Home LiteratureArticle Details
PMID: 1756734 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

A component of the multisynthetase complex is a multifunctional aminoacyl-tRNA synthetase.

The EMBO journal ·Vol. 10 ·No. 13 ·1991-12-00 ·Pages 4267-77

Cerini C, Kerjan P, Astier M, Gratecos D, Mirande M, Sémériva M

Abstract

In higher eukaryotes, nine aminoacyl-tRNA synthetases are associated within a multienzyme complex which is composed of 11 polypeptides with molecular masses ranging from 18 to 150 kDa. We have cloned and sequenced a cDNA from Drosophila encoding the largest polypeptide of this complex. We demonstrate here that the corresponding protein is a multifunctional aminoacyl-tRNA synthetase. It is composed of three major domains, two of them specifying distinct synthetase activities. The amino and carboxy-terminal domains were expressed separately in Escherichia coli, and were found to catalyse the aminoacylation of glutamic acid and proline tRNA species, respectively. The central domain is made of six 46 amino acid repeats. In prokaryotes, these two aminoacyl-tRNA synthetases are encoded by distinct genes. The emergence of a multifunctional synthetase by a gene fusion event seems to be a specific, but general attribute of all higher eukaryotic cells. This type of structural organization, in relation to the occurrence of multisynthetase complexes, could be a mechanism to integrate several catalytic domains within the same particle. The involvement of the internal repeats in mediating complex assembly is discussed.

MeSH Terms
Amino Acid Sequence Amino Acyl-tRNA Synthetases/metabolism Animals Base Sequence Blotting, Northern Cloning, Molecular DNA/genetics Drosophila melanogaster/genetics Escherichia coli/genetics Gene Expression Genes, Bacterial Molecular Sequence Data Multienzyme Complexes/genetics,metabolism Nucleic Acid Hybridization RNA, Messenger/genetics RNA, Transfer, Glu/metabolism RNA, Transfer, Pro/metabolism Repetitive Sequences, Nucleic Acid Restriction Mapping Sequence Homology, Nucleic Acid
Chemicals
Multienzyme Complexes RNA, Messenger RNA, Transfer, Glu RNA, Transfer, Pro DNA Amino Acyl-tRNA Synthetases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Cerini C
Laboratoire de Génétique et Biologie Cellulaires, CNRS, Marseille, France.
Kerjan P
Astier M
Gratecos D
Mirande M
Sémériva M
References (50)
50 references, click to expand
  1. Lambda ZAP: a bacteriophage lambda expression vector with in vivo excision properties.
    Nucleic Acids Res. 1988 Aug 11;16(15):7583-600 PMID: 2970625
  2. Isolation and characterization of the gene encoding Drosophila DNA topoisomerase II.
    Proc Natl Acad Sci U S A. 1986 Jun;83(11):3664-8 PMID: 3012525
  3. Unidirectional digestion with exonuclease III in DNA sequence analysis.
    Methods Enzymol. 1987;155:156-65 PMID: 3323819
  4. 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
  5. 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
  6. Cloning and expression of a mammalian peptide chain release factor with sequence similarity to tryptophanyl-tRNA synthetases.
    Proc Natl Acad Sci U S A. 1990 May;87(9):3508-12 PMID: 2185472
  7. Linkage map of Escherichia coli K-12, edition 8.
    Microbiol Rev. 1990 Jun;54(2):130-97 PMID: 2194094
  8. Organization and expression of eucaryotic split genes coding for proteins.
    Annu Rev Biochem. 1981;50:349-83 PMID: 6791577
  9. Escherichia coli glutaminyl-tRNA synthetase. II. Characterization of the glnS gene product.
    J Biol Chem. 1982 Oct 10;257(19):11644-50 PMID: 6749844
  10. Seven mammalian aminoacyl-tRNA synthetases co-purified as high molecular weight entities are associated within the same complex.
    EMBO J. 1982;1(6):733-6 PMID: 7188359
  11. Perturbation of the aminoacyl-tRNA synthetase complex by salts and detergents. Importance of hydrophobic interactions and possible involvement of lipids.
    J Biol Chem. 1983 Oct 10;258(19):11846-50 PMID: 6555192
  12. Macromolecular complexes from sheep and rabbit containing seven aminoacyl-tRNA synthetases. III. Assignment of aminoacyl-tRNA synthetase activities to the polypeptide components of the complexes.
    J Biol Chem. 1982 Sep 25;257(18):11056-63 PMID: 7107646
  13. Macromolecular complexes from sheep and rabbit containing seven aminoacyl-tRNA synthetases. II. Structural characterization of the polypeptide components and immunological identification of the methionyl-tRNA synthetase subunit.
    J Biol Chem. 1982 Sep 25;257(18):11049-55 PMID: 7107645
  14. Purification and characterization of lysyl-tRNA synthetase after dissociation of the particulate aminoacyl-tRNA synthetases from rat liver.
    J Biol Chem. 1980 May 10;255(9):4362-6 PMID: 7372681
  15. Primary structure of a large aminoacyl-tRNA synthetase.
    Science. 1981 Sep 25;213(4515):1497-501 PMID: 7025207
  16. Nucleotide sequence of the thrA gene of Escherichia coli.
    Proc Natl Acad Sci U S A. 1980 Oct;77(10):5730-3 PMID: 7003595
  17. Prediction of the secondary structure of proteins from their amino acid sequence.
    Adv Enzymol Relat Areas Mol Biol. 1978;47:45-148 PMID: 364941
  18. DNA sequencing with chain-terminating inhibitors.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463-7 PMID: 271968
  19. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.
    Biochemistry. 1979 Nov 27;18(24):5294-9 PMID: 518835
  20. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins.
    J Mol Biol. 1978 Mar 25;120(1):97-120 PMID: 642007
  21. Chromatography of Drosophila tRNA on BD-cellulose.
    Can J Biochem. 1973 Jun;51(6):896-902 PMID: 4197825
  22. The use of helical net-diagrams to represent protein structures.
    Biophys J. 1968 Jul;8(7):865-75 PMID: 5699810
  23. The primary structure of human glutaminyl-tRNA synthetase. A highly conserved core, amino acid repeat regions, and homologies with translation elongation factors.
    J Biol Chem. 1991 Jan 25;266(3):1448-55 PMID: 1988429
  24. Class II aminoacyl transfer RNA synthetases: crystal structure of yeast aspartyl-tRNA synthetase complexed with tRNA(Asp).
    Science. 1991 Jun 21;252(5013):1682-9 PMID: 2047877
  25. Aminoacyl-tRNA synthetase family from prokaryotes and eukaryotes: structural domains and their implications.
    Prog Nucleic Acid Res Mol Biol. 1991;40:95-142 PMID: 2031086
  26. Sequence determination and modeling of structural motifs for the smallest monomeric aminoacyl-tRNA synthetase.
    Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):976-80 PMID: 1992490
  27. Cysteinyl-tRNA synthetase: determination of the last E. coli aminoacyl-tRNA synthetase primary structure.
    Nucleic Acids Res. 1991 Jan 25;19(2):265-9 PMID: 2014166
  28. Aspartyl-tRNA synthetase from Escherichia coli: cloning and characterisation of the gene, homologies of its translated amino acid sequence with asparaginyl- and lysyl-tRNA synthetases.
    Nucleic Acids Res. 1990 Dec 11;18(23):7109-18 PMID: 2129559
  29. Crystallographic study at 2.5 A resolution of the interaction of methionyl-tRNA synthetase from Escherichia coli with ATP.
    J Mol Biol. 1990 Nov 20;216(2):411-24 PMID: 2254937
  30. Glutamyl-tRNA synthetases of Bacillus subtilis 168T and of Bacillus stearothermophilus. Cloning and sequencing of the gltX genes and comparison with other aminoacyl-tRNA synthetases.
    J Biol Chem. 1990 Oct 25;265(30):18248-55 PMID: 2120226
  31. Glutaminyl-tRNA synthetase as a component of the high-molecular weight complex of human aminoacyl-tRNA synthetases. An immunological study.
    Biochim Biophys Acta. 1990 Oct 23;1087(2):226-34 PMID: 2223884
  32. BISANCE: a French service for access to biomolecular sequence databases.
    Comput Appl Biosci. 1990 Oct;6(4):355-6 PMID: 2257496
  33. Valyl-tRNA synthetase from rabbit liver. I. Purification as a heterotypic complex in association with elongation factor 1.
    J Biol Chem. 1989 Dec 15;264(35):21131-7 PMID: 2556394
  34. Mammalian valyl-tRNA synthetase forms a complex with the first elongation factor.
    FEBS Lett. 1988 Oct 10;238(2):262-4 PMID: 3169261
  35. Structure of E. coli glutaminyl-tRNA synthetase complexed with tRNA(Gln) and ATP at 2.8 A resolution.
    Science. 1989 Dec 1;246(4934):1135-42 PMID: 2479982
  36. Structure of tyrosyl-tRNA synthetase refined at 2.3 A resolution. Interaction of the enzyme with the tyrosyl adenylate intermediate.
    J Mol Biol. 1989 Jul 5;208(1):83-98 PMID: 2504923
  37. cDNA sequence, predicted primary structure, and evolving amphiphilic helix of human aspartyl-tRNA synthetase.
    J Biol Chem. 1989 Oct 5;264(28):16608-12 PMID: 2674137
  38. Molecular cloning and primary structure of cDNA encoding the catalytic domain of rat liver aspartyl-tRNA synthetase.
    J Biol Chem. 1989 Jan 15;264(2):842-7 PMID: 2642907
  39. The core region of human glutaminyl-tRNA synthetase homologies with the Escherichia coli and yeast enzymes.
    Nucleic Acids Res. 1988 Jun 24;16(12):5391-406 PMID: 3290852
  40. Isolation, structure and expression of mammalian genes for histidyl-tRNA synthetase.
    Nucleic Acids Res. 1987 Apr 24;15(8):3349-67 PMID: 3554142
  41. Aminoacyl tRNA synthetases: general scheme of structure-function relationships in the polypeptides and recognition of transfer RNAs.
    Annu Rev Biochem. 1987;56:125-58 PMID: 3304131
  42. Construction and analysis of deletions in the amino-terminal extension of glutamine tRNA synthetase of Saccharomyces cerevisiae.
    J Biol Chem. 1987 Aug 5;262(22):10807-13 PMID: 3301842
  43. Gene for yeast glutamine tRNA synthetase encodes a large amino-terminal extension and provides a strong confirmation of the signature sequence for a group of the aminoacyl-tRNA synthetases.
    J Biol Chem. 1987 Aug 5;262(22):10801-6 PMID: 3301841
  44. Sequence similarities among the family of aminoacyl-tRNA synthetases.
    Biochimie. 1986 Sep;68(9):1071-8 PMID: 3096385
  45. Leucyl-tRNA and lysyl-tRNA synthetases, derived from the high-Mr complex of sheep liver, are hydrophobic proteins.
    Eur J Biochem. 1985 Aug 15;151(1):101-10 PMID: 3896782
  46. A complex from cultured Chinese hamster ovary cells containing nine aminoacyl-tRNA synthetases. Thermolabile leucyl-tRNA synthetase from the tsH1 mutant cell line is an integral component of this complex.
    Eur J Biochem. 1985 Mar 1;147(2):281-9 PMID: 3971983
  47. Purification and characterization of the isoleucyl-tRNA synthetase component from the high molecular weight complex of sheep liver: a hydrophobic metalloprotein.
    Biochemistry. 1985 Sep 10;24(19):5099-106 PMID: 4074679
  48. Glutamyl-tRNA synthetase of Escherichia coli. Isolation and primary structure of the gltX gene and homology with other aminoacyl-tRNA synthetases.
    J Biol Chem. 1986 Aug 15;261(23):10610-7 PMID: 3015933
  49. Nucleotide sequence of the gene coding for yeast cytoplasmic aspartyl-tRNA synthetase (APS); mapping of the 5' and 3' termini of AspRS mRNA.
    Nucleic Acids Res. 1986 Feb 25;14(4):1657-66 PMID: 3513127
  50. Protein biosynthesis in organelles requires misaminoacylation of tRNA.
    Nature. 1988 Jan 14;331(6152):187-90 PMID: 3340166
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1991-12-00
Pages
4267-77
Language
English
Region
England
NLM ID
8208664
PMCID
PMC453179
Subset
IM
Databases
GENBANK
M62513, M62514, M62515, M74104, S65080, S65083, S72609, S72775, X59372, X59373, X61585
External Links
PubMed source PMC Full Text View journal details
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: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2