Home LiteratureArticle Details
PMID: 7539919 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Operational RNA code for amino acids: species-specific aminoacylation of minihelices switched by a single nucleotide.

Hipps D, Shiba K, Henderson B, Schimmel P

Abstract

The genetic code is based on aminoacylation reactions where specific amino acids are attached to tRNAs bearing anticodon trinucleotides. However, the anticodon-independent specific aminoacylation of RNA minihelix substrates by bacterial and yeast tRNA synthetases suggested an operational RNA code for amino acids whereby specific RNA sequences/structures in tRNA acceptor stems correspond to specific amino acids. Because of the possible significance of the operational RNA code for the development of the genetic code, we investigated aminoacylation of synthetic RNA minihelices with a human enzyme to understand the sequences needed for that aminoacylation compared with those needed for a microbial system. We show here that the species-specific aminoacylation of glycine tRNAs is recapitulated by a species-specific aminoacylation of minihelices. Although the mammalian and Escherichia coli minihelices differ at 6 of 12 base pairs, two of the three nucleotides essential for aminoacylation by the E. coli enzyme are conserved in the mammalian minihelix. The two conserved nucleotides were shown to be also important for aminoacylation of the mammalian minihelix by the human enzyme. A simple interchange of the differing nucleotide enabled the human enzyme to now charge the bacterial substrate and not the mammalian minihelix. Conversely, this interchange made the bacterial enzyme specific for the mammalian substrate. Thus, the positional locations (if not the actual nucleotides) for the operational RNA code for glycine appear conserved from bacteria to mammals.

MeSH Terms
Amino Acyl-tRNA Synthetases/metabolism Base Sequence Escherichia coli/enzymology,genetics Glycine-tRNA Ligase/metabolism Humans Molecular Sequence Data Nucleic Acid Conformation RNA/chemistry,genetics,metabolism Species Specificity
Chemicals
RNA Amino Acyl-tRNA Synthetases Glycine-tRNA Ligase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Hipps D
Department of Biology, Massachusetts Institute of Technology, Cambridge 02139, USA.
Shiba K
Henderson B
Schimmel P
References (19)
19 references, click to expand
  1. Gene for Escherichia coli glycyl-tRNA synthetase has tandem subunit coding regions in the same reading frame.
    J Biol Chem. 1982 Nov 10;257(21):12503-8 PMID: 6290471
  2. Human glycyl-tRNA synthetase. Wide divergence of primary structure from bacterial counterpart and species-specific aminoacylation.
    J Biol Chem. 1994 Nov 25;269(47):30049-55 PMID: 7962006
  3. Deletions in the large (beta) subunit of a hetero-oligomeric aminoacyl-tRNA synthetase.
    J Biol Chem. 1990 Jan 15;265(2):1000-4 PMID: 2404005
  4. Partition of tRNA synthetases into two classes based on mutually exclusive sets of sequence motifs.
    Nature. 1990 Sep 13;347(6289):203-6 PMID: 2203971
  5. A second class of synthetase structure revealed by X-ray analysis of Escherichia coli seryl-tRNA synthetase at 2.5 A.
    Nature. 1990 Sep 20;347(6290):249-55 PMID: 2205803
  6. Identity elements for specific aminoacylation of yeast tRNA(Asp) by cognate aspartyl-tRNA synthetase.
    Science. 1991 Jun 21;252(5013):1696-9 PMID: 2047878
  7. Specificity for aminoacylation of an RNA helix: an unpaired, exocyclic amino group in the minor groove.
    Science. 1991 Aug 16;253(5021):784-6 PMID: 1876835
  8. Enzymatic aminoacylation of sequence-specific RNA minihelices and hybrid duplexes with methionine.
    Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):65-9 PMID: 1729719
  9. Overlapping nucleotide determinants for specific aminoacylation of RNA microhelices.
    Science. 1992 Feb 28;255(5048):1121-5 PMID: 1546312
  10. Functional contacts of a transfer RNA synthetase with 2'-hydroxyl groups in the RNA minor groove.
    Nature. 1992 Jun 11;357(6378):513-5 PMID: 1608452
  11. Striking effects of coupling mutations in the acceptor stem on recognition of tRNAs by Escherichia coli Met-tRNA synthetase and Met-tRNA transformylase.
    Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9262-6 PMID: 1409632
  12. Primary structure of the gene for glycyl-tRNA synthetase from Bombyx mori.
    J Biol Chem. 1993 Apr 15;268(11):7660-7 PMID: 8463296
  13. Compilation of tRNA sequences and sequences of tRNA genes.
    Nucleic Acids Res. 1993 Jul 1;21(13):3011-5 PMID: 7687348
  14. Aminoacylation of RNA minihelices: implications for tRNA synthetase structural design and evolution.
    Crit Rev Biochem Mol Biol. 1993;28(4):309-22 PMID: 7691478
  15. An operational RNA code for amino acids and possible relationship to genetic code.
    Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):8763-8 PMID: 7692438
  16. Molecular recognition of the identity-determinant set of isoleucine transfer RNA from Escherichia coli.
    J Mol Biol. 1994 Feb 25;236(3):710-24 PMID: 8114089
  17. Efficient aminoacylation of resected RNA helices by class II aspartyl-tRNA synthetase dependent on a single nucleotide.
    EMBO J. 1994 May 1;13(9):2218-26 PMID: 8187774
  18. Primary structure and functional expression of human Glycyl-tRNA synthetase, an autoantigen in myositis.
    J Biol Chem. 1994 Nov 18;269(46):28790-7 PMID: 7961834
  19. Primary structures of both subunits of Escherichia coli glycyl-tRNA synthetase.
    J Biol Chem. 1983 Sep 10;258(17):10637-41 PMID: 6309809
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
1995-06-06
Pages
5550-2
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC41733
Subset
IM
Grants
NIGMS NIH HHS · GM15539 · United States
Databases
GENBANK
D30658
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