Kinetics of reactions of the Actinomadura R39 DD -Peptidase with specific substrates

Biochemistry

Volumn 50, Issue 3, 2011, Pages 376-387

  Adediran, S A ^a   Kumar, Ish ^a   Nagarajan, Rajesh ^a,c   Sauvage, Eric ^b   Pratt, R F ^a  

^a WESLEYAN UNIVERSITY   (United States)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c BOISE STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINOMADURA R39 DD-PEPTIDASE; ACTIVE SITE; ACYL GROUP; AMINOLYSIS; CARBOXYPEPTIDASE; CLASS A; D-AMINO ACID; DEACYLATION; DEPSIPEPTIDES; DEUTERIUM ISOTOPE EFFECT; FRACTIONATION FACTORS; IN-VIVO; LACTAMASES; LEAVING GROUPS; LOCAL STRUCTURE; N-TERMINALS; PEPTIDOGLYCANS; PROTON DISSOCIATION; RATE PROFILES; SIDE CHAINS; SOLVENT KINETICS; STRUCTURAL SPECIFICITY; SUBSTRATE SPECIFICITY;

AMIDES; AMINATION; AMINO ACIDS; CATALYSIS; DEUTERIUM; ENZYMES; ISOMERS; PEPTIDES; PROTONS;

SUBSTRATES;

ACID; BASE; BETA LACTAM; BETA LACTAMASE; CARBOXYPEPTIDASE; DEUTERIUM; DEXTRO ALANINE; DEXTRO AMINO ACID; DEXTRO PHENYLALANINE; GAMMA GLUTAMYLTRANSFERASE; HYDROGEN; LACTIC ACID; NUCLEOPHILE; PEPTIDASE; PEPTIDOGLYCAN; PEPTIDOMIMETIC AGENT; POLYMER; PROTEINASE;

ACTINOMADURA; ACYLATION AND DEACYLATION; AMINO TERMINAL SEQUENCE; AMINOLYSIS; ARTICLE; CATALYSIS; CROSS LINKING; DISSOCIATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; NONHUMAN; PH; PRIORITY JOURNAL; SOLVENT EFFECT; STEADY STATE;

ACTINOMYCETALES; ACYLATION; ALANINE; BETA-LACTAMS; KINETICS; MODELS, CHEMICAL; MOLECULAR MIMICRY; PEPTIDOGLYCAN; SERINE-TYPE D-ALA-D-ALA CARBOXYPEPTIDASE; SUBSTRATE SPECIFICITY; SULFHYDRYL COMPOUNDS;

ACTINOMADURA;

EID: 78751556860     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101760p     Document Type: Article

References (47)

1. Vollmer, W. and Bertsche, U. (2007) Murein (peptidoglycan) structure, architecture and biosynthesis in Escherichia coli Biochim. Biophys. Acta 1778, 1714-1734
2. Sauvage, E., Kerff, F., Terrak, M., Ayala, J. A., and Charlier, P. (2008) The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis FEMS Microbiol. Rev. 32, 234-258
3. Waxman, D. J. and Strominger, J. L. (1983) Penicillin-binding proteins and the mechanism of action of δ-lactam antibiotics Annu. Rev. Biochem. 52, 825-869
4. Pratt, R. F. (2002) Functional evolution of the serine δ-lactamase active site J. Chem. Soc. Perkin 2, 851-861
5. Payne, D. J., Gwynn, M. N., Holmes, D. J., and Pompliano, D. L. (2007) Drugs for bad bugs: confronting the challenges of antibacterial discovery Nat. Rev. Drug Discov. 6, 29-40
6. Boucher, H. W., Talbot, G. H., Bradley, J. S., Edwards, T. E., Gilbert, D., Rice, L. B., Scheld, M., Spellberg, B., and Bartlett, J. (2009) Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America Clin. Infect. Dis. 48, 1-12
7. Ghuysen, J.-M. (1991) Serine δ-lactamases and penicillin-binding proteins Annu. Rev. Microbiol. 45, 37-67
8. Goffin, C. and Ghuysen, J.-M. (1998) Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs Microbiol. Mol. Biol. Rev. 62, 1079-1093
9. Pratt, R. F. (2008) Substrate specificity of bacterial dd -peptidases (penicillin-binding proteins) Cell. Mol. Life Sci. 65, 2138-2155
10. Anderson, J. W. and Pratt, R. F. (2000) Dipeptide binding to the extended active site of the S treptomyces R61 d -alanyl- d -alanine peptidase: the path to a specific substrate Biochemistry 39, 12200-12209
11. Anderson, J. W., Adediran, S. A., Charlier, P., Nguyen-Distèche, M., Frère, J.-M., Nicholas, R. A., and Pratt, R. F. (2003) On the substrate specificity of bacterial dd -peptidases: evidence from two series of peptidoglycan-mimetic peptides Biochem. J. 373, 949-955
12. McDonough, M. A., Anderson, J. W., Silvaggi, N. R., Pratt, R. F., Knox, J. R., and Kelly, J. A. (2002) Structures of two kinetic intermediates reveal species specificity of penicillin-binding proteins J. Mol. Biol. 322, 111-122
13. Silvaggi, N. R., Anderson, J. W., Brinsmade, S. R., Pratt, R. F., and Kelly, J. A. (2003) The crystal structure of a phosphonate-inhibited d -Ala- d -Ala peptidase reveals an analogue of a tetrahedral transition state Biochemistry 42, 1199-1208
14. Silvaggi, N. R., Josephine, H. R., Kuzin, A. P., Nagarajan, R., Pratt, R. F., and Kelly, J. A. (2005) Crystal structures of complexes between the R61 dd -peptidase and peptidoglycan-mimetic β-lactams: a non-covalent complex with a "perfect penicillin. J. Mol. Biol. 345, 521-533
15. Sauvage, E., Powell, A. J., Heilemann, J., Josephine, H. R., Charlier, P., Davies, C., and Pratt, R. F. (2008) Crystal structures of complexes of bacterial dd -peptidases with peptidoglycan-mimetic ligands; the substrate specificity puzzle J. Mol. Biol. 381, 383-393
16. Dzhekieva, L., Rocaboy, M., Kerff, F., Charlier, P., Sauvage, E., and Pratt, R. F. (2010) Crystal structure of a complex between the Actinomadura R39 dd -peptidase and a peptidoglycan-mimetic boronate inhibitor: interpretation of a transition state analogue in terms of catalytic mechanism Biochemistry 49, 6411-6419
17. Ghuysen, J.-M., Frère, J.-M., Leyh-Bouille, M., Coyette, J., Dusart, J., and Nguyen-Distèche, M. (1977) Use of model enzymes in determination of the mode of action of penicillins and Δ3-cephalosporins Annu. Rev. Biochem. 48, 73-101
18. Zhao, G.-H., Duez, C., LePage, S., Forceille, C., Rhazi, N., Klein, D., Ghuysen, J.-M., and Frère, J.-M. (1997) Site-directed mutagenesis of the Actinomadura R39 dd -peptidase Biochem. J. 327, 377-381
19. Sauvage, E., Herman, R., Petrella, S., Duez, C., Bouillenne, F., Frère, J.-M., and Charlier, P. (2005) Crystal structure of the Actinomadura R39 dd -peptidase reveals new domains in penicillin-binding proteins J. Biol. Chem. 280, 31249-31256
20. Granier, B., Duez, C., Lepange, S., Englebert, S., Dusart, J., Dideberg, O., Van Beeumen, J., Frère, J.-M., and Ghuysen, J.-M. (1992) Primary and predicted secondary structures of the Actinomadura R39 extracellular dd -peptidase, a penicillin-binding protein (PBP) related to Escherichia coli PBP4 Biochem. J. 282, 781-788
21. Nagarajan, R. and Pratt, R. F. (2004) Synthesis and evaluation of new substrate analogues of Streptomyces R61 dd -peptidase: dissection of a specific ligand J. Org. Chem. 69, 7472-7478
22. Johnson, K. A., Simpson, Z. B., and Blom, T. (2009) A new computer program for dynamic simulations and fitting of kinetic data Anal. Biochem. 387, 20-29
23. Kuzmic, P. (1996) Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase Anal. Biochem. 237, 260-273
24. Frére, J.-M., Leyh-Bouille, M., Ghuysen, J.-M., Nieto, M., and Perkins, H. R. (1976) Exocellular dd -carboxypeptidase-transpeptidases from Streptomyces Methods Enzymol. 45, 610-636
25. Fuad, N., Frére, J.-M., Ghuysen, J.-M., Duez, C., and Iwatsubo, M. (1974) Mode of interaction between δ-lactam antibiotics and the exocellular dd -carboxypeptidase-transpeptidase from Streptomyces R39 Biochem. J. 155, 623-629
26. Adediran, S. A., Deraniyagala, S. A., Xu, Y., and Pratt, R. F. (1996) δ-Secondary and solvent deuterium kinetic isotope effects on δ-lactamase catalysis Biochemistry 35, 3604-3613
27. Stein, R. L. (1983) Catalysis by human leukocyte elastase: substrate structural operation of the charge relay system J. Am. Chem. Soc. 105, 5111-5116
28. Adediran, S. A., Kumar, I., and Pratt, R. F. (2006) Deacylation transition states of a bacterial dd -peptidase Biochemistry 45, 13074-13082
29. Kumar, I. and Pratt, R. F. (2005) Transpeptidation reactions of a specific substrate catalyzed by the Streptomyces R61 dd -peptidase: characterization of a chromogenic substrate and acyl acceptor design Biochemistry 30, 9971-9979 (Pubitemid 41076793)
30. Adam, M., Damblon, C., Plaitin, B., Christiaens, L., and Frère, J.-M. (1990) Chromogenic depsipeptide substrates for δ-lactamases and penicillin-sensitive dd -peptidases Biochem. J. 270, 525-529
31. Jamin, M., Adam, M., Damblon, C., Christiaens, L., and Frère, J.-M. (1991) Accumulation of acyl-enzymes in dd -peptidase-catalyzed reactions with analogues of peptide substrates Biochem. J. 280, 499-506
32. Kumar, I. and Pratt, R. F. (2005) Transpeptidation reactions of a specific substrate catalyzed by the Streptomyces R61 dd -peptidase: the structural basis of acyl acceptor specificity Biochemistry 44, 9961-9970 (Pubitemid 41076792)
33. Peller, L. and Alberty, R. A. (1959) Multiple intermediates in steady state enzyme kinetics. I. The mechanism involving a single substrate and product J. Am. Chem. Soc. 81, 5907-5914
34. Knowles, J. R. (1976) The intrinsic pKa values of functional groups in enzymes: improper deductions from the pH-dependence of steady state parameters CRC Crit. Rev. Biochem. 4, 165-173
35. Cleland, W. W. (1977) Determining the chemical mechanisms of enzyme-catalyzed reactions by kinetics studies Adv. Enzymol. 45, 273-387
36. Hardy, L. W., Nishida, C. H., and Kirsch, J. F. (1984) Anomalous pH dependence of the reactions of carbenicillin and sulbenicillin with Bacillus cereus δ-lactamase I. Influence of the α-substituent charge on the kinetic parameters Biochemistry 23, 1288-1294
37. Kóczián, K., Szakács, Z., Kökösi, J., and Noszál, B. (2007) Site-specific protonation micro equilibria of penicillin and cephalosporin beta-lactam core molecules Eur. J. Pharm. Sci. 32, 1-7
38. Varetto, L., Frère, J.-M., Nguyen-Distèche, M., Ghuysen, J.-M., and Houssier, C. (1987) The pH dependence of the active site serine dd -peptidase of Streptomyces R61 Eur. J. Biochem. 162, 525-531
39. Stevanova, M. E., Tomberg, J., Olesky, M., Höltje, J.-V., Gutheil, W. G., and Nicholas, R. A. (2003) Neisseria gonorrhoeae penicillin-binding protein 3 exhibits exceptionally high carboxypeptidase and δ-lactam binding activities Biochemistry 42, 14614-14625
40. Stefanova, M. E., Tomberg, J., Davies, C., Nicholas, R. A., and Gutheil, W. G. (2004) Overexpression and enzymatic characterization of Neisseria gonorrhoeae penicillin-binding protein 4 Eur. J. Biochem. 271, 23-32
41. Thomas, B., Wang, Y., and Stein, R. L. (2001) Kinetic and mechanistic studies of penicillin-binding protein 2x from Streptococcus pneumoniae Biochemistry 40, 15811-15823
42. Stefanova, M. E., Davies, C., Nicholas, R. A., and Gutheil, W. G. (2009) pH, inhibitor and substrate specificity studies on Escherichia coli penicillin-binding protein 5 Biochim. Biophys. Acta 1597, 292-300
43. Zhang, W., Shi, Q., Meroueh, S. O., Vakulenko, S. B., and Mobashery, S. (2007) Catalytic mechanism of penicillin-binding protein 5 of Escherichia coli Biochemistry 46, 10113-10121
44. Adediran, S. A. and Pratt, R. F. (1999) δ-Secondary and solvent deuterium isotope effects on catalysis by the Streptomyces R61 dd -peptidase: comparisons with a structurally similar class C δ-lactamase Biochemistry 38, 1469-1477
45. Page, M. I., Vilanova, B., and Layland, N. J. (1995) pH dependence of and kinetic solvent isotope effects on the methanolysis and hydrolysis of β-lactams catalyzed by class C δ-lactamase J. Am. Chem. Soc. 117, 12092-12095
46. Korat, B., Mottl, H., and Keck, W. (1991) Penicillin-binding protein 4 of Escherichia coli: molecular cloning of the dac B gene, controlled overexpression, and alterations in murein composition Mol. Microbiol. 5, 675-684
47. Duez, C., Zervosen, A., Teller, N., Melkonian, R., Banzubazé, E., Bouillenne, F., Luxen, A., and Frère, J.-M. (2009) Characterization of the proteins encoded by the Bacillus subtilis yoxA-dacC operon FEMS Microbiol. Lett. 300, 42-47