Abstract
We present evidence that a subset of mRNAs in the human parasitic trematode Schistosoma mansoni contain an identical 36-nucleotide spliced leader (SL) sequence at their 5' termini. The SL is derived from a 90-nucleotide nonpolyadenylylated RNA (SL RNA), presumably by trans-splicing. Neither the SL nor the SL RNA share significant sequence identity with previously described trans-spliced leaders and SL RNAs in trypanosomatid protozoans or nematodes. However, several features, such as predicted secondary structure, trimethylguanosine cap, and potential Sm binding site, suggest similarities among SL RNAs in widely divergent organisms. Our evidence also indicates that the exon 3 acceptor site of the 3-hydroxy-3-methylglutaryl-CoA reductase gene can be spliced either to the SL by trans-splicing or to an upstream exon, 2, by cis-splicing. The presence of a SL sequence in S. mansoni, a member of the phylum Platyhelminthes, suggests that transplicing may be a common feature of other lower invertebrates.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bektesh S. L., Hirsh D. I. C. elegans mRNAs acquire a spliced leader through a trans-splicing mechanism. Nucleic Acids Res. 1988 Jun 24;16(12):5692–5692. doi: 10.1093/nar/16.12.5692. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bektesh S., Van Doren K., Hirsh D. Presence of the Caenorhabditis elegans spliced leader on different mRNAs and in different genera of nematodes. Genes Dev. 1988 Oct;2(10):1277–1283. doi: 10.1101/gad.2.10.1277. [DOI] [PubMed] [Google Scholar]
- Blumenthal T., Thomas J. Cis and trans mRNA splicing in C. elegans. Trends Genet. 1988 Nov;4(11):305–308. doi: 10.1016/0168-9525(88)90107-2. [DOI] [PubMed] [Google Scholar]
- Bobek L. A., Rekosh D. M., LoVerde P. T. Small gene family encoding an eggshell (chorion) protein of the human parasite Schistosoma mansoni. Mol Cell Biol. 1988 Aug;8(8):3008–3016. doi: 10.1128/mcb.8.8.3008. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Borst P. Discontinuous transcription and antigenic variation in trypanosomes. Annu Rev Biochem. 1986;55:701–732. doi: 10.1146/annurev.bi.55.070186.003413. [DOI] [PubMed] [Google Scholar]
- Bruzik J. P., Van Doren K., Hirsh D., Steitz J. A. Trans splicing involves a novel form of small nuclear ribonucleoprotein particles. Nature. 1988 Oct 6;335(6190):559–562. doi: 10.1038/335559a0. [DOI] [PubMed] [Google Scholar]
- Davis R. E., Davis A. H., Carroll S. M., Rajkovic A., Rottman F. M. Tandemly repeated exons encode 81-base repeats in multiple, developmentally regulated Schistosoma mansoni transcripts. Mol Cell Biol. 1988 Nov;8(11):4745–4755. doi: 10.1128/mcb.8.11.4745. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
- Freistadt M. S., Cross G. A., Branch A. D., Robertson H. D. Direct analysis of the mini-exon donor RNA of Trypanosoma brucei: detection of a novel cap structure also present in messenger RNA. Nucleic Acids Res. 1987 Dec 10;15(23):9861–9879. doi: 10.1093/nar/15.23.9861. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Golde T. E., Estus S., Usiak M., Younkin L. H., Younkin S. G. Expression of beta amyloid protein precursor mRNAs: recognition of a novel alternatively spliced form and quantitation in Alzheimer's disease using PCR. Neuron. 1990 Feb;4(2):253–267. doi: 10.1016/0896-6273(90)90100-t. [DOI] [PubMed] [Google Scholar]
- Hattori M., Sakaki Y. Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986 Feb 1;152(2):232–238. doi: 10.1016/0003-2697(86)90403-3. [DOI] [PubMed] [Google Scholar]
- Huang X. Y., Hirsh D. A second trans-spliced RNA leader sequence in the nematode Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1989 Nov;86(22):8640–8644. doi: 10.1073/pnas.86.22.8640. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krainer A. R. Pre-mRNA splicing by complementation with purified human U1, U2, U4/U6 and U5 snRNPs. Nucleic Acids Res. 1988 Oct 25;16(20):9415–9429. doi: 10.1093/nar/16.20.9415. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Krause M., Hirsh D. A trans-spliced leader sequence on actin mRNA in C. elegans. Cell. 1987 Jun 19;49(6):753–761. doi: 10.1016/0092-8674(87)90613-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maroney P. A., Hannon G. J., Nilsen T. W. Transcription and cap trimethylation of a nematode spliced leader RNA in a cell-free system. Proc Natl Acad Sci U S A. 1990 Jan;87(2):709–713. doi: 10.1073/pnas.87.2.709. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Murphy W. J., Watkins K. P., Agabian N. Identification of a novel Y branch structure as an intermediate in trypanosome mRNA processing: evidence for trans splicing. Cell. 1986 Nov 21;47(4):517–525. doi: 10.1016/0092-8674(86)90616-1. [DOI] [PubMed] [Google Scholar]
- Nilsen T. W., Shambaugh J., Denker J., Chubb G., Faser C., Putnam L., Bennett K. Characterization and expression of a spliced leader RNA in the parasitic nematode Ascaris lumbricoides var. suum. Mol Cell Biol. 1989 Aug;9(8):3543–3547. doi: 10.1128/mcb.9.8.3543. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nilsen T. W. Trans-splicing in nematodes. Exp Parasitol. 1989 Nov;69(4):413–416. doi: 10.1016/0014-4894(89)90191-4. [DOI] [PubMed] [Google Scholar]
- Perry K. L., Watkins K. P., Agabian N. Trypanosome mRNAs have unusual "cap 4" structures acquired by addition of a spliced leader. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8190–8194. doi: 10.1073/pnas.84.23.8190. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rajkovic A., Simonsen J. N., Davis R. E., Rottman F. M. Molecular cloning and sequence analysis of 3-hydroxy-3-methylglutaryl-coenzyme A reductase from the human parasite Schistosoma mansoni. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8217–8221. doi: 10.1073/pnas.86.21.8217. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ram D., Grossman Z., Markovics A., Avivi A., Ziv E., Lantner F., Schechter I. Rapid changes in the expression of a gene encoding a calcium-binding protein in Schistosoma mansoni. Mol Biochem Parasitol. 1989 May 1;34(2):167–175. doi: 10.1016/0166-6851(89)90008-x. [DOI] [PubMed] [Google Scholar]
- Simurda M. C., van Keulen H., Rekosh D. M., LoVerde P. T. Schistosoma mansoni: identification and analysis of an mRNA and a gene encoding superoxide dismutase (Cu/Zn). Exp Parasitol. 1988 Oct;67(1):73–84. doi: 10.1016/0014-4894(88)90010-0. [DOI] [PubMed] [Google Scholar]
- Sutton R. E., Boothroyd J. C. Evidence for trans splicing in trypanosomes. Cell. 1986 Nov 21;47(4):527–535. doi: 10.1016/0092-8674(86)90617-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sutton R. E., Boothroyd J. C. The cap of both miniexon-derived RNA and mRNA of trypanosomes is 7-methylguanosine. Mol Cell Biol. 1988 Jan;8(1):494–496. doi: 10.1128/mcb.8.1.494. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takacs A. M., Denker J. A., Perrine K. G., Maroney P. A., Nilsen T. W. A 22-nucleotide spliced leader sequence in the human parasitic nematode Brugia malayi is identical to the trans-spliced leader exon in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 1988 Nov;85(21):7932–7936. doi: 10.1073/pnas.85.21.7932. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas J. D., Conrad R. C., Blumenthal T. The C. elegans trans-spliced leader RNA is bound to Sm and has a trimethylguanosine cap. Cell. 1988 Aug 12;54(4):533–539. doi: 10.1016/0092-8674(88)90075-x. [DOI] [PubMed] [Google Scholar]
- Van Doren K., Hirsh D. Trans-spliced leader RNA exists as small nuclear ribonucleoprotein particles in Caenorhabditis elegans. Nature. 1988 Oct 6;335(6190):556–559. doi: 10.1038/335556a0. [DOI] [PubMed] [Google Scholar]
- Wang A. M., Doyle M. V., Mark D. F. Quantitation of mRNA by the polymerase chain reaction. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9717–9721. doi: 10.1073/pnas.86.24.9717. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zuker M. On finding all suboptimal foldings of an RNA molecule. Science. 1989 Apr 7;244(4900):48–52. doi: 10.1126/science.2468181. [DOI] [PubMed] [Google Scholar]