Home LiteratureArticle Details
PMID: 10611278 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

A complex ligase ribozyme evolved in vitro from a group I ribozyme domain.

Jaeger L, Wright MC, Joyce GF

Abstract

Like most proteins, complex RNA molecules often are modular objects made up of distinct structural and functional domains. The component domains of a protein can associate in alternative combinations to form molecules with different functions. These observations raise the possibility that complex RNAs also can be assembled from preexisting structural and functional domains. To test this hypothesis, an in vitro evolution procedure was used to isolate a previously undescribed class of complex ligase ribozymes, starting from a pool of 10(16) different RNA molecules that contained a constant region derived from a large structural domain that occurs within self-splicing group I ribozymes. Attached to this constant region were three hypervariable regions, totaling 85 nucleotides, that gave rise to the catalytic motif within the evolved catalysts. The ligase ribozymes catalyze formation of a 3',5'-phosphodiester linkage between adjacent template-bound oligonucleotides, one bearing a 3' hydroxyl and the other a 5' triphosphate. Ligation occurs in the context of a Watson-Crick duplex, with a catalytic rate of 0.26 min(-1) under optimal conditions. The constant region is essential for catalytic activity and appears to retain the tertiary structure of the group I ribozyme. This work demonstrates that complex RNA molecules, like their protein counterparts, can share common structural domains while exhibiting distinct catalytic functions.

Keywords
NASA Discipline Exobiology Non-NASA Center
MeSH Terms
Animals Base Sequence Catalysis Catalytic Domain Directed Molecular Evolution Gene Library Molecular Sequence Data Nucleic Acid Conformation Polynucleotide Ligases/classification,genetics,metabolism RNA, Catalytic/classification,genetics,metabolism Tetrahymena/enzymology
Chemicals
RNA, Catalytic Polynucleotide Ligases
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Jaeger L
Institut de Biologie Moléculaire et Cellulaire du Centre National de la Recherche Scientifique, 15 rue Descartes, 67084 Strasbourg, France. gjoyce@scripps.edu
Wright M C
Joyce G F
Investigators
1 investigators, click to expand
Bada J L
U CA San Diego, La Jolla
References (34)
34 references, click to expand
  1. Monitoring of the cooperative unfolding of the sunY group I intron of bacteriophage T4. The active form of the sunY ribozyme is stabilized by multiple interactions with 3' terminal intron components.
    J Mol Biol. 1993 Nov 20;234(2):331-46 PMID: 8230218
  2. Directed evolution of a fucosidase from a galactosidase by DNA shuffling and screening.
    Proc Natl Acad Sci U S A. 1997 Apr 29;94(9):4504-9 PMID: 9114019
  3. Involvement of a GNRA tetraloop in long-range RNA tertiary interactions.
    J Mol Biol. 1994 Mar 11;236(5):1271-6 PMID: 7510342
  4. In vitro evolution of new ribozymes with polynucleotide kinase activity.
    Nature. 1994 Sep 1;371(6492):31-6 PMID: 7521014
  5. Frequent use of the same tertiary motif by self-folding RNAs.
    EMBO J. 1995 Mar 15;14(6):1276-85 PMID: 7720718
  6. Mobilities of modified ribonucleotides on two-dimensional cellulose thin-layer chromatography.
    Biochimie. 1995;77(1-2):142-4 PMID: 7599271
  7. Structurally complex and highly active RNA ligases derived from random RNA sequences.
    Science. 1995 Jul 21;269(5222):364-70 PMID: 7618102
  8. The New World of ribozymes.
    Curr Opin Struct Biol. 1997 Jun;7(3):324-35 PMID: 9204273
  9. Why genes in pieces?
    Nature. 1978 Feb 9;271(5645):501 PMID: 622185
  10. A model for the RNA-catalyzed replication of RNA.
    Proc Natl Acad Sci U S A. 1986 Jun;83(12):4360-3 PMID: 2424025
  11. The excision of intervening sequences from Salmonella 23S ribosomal RNA.
    Cell. 1990 Feb 9;60(3):405-14 PMID: 2406020
  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. Reconstitution of a group I intron self-splicing reaction with an activator RNA.
    Proc Natl Acad Sci U S A. 1991 Jan 1;88(1):184-8 PMID: 1986364
  14. Randomization of genes by PCR mutagenesis.
    PCR Methods Appl. 1992 Aug;2(1):28-33 PMID: 1490172
  15. An independently folding domain of RNA tertiary structure within the Tetrahymena ribozyme.
    Biochemistry. 1993 May 25;32(20):5291-300 PMID: 7684607
  16. Isolation of new ribozymes from a large pool of random sequences [see comment].
    Science. 1993 Sep 10;261(5127):1411-8 PMID: 7690155
  17. 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
  18. Isolation of novel ribozymes that ligate AMP-activated RNA substrates.
    Chem Biol. 1997 Aug;4(8):607-17 PMID: 9281527
  19. Nonenzymatic, template-directed ligation of oligoribonucleotides is highly regioselective for the formation of 3'-5' phosphodiester bonds.
    J Am Chem Soc. 1996 Apr 10;118(14):3340-4 PMID: 11539268
  20. Kinetic and mechanistic analysis of nonenzymatic, template-directed oligoribonucleotide ligation.
    J Am Chem Soc. 1996 Apr 10;118(14):3332-9 PMID: 11539267
  21. Chance and necessity in the selection of nucleic acid catalysts.
    Acc Chem Res. 1996 Feb;29(2):103-10 PMID: 11539421
  22. Accessing rare activities from random RNA sequences: the importance of the length of molecules in the starting pool.
    Chem Biol. 1997 Oct;4(10):767-74 PMID: 9375255
  23. Creating novel enzymes by applied molecular evolution.
    Chem Biol. 1997 Dec;4(12):889-98 PMID: 9427661
  24. 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
  25. RNA folding at millisecond intervals by synchrotron hydroxyl radical footprinting.
    Science. 1998 Mar 20;279(5358):1940-3 PMID: 9506944
  26. Kinetic intermediates trapped by native interactions in RNA folding.
    Science. 1998 Mar 20;279(5358):1943-6 PMID: 9506945
  27. The secondary structure and sequence optimization of an RNA ligase ribozyme.
    Nucleic Acids Res. 1995 Aug 25;23(16):3231-8 PMID: 7667099
  28. In vitro evolution of randomized ribozymes.
    Methods Enzymol. 1996;267:410-26 PMID: 8743329
  29. Domain structure of the ribozyme from eubacterial ribonuclease P.
    RNA. 1996 Jun;2(6):551-63 PMID: 8718684
  30. Crystal structure of a group I ribozyme domain: principles of RNA packing.
    Science. 1996 Sep 20;273(5282):1678-85 PMID: 8781224
  31. RNA tertiary structure mediation by adenosine platforms.
    Science. 1996 Sep 20;273(5282):1696-9 PMID: 8781229
  32. Assembly of an active enzyme by the linkage of two protein modules.
    Proc Natl Acad Sci U S A. 1997 Feb 18;94(4):1069-73 PMID: 9037007
  33. RNA tectonics: towards RNA design.
    Fold Des. 1996;1(4):R78-88 PMID: 9079386
  34. GAAA tetraloop and conserved bulge stabilize tertiary structure of a group I intron domain.
    J Mol Biol. 1994 Feb 11;236(1):49-63 PMID: 8107125
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1999-12-21
Pages
14712-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC24713
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com