code. Selection at the dinucleotide level in methylation and polyribonucleotide cleavage. Proc Natl Acad Sci USA 86: 192–196PubMedCrossRefGoogle Scholar
  11. Björk GR, Ericson JU, Gustafsson CED, Hagervall TG, Jonsson YH, Wikström PM (1987) Transfer RNA modification. Annu Rev Biochem 56: 263–287PubMedCrossRefGoogle Scholar
  12. Bostrom K, Lauer SJ, Poksay KS, Garcia Z, Taylor JM, Innerarity TL Apolipoprotein B48 RNA editing in chimeric apolipoprotein EB. J Biol Chem 264 (26): 15701–15708Google Scholar
  13. Brown MS, Goldstein JL (1987) Teaching old dogmas new tricks. Nature 330: 113–114PubMedCrossRefGoogle Scholar
  14. Cattaneo R, Kaelin K, Baczko K, Billeter MA (1989) Measles virus editing provides an additional cysteine-rich protein. Cell 56: 759–764PubMedCrossRefGoogle Scholar
  15. Cattaneo R, Schmid A, Spielhofer P, Kaelin K, Baczko K, Ter Meulen V, Pardowitz J, Flanagan S, Rima BK, Udem SA, Billeter MA Mutated and hypermutated genes of persistent measles viruses which caused lethal human brain diseases. Virology (in press)Google Scholar
  16. Chen SH, Habib G, Yang CY, Gu ZW, Lee BR, Weng SA, Silberman SR, Cai SJ, Deslypere JP, Rosseneu M, Gotto AM Jr, Li WH, 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
  17. Chen SH, Wu JH, Li X, Liao WSI, Chan L (1989) RNA editing in mammals is not confined to apolipoprotein B. Cell Biol 109: 96a (abstr)Google Scholar
  18. Covello PS, Gray MW (1989) RNA editing in plant mitochondria. Nature 341: 662–666PubMedCrossRefGoogle Scholar
  19. 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
  20. Davies MS, Wallis SC, Driscoll DM, Wynne JK, Williams GW, Powell LM, Scott J (1989) Sequence requirements for apolipoprotein B RNA editing in transfected rat hepatoma cells. J Biol Chem 264: 13395–13398PubMedGoogle Scholar
  21. Desrosiers RC, Friderici KH, Rottman FM (1975) Characterization of Novikoff hepatoma mRNA methylation and heterogeneity in the methylated 5′ termini. Biochemistry 14: 4367–4374PubMedCrossRefGoogle Scholar
  22. Driscoll DM, Wynne JK, Wallis SC, Scott J (1989) An in vitro system for the editing of apolipoprotein B mRNA. Cell 58: 519–525PubMedCrossRefGoogle Scholar
  23. Elliott MS, Trewyn RW (1984) Inosine biosynthesis in transfer RNA by an enzymatic insertion of hypoxanthine. J Biol Chem 259: 2407–2410PubMedGoogle Scholar
  24. Feagin JE, Jasmer DP, Stuart K (1987) Developmentally regulated addition of nucleotides within apocytochrome b transcripts in Trypanosoma brucei. Cell 49: 337–345PubMedCrossRefGoogle Scholar
  25. Feagin JE, Abraham JM, Stuart K (1988) Extensive editing of the cytochrome c oxidase III transcript in Trypanosoma brucei. Cell 53: 413–422PubMedCrossRefGoogle Scholar
  26. Ford MJ, Anton I A, Lane DP (1988) Nuclear protein with sequence homology to translation initiation factor elF-4A. Nature 332: 736–738PubMedCrossRefGoogle Scholar
  27. Grossman L (1981) Enzymes involved in the repair of damaged DNA. Arch Biochem Biophys 211: 511–522PubMedCrossRefGoogle Scholar
  28. Gualberto JM, Lamattina L, Bonnard G, Weil JH, Grienenberger JM (1989) RNA editing in wheat mitochondria results in the conservation of protein sequences. Nature 341: 660–662PubMedCrossRefGoogle Scholar
  29. Hiesel R, Wissinger B, Schuster W, Brennicke A RNA editing in plant mitochondria. Science (in press)Google Scholar
  30. Hirling H, Scheffner M, Restle T, Stahl H (1989) RNA helicase activity associated with the human p68 protein. Nature 339: 562–564PubMedCrossRefGoogle Scholar
  31. Hospattankar AV, Higuchi K, Law SW, Meglin NM, Brewer HB Jr (1987) Identification of a novel in-frame translational stop codon in human intestine apo-B mRNA. Biochem Biophys Res Commun 148: 279–285PubMedCrossRefGoogle Scholar
  32. Kimelman D, Kirschner MW (1989) An antisense mRNA directs the covalent modification of the transcript encoding fibroblast growth factor in Xenopus oocytes. Cell 59 (4): 687–696PubMedCrossRefGoogle Scholar
  33. Lindahl T (1982) DNA repair enzymes. Ann Rev Biochem 51: 61–87PubMedCrossRefGoogle Scholar
  34. Maizels N, Weiner A (1988) In search of a template. Nature 334: 469–470PubMedCrossRefGoogle Scholar
  35. Makino S, Soe LH, Shieh CK, Lai MMC (1988a) Discontinuous transcription generates heterogeneity at the leader fusion sites of Coronavirus mRNAs. J Virol 62: 3870–3873PubMedGoogle Scholar
  36. Makino S, Shieh S, Soe L, Baker S, Lai M (1988b) Primary structure and translation of a defective interfering RNA of murine Coronavirus. Virology 166: 550–560PubMedCrossRefGoogle Scholar
  37. Narayan P, Rottman FM (1988) An in vitro system for accurate methylation of internal adenosine residues in messenger RNA. Science 242: 1159–1161PubMedCrossRefGoogle Scholar
  38. Okada N, Nishimura S (1979) Isolation and characterization of a guanine insertion enzyme, a specific tRNA transglycosylase, from Escherichia coli. J Biol Chem 254: 3061–3066PubMedGoogle Scholar
  39. Okada N, Noguchi S, Kasai H, Shindo-Okada N, Ohgi T, Goto T, Nishimura S (1979) Novel mechanism of post-transcriptional modification of tRNA. J Biol Chem 254: 3067–3073PubMedGoogle Scholar
  40. Paterson RG, Thomas SM, Lamb RA (1989) Specific non-templated nucleotide addition to a simian virus 5 mRNA: prediction of a common mechanism by which unrecognized hybrid P-cysteine-rich proteins are encoded by paramyxovirus “P” genes. In: Kolakofsky D, Mahy BWJ (eds) Genetics and pathogenicity of negative strand viruses. Elsevier, London, pp 232–245Google Scholar
  41. 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
  42. Rebagliati MR, Melton DA (1987) Antisense RNA injections in fertilized frog eggs reveal an RNA duplex unwinding activity. Cell 48: 599–605PubMedCrossRefGoogle Scholar
  43. Scheffner M, Knippers R, Stahl H (1989) RNA unwinding activity of SV40 large T antigen. Cell 57: 955–963PubMedCrossRefGoogle Scholar
  44. Schwer B, Stunnenberg HG (1988) Vaccinia virus late transcripts generated in vitro have a poly(A) head. EMBO J 7: 1183–1190PubMedGoogle Scholar
  45. Simpson L, Shaw J (1989) RNA editing and the mitochondrial cryptogenes of kinetoplastid protozoa. Cell 57: 355–366PubMedCrossRefGoogle Scholar
  46. Stuart K (1989) Minireview - trypanosomatids: mitochondrial RNA editing. Exp Parasitol 68: 486–490PubMedCrossRefGoogle Scholar
  47. Stuart K, Feagin JE, Abraham JM (1989) RNA editing: the creation of nucleotide sequences in mRNA - a minireview. Gene 82 (1): 155–160PubMedCrossRefGoogle Scholar
  48. Thomas SM, Lamb RA, Paterson RG (1988) Two mRNAs that differ by two nontemplated nucleotides encode the amino coterminal proteins P and V of the paramyxovirus SV5. Cell 54: 891–902PubMedCrossRefGoogle Scholar
  49. Wagner RW, Nishikura K (1989) An activity in mammalian cells which modifies adenosines to inosines in double-stranded RNA. J Cell Biol 109: 96a (abstr)Google Scholar
  50. Wagner RW, Smith JE, Cooperman BS, Nishikura K (1989) A double-stranded RNA unwinding activity introduces structural alterations by means of adenosine to inosine conversions in mammalian cells and Xenopus eggs. Proc Natl Acad Sei USA 86: 2647–2651CrossRefGoogle Scholar
  51. Wiebauer K, Jiricny J (1989) In vitro correction of GT mispairs to G-C pairs in nuclear extracts from human cells. Nature 339: 234–236PubMedCrossRefGoogle Scholar
  52. Zielke CL Suelter CH (1971) Purine, purine nucleoside and purine nucleotide aminohydro- lases. In: Boyer PD (ed) The enzymes, vol 4. Academic Press, New York, pp 47–78Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1990

Authors and Affiliations

  • J. Scott
    • 1
  1. 1.Division of Molecular MedicineMRC Clinical Research CentreHarrow, MiddxUK

Personalised recommendations