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PMID: 16373492 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural

The interaction between C75 of tRNA and the A loop of the ribosome stimulates peptidyl transferase activity.

RNA (New York, N.Y.) ·Vol. 12 ·No. 1 ·2006-01-00 ·Pages 33-9

Brunelle JL, Youngman EM, Sharma D, Green R

Abstract

Ribosomal variants carrying mutations in active site nucleotides are severely compromised in their ability to catalyze peptide bond formation (PT) with minimal aminoacyl tRNA substrates such as puromycin. However, catalysis of PT by these same ribosomes with intact aminoacyl tRNA substrates is uncompromised. These data suggest that these active site nucleotides play an important role in the positioning of minimal aminoacyl tRNA substrates but are not essential for catalysis per se when aminoacyl tRNAs are positioned by more remote interactions with the ribosome. Previously reported biochemical studies and atomic resolution X-ray structures identified a direct Watson-Crick interaction between C75 of the A-site substrate and G2553 of the 23S rRNA. Here we show that the addition of this single cytidine residue (the C75 equivalent) to puromycin is sufficient to suppress the deficiencies of active site ribosomal variants, thus restoring "tRNA-like" behavior to this minimal substrate. Studies of the binding parameters and the pH-dependence of catalysis with this minimal substrate indicate that the interaction between C75 and the ribosomal A loop is an essential feature for robust catalysis and further suggest that the observed effects of C75 on peptidyl transfer activity reflect previously reported conformational rearrangements in this active site.

MeSH Terms
Binding Sites Catalysis Hydrogen-Ion Concentration Mutation Peptidyl Transferases/metabolism,pharmacokinetics Puromycin/metabolism RNA, Ribosomal/chemistry,genetics Ribosomes/chemistry,enzymology,genetics
Chemicals
RNA, Ribosomal Puromycin Peptidyl Transferases
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Brunelle Julie L
Howard Hughes Medical Institute, Department of Molecular Biology and Genetics, Johns Hopkins University School of Medicine, 725 N. Wolfe Street, 702A PCTB, Baltimore, MD 21205, USA.
Youngman Elaine M
Sharma Divya
Green Rachel
References (27)
27 references, click to expand
  1. Exploration of the conserved A+C wobble pair within the ribosomal peptidyl transferase center using affinity purified mutant ribosomes.
    Nucleic Acids Res. 2004;32(12):3760-70 PMID: 15256541
  2. The active site of the ribosome is composed of two layers of conserved nucleotides with distinct roles in peptide bond formation and peptide release.
    Cell. 2004 May 28;117(5):589-99 PMID: 15163407
  3. Hydrolysis of fMet-tRNA by peptidyl transferase.
    Proc Natl Acad Sci U S A. 1971 Dec;68(12):3163-7 PMID: 4943558
  4. Transfer RNA shields specific nucleotides in 16S ribosomal RNA from attack by chemical probes.
    Cell. 1986 Dec 26;47(6):985-94 PMID: 2430725
  5. Site-directed mutagenesis and NMR spectroscopic approaches to the elucidation of the structure-function relationships in translation initiation factors IF1 and IF3.
    Biochimie. 1991 Jul-Aug;73(7-8):1001-6 PMID: 1742345
  6. Purification procedure for bacterial translational initiation factors IF2 and IF3.
    Protein Expr Purif. 1994 Apr;5(2):118-24 PMID: 8054843
  7. pH dependencies of the Tetrahymena ribozyme reveal an unconventional origin of an apparent pKa.
    Biochemistry. 1996 Feb 6;35(5):1560-70 PMID: 8634287
  8. Nucleotides in 16S rRNA protected by the association of 30S and 50S ribosomal subunits.
    J Mol Biol. 1999 Jan 8;285(1):97-105 PMID: 9878391
  9. X-ray crystal structures of 70S ribosome functional complexes.
    Science. 1999 Sep 24;285(5436):2095-104 PMID: 10497122
  10. Substrate-assisted catalysis of peptide bond formation by the ribosome.
    Nat Struct Mol Biol. 2004 Nov;11(11):1101-6 PMID: 15475967
  11. Kinetic isotope effect analysis of the ribosomal peptidyl transferase reaction.
    Biochemistry. 2005 Mar 15;44(10):4018-27 PMID: 15751978
  12. Uncovering the enzymatic pKa of the ribosomal peptidyl transferase reaction utilizing a fluorinated puromycin derivative.
    Biochemistry. 2005 May 3;44(17):6675-84 PMID: 15850401
  13. Affinity purification of in vivo-assembled ribosomes for in vitro biochemical analysis.
    Methods. 2005 Jul;36(3):305-12 PMID: 16076457
  14. An induced-fit mechanism to promote peptide bond formation and exclude hydrolysis of peptidyl-tRNA.
    Nature. 2005 Nov 24;438(7067):520-4 PMID: 16306996
  15. Base-pairing between 23S rRNA and tRNA in the ribosomal A site.
    Mol Cell. 1999 Nov;4(5):859-64 PMID: 10619032
  16. Puromycin-rRNA interaction sites at the peptidyl transferase center.
    RNA. 2000 May;6(5):744-54 PMID: 10836795
  17. Interaction of translation initiation factor IF1 with the E. coli ribosomal A site.
    J Mol Biol. 2000 May 26;299(1):1-15 PMID: 10860719
  18. The structural basis of ribosome activity in peptide bond synthesis.
    Science. 2000 Aug 11;289(5481):920-30 PMID: 10937990
  19. A conformational change in the ribosomal peptidyl transferase center upon active/inactive transition.
    Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10096-101 PMID: 11517305
  20. pH-dependent conformational flexibility within the ribosomal peptidyl transferase center.
    RNA. 2001 Oct;7(10):1403-15 PMID: 11680845
  21. Interaction of translation initiation factor 3 with the 30S ribosomal subunit.
    Mol Cell. 2001 Oct;8(4):855-64 PMID: 11684020
  22. A pre-translocational intermediate in protein synthesis observed in crystals of enzymatically active 50S subunits.
    Nat Struct Biol. 2002 Mar;9(3):225-30 PMID: 11828326
  23. Puromycin oligonucleotides reveal steric restrictions for ribosome entry and multiple modes of translation inhibition.
    RNA. 2002 Jul;8(7):890-903 PMID: 12166644
  24. Important contribution to catalysis of peptide bond formation by a single ionizing group within the ribosome.
    Mol Cell. 2002 Aug;10(2):339-46 PMID: 12191479
  25. The G2447A mutation does not affect ionization of a ribosomal group taking part in peptide bond formation.
    RNA. 2003 Aug;9(8):919-22 PMID: 12869702
  26. The ribosome as an entropy trap.
    Proc Natl Acad Sci U S A. 2004 May 25;101(21):7897-901 PMID: 15141076
  27. The inactivation and reactivation of ribosomal-peptidyl transferase of E. coli.
    Biochem Biophys Res Commun. 1968 Nov 25;33(4):551-7 PMID: 4880391
Article Info
Journal
RNA (New York, N.Y.)
Abbr.
RNA
ISSN
1355-8382
Published
2006-01-00
Pages
33-9
Language
English
Region
United States
NLM ID
9509184
PMCID
PMC1370883
Subset
IM
Grants
NIGMS NIH HHS · R01 GM059425 · United States
NIGMS NIH HHS · R01GM059425 · United States
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