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PMID: 11101502 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Crystal structure of the peptidyl-cysteine decarboxylase EpiD complexed with a pentapeptide substrate.

The EMBO journal ·Vol. 19 ·No. 23 ·2000-12-01 ·Pages 6299-310

Blaesse M, Kupke T, Huber R, Steinbacher S

Abstract

Epidermin from Staphylococcus epidermidis Tü3298 is an antimicrobial peptide of the lantibiotic family that contains, amongst other unusual amino acids, S:-[(Z:)- 2-aminovinyl]-D-cysteine. This residue is introduced by post-translational modification of the ribosomally synthesized precursor EpiA. Modification starts with the oxidative decarboxylation of its C-terminal cysteine by the flavoprotein EpiD generating a reactive (Z:)-enethiol intermediate. We have determined the crystal structures of EpiD and EpiD H67N in complex with the substrate pentapeptide DSYTC at 2.5 A resolution. Rossmann-type monomers build up a dodecamer of 23 point symmetry with trimers disposed at the vertices of a tetrahedron. Oligomer formation is essential for binding of flavin mononucleotide and substrate, which is buried by an otherwise disordered substrate recognition clamp. A pocket for the tyrosine residue of the substrate peptide is formed by an induced fit mechanism. The substrate contacts flavin mononucleotide only via Cys-Sgamma, suggesting its oxidation as the initial step. A thioaldehyde intermediate could undergo spontaneous decarboxylation. The unusual substrate recognition mode and the type of chemical reaction performed provide insight into a novel family of flavoproteins.

MeSH Terms
Amino Acid Sequence Anti-Bacterial Agents/chemistry Binding Sites Carboxy-Lyases Crystallography, X-Ray Cysteine/metabolism Flavin Mononucleotide/metabolism Flavoproteins/metabolism Models, Molecular Molecular Sequence Data Oxidoreductases/chemistry,metabolism Oxygen/metabolism Peptides/chemistry Protein Processing, Post-Translational Protein Structure, Secondary Recombinant Proteins/chemistry Ribosomes/metabolism Sequence Homology, Amino Acid Staphylococcus epidermidis/chemistry Tyrosine/chemistry
Chemicals
Anti-Bacterial Agents Flavoproteins Peptides Recombinant Proteins Tyrosine Flavin Mononucleotide Oxidoreductases epidermin decarboxylase Carboxy-Lyases Cysteine Oxygen
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Blaesse M
Abteilung für Strukturforschung, Max-Planck-Institut für Biochemie, Am Klopferspitz 18a, 82152, Germany.
Kupke T
Huber R
Steinbacher S
References (36)
36 references, click to expand
  1. Antimicrobial peptides in mammalian and insect host defence.
    Curr Opin Immunol. 1999 Feb;11(1):23-7 PMID: 10047545
  2. Structure of the oxidized long-chain flavodoxin from Anabaena 7120 at 2 A resolution.
    Protein Sci. 1992 Nov;1(11):1413-27 PMID: 1303762
  3. The crystal structure and mechanism of orotidine 5'-monophosphate decarboxylase.
    Proc Natl Acad Sci U S A. 2000 Feb 29;97(5):2005-10 PMID: 10681442
  4. Lantibiotics: biosynthesis and biological activities of uniquely modified peptides from gram-positive bacteria.
    Annu Rev Microbiol. 1998;52:41-79 PMID: 9891793
  5. Purification and characterization of EpiD, a flavoprotein involved in the biosynthesis of the lantibiotic epidermin.
    J Bacteriol. 1992 Aug;174(16):5354-61 PMID: 1644762
  6. Arabidopsis thaliana AtHAL3: a flavoprotein related to salt and osmotic tolerance and plant growth.
    Plant J. 1999 Dec;20(5):529-39 PMID: 10652125
  7. Mass spectroscopic analysis of a novel enzymatic reaction. Oxidative decarboxylation of the lantibiotic precursor peptide EpiA catalyzed by the flavoprotein EpiD.
    J Biol Chem. 1994 Feb 25;269(8):5653-9 PMID: 8119901
  8. Molecular recognition. Conformational analysis of limited proteolytic sites and serine proteinase protein inhibitors.
    J Mol Biol. 1991 Jul 20;220(2):507-30 PMID: 1856871
  9. Structure of oxidized flavodoxin from Anacystis nidulans.
    J Mol Biol. 1983 Apr 25;165(4):737-53 PMID: 6406674
  10. Epidermin: sequencing of a heterodetic tetracyclic 21-peptide amide antibiotic.
    Eur J Biochem. 1986 Oct 1;160(1):9-22 PMID: 3769923
  11. Biosynthesis of the lantibiotic mersacidin: organization of a type B lantibiotic gene cluster.
    Appl Environ Microbiol. 2000 Jun;66(6):2565-71 PMID: 10831439
  12. Crystallography & NMR system: A new software suite for macromolecular structure determination.
    Acta Crystallogr D Biol Crystallogr. 1998 Sep 1;54(Pt 5):905-21 PMID: 9757107
  13. Improved methods for building protein models in electron density maps and the location of errors in these models.
    Acta Crystallogr A. 1991 Mar 1;47 ( Pt 2):110-9 PMID: 2025413
  14. Role of lipid-bound peptidoglycan precursors in the formation of pores by nisin, epidermin and other lantibiotics.
    Mol Microbiol. 1998 Oct;30(2):317-27 PMID: 9791177
  15. Chemical and biological evolution of nucleotide-binding protein.
    Nature. 1974 Jul 19;250(463):194-9 PMID: 4368490
  16. Oxidative decarboxylation of peptides catalyzed by flavoprotein EpiD. Determination of substrate specificity using peptide libraries and neutral loss mass spectrometry.
    J Biol Chem. 1995 May 12;270(19):11282-9 PMID: 7744764
  17. The Protein Data Bank: a computer-based archival file for macromolecular structures.
    J Mol Biol. 1977 May 25;112(3):535-42 PMID: 875032
  18. Use of the cell wall precursor lipid II by a pore-forming peptide antibiotic.
    Science. 1999 Dec 17;286(5448):2361-4 PMID: 10600751
  19. C-H...O hydrogen bonding in biology.
    Trends Biochem Sci. 1997 Mar;22(3):97-102 PMID: 9066260
  20. Automated protein model building combined with iterative structure refinement.
    Nat Struct Biol. 1999 May;6(5):458-63 PMID: 10331874
  21. Prepeptide sequence of epidermin, a ribosomally synthesized antibiotic with four sulphide-rings.
    Nature. 1988 May 19;333(6170):276-8 PMID: 2835685
  22. Bacteriocins of gram-positive bacteria.
    Microbiol Rev. 1995 Jun;59(2):171-200 PMID: 7603408
  23. beta-Alanine auxotrophy associated with dfp, a locus affecting DNA synthesis in Escherichia coli.
    J Bacteriol. 1988 Feb;170(2):872-6 PMID: 3123465
  24. Molecular characterization of lantibiotic-synthesizing enzyme EpiD reveals a function for bacterial Dfp proteins in coenzyme A biosynthesis.
    J Biol Chem. 2000 Oct 13;275(41):31838-46 PMID: 10922366
  25. dfp Gene of Escherichia coli K-12, a locus affecting DNA synthesis, codes for a flavoprotein.
    J Bacteriol. 1985 Dec;164(3):994-1003 PMID: 2999089
  26. The enethiolate anion reaction products of EpiD. Pka value of the enethiol side chain is lower than that of the thiol side chain of peptides.
    J Biol Chem. 1997 Feb 21;272(8):4759-62 PMID: 9030529
  27. Flavoenzymes: diverse catalysts with recurrent features.
    Trends Biochem Sci. 2000 Mar;25(3):126-32 PMID: 10694883
  28. SCOP: a structural classification of proteins database for the investigation of sequences and structures.
    J Mol Biol. 1995 Apr 7;247(4):536-40 PMID: 7723011
  29. Purification of mutacin III from group III Streptococcus mutans UA787 and genetic analyses of mutacin III biosynthesis genes.
    Appl Environ Microbiol. 1999 Sep;65(9):3880-7 PMID: 10473390
  30. Mechanisms of flavoprotein-catalyzed reactions.
    Eur J Biochem. 1989 Apr 15;181(1):1-17 PMID: 2653819
  31. The CCP4 suite: programs for protein crystallography.
    Acta Crystallogr D Biol Crystallogr. 1994 Sep 1;50(Pt 5):760-3 PMID: 15299374
  32. Tertiary structure of oxidized flavodoxin from an eukaryotic red alga Chondrus crispus at 2.35-A resolution. Localization of charged residues and implication for interaction with electron transfer partners.
    J Biol Chem. 1990 Sep 15;265(26):15804-12 PMID: 2394748
  33. Regulation of cation transport in Saccharomyces cerevisiae by the salt tolerance gene HAL3.
    Mol Cell Biol. 1995 Oct;15(10):5470-81 PMID: 7565698
  34. The X-ray structure of the FMN-binding protein AtHal3 provides the structural basis for the activity of a regulatory subunit involved in signal transduction.
    Structure. 2000 Sep 15;8(9):961-9 PMID: 10986463
  35. The application of direct methods and Patterson interpretation to high-resolution native protein data.
    Acta Crystallogr D Biol Crystallogr. 1993 Jan 1;49(Pt 1):18-23 PMID: 15299542
  36. On the interpretation of quantitative structure-function activity relationship data for lactate oxidase.
    Proc Natl Acad Sci U S A. 2000 Mar 14;97(6):2480-5 PMID: 10706608
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2000-12-01
Pages
6299-310
Language
English
Region
England
NLM ID
8208664
PMCID
PMC305864
Subset
IM
Databases
PDB
Analysis Services
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