The maturase encoded by a group I intron from Aspergillus nidulans stabilizes RNA tertiary structure and promotes rapid splicing

Journal of Molecular Biology

Volumn 292, Issue 5, 1999, Pages 987-1001

  Ho, Yugong ^a   Waring, Richard B ^a  

^a Temple University   (United States)

Author keywords

Homing endonuclease; Mitochondria; Ribozyme; RNA folding; RNA splicing protein

Indexed keywords

FUNGAL PROTEIN; FUNGAL RNA; MAGNESIUM ION; MATURASE; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS NIDULANS; CONTROLLED STUDY; INTRON; NONHUMAN; PH; PKA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN RNA BINDING; RIBONUCLEASE PROTECTION ASSAY; RNA DEGRADATION; RNA SEQUENCE; RNA SPLICING; RNA STRUCTURE;

ASPERGILLUS; ASPERGILLUS NIDULANS; EMERICELLA NIDULANS; FUNGI; MYXOGASTRIA;

EID: 0033536621     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3070     Document Type: Article

References (60)

1. Akins R. A., Lambowitz A. M. A protein required for splicing group I introns in Neurospora mitochondria is mitochondrial tyrosyl-tRNA synthetase or a derivative thereof. Cell. 50:1987;331-345.
2. Banerjee A. R., Turner D. H. The time dependence of chemical modification reveals slow steps in the folding of a group I ribozyme. Biochemistry. 34:1995;6504-6512.
3. Belfort M., Roberts R. J. Homing endonucleases: keeping the house in order. Nucl. Acids Res. 25:1997;3379-3388.
4. Brehm S. L., Cech T. R. Fate of an intervening sequence ribonucleic acid: excision and cyclization of the Tetrahymena ribosomal ribonucleic acid intervening sequence in vivo. Biochemistry. 22:1983;2390-2397.
5. Caprara M. G., Waring R. B. Important 2′-hydroxyl groups within the core of a group I intron. Biochemistry. 32:1993;3604-3610.
6. Caprara M. G., Mohr G., Lambowitz A. M. A tyrosyl-tRNA synthetase protein induces tertiary folding of the group I intron catalytic core. J. Mol. Biol. 257:1996;512-531.
7. Cate J. H., Gooding A. R., Podell E., Zhou K. H., Golden B. L., Kundrot C. E., Cech T. R., Doudna J. A. Crystal structure of a group I ribozyme domain: principles of RNA packing. Science. 273:1996;1678-1685.
8. Cech T. R. Self-splicing of group I introns. Annu. Rev. Biochem. 59:1990;543-568.
9. Celander D. W., Cech T. R. Visualizing the higher order folding of a catalytic RNA molecule. Science. 251:1991;401-407.
10. Coetzee T., Herschlag D., Belfort M. Escherichia coli proteins, including ribosomal protein S12, facilitate in vitro splicing of phage T4 introns by acting as RNA chaperones. Genes Dev. 8:1994;1575-1588.
11. Cohen S. B., Cech T. R. Dynamics of thermal motions within a large catalytic RNa investigated by cross-linking with thiol-disulfide intercharge. J. Am. Chem. Soc. 119:1997;6259-6268.
12. Cole P. E., Yang S. K., Crothers D. M. Conformational changes of transfer ribonucleic acid. Equilibrium phase diagrams. Biochemistry. 11:1972;4358-4368.
13. Costa M., Michel F. Frequent use of the same tertiary motif by self-folding RNAs. EMBO J. 14:1995;1276.
14. Costa M., Michel F. Rules for RNA recognition of GNRA tetraloops deduced by in vitro selection: comparison with in vivo evolution. EMBO J. 16:1997;3289-3302.
15. Downs W. D., Cech T. R. Kinetic pathway for folding of the Tetrahymena ribozyme revealed by three UV-inducible crosslinks. RNA. 2:1996;718-732.
16. Draper D. E. Parallel worlds. Nature Struct. Biol. 3:1996;397-400.
17. Dujon B. Group I introns as mobile genetic elements: facts and mechanistic speculations: a review. Gene. 82:1989;91-114.
18. Ehresmann C., Baudin F., Mougel M., Romby P., Ebel J.-P., Ehresmann B. Probing the structure of RNAs in solution. Nucl. Acids Res. 15:1987;9109-9128.
19. Esteban J. A., Banerjee A. R., Bruke J. M. Kinetic mechanism of the hairpin ribozyme - Identification and characterization of two nonexchangeable conformations. J. Biol. Chem. 272:1997;13629-13639.
20. Fierke C. A., Hammes G. G. Transient kinetic approaches to enzyme mechanisms. Methods Enzymol. 249:1995;3-38.
21. Fersht A. Enzyme Structure and Mechanism. 1985;W.H. Freeman & Co. New York.
22. Gampel A., Nishikimi M., Tzagoloff A. CBP2 protein promotes in vitro excision of a yeast mitochondrial group I intron. Mol. Cell Biol. 9:1989;5424-5433.
23. Garriga G., Lambowitz A. M. RNA splicing in neurospora mitochondria: self-splicing of a mitochondrial intron in vitro. Cell. 39:1984;631-641.
24. Herschlag D. RNA chaperones and the RNA folding problem. J. Biol. Chem. 270:1995;20871-20874.
25. Herschlag D., Khosla M. Comparison of pH dependencies of the Tetrahymena ribozyme reactions with RNA 2′-substituted and phosphorothioate substrates reveals a rate-limiting conformational step. Biochemistry. 33:1994;5291-5297.
26. Heus H. A., Pardi A. Structural features that give rise to the unusual stability of RNA hairpins containing GNRA loops. Science. 253:1991;191-194.
27. Ho Y., Kim S. J., Waring R. B. A protein encoded by a group I intron in Aspergillus nidulans directly assists RNA splicing and is a DNA endonuclease. Proc Natl Acad. Sci. USA. 94:1997;8994-8999.
28. Hur M., Geese W. J., Waring R. B. Self-splicing activity of the mitochondrial group-I introns from Aspergillus nidulans and related introns from other species. Curr. Genet. 32:1997;399-407.
29. Jaeger L., Westhof E., Michel F. Function of P11, a tertiary base pairing in self-splicing introns of subgroup IA. J. Mol. Biol. 221:1991;1153-1164.
30. Jaeger L., Michel F., Westhof E. Involvement of a GNRA tetraloop in long-range RNA tertiary interactions. J. Mol. Biol. 236:1994;1271-1276.
31. Laggerbauer B., Murphy F. L., Cech T. R. Two major tertiary folding transitions of the Tetrahymena catalytic RNA. EMBO J. 13:1994;2669-2676.
32. Lambowitz A. M., Perlman P. S. Involvement of aminoacyl-tRNA synthetases and other proteins in group I and group II intron splicing. Trends. Biochem. Sci. 15:1990;440-444.
33. Lambowitz A. M., Caprara M. G., Zimmerly S., Perlman P. S. Group I and group II ribozymes as RNPs: clues to the past and guides to the future. Gesteland R. F., Atkins J. F., Cech T. R. The RNA World II. 1999;451-485 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
34. Latham J. A., Cech T. R. Defining the inside and outside of a catalytic RNA molecule. Science. 245:1989;276-282.
35. Lazowska J., Jacq C., Slonimiski P. P. Sequence of intron and flanking exons in wild-type and box3 mutants of cytochrome b reveals an interlaced splicing protein coded by an intron. Cell. 22:1980;333-348.
36. Lehnert V., Jaeger L., Michel F., Westhof E. New loop-loop tertiary interactions in self-splicing introns of sub-group IC and ID: a complete 3D model of the Tetrahymena thermophila ribozyme. Chem. Biol. 3:1996;993-1009.
37. Lewin A. S., Thomas J. Jr, Tirupata H. K. Cotranscriptional splicing of a group I intron is facilitated by the Cbp2 protein. Mol. Cell Biol. 15:1995;6971-6978.
38. Maglott E. J., Deo S. S., Przykorska A., Glick G. D. Conformational transitions of an unmodified tRNA: implications for RNA folding. Biochemistry. 37:1998;16349-16359.
39. Matsuura M., Saldanha R., Ma H. W., Wank H., Yang J., Mohr G., Cavanagh S., Dunny G. M., Belfort M., Lambowitz A. M. A bacterial group II intron encoding reverse transcriptase, maturase, DNA endonuclease activities: biochemical demonstration of maturase activity and insertion of new genetic information within the intron. Genes Dev. 11:1997;2910-2924.
40. Michel F., Westhof E. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis. J. Mol. Biol. 216:1990;585-610.
41. Murphy F. L., Cech T. R. An independently folding domain of RNA tertiary structure within the Tetrahymena ribozyme. Biochemistry. 32:1993;5291-5300.
42. Murphy F. L., Cech T. R. GAAA tetraloop and conserved bulge stabilize tertiary structure of a group I intron domain. J. Mol. Biol. 236:1994;49-63.
43. Pan J., Woodson S. A. Folding intermediates of a self-splicing RNA: mispairing of the catalytic core. J. Mol. Biol. 280:1998;597-609.
44. Perbandt M., Notle A., Lorenz S., Bald R., Betzel C., Erdmann V. A. Crystal structure of domain E of Thermus flavus 5S rRNA: a helical RNA structure including a hairpin loop. FEBS Letters. 429:1998;211-215.
45. Pley H. W., Flaherty K. M., McKay D. B. Model for an RNA tertiary interaction from the structure of an intermolecular complex between a GAAA tetraloop and an RNA helix. Nature. 372:1994;111-113.
46. Saldanha R. J., Patel S. S., Surendran R., Lee J. C., Lambowitz A. M. Involvement of Neurospora mitochondrial tyrosyl-tRNA synthetase in RNA splicing. A new method for purifying the protein and characterization of physical and enzymatic properties pertinent to splicing. Biochemistry. 34:1995;1275-1287.
47. Saldanha R., Ellington A., Lambowitz A. M. Analysis of the CYT-18 protein binding site at the junction of stacked helices in a group I intron RNA by quantitative binding assays and in vitro selection. J. Mol. Biol. 261:1996;23-42.
48. Sclavi B., Sullivan M., Chance M. R., Brenowitz M., Woodson S. A. RNa folding at millisecond intervals by synchrotron hydroxyl radical footprinting. Science. 279:1998;1940-1943.
49. Shaw L. C., Lewin A. S. Protein-induced folding of a group I intron in cytochrome b pre-mRNA. J. Biol. Chem. 270:1995;21552-21562.
50. Sjogren A. S., Stroemberg R., Sjoeberg B. M. pH dependence of self-splicing by the group IA2 intron in a pre-mRNA derived from the nrdB gene of bacteriophage T4. Nucl. Acids Res. 25:1997;3543-3549.
51. Stage-Zimmermann T. K., Uhlenbeck O. C. Hammerhead ribozyme kinetics. RNA. 4:1998;875-889.
52. Suh E. R., Waring R. B. The conserved terminal guanosine of a group I intron can help prevent reopening of the ligated exons. J. Mol. Biol. 232:1993;375-385.
53. Treiber D. K., Rook M. S., Zarrinkar P. P., Williamson J. R. Kinetic intermediates trapped by native interactions in RNA folding. Science. 279:1998;1943-1946.
54. Weeks K. M. Protein-facilitated RNA folding. Curr. Opin. Struct. Biol. 7:1997;336-342.
55. Weeks K. M., Cech T. R. Efficient protein-facilitated splicing of the yeast mitochondrial bI5 intron. Biochemistry. 34:1995;7728-7738.
56. Weeks K. M., Cech T. R. Assembly of a ribonucleoprotein catalyst by tertiary structure capture. Science. 271:1996;345-348.
57. Zarrinkar P. P., Williamson J. R. Kinetic intermediates in RNA folding. Science. 265:1994;918-924.
58. Zarrinkar P. P., Williamson J. R. The kinetic folding pathway of the Tetrahymena ribozyme reveals possible similarities between RNA and protein folding. Nature Struct. Biol. 3:1996;432-438.
59. Zaug A. J., Kent J. R., Cech T. R. Reactions of the intervening sequence of the Tetrahymena ribosomal ribonucleic acid precursor: pH dependence of cyclization and site-specific hydrolysis. Biochemistry. 24:1985;6211-6218.
60. Zaug A. J., Davila-Aponte J. A., Cech T. R. Catalysis of RNA cleavage by a ribozyme derived from the group I intron of Anabaena pre-tRNALeu. Biochemistry. 33:1994;14935-14947.