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PMID: 18768647 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Toward predicting self-splicing and protein-facilitated splicing of group I introns.

RNA (New York, N.Y.) ·Vol. 14 ·No. 10 ·2008-10-00 ·Pages 2013-29

Vicens Q, Paukstelis PJ, Westhof E, Lambowitz AM, Cech TR

Abstract

In the current era of massive discoveries of noncoding RNAs within genomes, being able to infer a function from a nucleotide sequence is of paramount interest. Although studies of individual group I introns have identified self-splicing and nonself-splicing examples, there is no overall understanding of the prevalence of self-splicing or the factors that determine it among the >2300 group I introns sequenced to date. Here, the self-splicing activities of 12 group I introns from various organisms were assayed under six reaction conditions that had been shown previously to promote RNA catalysis for different RNAs. Besides revealing that assessing self-splicing under only one condition can be misleading, this survey emphasizes that in vitro self-splicing efficiency is correlated with the GC content of the intron (>35% GC was generally conductive to self-splicing), and with the ability of the introns to form particular tertiary interactions. Addition of the Neurospora crassa CYT-18 protein activated splicing of two nonself-splicing introns, but inhibited the second step of self-splicing for two others. Together, correlations between sequence, predicted structure and splicing begin to establish rules that should facilitate our ability to predict the self-splicing activity of any group I intron from its sequence.

MeSH Terms
Base Composition Base Sequence Catalysis Introns Neurospora crassa/enzymology Nucleic Acid Conformation RNA Splicing RNA, Catalytic/chemistry RNA, Messenger/chemistry Tyrosine-tRNA Ligase/chemistry
Chemicals
RNA, Catalytic RNA, Messenger Tyrosine-tRNA Ligase
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Vicens Quentin
Howard Hughes Medical Institute, University of Colorado, Department of Chemistry and Biochemistry, Boulder, Colorado 80309-0215, USA. quentin.vicens@colorado.edu
Paukstelis Paul J
Westhof Eric
Lambowitz Alan M
Cech Thomas R
References (81)
81 references, click to expand
  1. Protein facilitation of group I intron splicing by assembly of the catalytic core and the 5' splice site domain.
    Cell. 1995 Jul 28;82(2):221-30 PMID: 7628013
  2. Function of P11, a tertiary base pairing in self-splicing introns of subgroup IA.
    J Mol Biol. 1991 Oct 20;221(4):1153-64 PMID: 1942046
  3. Self-assembly of a group I intron active site from its component tertiary structural domains.
    RNA. 1995 Mar;1(1):36-45 PMID: 7489486
  4. Autocatalytic cyclization of an excised intervening sequence RNA is a cleavage-ligation reaction.
    Nature. 1983 Feb 17-23;301(5901):578-83 PMID: 6186917
  5. A tyrosyl-tRNA synthetase suppresses structural defects in the two major helical domains of the group I intron catalytic core.
    J Mol Biol. 1996 Sep 20;262(2):87-104 PMID: 8831782
  6. Structure of a tyrosyl-tRNA synthetase splicing factor bound to a group I intron RNA.
    Nature. 2008 Jan 3;451(7174):94-7 PMID: 18172503
  7. Protein-dependent transition states for ribonucleoprotein assembly.
    J Mol Biol. 2001 Jun 22;309(5):1087-100 PMID: 11399081
  8. An intron in the nuclear ribosomal DNA of Didymium iridis codes for a group I ribozyme and a novel ribozyme that cooperate in self-splicing.
    Cell. 1994 Feb 25;76(4):725-34 PMID: 8124711
  9. Phylogenetic and genetic evidence for base-triples in the catalytic domain of group I introns.
    Nature. 1990 Oct 11;347(6293):578-80 PMID: 2215683
  10. The Neurospora crassa CYT-18 protein C-terminal RNA-binding domain helps stabilize interdomain tertiary interactions in group I introns.
    RNA. 2004 Apr;10(4):634-44 PMID: 15037773
  11. New reactions of the ribosomal RNA precursor of Tetrahymena and the mechanism of self-splicing.
    J Mol Biol. 1986 May 5;189(1):143-65 PMID: 2431151
  12. Modelling of the three-dimensional architecture of group I catalytic introns based on comparative sequence analysis.
    J Mol Biol. 1990 Dec 5;216(3):585-610 PMID: 2258934
  13. Structural analysis of the Neurospora mitochondrial large rRNA intron and construction of a mini-intron that shows protein-dependent splicing.
    J Biol Chem. 1991 Jan 25;266(3):1809-19 PMID: 1824845
  14. Two distinct binding modes of a protein cofactor with its target RNA.
    J Mol Biol. 2006 Aug 25;361(4):771-84 PMID: 16872630
  15. Kinetic intermediates in RNA folding.
    Science. 1994 Aug 12;265(5174):918-24 PMID: 8052848
  16. Processing of phage T4 td-encoded RNA is analogous to the eukaryotic group I splicing pathway.
    Proc Natl Acad Sci U S A. 1986 Aug;83(16):5875-9 PMID: 3526343
  17. Catalytic activity is retained in the Tetrahymena group I intron despite removal of the large extension of element P5.
    Nucleic Acids Res. 1989 Oct 11;17(19):7879-89 PMID: 2477801
  18. Molecular modelling of the GIR1 branching ribozyme gives new insight into evolution of structurally related ribozymes.
    EMBO J. 2008 Feb 20;27(4):667-78 PMID: 18219270
  19. New loop-loop tertiary interactions in self-splicing introns of subgroup IC and ID: a complete 3D model of the Tetrahymena thermophila ribozyme.
    Chem Biol. 1996 Dec;3(12):993-1009 PMID: 9000010
  20. Involvement of aminoacyl-tRNA synthetases and other proteins in group I and group II intron splicing.
    Trends Biochem Sci. 1990 Nov;15(11):440-4 PMID: 2278103
  21. RNA chaperone StpA loosens interactions of the tertiary structure in the td group I intron in vivo.
    Genes Dev. 2002 Sep 1;16(17):2300-12 PMID: 12208852
  22. Complementary sets of noncanonical base pairs mediate RNA helix packing in the group I intron active site.
    Nat Struct Biol. 1998 Jan;5(1):60-6 PMID: 9437431
  23. In vitro self-splicing reactions of chloroplast and mitochondrial group-I introns in Chlamydomonas eugametos and Chlamydomonas moewusii.
    Curr Genet. 1995 Jan;27(2):177-83 PMID: 7788721
  24. Identification and evolution of fungal mitochondrial tyrosyl-tRNA synthetases with group I intron splicing activity.
    Proc Natl Acad Sci U S A. 2008 Apr 22;105(16):6010-5 PMID: 18413600
  25. Crystal structure of a self-splicing group I intron with both exons.
    Nature. 2004 Jul 1;430(6995):45-50 PMID: 15175762
  26. A protein required for splicing group I introns in Neurospora mitochondria is mitochondrial tyrosyl-tRNA synthetase or a derivative thereof.
    Cell. 1987 Jul 31;50(3):331-45 PMID: 3607872
  27. Motif prediction in ribosomal RNAs Lessons and prospects for automated motif prediction in homologous RNA molecules.
    Biochimie. 2002 Sep;84(9):961-73 PMID: 12458088
  28. Conserved sequences and structures of group I introns: building an active site for RNA catalysis--a review.
    Gene. 1988 Dec 20;73(2):259-71 PMID: 3072259
  29. Mutational analysis of conserved nucleotides in a self-splicing group I intron.
    J Mol Biol. 1990 Oct 5;215(3):345-58 PMID: 1700131
  30. Atomic level architecture of group I introns revealed.
    Trends Biochem Sci. 2006 Jan;31(1):41-51 PMID: 16356725
  31. Self-splicing of a group I intron reveals partitioning of native and misfolded RNA populations in yeast.
    RNA. 2006 Dec;12(12):2149-59 PMID: 17135489
  32. Minimal catalytic domain of a group I self-splicing intron RNA.
    Nat Struct Biol. 2000 Nov;7(11):1032-5 PMID: 11062558
  33. Self-splicing of the group I intron from Anabaena pre-tRNA: requirement for base-pairing of the exons in the anticodon stem.
    Biochemistry. 1993 Aug 10;32(31):7946-53 PMID: 8347600
  34. 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. 1996 Aug 9;261(1):23-42 PMID: 8760500
  35. A tyrosyl-tRNA synthetase recognizes a conserved tRNA-like structural motif in the group I intron catalytic core.
    Cell. 1996 Dec 13;87(6):1135-45 PMID: 8978617
  36. Active site constraints in the hydrolysis reaction catalyzed by bacterial RNase P: analysis of precursor tRNAs with a single 3'-S-phosphorothiolate internucleotide linkage.
    Nucleic Acids Res. 2000 Feb 1;28(3):720-7 PMID: 10637323
  37. Mitochondrial introns: a critical view.
    Trends Genet. 2007 Mar;23(3):119-25 PMID: 17280737
  38. Function of the Neurospora crassa mitochondrial tyrosyl-tRNA synthetase in RNA splicing. Role of the idiosyncratic N-terminal extension and different modes of interaction with different group I introns.
    J Mol Biol. 2001 Mar 16;307(1):75-92 PMID: 11243805
  39. Self-splicing introns in tRNA genes of widely divergent bacteria.
    Nature. 1992 May 14;357(6374):173-6 PMID: 1579169
  40. The ability to form full-length intron RNA circles is a general property of nuclear group I introns.
    RNA. 2003 Dec;9(12):1464-75 PMID: 14624003
  41. Mfold web server for nucleic acid folding and hybridization prediction.
    Nucleic Acids Res. 2003 Jul 1;31(13):3406-15 PMID: 12824337
  42. An independently folding domain of RNA tertiary structure within the Tetrahymena ribozyme.
    Biochemistry. 1993 May 25;32(20):5291-300 PMID: 7684607
  43. Assembly of a ribonucleoprotein catalyst by tertiary structure capture.
    Science. 1996 Jan 19;271(5247):345-8 PMID: 8553068
  44. The RNA Ontology Consortium: an open invitation to the RNA community.
    RNA. 2006 Apr;12(4):533-41 PMID: 16484377
  45. Crystal structure of a phage Twort group I ribozyme-product complex.
    Nat Struct Mol Biol. 2005 Jan;12(1):82-9 PMID: 15580277
  46. Characterization of Neurospora mitochondrial group I introns reveals different CYT-18 dependent and independent splicing strategies and an alternative 3' splice site for an intron ORF.
    RNA. 1997 Feb;3(2):114-31 PMID: 9042940
  47. Self-splicing activity of the mitochondrial group-I introns from Aspergillus nidulans and related introns from other species.
    Curr Genet. 1997 Dec;32(6):399-407 PMID: 9388295
  48. Long-term evolution of the S788 fungal nuclear small subunit rRNA group I introns.
    RNA. 2004 Jul;10(7):1084-96 PMID: 15208444
  49. Influence of specific mutations on the thermal stability of the td group I intron in vitro and on its splicing efficiency in vivo: a comparative study.
    RNA. 1999 Jul;5(7):947-58 PMID: 10411138
  50. 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):10147-58 PMID: 2271644
  51. Recurrent invasion and extinction of a selfish gene.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):13880-5 PMID: 10570167
  52. Kinetic pathway for folding of the Tetrahymena ribozyme revealed by three UV-inducible crosslinks.
    RNA. 1996 Jul;2(7):718-32 PMID: 8756414
  53. Preparation and characterization of RNase P from Escherichia coli.
    Methods Enzymol. 1990;181:569-82 PMID: 2199767
  54. Searching genomes for ribozymes and riboswitches.
    Genome Biol. 2007;8(4):210 PMID: 17472738
  55. Structure of the Tetrahymena ribozyme: base triple sandwich and metal ion at the active site.
    Mol Cell. 2004 Nov 5;16(3):351-62 PMID: 15525509
  56. Evolution from DNA to RNA recognition by the bI3 LAGLIDADG maturase.
    Nat Struct Mol Biol. 2005 Sep;12(9):779-87 PMID: 16116439
  57. Predicting the secondary structures and tertiary interactions of 211 group I introns in IE subgroup.
    Nucleic Acids Res. 2005 Apr 20;33(7):2118-28 PMID: 15843683
  58. Frequent use of the same tertiary motif by self-folding RNAs.
    EMBO J. 1995 Mar 15;14(6):1276-85 PMID: 7720718
  59. A tyrosyl-tRNA synthetase adapted to function in group I intron splicing by acquiring a new RNA binding surface.
    Mol Cell. 2005 Feb 4;17(3):417-28 PMID: 15694342
  60. Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena.
    Cell. 1982 Nov;31(1):147-57 PMID: 6297745
  61. In vitro genetic analysis of the Tetrahymena self-splicing intron.
    Nature. 1990 Sep 27;347(6291):406-8 PMID: 2215650
  62. Structural basis for altering the stability of homologous RNAs from a mesophilic and a thermophilic bacterium.
    RNA. 2006 Apr;12(4):598-606 PMID: 16581805
  63. Crystal structure of human mitochondrial tyrosyl-tRNA synthetase reveals common and idiosyncratic features.
    Structure. 2007 Nov;15(11):1505-16 PMID: 17997975
  64. In vitro selection of RNAs with increased tertiary structure stability.
    RNA. 1999 Aug;5(8):1119-29 PMID: 10445885
  65. Evolution of Tetrahymena ribozyme mutants with increased structural stability.
    Nat Struct Biol. 2002 Nov;9(11):855-61 PMID: 12368901
  66. Rules for RNA recognition of GNRA tetraloops deduced by in vitro selection: comparison with in vivo evolution.
    EMBO J. 1997 Jun 2;16(11):3289-302 PMID: 9214644
  67. A self-splicing group I intron in the nuclear pre-rRNA of the green alga, Ankistrodesmus stipitatus.
    Nucleic Acids Res. 1991 Aug 25;19(16):4429-36 PMID: 1886767
  68. RNA splicing in Neurospora mitochondria. Defective splicing of mitochondrial mRNA precursors in the nuclear mutant cyt18-1.
    J Mol Biol. 1985 Aug 5;184(3):413-28 PMID: 2413216
  69. Geometric nomenclature and classification of RNA base pairs.
    RNA. 2001 Apr;7(4):499-512 PMID: 11345429
  70. Self-splicing of the Tetrahymena pre-rRNA is decreased by misfolding during transcription.
    Biochemistry. 1993 Dec 21;32(50):14062-7 PMID: 8268185
  71. A Group I intron in the nuclear small subunit rRNA gene of Cryptendoxyla hypophloia, an ascomycetous fungus: evidence for a new major class of Group I introns.
    J Mol Evol. 1999 May;48(5):493-500 PMID: 10198116
  72. The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs.
    BMC Bioinformatics. 2002;3:2 PMID: 11869452
  73. tRNA-like recognition of group I introns by a tyrosyl-tRNA synthetase.
    Proc Natl Acad Sci U S A. 2002 Mar 5;99(5):2630-5 PMID: 11854463
  74. The neurospora CYT-18 protein suppresses defects in the phage T4 td intron by stabilizing the catalytically active structure of the intron core.
    Cell. 1992 May 1;69(3):483-94 PMID: 1533818
  75. Characterization of the intron in the phage T4 thymidylate synthase gene and evidence for its self-excision from the primary transcript.
    Cell. 1986 Apr 25;45(2):157-66 PMID: 3698096
  76. A common motif organizes the structure of multi-helix loops in 16 S and 23 S ribosomal RNAs.
    J Mol Biol. 1998 Oct 30;283(3):571-83 PMID: 9784367
  77. A tyrosyl-tRNA synthetase can function similarly to an RNA structure in the Tetrahymena ribozyme.
    Nature. 1994 Jul 14;370(6485):147-50 PMID: 8022484
  78. Unexpected abundance of self-splicing introns in the genome of bacteriophage Twort: introns in multiple genes, a single gene with three introns, and exon skipping by group I ribozymes.
    Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):7005-10 PMID: 10359829
  79. An unspliced group I intron in 23S rRNA links Chlamydiales, chloroplasts, and mitochondria.
    J Bacteriol. 1999 Aug;181(16):4734-40 PMID: 10438738
  80. A preorganized active site in the crystal structure of the Tetrahymena ribozyme.
    Science. 1998 Oct 9;282(5387):259-64 PMID: 9841391
  81. Minor groove recognition of the conserved G.U pair at the Tetrahymena ribozyme reaction site.
    Science. 1995 Feb 3;267(5198):675-9 PMID: 7839142
Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1469-9001
Published
2008-10-00
Epub
2008-00-03
Pages
2013-29
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC2553746
Subset
IM
Grants
NIGMS NIH HHS · R01 GM037951 · United States
NIGMS NIH HHS · R37 GM037951 · United States
Howard Hughes Medical Institute · United States
NIGMS NIH HHS · GM037951 · United States
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