Novel peptide inhibiting both TEM-1 beta-lactamase and penicillin-binding proteins.

Antibodies, Catalytic/chemistry/genetics; Bacteriophage M13/genetics; Catalytic Domain; Kinetics; Models, Molecular; Mutagenesis; Penicillin-Binding Proteins/antagonists & inhibitors; Peptide Library; Peptides, Cyclic/chemistry/genetics/pharmacology; Peptidomimetics/chemistry/pharmacology; Protein Engineering; Tryptophan/chemistry; beta-Lactamase Inhibitors

Abstract :

[en] 9G4H9, a catalytic antibody displaying beta-lactamase-like activity, has been developed by the anti-idiotypic approach using beta-lactamase as the first antigen. Thus 9G4H9 represents the 'internal image' of beta-lactamase. We selected a cyclic peptide anchored to a bacteriophage M13 library using 9G4H9 as the target. Pep90 is a cyclic heptapeptide enclosed between two cysteine residues. We showed that Pep90 could inhibit both TEM-1 beta-lactamase (K(i) = 333 mum) and several penicillin-binding proteins (IC(5)(0) values ranging from 6-62 mum). We determined that the tryptophan residue of Pep90 is of crucial importance for its inhibitory activity. Using Pep90 as a scaffold, we generated a new class of peptidomimetics that retained inhibitory activity towards TEM-1 beta-lactamase.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Phichith, Denis

Bun, Sylvie

Padiolleau-Lefevre, Severine

Guellier, Adeline

Banh, Soun

Galleni, Moreno ; Université de Liège - ULiège

Frère, Jean-Marie ; Université de Liège > Département des sciences de la vie > Centre d'ingénierie des protéines

Thomas, Daniel

Friboulet, Alain

Avalle, Berangere

Language :

English

Title :

Novel peptide inhibiting both TEM-1 beta-lactamase and penicillin-binding proteins.

Publication date :

2010

Journal title :

FEBS Journal

ISSN :

1742-464X

eISSN :

1742-4658

Publisher :

Blackwell, Oxford, United Kingdom

Volume :

277

Issue :

Pages :

4965-72

Peer reviewed :

Peer Reviewed verified by ORBi

Commentary :

Available on ORBi :

since 27 November 2015

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Bibliography

Ghuysen JM (1997) Penicillin-binding proteins. Wall peptidoglycan assembly and resistance to penicillin: facts, doubts and hopes. Int J Antimicrob Agents 8, 45-60.
Goffin C & Ghuysen JM (1998) Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol Mol Biol Rev 62, 1079-1093.
Galleni M & Frère JM (2007) Kinetics of beta-lactamases and penicillin-binding proteins. In Enzyme-Mediated Resistance to Antibiotics: Mechanisms, Dissemination, and Prospects for Inhibition (Bonomo RA & Tomasky ME eds), pp 195-213. ASM Press, Washington, DC.
Ghuysen JM (1991) Serine beta-lactamases and penicillin-binding proteins. Annu Rev Microbiol 250, 313-324.
Urbach C, Evrard C, Pudzaitis V, Fastrez J, Soumillion P & Declercq JP (2009) Structure of PBP-A Thermosynechococcus elongatus, a penicillin-binding protein closely related to class A β-lactamases. J Mol Biol 386, 109-120.
Herzberg O (1991) Refined crystal structural of β-lactamase from Staphylococcus aureus PC1 at 2.0 Å resolution. J Mol Biol 217, 701-719.
Samraoui B, Sutton BJ, Todd RJ, Artymiuk PJ, Waley SG & Phillips DC (1986) Tertiary structural similarity between a class A β-lactamase and a penicillin-sensitive d-alanyl carboxypeptidase-transpeptidase. Nature 320, 378-380.
Joris B, Ghuysen JM, Dive G, Renard A, Dideberg O, Charlier P, Frère JM, Kelly JA, Boyington JC, Moews PC et al. (1988) The active-site-serine penicillin-recognizing enzymes as members of the Streptomyces R61 dd-peptidase family. Biochem J 250, 313-324.
Phichith D, Bun S, Padiolleau-Lefèvre S, Banh S, Thomas D, Friboulet A & Avalle B (2009) Mutational and inhibitory analysis of a catalytic antibody. Implication for drug discovery. Mol Immunol 47, 348-356.
Jerne N (1974) Toward a network theory of the immune system. Ann Immunol (Paris) 125c, 373-389.
Avalle B, Thomas D & Friboulet A (1998) Functional mimicry: elicitation of a monoclonal anti-idiotypic antibody hydrolysing β-lactams. FASEB J 11, 1055-1060.
Padiolleau-Lefèvre S, Débat H, Phichith D, Thomas D, Friboulet A & Avalle B (2006) Expression of a functional scFv fragment of an anti-idiotypic antibody with a β-lactam hydrolytic activity. Immunol Lett 103, 39-44.
Yribarren AS, Thomas D, Friboulet A & Avalle B (2003) Selection of peptides inhibiting a β-lactamase-like activity. Eur J Biochem 270, 2789-2795.
Lefèvre S, Débat H, Thomas D, Friboulet A & Avalle B (2001) A suicide substrate mechanism for hydrolysis of β-lactams by an anti-idiotypic catalytic antibody. FEBS Lett 489, 25-28.
Fisher JF & Mobashery S (2009) Three decades of the class A beta-lactamase acyl-enzyme. Curr Protein Pept Sci 10, 401-407.
Rudgers GW, Huang W & Palzkill T (2001) Binding properties of a peptide derived from β-lactamase inhibitory protein. Antimicrob Agents Chemother 45, 3279-3286.
Rudgers GW & Palzkill T (1999) Identification of residues in β-lactamase critical for binding β-lactamase inhibitory protein. Antimicrob Agents Chemother 274, 6963-6971.
Kong L, Lee K, Tong JC, Tan TW & Ranganathan S (2004) SDPMOD: an automated comparative modeling server for small disulfide-bonded proteins. Nucleic Acids Res 32, W356-W359.
Katz BA (1995) Binding to protein targets of peptidic leads discovered by phage display: crystal structures of streptavidin-bound linear and cyclic peptide ligands containing the HPQ sequence. Biochemistry 34, 15421-15429.
Tovchigrechko A & Vakser IA (2006) GRAMM-X public web server for protein-protein docking. Nucleic Acids Res 34, 310-314.
Stec B, Holtz KM, Wojciechowski CL & Kantrowitz ER (2005) Structure of the wild-type TEM-1 β-lactamase at 1.55 Å and the mutant enzyme Ser70Ala at 2.1 Å suggest the mode of noncovalent catalysis for the mutant enzyme. Acta Crystallogr D Biol Crystallogr 61, 1072-1079.
Padiolleau-Lefèvre S, Débat H, Thomas D, Friboulet A & Avalle B (2003) In vivo evolution of a β-lactamase-like activity throughout the idiotypic pathway. Biocatal Biotransformation 21, 79-85.
Howl J & Wheatley M (1996) Molecular recognition of peptide and non-peptide ligands by the extracellular domains of neurohypophysial hormone receptors. Biochem J 317, 577-582.
Szelke M, Leckie B, Hallet A, Jones DM, Sueiras J, Atrash B & Lever AF (1982) Potent new inhibitors of human renin. Nature 299, 555-557.
Gante J (1994) Peptidomimetics - tailored enzyme inhibitors. Angew Chem Int Ed Engl 33, 1699-1720.
Giannis A & Kolter T (1993) Peptidomimetics for receptor ligands: discovery, development, and medical perspectives. Angew Chem Int Ed Engl 32, 1244-1267.
De Vega MJ, Martin-Martinez M & Gonzalez-Muniz R (2007) Modulation of protein-protein interactions by stabilizing/mimicking protein secondary structure elements. Curr Top Med Chem 7, 33-62.
Gabriel GJ & Tew GN (2008) Conformationally rigid proteomimetics: a case study in designing antimicrobial aryl oligomers. Org Biomol Chem 6, 417-423.
Berezov A, Chen J, Liu Q, Zhang HT, Greene MI & Murali R (2002) Disabling receptor ensembles with rationally designed interface peptidomimetics. J Biol Chem 277, 28330-28339.
Turkson J, Kim JS, Zhang S, Yuan J, Huang M, Glenn M, Haura E, Sebti S, Hamilton AD & Jove R (2004) Novel peptidomimetic inhibitors of signal transducer and activator of transcription 3 dimerization and biological activity. Mol Cancer Ther 3, 261-269.
Chorev M & Goodman M (1995) Recent developments in retro peptides and proteins - an ongoing topochemical exploration. Trends Biotechnol 13, 438-445.
Burke TJ, Barchi JJ, George C, Wolf G, Shoelson SE & Yan X (1995) Conformationally constrained phosphotyrosyl mimetics designed as monomeric Src homology 2 domain inhibitors. Med Chem 38, 1386-1396.
Smithgall TE (1995) SH2 and SH3 domains: potential targets for anti-cancer drug design. J Pharmacol Toxicol Methods 34, 125-132.
Orfi L, Waczek F, Kövesdi I, Mészaros G, Idei M, Horvath A, Hollosy F, Mak M, Szegedi Z, Szende B et al. (1999) New antitumor leads from a peptidomimetic library. Lett Pept Sci 6, 325-333.
Giebel LB, Cas RT, Milligan DL, Young DC, Arze R & Johnson CR (1995) Screening of cyclic peptide phage libraries identifies ligands that bind streptavidin with high affinities. Biochemistry 34, 15430-15435.
Luzzago A, Felici F, Tramontano A, Pessi A & Cortes R (1993) Mimicking of discontinuous epitopes by phage-displayed peptides. I. Epitope mapping of human H ferritin using a phage library of constrained peptides. Gene 128, 51-57.
Kieber-Emmons T, Murali R & Greene MI (1997) Therapeutic peptides and peptidomimetics. Curr Opin Chem Biol 8, 435-441.
Rotem S & Mor A (2009) Antimicrobial peptide mimics for improved therapeutic properties. Biochim Biophys Acta 1788, 1582-1592.
Vaara M (2009) New approaches in peptide antibiotics. Curr Opin Pharmacol 9, 571-576.
Kunkel TA (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci USA 82, 435-492.
Galleni M, Lakaye B, Lepage S, Jamin M, Thamm I, Joris B & Frère JM (1993) A new, highly sensitive method for the detection and quantification of penicillin-binding proteins. Biochem J 291, 19-21.
Lakaye B, Damblon C, Jamin M, Galleni M, Lepage S, Joris B, Marchand-Brynaert J, Frydrych C & Frère JM (1994) Synthesis, purification and kinetic properties of fluorescein-labelled penicillins. Biochem J 300, 141-145.