Abstract
In a significant fraction of the Escherichia coli cytosolic proteins, the N-terminal methionine residue incorporated during the translation initiation step is excised. The N-terminal methionine excision is catalyzed by methionyl-aminopeptidase (MAP). Previous studies have suggested that the action of this enzyme could depend mainly on the nature of the second amino acid residue in the polypeptide chain. In this study, to achieve a systematic analysis of the specificity of MAP action, each of the 20 amino acids was introduced at the penultimate position of methionyl-tRNA synthetase of E. coli and the extent of in vivo methionine excision was measured. To facilitate variant protein purification and N-terminal sequence determination, an expression shuttle vector based on protein fusion with beta-galactosidase was used. From our results, methionine excision catalyzed by MAP is shown to obey the following rule: the catalytic efficiency of MAP, and therefore the extent of cleavage, decreases in parallel with the increasing of the maximal side-chain length of the amino acid in the penultimate position. This molecular model accounts for the rate of N-terminal methionine excision in E. coli, as deduced from the analysis of 100 protein N-terminal sequences.
MeSH Terms
Amino Acid Sequence
Bacterial Proteins/genetics,isolation & purification
Chimera
Codon/genetics
Cysteine/metabolism
Escherichia coli/genetics,metabolism
Genes, Bacterial
Genetic Vectors
Molecular Sequence Data
Mutation
Protein Processing, Post-Translational
Chemicals
Bacterial Proteins
Codon
Cysteine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Hirel P H
Laboratoire de Biochimie, Unité Associée 240 Centre National de la Recherche Scientifique, Ecole Polytechnique, Palaiseu, France.
Schmitter M J
Dessen P
Fayat G
Blanquet S
References (30)
30 references, click to expand
-
Amidohydrolase activity of Escherichia coli extracts with formylated amino acids and dipeptides as substrates.
J Mol Biol. 1967 Sep 28;28(3):423-33
PMID: 4861179
-
Molecular cloning and primary structure of the Escherichia coli methionyl-tRNA synthetase gene.
J Bacteriol. 1984 Dec;160(3):1115-22
PMID: 6094501
-
Kinetics of maturation of the amino termini of the cell proteins of Escherichia coli.
Biochim Biophys Acta. 1969 Jan 21;174(1):359-72
PMID: 4885696
-
Deformylation and protein biosynthesis.
Biochemistry. 1969 Jan;8(1):435-43
PMID: 4887858
-
Purification and properties of an aminopeptidase from Escherichia coli.
J Biol Chem. 1970 Sep 25;245(18):4760-9
PMID: 4917241
-
Environment and exposure to solvent of protein atoms. Lysozyme and insulin.
J Mol Biol. 1973 Sep 15;79(2):351-71
PMID: 4760134
-
Transport systems for L-methionine in Escherichia coli.
J Bacteriol. 1974 Jan;117(1):232-41
PMID: 4587605
-
Macromolecular composition during steady-state growth of Escherichia coli B-r.
J Bacteriol. 1974 Jul;119(1):270-81
PMID: 4600702
-
Rapid and efficient site-specific mutagenesis without phenotypic selection.
Proc Natl Acad Sci U S A. 1985 Jan;82(2):488-92
PMID: 3881765
-
Amino-terminal processing of mutant forms of yeast iso-1-cytochrome c. The specificities of methionine aminopeptidase and acetyltransferase.
J Biol Chem. 1985 May 10;260(9):5382-91
PMID: 2985590
-
Hydrophobicity of amino acid residues in globular proteins.
Science. 1985 Aug 30;229(4716):834-8
PMID: 4023714
-
Separation of recombinant human interleukin-2 and methionyl interleukin-2 produced in Escherichia coli.
Biochem Biophys Res Commun. 1986 Mar 28;135(3):837-43
PMID: 3485976
-
Rapid purification of DNA fragments by high-performance size-exclusion chromatography.
J Chromatogr. 1986 Jun 13;378(2):462-6
PMID: 3734002
-
In vivo half-life of a protein is a function of its amino-terminal residue.
Science. 1986 Oct 10;234(4773):179-86
PMID: 3018930
-
Processing of the initiation methionine from proteins: properties of the Escherichia coli methionine aminopeptidase and its gene structure.
J Bacteriol. 1987 Feb;169(2):751-7
PMID: 3027045
-
N-terminal methionine-specific peptidase in Salmonella typhimurium.
Proc Natl Acad Sci U S A. 1987 May;84(9):2718-22
PMID: 3106976
-
A procedure for in situ alkylation of cystine residues on glass fiber prior to protein microsequence analysis.
Anal Biochem. 1987 Mar;161(2):524-8
PMID: 2883913
-
Influence of the codon following the AUG initiation codon on the expression of a modified lacZ gene in Escherichia coli.
EMBO J. 1987 Aug;6(8):2489-92
PMID: 3311730
-
Specificity of cotranslational amino-terminal processing of proteins in yeast.
Biochemistry. 1987 Dec 15;26(25):8242-6
PMID: 3327521
-
Cotranslational amino-terminal processing of cytosolic proteins. Cell-free expression of site-directed mutants of human hemoglobin.
J Biol Chem. 1988 Jun 15;263(17):8443-9
PMID: 3372535
-
Analytical strategy for determination of active site sequences in aminoacyl-tRNA synthetases.
J Chromatogr. 1988 Apr 22;438(2):347-57
PMID: 2838497
-
Genetic engineering of methionyl-tRNA synthetase: in vitro regeneration of an active synthetase by proteolytic cleavage of a methionyl-tRNA synthetase--beta-galactosidase chimeric protein.
Biochimie. 1988 Jun;70(6):773-82
PMID: 3139093
-
THE NH2-TERMINAL RESIDUES OF THE PROTEINS FROM CELL-FREE EXTRACTS OF E. COLI.
J Mol Biol. 1963 Nov;7:483-96
PMID: 14079588
-
N-FORMYL-METHIONYL-S-RNA.
J Mol Biol. 1964 Jun;8:835-40
PMID: 14187409
-
A simplified representation of protein conformations for rapid simulation of protein folding.
J Mol Biol. 1976 Jun 14;104(1):59-107
PMID: 957439
-
In vitro gene fusions that join an enzymatically active beta-galactosidase segment to amino-terminal fragments of exogenous proteins: Escherichia coli plasmid vectors for the detection and cloning of translational initiation signals.
J Bacteriol. 1980 Aug;143(2):971-80
PMID: 6162838
-
Oligonucleotide-directed mutagenesis of DNA fragments cloned into M13 vectors.
Methods Enzymol. 1983;100:468-500
PMID: 6225933
-
Principles that determine the structure of proteins.
Annu Rev Biochem. 1984;53:537-72
PMID: 6383199
-
One-step purification of hybrid proteins which have beta-galactosidase activity.
Gene. 1984 Jul-Aug;29(1-2):27-31
PMID: 6436145
-
On the release of the formyl group from nascent protein.
J Mol Biol. 1968 May 14;33(3):571-89
PMID: 4973445