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RNA editing in trypanosomes

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EJB Reviews 1994

Part of the book series: EJB Reviews 1994 ((EJB REVIEWS,volume 1994))

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Abstract

The nucleotide sequence of mitochondrial pre-mRNAs in trypanosomes is posttranscriptionally edited by the insertion and deletion of uridylate (U) residues. In some RNAs editing is limited to small sections but in African trypanosomes, such as Trypanosoma brucei, 9 of the 18 known mitochondrial mRNAs are created by massive editing which can produce more than 50% of the coding sequence. In all cases, however, RNA editing is a key event in gene expression during which translatable RNAs are generated. The information for the editing process and possibly also the inserted Us are provided by small guide RNAs, which are encoded in both the maxicircle and minicircle components of the trypanosome mitochondrial DNA. Current models of editing are largely based on the characteristics of partially edited RNAs and on the occurrence in vivo and the possibility of synthesis in vitro of chimeric molecules in which a guide RNA is covalently linked through its 3′ oligo(U) tail to an editing site in pre-mRNA. In this paper, I will review the research in this rapidly growing field and illustrate how different interpretations of the available data can lead to different views of the mechanism and the biochemistry of the editing process.

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Abbreviations

gRNA:

guide RNA

mt:

mitochondrial

PCR:

polymerase chain reaction

RPS:

ribosomal protein of the small subunit

ATP:

ATP synthase

cox:

cytochrome c oxidase

CYb:

apocytochrome b

G(CR):

gene producing G-rich pre- mRNA (from a C-rich template strand)

ND:

NADH-dehydrogenase

MURF:

maxicircle unidentified reading frame.

References

  1. Benne, R., Van den Burg, J., Brakenhoff, J. P. J., Sloof, P, Van Boom, J. H. & Tromp, M. C. (1986) Major transcript of the frameshifted coxll gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA, Cell 46, 819–826.

    PubMed  CAS  Google Scholar 

  2. Feagin, J. E., Jasmer, D. P. & Stuart, K. (1987) Developmentally regulated addition of nucleotides within apocytochrome b transcripts in Trypanosoma brucei, Cell 49, 337–345.

    PubMed  CAS  Google Scholar 

  3. Shaw, J. M., Feagin, J. E., Stuart, K. & Simpson, L. (1988) Editing of kinetoplastid mitochondrial mRNAs by uridine addition and deletion generates conserved amino acid sequences and AUG initiation codons, Cell 52, 401–411.

    Google Scholar 

  4. Van der Spek, H., Van den Burg, J., Croiset, A., Van den Broek, M., Sloof, P. & Benne, R. (1988) Transcripts from the frameshifted MURF3 gene from Crithidia fasciculata are edited by U insertion at multiple sites, EMBO J. 7, 2509–2514.

    PubMed  Google Scholar 

  5. Feagin, J. E., Abraham, J. M. & Stuart, K. (1988) Extensive editing of the cytochrome c oxidase III transcript in Trypanosoma brucei, Cell 53, 413–422.

    PubMed  CAS  Google Scholar 

  6. Simpson, L. & Shaw, J. M. (1989) RNA editing and the mitochondrial cryptogenes of kinetoplast protozoa, Cell 57, 355–366.

    PubMed  CAS  Google Scholar 

  7. Stuart, K. (1991) RNA editing in mitochondrial mRNA of try- panosomatids, Trends Biochem. Sci. 16, 68–72.

    PubMed  Google Scholar 

  8. Benne, R. (1990) RNA editing in trypanosomes - is there a message? Trends Genet. 6, 177–181.

    PubMed  CAS  Google Scholar 

  9. Hajduk, S. L., Harris, M. E. & Pollard, V. W. (1993) RNA editing in kinetoplastid mitochondria, FASEB J. 7, 54–63.

    PubMed  CAS  Google Scholar 

  10. Harris, M. E., Moore, D. R. & Hajduk, S. L. (1990) Addition of uridines to edited RNAs in trypanosome mitochondria occurs independently of transcription, J. Biol. Chem. 265, 11368–11376.

    PubMed  CAS  Google Scholar 

  11. Miller, D., Mahendran, R., Spottswood, M., Ling, M., Wang, S., Yang, N. & Constandy, H. (1993) in RNA editing, the alteration of protein coding sequences of RNA (Benne, R., ed.) pp. 87–101, Ellis Horwood, Chichester.

    Google Scholar 

  12. Kolakofsky, D., Curran, J., Pelet, T. & Jacques, J.-P. (1993) in RNA editing, the alteration of protein coding sequences of RNA (Benne, R., ed.) pp. 105–123, Ellis Horwood, Chichester.

    Google Scholar 

  13. Ojala, D., Montoya, J. & Attardi, G. (1981) tRNA punctuation model of RNA processing in human mitochondria, Nature 290, 470–474.

    PubMed  CAS  Google Scholar 

  14. Hodges, P. J. & Scott, J. (1992) Apolipoprotein B mRNA editing: a new tier for the control of gene expression, Trends Biochem. Sci. 17, 77–81.

    PubMed  CAS  Google Scholar 

  15. Chan, L. (1993) RNA editng: exploring one mode with apolipoprotein B mRNA, BioEssays 15, 33–41.

    PubMed  CAS  Google Scholar 

  16. Gray, M. W. & Covello, P. S. (1993) RNA editing in plant mitochondria and chloroplasts, FASEB J. 7, 64–71.

    PubMed  CAS  Google Scholar 

  17. Cattaneo, R. (1992) RNA editing: in chloroplasts and brain, Trends Biochem. Sci. 17, 4–5.

    PubMed  CAS  Google Scholar 

  18. Wissinger, B., Brennicke, A. & Schuster, W. (1992) Trends Genet. 8, 322–328.

    PubMed  CAS  Google Scholar 

  19. Grienenberger, J. M. (1993) in RNA editing, the alteration of protein coding sequences of RNA (Benne, R., ed.) pp. 153–177, Ellis Horwood, Chichester.

    Google Scholar 

  20. Zheng, H., Fu, T. B., Lazinsky, D. & Taylor, J. (1992) Editing of the genomic RNA of human hepatitis delta virus, J. Virol. 66, 4693–4697.

    PubMed  CAS  Google Scholar 

  21. Diamond, A. M., Montero-Puemer, Y., Lee, B. J. & Hatfield, D. (1990) Selenocysteine inserting tRNAs are likely generated by tRNA editing, Nucleic Acids Res. 18, 6727.

    PubMed  CAS  Google Scholar 

  22. Beier, H., Lee, M. C., Sekiya, T., Kuchino, Y. & Nishimura, S. (1992) Two nucleotides next to the anticodon of cytoplasmic rat transfer RNA are likely generated by RNA editing, Nucleic Acids Res. 20, 2679–2683.

    PubMed  CAS  Google Scholar 

  23. Lonergan, K. M. & Gray, M. W. (1993) Editing of transfer RNAs in Acanthamoeba castelanii mitochondria, Science 259, 812–815.

    PubMed  CAS  Google Scholar 

  24. Simpson, L. (1986) Kinetoplast DNA in trypanosomatid flagellates, Int. Rev. Cytol. 99, 119–179.

    PubMed  CAS  Google Scholar 

  25. Borst, P. & Hoeijmakers, J. H. J. (1979) Kinetoplast DNA, Plasmid 2, 20–40.

    PubMed  CAS  Google Scholar 

  26. Lumsden, W. H. R. & Evans, D. A. (1976) Biology of the Kinetoplastida, vols 1 and 2, Academic Press, London.

    Google Scholar 

  27. Benne, R. (1985) Mitochondrial genes in trypanosomes, Trends Genet. 1, 117–121.

    CAS  Google Scholar 

  28. Simpson, L. (1987) The mitochondrial genome of kinetoplastid protozoa: genomic organization, transcription, replication and evolution, Annu. Rev. Microbiol. 41, 363–382.

    PubMed  CAS  Google Scholar 

  29. Stuart, K. (1993) The RNA editing process in Trypanosoma brucei, Sem. Cell Biol. 4, 251–260.

    CAS  Google Scholar 

  30. Simpson, L., Maslov, D. & Blum, B. (1993) in RNA editing, the alteration of protein coding sequences of RNA (Benne, R., ed.) pp. 53–85, Ellis Horwood, Chichester.

    Google Scholar 

  31. Sloof, P. & Benne, R. (1993) RNA editing in trypanosome mitochondria: guidelines for models, FEBS Lett. 325, 146–151.

    PubMed  CAS  Google Scholar 

  32. Stuart, K. (1991) RNA editing in trypanosomatid mitochondria, Annu. Rev. Microbiol 45, 327–344.

    PubMed  CAS  Google Scholar 

  33. Stuart, K. (1993) in RNA editing, the alteration of protein coding sequences of RNA (Benne, R., ed.) pp. 25–52, Ellis Horwood, Chichester.

    Google Scholar 

  34. Van der Spek, H., Speijer, D., Arts, G. J., Van den Burg, J., Van Steeg, H., Sloof, P. & Benne, R. (1990) RNA editing in transcripts of the mitochondrial genes of the insect trypanosome Crithidia fasciculata, EMBO J. 9, 257–262.

    PubMed  Google Scholar 

  35. Simpson, L., Neckelmann, N., de la Cruz, V. F., Simpson, A. M., Feagin, J. E., Jasmer, D. P. & Stuart, K. (1987) Comparison of the maxicircle (mitochondrial) genomes of Leishmania tarentolae and Trypanosoma brucei at the level of nucleotide sequence J. Biol. Chem. 262, 6182–6196.

    PubMed  CAS  Google Scholar 

  36. Benne, R. (1993) RNA editing in mitochondria of Leishmania tarentolae and Crithidia fasciculata, Sem. Cell Biol. 4, 241–249.

    CAS  Google Scholar 

  37. Koslowsky, D. J., Bhat, G. J., Perrolaz, A. L., Feagin, J. E. & Stuart, K. (1990) The MURF3 gene of T. brucei contains multiple domains of extensive editing and is homologous to a subunit of NADH dehydrogenase, Cell 62, 901–911.

    PubMed  CAS  Google Scholar 

  38. Maslov, D. A., Sturm, N. R., Niner, B. M., Gruszinsky, E. S., Peris, M. & Simpson, L. (1992) An intergenic G-rich region in Leishmania tarentolae kinetoplast maxicircle DNA is a pan-edited cryptogene encoding ribosomal protein SI2, Mol. Cell. Biol. 12, 56–67.

    PubMed  CAS  Google Scholar 

  39. Bhat, G. J., Koslowsky, D. J., Feagin, J. E., Smiley, B. L. & Stuart, K. (1990) An extensively edited mitochondrial transcript in kinetoplastids encodes a protein homologous to ATPase subunit-6, Cell 61, 885–894.

    PubMed  CAS  Google Scholar 

  40. Souza, A. E., Myler, P. J. & Stuart, K. (1992) Maxicircle CR1 transcripts of Trypanosoma brucei are edited and developmentally regulated and encode a putative iron-sulfur protein homologous to an NADH dehydrogenase subunit, Mol. Cell. Biol. 12, 2100–2107.

    PubMed  CAS  Google Scholar 

  41. Read, L. K., Myler, P. J. & Stuart, K. (1992) Extensive editing of both processed and preprocessed maxicircle CR6 transcripts in Trypanosoma brucei, J. Biol Chem. 267, 1123–1128.

    PubMed  CAS  Google Scholar 

  42. Borst, P., Weijers, P. J. & Brakenhoff, G. J. (1982) Analysis by electron microscopy of the variable segment in the maxicircle of kinetoplast DNA from Trypanosoma brucei, Biochim. Biophys. Acta 699, 272–280.

    PubMed  CAS  Google Scholar 

  43. Muhich, M. L., Neckelmann, N. & Simpson, L. (1985) The divergent region of the L. tarentolae kinetoplast maxicircle DNA contains a diverse set of repetitive sequences, Nucleic Acids Res. 13, 3241–3260.

    PubMed  CAS  Google Scholar 

  44. Sloof, P., De Haan, A., Eier, W., Van Iersel, M., Boel, E., Van Steeg, H. & Benne, R. (1992) The nucleotide sequence of the variable region in Trypanosoma brucei completes the sequence analysis of the maxicircle component of mitochondrial kinetoplast DNA, Mol. Biochem. Parasitol. 56, 289–300.

    PubMed  CAS  Google Scholar 

  45. Myler, P. J., Glick, D., Feagin, J. E., Morales, T. H. & Stuart, K. (1993) Structural organization of the maxicircle variable region of Trypanosoma brucei: identification of potential replication origins and topoisomerase II binding sites, Nucleic Acids Res. 21, 687–694.

    PubMed  CAS  Google Scholar 

  46. Ryan, K. A., Shapiro, T. A., Rauch, C. A. & Englund, P. T. (1988) Replication of kinetoplast DNA in trypanosomes, Annu. Rev. Microbiol. 9, 93–104.

    Google Scholar 

  47. Attardi, G. & Schatz, G. (1988) Biogenesis of mitochondria, Annu. Rev. Cell. Biol. 4, 289–333.

    PubMed  CAS  Google Scholar 

  48. Grivell, L. A. (1989) Nucleo-mitochondrial interactions in yeast mitochondrial biogenesis, Eur. J. Biochem. 182, 477–493.

    PubMed  CAS  Google Scholar 

  49. Simpson, A. M., Suyama, Y., Dewes, H., Campbell, D. A. & Simpson, L. (1989) Kinetoplastid mitochondria contain functional tRNAs which are encoded in nuclear DNA and also contain small minicircle and maxicircle transcripts of unknown function, Nucleic Acids Res. 17, 5427–5445.

    PubMed  CAS  Google Scholar 

  50. Hancock, K. & Hajduk, S. L. (1990) The mitochondrial tRNAs of T. brucei are nuclear encoded, J. Biol Chem. 265, 1920819215.

    Google Scholar 

  51. Van der Spek, H., Arts, G. J., Zwaal, R. R., Van den Burg, J., Sloof, P. & Benne, R. (1991) Conserved genes encode guide RNAs in mitochondria of Crithidia fasciculata, EMBO J. 10, 1217–1224.

    PubMed  Google Scholar 

  52. Blum, B., Bakalara, N. & Simpson, L. (1990) A model for RNA editing in kinetoplast mitochondria: ‘guide’ RNA molecules transcribed from maxicircle DNA provide the edited information, Cell 60, 189–198.

    PubMed  CAS  Google Scholar 

  53. Sturm, N. R. & Simpson, L. (1990) Kinetoplast DNA minicircles encode guide RNAs for editing of cytochrome oxidase subunit-III messenger RNA, Cell 61, 879–884.

    PubMed  CAS  Google Scholar 

  54. Sturm, N. R. & Simpson, L. (1991) Leishmania tarentolae minicircles of different sequence classes encode single guide RNAs located in the variable region approximately 150 bp from the conserved region, Nucleic Acids Res. 19, 6277–6281.

    PubMed  CAS  Google Scholar 

  55. Maslov, D. A. & Simpson, L. (1992) The polarity of editing within a multiple gRNA-mediated domain is due to formation of anchors for upstream gRNAs by downstream editing, Cell 70, 459–467.

    PubMed  CAS  Google Scholar 

  56. Pollard, V. W., Rohrer, S. P., Michelotti, E. F., Hancock, K. & Hajduk, S. L. (1990) Organization of minicircle genes for guide RNAs in Trypanosoma brucei, Cell 63, 783–790.

    PubMed  CAS  Google Scholar 

  57. Koslowsky, D. J., Riley, G. R., Feagin, J. E. & Stuart, K. (1992) Guide RNAs for transcripts with developmentally regulated RNA editing are present in both life-cycle stages of Trypanosoma brucei, Mol. Cell. Biol. 12, 2043–2049.

    PubMed  CAS  Google Scholar 

  58. Shu, H.-H. & Stuart, K. (1993) A Trypanosoma brucei minicircle encodes the same gRNAs as do minicircles of T. equiper- dum ATCC 30019 and T. evansi type-A minicircles, Nucleic Acids Res. 21, 2951.

    PubMed  CAS  Google Scholar 

  59. Corell, R. A., Feagin, J. E., Riley, G. R., Strickland, T., Guderian, J. A., Myler, P. J. & Stuart, K. (1993) Trypanosoma brucei minicircles encode multiple guide RNAs which can direct editing of extensively overlapping sequences, Nucleic Acids Res. 21, 4313–4320.

    PubMed  CAS  Google Scholar 

  60. Pollard, V. W. & Hajduk, S. L. (1991) Trypanosoma equiperdum minicircles encode three distinct primary transcripts which exhibit guide RNA characteristics, Mol. Cell. Biol 11, 1668–1675.

    PubMed  CAS  Google Scholar 

  61. Gajendram, N., Vanbecke, D., Bajyana Songa, E. & Hamers R. (1992) Kinetoplast minicircle DNA of Trypanosoma evansi encode guide RNA genes, Nucleic Acids Res. 20, 614.

    Google Scholar 

  62. Blum, B. & Simpson, L. (1990) Guide RNAs in kinetoplastid mitochondria have a nonencoded 3′ oligo(U) tail involved in recognition of the preedited region, Cell 62, 391–397.

    PubMed  CAS  Google Scholar 

  63. White, T. C. & Borst, P. (1987) RNA end-labeling and RNA ligase activities can produce a circular rRNA in whole cell extracts from trypanosomes, Nucleic Acids Res. 15, 3275–3289.

    PubMed  CAS  Google Scholar 

  64. Bakalara, N., Simpson, A. M. & Simpson, L. (1989) The Leishmania kinetoplast mitochondrion contains terminal uri- dylyltransferase and RNA ligase activities, J. Biol. Chem. 264, 18679–18686.

    PubMed  CAS  Google Scholar 

  65. Arts, G. J., Van der Spek, H., Speijer, D., Van den Burg, J., Van Steeg, H., Sloof, P. & Benne, R. (1993) Implications of novel guide RNA features for the mechanism of RNA editing in Crithidia fasciculata, EMBO J. 12, 1523–1532.

    PubMed  CAS  Google Scholar 

  66. Read, L. K., Corell, R. A. & Stuart, K. (1992) Chimeric and truncated RNAs in Trypanosoma brucei suggest transesterifications at non-consecutive sites during RNA editing, Nucleic Acids Res. 20, 2341–2347.

    PubMed  CAS  Google Scholar 

  67. Steinert, M. & van Assel, S. (1980) Sequence heterogeneity in kinetoplast DNA: reassociation kinetics, Plasmid 3, 7–17.

    PubMed  CAS  Google Scholar 

  68. Gomez-Eichelmann, C., Holz, G., Beach, D., Simpson, A. & Simpson, L. (1988) Comparison of several lizard Leishmania species and strains in terms of kinetoplast minicircle and maxicircle DNA sequences, nuclear chromosomes and membrane lipids, Mol. Biochem. Parasitol. 27, 143–157.

    PubMed  CAS  Google Scholar 

  69. Hagerman, P. J. (1990) Sequence-directed curvature of DNA, Annu. Rev. Biochem. 59, 755–781.

    PubMed  CAS  Google Scholar 

  70. Blum, B., Sturm, N. R., Simpson, A. M. & Simpson, L. (1991) Chimeric gRNA-mRNA molecules with oligo(U) tails covalently linked at sites of RNA editing suggest that U addition occurs by transesterification, Cell 65, 543–550.

    PubMed  CAS  Google Scholar 

  71. Harris, M. E. & Hajduk, S. L. (1992) Kinetoplastid RNA editing: in vitro formation of cytochrome b gRNA-mRNA chimeras from synthetic substrate RNAs, Cell 68, 1091–1099.

    PubMed  CAS  Google Scholar 

  72. Koslowsky, D. J., Göringer, H. U., Morales, T. H. & Stuart, K. (1992) In vitro guide RNA/mRNA chimaera formation in Trypanosoma brucei RNA editing, Nature 356, 807–809.

    PubMed  CAS  Google Scholar 

  73. Blum, B. & Simpson, L. (1992) Formation of gRNA/mRNA chimeric molecules in vitro, the initial step of RNA editing, is dependent on an anchor sequence, Proc. Natl Acad. Sci. USA 89, 11944–11948.

    PubMed  CAS  Google Scholar 

  74. Abraham, J. M., Feagin, J. E. & Stuart, K. (1988) Characterization of cytochrome c oxidase III transcripts that are edited only in the 3’ region, Cell 55, 267–272.

    PubMed  CAS  Google Scholar 

  75. Sturm, N. R. & Simpson, L. (1990) Partially edited mRNAs for cytochrome b and subunit III of cytochrome oxidase from Leishmania tarentolae mitochondria - RNA editing intermediates, Cell 61, 871–878.

    PubMed  CAS  Google Scholar 

  76. Decker, C. J. & Sollner-Webb, B. (1990) RNA editing involves indiscriminate U changes throughout precisely defined editing domains, Cell 61, 1001–1011.

    PubMed  CAS  Google Scholar 

  77. Sturm, N. R., Maslov, D. A., Blum, B. & Simpson, L. (1992) Generation of unexpected editing patterns in Leishmania tarentolae mitochondrial mRNAs: misediting produced by misguiding, Cell 70, 469–476.

    PubMed  CAS  Google Scholar 

  78. Koslowsky, D. J., Bhat, G. J., Read, L. K. & Stuart, K. (1991) Cycles of progressive realignment of gRNA with mRNA in RNA editing, Cell 67, 537–546.

    PubMed  CAS  Google Scholar 

  79. Cech, T. R. (1991) RNA editing: world’s smallest introns? Cell 64, 667–669.

    PubMed  CAS  Google Scholar 

  80. Sugisaki, H. & Takanami, M. (1993) The 5’-terminal region of the apocytochrome b transcript in Crithidia fasciculata is successively edited by two guide RNAs in the 3’ to 5’ direction, J. Biol. Chem. 268, 887–891.

    PubMed  CAS  Google Scholar 

  81. Cech, T. R. (1986) The generality of self-splicing RNA: relationship to nuclear splicing, Cell 44, 207–210.

    PubMed  CAS  Google Scholar 

  82. Woodson, S. A. & Cech, T. R. (1989) Reverse self-splicing of the Tetrahymena group I intron: implication for the directionality of splicing and for intron transposition, Cell 57, 335–345.

    PubMed  CAS  Google Scholar 

  83. Tabak, H. F. & Grivell, L. A. (1986) RNA catalysis in the excision of yeast mitochondrial introns, Trends Genet. 2, 51–55.

    CAS  Google Scholar 

  84. Jacquier, A. & Michel, F. (1987) Multiple exon-binding sites in class II self-splicing introns, Cell 50, 17–29.

    PubMed  CAS  Google Scholar 

  85. Goldschmidt-Clermont, M., Choquet, Y., Girard-Bascou, J., Michel, F., Schirmer-Rahire, M. & Rochaix, J.-D. (1991) A small chloroplast RNA may be required for trans-splicing in Chlamidomonas reinhardtii, Cell 65, 135–143.

    PubMed  CAS  Google Scholar 

  86. Mueller, M. W., Hetzer, M. & Schweyen, R. J. (1993) Group II intron RNA catalysis of progressive nucleotide insertion: a model for RNA editing, Science 261, 1035–1038.

    PubMed  CAS  Google Scholar 

  87. Harris, M. E., Decker, C., Sollner-Webb, B. & Hajduk, S. L. (1991) Specific cleavage of pre-edited mRNAs in trypano- some mitochondrial extracts, Mol. Cell. Biol. 12, 2591–2598.

    Google Scholar 

  88. Simpson, A. M., Bakalara, N. & Simpson, L. (1992) A ribo- nuclease activity is activated by heparin or by digestion with proteinase K in mitochondrial extracts of Leishmania tarentolae, J. Biol. Chem. 267, 6782–6788.

    PubMed  CAS  Google Scholar 

  89. Sollner-Webb, B. (1992) Guides to experiments, Nature 356, 743–744.

    PubMed  CAS  Google Scholar 

  90. Pollard, V. W., Harris, M. E. & Hajduk, S. L. (1992) Native mRNA editing complexes from Trypanosoma brucei mitochondria, EMBO J. 11, 4429–4438.

    PubMed  CAS  Google Scholar 

  91. McSwiggen, J. A. & Cech, T. R. (1989) Stereochemistry of RNA cleavage by the Tetrahymena ribozyme and evidence that the chemical step is not rate limiting, Science 244, 679–683.

    PubMed  CAS  Google Scholar 

  92. Rajagopal, J., Doudna, J. A. & Szostak, J. W. (1989) Stereochemical course of catalysis by the Tetrahymena ribozyme, Science 244, 692–694.

    PubMed  CAS  Google Scholar 

  93. Moore, M. J. & Sharp, P. A. (1993) Evidence for two active sites in the spliceosome provided by stereochemistry of pre- mRNA splicing, Nature 365, 364–368.

    PubMed  CAS  Google Scholar 

  94. Freier, S. M., Kierzek, R., Jaeger, J. A., Sugimoto, N., Caruthers, M. H., Neilson, T. & Turner, D. H. (1986) Improved free- energy parameters for predictions of RNA duplex stability, Proc. Natl Acad. Sci. USA 83, 9373–9377.

    PubMed  CAS  Google Scholar 

  95. Shaw, J. M., Campbell, D. & Simpson, L. (1989) Internal frameshifts within the mitochondrial genes for cytochrome oxidase subunit II and maxicircle unidentified reading frame 3 of Leishmania tarentolae are corrected by RNA editing: evidence for translation of the edited cytochrome oxidase II mRNA, Proc. Natl Acad. Sci. USA 86, 6220–6224.

    PubMed  CAS  Google Scholar 

  96. Landweber, L. F. & Gilbert, W. (1993) RNA editing as a source of genetic variation, Nature 363, 179–182.

    PubMed  CAS  Google Scholar 

  97. Lake, J. A., De la Cruz, V., Ferreira, P., Morel, C. & Simpson, L. (1988) Evolution of parasitism: kinetoplastid history reconstructed from mitochondrial rRNA sequences, Proc. Natl Acad. Sci. USA 85, 4779–4783.

    PubMed  CAS  Google Scholar 

  98. Sogin, M. L., Gunderson, J. H., Elwood, H. J., Alonso, R. A. & Peattie, D. A. (1989) Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia, Science 243, 75–77.

    PubMed  CAS  Google Scholar 

  99. Gray, M. W. (1989) The evolutionary origin of organelles, Trends Genet. 5, 294–299

    PubMed  CAS  Google Scholar 

  100. Benne, R. (1992) Guide RNA tails of the unexpected, Curr. Biol. 2, 425–427.

    PubMed  CAS  Google Scholar 

  101. Hajduk, S. L., Siqueira, A. M. & Vickerman, K. (1986) Kineto plast DNA of Bo do caudatus: a noncatenated structure, Mol. Cell. Biol. 6, 4372–4378.

    PubMed  CAS  Google Scholar 

  102. Borst, P. (1991) Why kinetoplast DNA networks? Trends Genet. 7, 139–141.

    PubMed  CAS  Google Scholar 

  103. Dujon, B. (1989) Group I introns as mobile genetic elements: facts and mechanistic speculations - a review, Gene 82, 91–114.

    PubMed  CAS  Google Scholar 

  104. Van der Spek, H. (1992) PhD thesis, University of Amsterdam.

    Google Scholar 

  105. Bellofatto, V. & Cross, G. A. M. (1989) Expression of a bacterial gene in a trypanosomatid protozoan, Science 244, 1167–1169.

    PubMed  CAS  Google Scholar 

  106. Ten Asbroek, A. L. M. A., Ouellette, M. & Borst, P. (1990) Targeted insertion of the neomycin phosphotransferase gene into the tubulin gene cluster of Trypanosoma brucei, Nature 348, 174–175.

    PubMed  Google Scholar 

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Benne, R. (1994). RNA editing in trypanosomes. In: EJB Reviews 1994. EJB Reviews 1994, vol 1994. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-79502-2_6

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