Protonation states of active-site lysines of penicillin-binding protein 6 from Escherichia coli and the mechanistic implications

Proteins: Structure, Function and Bioinformatics

Volumn 82, Issue 7, 2014, Pages 1348-1358

  Kumarasiri, Malika ^a   Zhang, Weilie ^a   Shi, Qicun ^a   Fisher, Jed F ^a   Mobashery, Shahriar ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

dd carboxypeptidase; PH profile; Thermodynamic integration

Indexed keywords

BACTERIAL PROTEIN; BETA LACTAMASE TEM 1; CARBOXYPEPTIDASE TRANSPEPTIDASE; CYSTEINE; LYSINE; MUTANT PROTEIN; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 6; UNCLASSIFIED DRUG; ESCHERICHIA COLI PROTEIN; PROTON; S-2-AMINOETHYL CYSTEINE;

ACYLATION AND DEACYLATION; ARTICLE; CATALYSIS; CHEMICAL REACTION KINETICS; DEACYLATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DENATURATION; ENZYME KINETICS; ENZYME SUBSTRATE; ESCHERICHIA COLI; HYDROGEN BOND; MOLECULAR DYNAMICS; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN REFOLDING; PROTON TRANSPORT; RENATURATION; WILD TYPE; ANALOGS AND DERIVATIVES; CHEMISTRY; METABOLISM; THERMODYNAMICS;

CYSTEINE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROGEN-ION CONCENTRATION; LYSINE; MOLECULAR DYNAMICS SIMULATION; PENICILLIN-BINDING PROTEINS; PROTONS; THERMODYNAMICS;

EID: 84902107295     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24501     Document Type: Article

References (49)

1. Bobba S, Gutheil W. Multivariate geometrical analysis of catalytic residues in the penicillin-binding proteins. Int J Biochem Cell Biol 2011;43:1490-1499.
2. Dzhekieva L, Rocaboy M, Kerff F, Charlier P, Sauvage E, Pratt R. 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 2010;49:6411-6419.
3. Pratt R, McLeish M. Structural relationship between the active sites of β-lactam-recognizing and amidase signature enzymes: convergent evolution? Biochemistry 2010;49:9688-9697.
4. Golemi-Kotra D, Meroueh S, Kim C, Vakulenko S, Bulychev A, Stemmler A, Stemmler T, Mobashery S. The importance of a critical protonation state and the fate of the catalytic steps in class A β-lactamases and PBPs. J Biol Chem 2004;279:34665-34673.
5. Zhang W, Shi Q, Meroueh SO, Vakulenko SB, Mobashery S. Catalytic mechanism of penicillin-binding protein 5 of Escherichia coli. Biochemistry 2007;46:10113-10121.
6. Ammon H, Prasad S, Gerlt J. Structure of thialysine hydrochloride. Acta Crystallogr C 1991;47:1476-1478.
7. Hopkins C, Hernandez G, Lee J, Tolan D. Aminoethylation in model peptides reveals conditions for maximizing thiol specificity. Arch Biochem Biophys 2005;443:1-10.
8. Li C, Gershon PD. pKa of the mRNA cap-specific 2′-O-methyltransferase catalytic lysine by HSQC NMR detection of a two-carbon probe. Biochemistry 2006;45:907-917.
9. Timms N, Windle CL, Polyakova A, Ault JR, Trinh CH, Pearson AR, Nelson A, Berry A. Structural insights into the recovery of aldolase activity in N-acetylneuraminic acid lyase by replacement of the catalytically active lysine with γ-thialysine by using a chemical mutagenesis strategy. ChemBioChem 2013;14:474-481.
10. Yakovleva L, Shuman S. Chemical mutagenesis of vaccinia DNA topoisomerase lysine 167 provides insights to the catalysis of DNA transesterification. Biochemistry 2013;52:984-991.
11. Denome S, Elf P, Henderson T, Nelson D, Young K. Escherichia coli mutants lacking all possible combinations of eight PBPs: viability, characteristics, and implications for peptidoglycan synthesis. J Bacteriol 1999;181:3981-3993.
12. Ghosh A, Chowdhury C, Nelson D. Physiological functions of d-alanine carboxypeptidases in Escherichia coli. Trends Microbiol 2008;16:309-317.
13. Dougherty T, Kennedy K, Kessler R, Pucci M. Direct quantitation of the number of individual penicillin-binding proteins per cell in Escherichia coli. J Bacteriol 1996;178:6110-6115.
14. Nelson D, Young K. Penicillin binding protein 5 affects cell diameter, contour, and morphology of Escherichia coli. J Bacteriol 2000;182:1714-1721.
15. Ghosh A, Young K. Sequences near the active site in chimeric PBP 5 and 6 affect uniform morphology of Escherichia coli. J Bacteriol 2003;185:2178-2186.
16. Potluri L, Karczmarek A, Verheul J, Piette A, Wilkin J, Werth N, Banzhaf M, Vollmer W, Young K, Nguyen-Disteche M, den Blaauwen T. Septal and lateral wall localization of PBP5, the major d, d-carboxypeptidase of Escherichia coli, requires substrate recognition and membrane attachment. Mol Microbiol 2010;77:300-323.
17. Chowdhury C, Nayak T, Young K, Ghosh A. A weak dd-carboxypeptidase activity explains the inability of PBP 6 to substitute for PBP 5 in maintaining normal cell shape in Escherichia coli. FEMS Microbiol Lett 2010;303:76-83.
18. Laubacher ME, Melquist AL, Chandramohan L, Young KD. Cell sorting enriches Escherichia coli mutants that rely on peptidoglycan endopeptidases to suppress highly aberrant morphologies. J Bacteriol 2013;195:855-866.
19. Chowdhury C, Ghosh A. Differences in active-site microarchitecture explain the dissimilar behaviors of PBP5 and 6 in Escherichia coli. J Mol Graph Model 2011;29:650-656.
20. Chen Y, Zhang W, Shi Q, Hesek D, Lee M, Mobashery S, Shoichet B. Crystal structures of penicillin-binding protein 6 from Escherichia coli. J Am Chem Soc 2009;131:14345-14354.
21. Nicholas RA, Strominger JL. Site-directed mutants of a soluble form of penicillin-binding protein 5 from Escherichia coli and their catalytic properties. J Biol Chem 1988;263:2034-2040.
22. Gutheil WG, Stefanova ME, Nicholas RA. Fluorescent coupled enzyme assays for d-alanine: application to penicillin-binding protein and vancomycin activity assays. Anal Biochem 2000;287:196-202.
23. Tripos. Sybyl 8.1. St. Louis, MO: Tripos Inc.; 2008.
24. Warshel A, Russell S. Calculations of electrostatic interactions in biological systems and in solutions. Q Rev Biophys 1984;17:283-422.
25. Russell S, Warshel A. Calculations of electrostatic energies in proteins. The energetics of ionized groups in bovine pancreatic trypsin inhibitor. J Mol Biol 1985;185:389-404.
26. Jorgensen W, Briggs J, Gao J. A priori calculations of pKa's for organic-compounds in water-the pKa of ethane. J Am Chem Soc 1987;109:6857-6858.
27. Merz K. Determination of the pKa's of ionizable groups in proteins: the pKa of Glu-7 and Glu-35 in hen egg-white lysozyme and Glu-106 in human carbonic anhydrase-II. J Am Chem Soc 1991;113:3572-3575.
28. Thurlkill RL, Grimsley GR, Scholtz JM, Pace CN. pKa values of the ionizable groups of proteins. Protein Sci 2006;15:1214-1218.
29. Pace CN, Grimsley GR, Scholtz JM. Protein ionizable groups: pKa values and their contribution to protein stability and solubility. J Biol Chem 2009;284:13285-13289.
30. Warshel A. Computer modeling of chemical reactions in enzymes and solutions. New York: John Wiley & Sons, Inc.; 1991.
31. Simonson T, Carlsson J, Case D. Proton binding to proteins: pKa calculations with explicit and implicit solvent models. J Am Chem Soc 2004;126:4167-4180.
32. Thomas B, Wang Y, Stein RL. Kinetic and mechanistic studies of penicillin-binding protein 2x from Streptococcus pneumoniae. Biochemistry 2001;40:15811-15823.
33. Tipton K, Dixon H. Effects of pH on enzymes. Methods Enzymol 1979;63:183-234.
34. Stefanova ME, Davies C, Nicholas RA, Gutheil WG. pH, inhibitor, and substrate specificity studies on Escherichia coli penicillin-binding protein 5. Biochim Biophys Acta 2002;1597:292-300.
35. Chimenti MS, Khangulov VS, Robinson AC, Heroux A, Majumdar A, Schlessman JL, Garcia-Moreno B. Structural reorganization triggered by charging of Lys residues in the hydrophobic interior of a protein. Structure 2012;20:1071-1085.
36. Mongan J, Case DA. Biomolecular simulations at constant pH. Curr Opin Struct Biol 2005;15:157-163.
37. Warshel A, Dryga A. Simulating electrostatic energies in proteins: perspectives and some recent studies of pKas, redox, and other crucial functional properties. Proteins 2011;79:3469-3484.
38. Alexov E, Mehler EL, Baker N, Baptista AM, Huang Y, Milletti F, Nielsen JE, Farrell D, Carstensen T, Olsson MH, Shen JK, Warwicker J, Williams S, Word JM. Progress in the prediction of pKa values in proteins. Proteins 2011;79:3260-3275.
39. Nelson D, Young K. Contributions of PBP 5 and dd-carboxypeptidase PBPs to maintenance of cell shape in Escherichia coli. J Bacteriol 2001;183:3055-3064.
40. Nelson D, Ghosh A, Paulson A, Young K. Contribution of membrane-binding and enzymatic domains of PBP 5 to maintenance of uniform cellular morphology of Escherichia coli. J Bacteriol 2002;184:3630-3639.
41. Buchanan CE, Sowell MO. Synthesis of penicillin-binding protein 6 by stationary-phase Escherichia coli. J Bacteriol 1982;151:491-494.
42. Sauvage E, Powell A, Heilemann J, Josephine H, Charlier P, Davies C, Pratt R. Crystal structures of complexes of bacterial dd-peptidases with peptidoglycan-mimetic ligands: the substrate specificity puzzle. J Mol Biol 2008;381:383-393.
43. Nicola G, Fedarovich A, Nicholas R, Davies C. A large displacement of the SXN motif of Cys115-modified penicillin-binding protein 5 from Escherichia coli. Biochem J 2005;392:55-63.
44. Shi Q, Meroueh S, Fisher J, Mobashery S. Investigation of the mechanism of the cell wall dd-carboxypeptidase reaction of penicillin-binding protein 5 of Escherichia coli by QM/MM calculations. J Am Chem Soc 2008;130:9293-9303.
45. Shi Q, Fisher J, Mobashery S. Transpeptidase reaction of penicillin-binding protein 1b of Streptococcus pneumoniae and cross-linking of the cell wall. J Am Chem Soc 2011;133:5274-5283.
46. Mark B, Vocadlo D, Oliver A. Providing β-lactams a helping hand: targeting the AmpC β-lactamase induction pathway. Future Microbiol 2011;6:1415-1427.
47. Vollmer W, Blanot D, de Pedro M. Peptidoglycan structure and architecture. FEMS Microbiol Rev 2008;32:149-167.
48. Lam H, Oh D, Cava F, Takacs C, Clardy J, de Pedro M, Waldor M. d-Amino acids govern stationary phase cell wall remodeling in bacteria. Science 2009;325:1552-1555.
49. Cava F, de Pedro M, Lam H, Davis B, Waldor M. Distinct pathways for modification of the bacterial cell wall by non-canonical d-amino acids. EMBO J 2011;30:3442-3453.