Abstract
Trans-splicing is a recently discovered phenomenon defined as the splicing together of two discrete RNA molecules to give a single hybrid RNA product. There are two distinct types of physiological trans-splicing. The first is found in organelles of eukaryotes. Very little is known of the mechanism or machinery involved in this process but so far it bears little resemblance to the cis-splicing of nuclear-encoded mRNAs (in terms of the sequences involved). The second process occurs in the nucleus of eukaryotic cells and is clearly related to the well-studied cis-splicing occurring on spliceosomes in these nuclei. “Nuclear” trans-splicing will be the major focus of this review. In it, I will attempt to cover the structures involved, as well as the possible mechanism, function and evolutionary significance of this unusual but important process.
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References
Bektesh S, K VanDoren, Hirsh D (1988) Presence of the Caenorhabditis elegans spliced leader on different mRNAs and in different genera of nematodes. Genes and Development 2: 1277–1283
Boothròyd JC (1985) Antigenic variation in african trypanosomes. Annu Rev Microbiol 39: 475–502
Borst P (1986) Discontinuous transcription and antigenic variation in trypanosomes. Annu Rev Biochem 55: 701–732
Breitbart RE, Andreadis A, Nadal-Ginard B (1987) Alternative splicing: A ubiquitous mechanism for the generation of multiple protein isoforms from single genes. Annu Rev Biochem 56: 467–495
Bruzik JP, Van Doren K, Hirsh D, Steitz JA (1988) SL snRNPs: Novel mediators of trans-splicing containing a chimeric spliced-leader-snRNA molecule. Nature 335: 559–562
Campbell DA, Thornton DA, Boothroyd JC (1984) Apparent discontinous transcription of Trypanosoma brucei variant surface antigen genes. Nature 311: 350–355
Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, Kuck U, Bennoun P, Rochaix J-D (1988) Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell 52: 903–913
Clayton CE (1985) Structure and regulated expression of genes encoding fructose biphosphate aldolase in Trypanosoma brucei. EMBO J 4: 2997–3003
Comelissen AWCA, Verspieren MP, Toulme J-J, Swinkels BW, Borst P (1986) The common 5’ terminal sequence on trypanosome mRNAs: a target for anti-messenger oligodeoxynucleotides. Nucleic Acids Res 14: 5605–5614
De Lange T, Berkvens TM, Veerman HJG, Carlos A, Frasch C, Barry JD, Borst P (1984) Comparison of the genes coding for the common 5’ terminal sequence of messenger RNAs in three trypanosome species. Nucleic Acids Res 12: 4431–4443
Dorfman D, Donelson J (1984) Characterization of the 1.35 kb DNA repeat unit containing the conserved 35 nucleotides at the 5’-termini of VSG mRNAs in Trypanosoma brucei. Nucleic Acids Res 12: 4907–4920
Freistadt M, Robertson HT, Branch A, Cross GAM (1987) Direct anaysis of the mini-exon-donor RNA of Trypanosoma brucei: Detection of a novel cap structure also present in messenger RNA. Nucleic Acids Res 15: 9861–9880
Fromm H, Edelman M, Koller B, Goloubinoff P, Galun E (1986) The enigma of the gene coding for ribosomal protein S12 in the chloroplasts of Nicotiana. Nucleic Acids Res 14: 883–898
Glass DJ, Polvere RI, Van der Ploeg LHT (1986) Conserved sequences and transcription of the HSP 70 gene family in Trypanosoma brucei. Mol Cell Biol 6: 4657–4666
Gonzalez A, Lemer TJ, Huccas M, Sosa-Pineda B, Nogueira N, Lizardi PM (1985) Apparent generation of a segmented mRNA from two separate tandem gene families in Trypanosoma cruzi. Nucleic Acids Res 13: 5789–5804
Imboden MA, Laird PW, Affolter M, Seebeck T (1987) Transcription of the intergenic regions of the tubulin gene cluster of Trypanosoma brucei: evidence for a polycistronic transcription unit in a eukaryote. Nucleic Acids Res 15: 7357–7370
Johnson PJ, KooterJM, Borst P (1987) Inactivation of transcription by UV irradiation of T. brucei provides evidence for a mulitcistronic transcription unit including a VSG gene. Cell 51: 273–281
Koller B, Fromm H, Galun E, Edelman M (1987) Evidence for in vivo Trans splicing of pre-mRNAs in tobacco chloroplasts. Cell 48: 111–119
Kooter JM, DeLange T, Borst P (1984) Alpha-amanitin-insensitive transcription of variant surface glycoprotein genes provides further evidence for discontinuous transcription in trypanosomes. Nucleic Acids Res 12: 9457–9472
Kooter J, Van-der-Spek H, Wagter R, d’Oliveira C, Van-der-Hooven F, Johnson P, Borst P (1987) The anatomy and transcription of a telomeric expression site for variant-specific surface antigens in T. brucei. Cell 51: 261–272
Krause M, Hirsh D (1987) A trans-spliced leader sequence on actin mRNA in C. elegans. Cell 49: 753–761
Laird PW, Zomerdijk JCBM, deKorte D, Borst P (1987) In vivo labelling of intermediates in the discontinuous synthesis of mRNAs in Trypanosoma brucei. EMBO J 6: 1055–1062
Landfear SM, Wirth DF (1985) Structure of mRNA encoded by tubulin genes in Leishmania enriettii. Mol Biochem Parasit 15: 61–82
Layden RE, Eisen H (1988) Alternative trans splicing inTrypanosoma equiperdum: Implications for splice site selection. Mol Cell Biol 8: 1352–1360
Michels PAM, Poliszczak A, Osinga KA, Misset O, Beeumen J Van, Werenga RK, Borst P, Opperdoes FR (1986) Two tandemly linked identical genes code for the glycosomal glyceraldehyde-phosphate dehydrogenase in Trypanosoma brucei. EMBO J 5: 1049–1056
Milhausen M, Nelson RG, Sather S, Selkirk M, Agabian N (1984) Identification of a small RNA containing the trypanosome spliced leaden a donor of shared 5’ sequences of trypanosomatid mRNAs? Cell 38: 721–729
Miller SI, Landfear SM, Wirth DF (1986) Cloning and characterization of a Leishmania gene encoding a RNA spliced leader sequence. Nucleic Acids Res 14: 7341–7360
Mottram J, Perry K, Lizardi P, Luhrmann R, Agabian N, Nelson R (1988) Isolation and sequence of four snRNA genes of Trypanosoma brucei brucei: identification of the trypanosome U2, U4 and U6 RNA analogues. Mol Cell Biol (in press)
Mowatt MR, Clayton CE (1987) Developmental regulation of a novel repetitive protein of Trypanosoma brucei. Mol Cell Biol 7: 2838–2844
Muhich ML, Boothroyd JC (1988) Polycistronic transcripts in trypanosomes and their accumulation during heat shock: evidence for a precursor role in mRNA synthesis. Mol Cell Biol 8: 3837–3846
Muhich ML, Hughes DE, Simpson AM, Simpson L (1987) The monogenetic kinetoplastid Crithidia fasciculata contains a transcriptionally active, multicopy mini-exon sequence. Nucleic Acids Res 15: 3141–3153
Murphy WJ, Watkins KP, Agabian N (1986) Identification of a novel Y branch structure as an intermediate in Trypanosome mRNA processing: evidence for Trans splicing. Cell 47: 517–525
Osinga KA, Swinkels BW, Gibson WC, Borst P, Veeneman GH, VanBoom JH, Michels PAM, Opperdoes FR (1985) Topogenesis of microbody enzymes: a sequence comparison of the genes for the glycosomal (microbody) and cytosolic phosphoglycerate kinases of Trypanosoma brucei. EMBO J 4: 3811–3817
Padgett RA, Grabowski PJ, Konarska MM, Seiler S, Sharp PA (1986) Splicing of messenger RNA precursors. Annu Rev Biochem 55: 1119–1150
Perry KL, Watkins KP, Agabian N (1987) Trypanosome mRNAs have unusual “cap4” structures acquired by spliced leader addition. Proc Natl Acad Sci USA 84: 8190–8194
Sather S, Agabian N (1985) A 5’ spliced leader is added in Trans to both alpha-and beta-tubulin transcripts in Trypanosoma brucei. Proc Natl Acad Sci USA 82: 5695–5699
Sharp P (1987) Trans splicing: variation on a familiar theme? Cell 50: 147–148
Sogin ML, Elwood HJ, Gunderson JH (1986) Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci USA 83: 1383–1387
Sutton RE, Boothroyd JC (1986) Evidence for trans splicing in trypanosomes. Cell 47: 527–535
Sutton RE, Boothroyd JC (1988a) The cap of both medRNA and mRNA of trypanosomes is 7-methylguanosine. Mol Cell Biol 8: 494–496
Sutton RE, Boothroyd JC (1988b) Trypanosome trans-splicing utilizes 2’-5’ branches and a corresponding debranching activity. EMBO J 7: 1431–1437
Takacs AM, Denker JA, Perrine KG, Maroney PA, Nilsen TW (1988) A 22-nucleotide spliced leader sequence in the human parasitic nematode Brugia malayi is identical to the transspliced leader exon in Caenorhabditis elegans. Proc Natl Acad Sci USA 85: 7932–7936
Thomas JD, Conrad RC, Blumenthal T (1988) The C. elegans trans-spliced leader RNA is bound to Sm and has a trimethylguanosine cap. Cell 54: 533–539
Torazawa K, Hayashida N, Obokata J, Shinozaki K, Sugiura M (1986) The 5’ part of the gene for ribosomal protein S 12 is located 30 kbp downstream from its 3’ part in tobacco chloroplast genome. Nucleic Acids Res 14: 3143
Tschudi C, Ullu E (1988) Polygene transcripts are precursors to calmodulin mRNAs in trypanosomes. EMBO J 7: 455–463
Tschudi C, Young AS, Ruben L, Patton CL, Richards FF (1985) Calmodulin genes in trypanosomes are tandemly repeated and produce multiple mRNAs with a common 5’ leader sequence. Proc Natl Acad Sci USA 82: 3998–4002
Tschudi C, Richards FF, Ullu E (1986) The U2 RNA analogue of Trypanosoma brucei gambiense: implications for a splicing mechanism in trypanosomes. Nucleic Acids Res 14: 8893–8903
Van Doren K, Hirsh D (1988) The trans-spliced leader RNA exists as an snRNP in C. elegans. Nature 335:556–559
Walder JA, Eder PS, Engman DM, Brentano ST, Walder RY, Knutzon DS, Dorfman DM, Donelson JE (1986) The 35-nucleotide spliced leader sequence is common to all trypanosome messenger RNAs. Science 233: 569–571
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© 1989 Springer-Verlag Berlin Heidelberg
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Boothroyd, J.C. (1989). Trans-Splicing of RNA. In: Eckstein, F., Lilley, D.M.J. (eds) Nucleic Acids and Molecular Biology. Nucleic Acids and Molecular Biology, vol 3. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-83709-8_14
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DOI: https://doi.org/10.1007/978-3-642-83709-8_14
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