The ponA gene of Enterococcus faecalis JH2-2 codes for a low-affinity class a penicillin-binding protein

[en] soluble derivative of the Enterococcus faecalis JH2-2 class A PBP1 (*PBP1) was overproduced and purified. It exhibited a glycosyltransferase activity on the Escherichia coli (14)C(-)labeled lipid 11 precursor. As a DD-peptidase, it could hydrolyze thiolester substrates with efficiencies similar to those of other class A penicillin-binding proteins (PBPs) and bind beta-lactams, but with k(2)/K (a parameter accounting for the acylation step efficiency) values characteristic of penicillin-resistant PBPs.

Disciplines :

Microbiology

Author, co-author :

Duez, Colette ; Université de Liège - ULiège > Centre d'ingénierie des protéines

Hallut, Séverine; Université de Liège - ULiège > CIP

Rhazi, Noureddine ; Université de Liège - ULiège > Centre d'ingénierie des protéines

Amoroso, Ana Maria ; Université de Liège - ULiège > Centre d'ingénierie des protéines

Bouillenne, Fabrice ; Université de Liège - ULiège > Centre d'ingénierie des protéines

Coyette, Jacques ; Université de Liège - ULiège > Services généraux (Faculté des sciences) > Relations académiques et scientifiques (Sciences)

Language :

English

Title :

The ponA gene of Enterococcus faecalis JH2-2 codes for a low-affinity class a penicillin-binding protein

Publication date :

July 2004

Journal title :

Journal of Bacteriology

ISSN :

0021-9193

eISSN :

1098-5530

Publisher :

Amer Soc Microbiology, Washington, United States - Washington

Volume :

186

Issue :

Pages :

4412-4416

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 10 February 2009

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Adam, M., C. Damblon, M. Jamin, W. Zorzi, V. Dusart, M. Galleni, A. El Kharroubi, G. Piras, B. G. Spratt, W. Keck, J. Coyette, J. M. Ghuysen, M. Nguyen-Distèche, and J. M. Frère. 1991. Acyltransferase activities of the high-molecular-mass essential penicillin-binding proteins. Biochem. J. 279: 601-604.
Adam, M., C. Fraipont, N. Rhazi, M. Nguyen-Disteche, B. Lakaye, J. M. Frère, B. Devreese, J. Van Beeumen, Y. van Heijenoort, J. van Heijenoort, and J. M. Ghuysen. 1997. The bimodular G57-V577 polypeptide chain of the class B penicillin-binding protein 3 of Escherichia coli catalyzes peptide bond formation from thiolesters and does not catalyze glycan chain polymerization from the lipid II intermediate. J. Bacteriol. 179:6005-6009.
Altschul, S. F., W. Gish, W. Miller, E. W. Myers, and D. J. Lipman. 1990. Basic local alignment search tool. J. Mol. Biol. 215:403-410.
Arbeloa, A., H. Segal, J.-E. Hugonnet, N. Josseaume, L. Dubost, J.-P. Brouard, L. Gutmann, D. Mengin-Lecreulx, and M. Arthur. 2004. Role of class A penicillin-binding proteins in PBP5-mediated β-lactam resistance in Enterococcus faecalis. J. Bacteriol. 186:1221-1228.
Broome-Smith, J. K., A. Edelman, S. Yousif, and B. G. Spratt. 1985. The nucleotide sequences of the ponA and ponB genes encoding penicillin-binding protein 1A and 1B of Escherichia coli K12. Eur. J. Biochem. 147:437-446.
Chenoweth, C., and D. Schaberg. 1990. The epidemiology of enterococci. Eur. J. Clin. Microbiol. Infect. Dis. 9:80-89.
Damblon, C., G. H. Zhao, M. Jamin, P. Ledent, A. Dubus, M. Vanhove, X. Raquet, L. Christiaens, and J. M. Frère. 1995. Breakdown of the stereospecificity of DD-peptidases and beta-lactamases with thiolester substrates. Biochem. J. 309:431-446.
Di Guilmi, A. M., A. Dessen, O. Dideberg, and T. Vernet. 2003. Functional characterization of penicillin-binding protein 1b from Streptococcus pneumoniae. J. Bacteriol. 185:1650-1658.
Di Guilmi, A. M., A. Dessen, O. Dideberg, and T. Vernet. 2003. The glycosyltransferase domain of penicillin-binding protein 2a from Streptococcus pneumoniae catalyzes the polymerization of murein glycan chains. J. Bacteriol. 185:4418-4423.
Di Guilmi, A. M., N. Mouz, J. P. Andrieu, J. Hoskins, S. R. Jaskunas, J. Gagnon, O. Dideberg, and T. Vernet. 1998. Identification, purification, and characterization of transpeptidase and glycosyltransferase domains of Streptococcus pneumoniae penicillin-binding protein 1a. J. Bacteriol. 180:5652-5659.
Di Guilmi, A. M., N. Mouz, L. Martin, J. Hoskins, S. R. Jaskunas, O. Dideberg, and T. Vernet. 1999. Glycosyltransferase domain of penicillin-binding protein 2a from Streptococcus pneumoniae is membrane associated. J. Bacteriol. 181:2773-2781.
Duez, C., W. Zorzi, F. Sapunaric, A. Amoroso, I. Thamm, and J. Coyette. 2001. The penicillin resistance of Enterococcus faecalis JH2-2r results from an overproduction of the low-affinity penicillin-binding protein PBP4 and does not involve a psr-like gene. Microbiology 147:2561-2569.
El Kharroubi, A., P. Jacques, G. Piras, J. Van Beeumen, J. Coyette, and J. M. Ghuysen. 1991. The Enterococcus hirae R40 penicillin-binding protein 5 and the methicillin-resistant Staphylococcus aureus penicillin-binding protein 2′ are similar. Biochem. J. 280:463-469.
Fernandez, S., A. Sorokin, and J. C. Alonso. 1998. Genetic recombination in Bacillus subtilis 168: effects of recU and recS mutations on DNA repair and homologous recombination. J. Bacteriol. 180:3405-3409.
Frère, J. M., J. M. Ghuysen, and M. Iwatsubo. 1975. Kinetics of interaction between the exocellular DD-carboxypeptidase-transpeptidase from Streptomyces R61 and beta-lactam antibiotics. A choice of models. Eur. J. Biochem. 57:343-351.
Goffin, C., and J. M. Ghuysen. 2002. Biochemistry and comparative genomics of SxxK superfamily acyltransferases offer a clue to the mycobacterial paradox: presence of penicillin-susceptible target proteins versus lack of efficiency of penicillin as therapeutic agent. Microbiol. Mol. Biol. Rev. 66: 702-738.
Goffin, C., and J. M. Ghuysen. 1998. Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs. Microbiol. Mol. Biol. Rev. 62:1079-1093.
Granier, B., M. Jamin, M. Adam, M. Galleni, B. Lakaye, W. Zorzi, J. Grandchamps, J. M. Wilkin, C. Fraipont, B. Joris, C. Duez, M. Nguyen-Distèche, J. Coyette, M. Leyh-Bouille, J. Dusart, L. Christiaens, J. M. Frère, and J. M. Ghuysen. 1994. Serine-type D-Ala-D-Ala peptidases and penicillin-binding proteins. Methods Enzymol. 244:249-266.
Hara, H., and H. Suzuki. 1984. A novel glycan polymerase that synthesizes uncross-linked peptidoglycan in Escherichia coli. FEBS Lett. 168:155-160.
Hoskins, J., P. Matsushima, D. L. Mullen, J. Tang, G. Zhao, T. I. Meier, T. I. Nicas, and S. R. Jaskunas. 1999. Gene disruption studies of penicillin-binding proteins 1a, 1b, and 2a in Streptococcus pneumoniae. J. Bacteriol. 181:6552-6555.
Huycke, M. M., D. F. Sahm, and M. S. Gilmore. 1998. Multiple drug resistance enterococci: the nature of the problem and an agenda for the future. Emerg. Infect. Dis. 4:239-249.
Jacob, A. E., and S. J. Hobbs. 1974. Conjugal transfer of plasmid-borne multiple antibiotic resistance in Streptococcus faecalis var. zymogenes. J. Bacteriol. 117:360-372.
Jamin, M., M. Adam, C. Damblon, L. Christiaens, and J. M. Frère. 1991. Accumulation of acyl-enzyme in DD-peptidase-catalysed reactions with analogues of peptide substrates. Biochem. J. 280:499-506.
Kato, J., H. Suzuki, and Y. Hirota. 1985. Dispensability of either penicillin-binding protein-1a or -1b involved in the essential process for cell elongation in Escherichia coli. Mol. Gen. Genet. 200:272-277.
Lakaye, B., C. Damblon, M. Jamin, M. Galleni, S. Lepage, B. Joris, J. Marchand-Brynaert, C. Frydrych, and J. M. Frère. 1994. Synthesis, purification and kinetic properties of fluorescein-labelled penicillins. Biochem. J. 300:141-145.
Lepage, S., P. Dubois, T. K. Ghosh, B. Joris, S. Mahapatra, M. Kundu, J. Basu, P. Chakrabarti, S. T. Cole, M. Nguyen-Distèche, and J. M. Ghuysen. 1997. Dual multimodular class A penicillin-binding proteins in Mycobacterium leprae. J. Bacteriol. 179:4627-4630.
Loureiro Dos Santos, A. L., and A. Chopin. 1987. Shotgun cloning in Streptococcus lactis. FEMS Microbiol. Lett. 42:209-212.
McPherson, D. C., and D. L. Popham. 2003. Peptidoglycan synthesis in the absence of class A penicillin-binding proteins in Bacillus subtilis. J. Bacteriol. 185:1423-1431.
Nguyen-Distèche, M., J. M. Ghuysen, J. J. Pollock, P. Reynolds, H. R. Perkins, J. Coyette, and M. R. Salton. 1974. Enzymes involved in wall peptide crosslinking in Escherichia coli K12, strain 44. Eur. J. Biochem. 41:447-455.
Nieto, M., H. R. Perkins, J. M. Frère, and J. M. Ghuysen. 1973. Fluorescence and circular dichroism studies on the Streptomyces R61 DD-carboxypeptidase-transpeptidase. Penicillin binding by the enzyme. Biochem. J. 135:493-505.
Paik, J., I. Kern, R. Lurz, and R. Hakenbeck. 1999. Mutational analysis of the Streptococcus pneumoniae bimodular class A penicillin-binding proteins. J. Bacteriol. 181:3852-3856.
Pearson, W. R., and D. J. Lipman. 1988. Improved tools for biological sequence comparison. Proc. Natl. Acad. Sci. USA 85:2444-2448.
Piras, G., A. El Kharroubi, J. van Beeumen, E. Coeme, J. Coyette, and J. M. Ghuysen. 1990. Characterization of an Enterococcus hirae penicillin-binding protein 3 with low penicillin affinity. J. Bacteriol. 172:6856-6862.
Popham, D. L., and P. Setlow. 1995. Cloning, nucleotide sequence, and mutagenesis of the Bacillus subtilis ponA operon, which codes for penicillin-binding protein (PBP) 1 and a PBP-related factor. J. Bacteriol. 177:326-335.
Popham, D. L., and P. Setlow. 1996. Phenotypes of Bacillus subtilis mutants lacking multiple class A high-molecular-weight penicillin-binding proteins. J. Bacteriol. 178:2079-2085.
Raze, D., O. Dardenne, S. Hallut, M. Martinez-Bueno, J. Coyette, and J. M. Ghuysen. 1998. The gene encoding the low-affinity penicillin-binding protein 3r in Enterococcus hirae S185R is borne on a plasmid carrying other antibiotic resistance determinants. Antimicrob. Agents Chemother. 42:534-539.
Rigden, D. J., P. Setlow, B. Setlow, I. Bagyan, R. A. Stein, and M. J. Jedrzejas. 2002. PrfA protein of Bacillus species: prediction and demonstration of endonuclease activity on DNA. Protein Sci. 11:2370-2381.
Signoretto, C., M. Boaretti, and P. Canepari. 1994. Cloning, sequencing and expression in Escherichia coli of the low-affinity penicillin binding protein of Enterococcus faecalis. FEMS Microbiol. Lett. 123:99-106.
Suzuki, H., Y. Nishimura, and Y. Hirota. 1978. On the process of cellular division in Escherichia coli: a series of mutants of E. coli altered in the penicillin-binding proteins. Proc. Natl. Acad. Sci. USA 75:664-668.
Terrak, M., T. K. Ghosh, J. van Heijenoort, J. Van Beeumen, M. Lampilas, J. Aszodi, J. A. Ayala, J. M. Ghuysen, and M. Nguyen-Distèche. 1999. The catalytic, glycosyl transferase and acyl transferase modules of the cell wall peptidoglycan-polymerizing penicillin-binding protein 1b of Escherichia coli. Mol. Microbiol. 34:350-364.
van HeUenoort, J. 2001. Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 11:25R-36R.
Yan, S., P. M. Mendelman, and D. L. Stevens. 1993. The in vitro antibacterial activity of ceftriaxone against Streptococcus pyogenes is unrelated to penicillin-binding protein 4. FEMS Microbiol. Lett. 110:313-317.
Zhao, G., W.-K. Yeh, R. H. Carnahan, J. Flokowitsch, T. I. Meier, W. E. Alborn, Jr., G. W. Becker, and S. R. Jaskunas. 1997. Biochemical characterization of penicillin-resistant and -sensitive penicillin-binding protein 2x transpeptidase activities of Streptococcus pneumoniae and mechanistic implications in bacterial resistance to β-lactam antibiotics. J. Bacteriol. 179:4901-4908.

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