Abstract
To study the cleavage mechanism of bacterial Nase P RNA, we have synthesized precursor tRNA substrates carrying a single Rp- or Sp-phosphorothioate modification at the RNase P cleavage site. Both the Sp- and the Rp-diastereomer reduced the rate of processing by Escherichia coli RNase P RNA at least 1000-fold under conditions where the chemical step is rate-limiting. The Rp-modification had no effect and the Sp-modification had a moderate effect on precursor tRNA ground state binding to RNase P RNA. Processing of the Rp-diastereomeric substrate was largely restored in the presence of the "thiophilic" Cd2+ as the only divalent metal ion, demonstrating direct metal ion coordination to the (pro)-Rp substituent at the cleavage site and arguing against a specific role for Mg(2+)-ions at the pro-Sp oxygen. For the Rp-diastereomeric substrate, Hill plot analysis revealed a cooperative dependence upon [Cd2+] of nH = 1.8, consistent with a two-metal ion mechanism. In the presence of the Sp-modification, neither Mn2+ nor Cd2+ was able to restore detectable cleavage at the canonical site. Instead, the ribozyme promotes cleavage at the neighboring unmodified phosphodiester with low efficiency. Dramatic inhibition of the chemical step by both the Rp- and Sp-phosphorothioate modification is unprecedented among known ribozymes and points to unique features of transition state geometry in the RNase P RNA-catalyzed reaction.
MeSH Terms
Base Sequence
Cadmium/metabolism
Endoribonucleases/metabolism
Escherichia coli/enzymology
Escherichia coli Proteins
Kinetics
Models, Chemical
Molecular Sequence Data
RNA Precursors/metabolism
RNA Processing, Post-Transcriptional
RNA, Bacterial/metabolism
RNA, Catalytic/metabolism
RNA, Transfer, Gly/metabolism
Ribonuclease P
Stereoisomerism
Thionucleotides
Chemicals
Escherichia coli Proteins
RNA Precursors
RNA, Bacterial
RNA, Catalytic
RNA, Transfer, Gly
Thionucleotides
Cadmium
Endoribonucleases
Ribonuclease P
ribonuclease P, E coli
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Warnecke J M
Medizinische Universität zu Lübeck, Institut für Biochemie, Germany.
Fürste J P
Hardt W D
Erdmann V A
Hartmann R K
References (23)
23 references, click to expand
-
RNA-ligant interactions. (I) Magnesium binding sites in yeast tRNAPhe.
Nucleic Acids Res. 1977 Aug;4(8):2811-20
PMID: 333395
-
Crystallization and preliminary diffraction studies of the structural domain E of Thermus flavus 5S rRNA.
FEBS Lett. 1995 Oct 30;374(2):292-4
PMID: 7589556
-
The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme.
Cell. 1983 Dec;35(3 Pt 2):849-57
PMID: 6197186
-
Stability constants of Mg2+ and Cd2+ complexes of adenine nucleotides and thionucleotides and rate constants for formation and dissociation of MgATP and MgADP.
Biochemistry. 1984 Oct 23;23(22):5262-71
PMID: 6334536
-
Bond order and charge localization in nucleoside phosphorothioates.
Science. 1985 May 3;228(4699):541-5
PMID: 2984773
-
Metal ion requirements and other aspects of the reaction catalyzed by M1 RNA, the RNA subunit of ribonuclease P from Escherichia coli.
Biochemistry. 1986 Apr 8;25(7):1509-15
PMID: 2423112
-
DNA and RNA sequence determination based on phosphorothioate chemistry.
Science. 1988 Jun 10;240(4858):1520-2
PMID: 2453926
-
Configurationally defined phosphorothioate-containing oligoribonucleotides in the study of the mechanism of cleavage of hammerhead ribozymes.
Nucleic Acids Res. 1991 Mar 25;19(6):1183-8
PMID: 1709484
-
Ribozyme-catalyzed and nonenzymatic reactions of phosphate diesters: rate effects upon substitution of sulfur for a nonbridging phosphoryl oxygen atom.
Biochemistry. 1991 May 21;30(20):4844-54
PMID: 2036355
-
Influence of metal ions on the ribonuclease P reaction. Distinguishing substrate binding from catalysis.
J Biol Chem. 1992 Feb 5;267(4):2429-36
PMID: 1370819
-
Site-specific modification of pre-mRNA: the 2'-hydroxyl groups at the splice sites.
Science. 1992 May 15;256(5059):992-7
PMID: 1589782
-
Analysis of the role of phosphate oxygens in the group I intron from Tetrahymena.
J Mol Biol. 1992 Dec 5;228(3):743-58
PMID: 1469712
-
Multiple magnesium ions in the ribonuclease P reaction mechanism.
Biochemistry. 1993 May 25;32(20):5273-81
PMID: 8499432
-
A general two-metal-ion mechanism for catalytic RNA.
Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6498-502
PMID: 8341661
-
Gel retardation analysis of E. coli M1 RNA-tRNA complexes.
Nucleic Acids Res. 1993 Jul 25;21(15):3521-7
PMID: 7688454
-
Evidence for the role of solvated metal hydroxide in the hammerhead cleavage mechanism.
Biochemistry. 1993 Dec 7;32(48):13040-5
PMID: 8241158
-
Phosphorothioates in pre-tRNAs can change the specificities of RNAses P or reduce the cleavage efficiencies.
Biochimie. 1993;75(11):955-62
PMID: 8123702
-
Selection of circularly permuted ribozymes from Bacillus subtilis RNAse P by substrate binding.
Biochemistry. 1994 Nov 29;33(47):14207-12
PMID: 7524672
-
The stereochemical course of group II intron self-splicing.
Science. 1994 Dec 9;266(5191):1685-8
PMID: 7527587
-
Higher order folding and domain analysis of the ribozyme from Bacillus subtilis ribonuclease P.
Biochemistry. 1995 Jan 24;34(3):902-9
PMID: 7827048
-
Kinetics and thermodynamics of the RNase P RNA cleavage reaction: analysis of tRNA 3'-end variants.
J Mol Biol. 1995 Mar 24;247(2):161-72
PMID: 7535857
-
Rp-phosphorothioate modifications in RNase P RNA that interfere with tRNA binding.
EMBO J. 1995 Jun 15;14(12):2935-44
PMID: 7540978
-
Diastereomers of the nucleoside phosphorothioates as probes of the structure of the metal nucleotide substrates and of the nucleotide binding site of yeast hexokinase.
J Biol Chem. 1979 Nov 10;254(21):10839-45
PMID: 387756