Abstract
Neurospora VS RNA performs an RNA-mediated self-cleavage reaction whose products contain 2',3'-cyclic phosphate and 5'-hydroxyl termini. This reaction is similar to those of hammerhead, hairpin, and hepatitis delta virus ribozymes; however, VS RNA is not similar in sequence to these other self-cleaving motifs. Here we propose a model for the secondary structure of the self-cleaving region of VS RNA, supported by site-directed mutagenesis and chemical modification structure probing data. The secondary structure of VS RNA is distinct from those of the other naturally occurring RNA self-cleaving domains. In addition to a unique secondary structure, several Mg-dependent interactions occur during the folding of VS RNA into its active tertiary conformation.
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.
- Banerjee A. R., Jaeger J. A., Turner D. H. Thermal unfolding of a group I ribozyme: the low-temperature transition is primarily disruption of tertiary structure. Biochemistry. 1993 Jan 12;32(1):153–163. doi: 10.1021/bi00052a021. [DOI] [PubMed] [Google Scholar]
- Been M. D. Cis- and trans-acting ribozymes from a human pathogen, hepatitis delta virus. Trends Biochem Sci. 1994 Jun;19(6):251–256. doi: 10.1016/0968-0004(94)90151-1. [DOI] [PubMed] [Google Scholar]
- Berzal-Herranz A., Joseph S., Chowrira B. M., Butcher S. E., Burke J. M. Essential nucleotide sequences and secondary structure elements of the hairpin ribozyme. EMBO J. 1993 Jun;12(6):2567–2573. doi: 10.1002/j.1460-2075.1993.tb05912.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bruce A. G., Uhlenbeck O. C. Reactions at the termini of tRNA with T4 RNA ligase. Nucleic Acids Res. 1978 Oct;5(10):3665–3677. doi: 10.1093/nar/5.10.3665. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collins R. A., Olive J. E. Reaction conditions and kinetics of self-cleavage of a ribozyme derived from Neurospora VS RNA. Biochemistry. 1993 Mar 23;32(11):2795–2799. doi: 10.1021/bi00062a009. [DOI] [PubMed] [Google Scholar]
- Crothers D. M., Cole P. E., Hilbers C. W., Shulman R. G. The molecular mechanism of thermal unfolding of Escherichia coli formylmethionine transfer RNA. J Mol Biol. 1974 Jul 25;87(1):63–88. doi: 10.1016/0022-2836(74)90560-9. [DOI] [PubMed] [Google Scholar]
- Ehresmann C., Baudin F., Mougel M., Romby P., Ebel J. P., Ehresmann B. Probing the structure of RNAs in solution. Nucleic Acids Res. 1987 Nov 25;15(22):9109–9128. doi: 10.1093/nar/15.22.9109. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Forster A. C., Symons R. H. Self-cleavage of virusoid RNA is performed by the proposed 55-nucleotide active site. Cell. 1987 Jul 3;50(1):9–16. doi: 10.1016/0092-8674(87)90657-x. [DOI] [PubMed] [Google Scholar]
- Gautheret D., Konings D., Gutell R. R. A major family of motifs involving G.A mismatches in ribosomal RNA. J Mol Biol. 1994 Sep 9;242(1):1–8. doi: 10.1006/jmbi.1994.1552. [DOI] [PubMed] [Google Scholar]
- Guo H. C., De Abreu D. M., Tillier E. R., Saville B. J., Olive J. E., Collins R. A. Nucleotide sequence requirements for self-cleavage of Neurospora VS RNA. J Mol Biol. 1993 Jul 20;232(2):351–361. doi: 10.1006/jmbi.1993.1395. [DOI] [PubMed] [Google Scholar]
- Hampel A., Tritz R., Hicks M., Cruz P. 'Hairpin' catalytic RNA model: evidence for helices and sequence requirement for substrate RNA. Nucleic Acids Res. 1990 Jan 25;18(2):299–304. doi: 10.1093/nar/18.2.299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Heus H. A., Pardi A. Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops. Science. 1991 Jul 12;253(5016):191–194. doi: 10.1126/science.1712983. [DOI] [PubMed] [Google Scholar]
- Inoue T., Cech T. R. Secondary structure of the circular form of the Tetrahymena rRNA intervening sequence: a technique for RNA structure analysis using chemical probes and reverse transcriptase. Proc Natl Acad Sci U S A. 1985 Feb;82(3):648–652. doi: 10.1073/pnas.82.3.648. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jaeger J. A., Turner D. H., Zuker M. Improved predictions of secondary structures for RNA. Proc Natl Acad Sci U S A. 1989 Oct;86(20):7706–7710. doi: 10.1073/pnas.86.20.7706. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jaeger J. A., Turner D. H., Zuker M. Predicting optimal and suboptimal secondary structure for RNA. Methods Enzymol. 1990;183:281–306. doi: 10.1016/0076-6879(90)83019-6. [DOI] [PubMed] [Google Scholar]
- Jaeger J. A., Zuker M., Turner D. H. Melting and chemical modification of a cyclized self-splicing group I intron: similarity of structures in 1 M Na+, in 10 mM Mg2+, and in the presence of substrate. Biochemistry. 1990 Nov 6;29(44):10147–10158. doi: 10.1021/bi00496a002. [DOI] [PubMed] [Google Scholar]
- Joseph S., Berzal-Herranz A., Chowrira B. M., Butcher S. E., Burke J. M. Substrate selection rules for the hairpin ribozyme determined by in vitro selection, mutation, and analysis of mismatched substrates. Genes Dev. 1993 Jan;7(1):130–138. doi: 10.1101/gad.7.1.130. [DOI] [PubMed] [Google Scholar]
- Kennell J. C., Saville B. J., Mohr S., Kuiper M. T., Sabourin J. R., Collins R. A., Lambowitz A. M. The VS catalytic RNA replicates by reverse transcription as a satellite of a retroplasmid. Genes Dev. 1995 Feb 1;9(3):294–303. doi: 10.1101/gad.9.3.294. [DOI] [PubMed] [Google Scholar]
- Krol A., Carbon P. A guide for probing native small nuclear RNA and ribonucleoprotein structures. Methods Enzymol. 1989;180:212–227. doi: 10.1016/0076-6879(89)80103-x. [DOI] [PubMed] [Google Scholar]
- Kunkel T. A., Roberts J. D., Zakour R. A. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 1987;154:367–382. doi: 10.1016/0076-6879(87)54085-x. [DOI] [PubMed] [Google Scholar]
- Peattie D. A. Direct chemical method for sequencing RNA. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1760–1764. doi: 10.1073/pnas.76.4.1760. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peattie D. A., Gilbert W. Chemical probes for higher-order structure in RNA. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4679–4682. doi: 10.1073/pnas.77.8.4679. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pley H. W., Flaherty K. M., McKay D. B. Three-dimensional structure of a hammerhead ribozyme. Nature. 1994 Nov 3;372(6501):68–74. doi: 10.1038/372068a0. [DOI] [PubMed] [Google Scholar]
- Rosenstein S. P., Been M. D. Evidence that genomic and antigenomic RNA self-cleaving elements from hepatitis delta virus have similar secondary structures. Nucleic Acids Res. 1991 Oct 11;19(19):5409–5416. doi: 10.1093/nar/19.19.5409. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rubino L., Tousignant M. E., Steger G., Kaper J. M. Nucleotide sequence and structural analysis of two satellite RNAs associated with chicory yellow mottle virus. J Gen Virol. 1990 Sep;71(Pt 9):1897–1903. doi: 10.1099/0022-1317-71-9-1897. [DOI] [PubMed] [Google Scholar]
- SantaLucia J., Jr, Kierzek R., Turner D. H. Context dependence of hydrogen bond free energy revealed by substitutions in an RNA hairpin. Science. 1992 Apr 10;256(5054):217–219. doi: 10.1126/science.1373521. [DOI] [PubMed] [Google Scholar]
- SantaLucia J., Jr, Kierzek R., Turner D. H. Effects of GA mismatches on the structure and thermodynamics of RNA internal loops. Biochemistry. 1990 Sep 18;29(37):8813–8819. doi: 10.1021/bi00489a044. [DOI] [PubMed] [Google Scholar]
- Saville B. J., Collins R. A. A site-specific self-cleavage reaction performed by a novel RNA in Neurospora mitochondria. Cell. 1990 May 18;61(4):685–696. doi: 10.1016/0092-8674(90)90480-3. [DOI] [PubMed] [Google Scholar]
- Stern S., Changchien L. M., Craven G. R., Noller H. F. Interaction of proteins S16, S17 and S20 with 16 S ribosomal RNA. J Mol Biol. 1988 Mar 20;200(2):291–299. doi: 10.1016/0022-2836(88)90241-0. [DOI] [PubMed] [Google Scholar]
- Symons R. H. Small catalytic RNAs. Annu Rev Biochem. 1992;61:641–671. doi: 10.1146/annurev.bi.61.070192.003233. [DOI] [PubMed] [Google Scholar]
- Weeks K. M., Crothers D. M. Major groove accessibility of RNA. Science. 1993 Sep 17;261(5128):1574–1577. doi: 10.1126/science.7690496. [DOI] [PubMed] [Google Scholar]
- Woese C. R., Winker S., Gutell R. R. Architecture of ribosomal RNA: constraints on the sequence of "tetra-loops". Proc Natl Acad Sci U S A. 1990 Nov;87(21):8467–8471. doi: 10.1073/pnas.87.21.8467. [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]