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Crystal structure of the Bacillus subtilis penicillin-binding protein 4a, and its complex with a peptidoglycan mimetic peptide.

Sauvage E, Duez C, Herman R, Kerff F, Petrella S, Anderson JW, Adediran SA, Pratt RF, Frère JM, Charlier P
J Mol Biol 371 528-39 (2007)
Cited: 29 times
EuropePMC logo PMID: 17582436

Abstract

The genome of Bacillus subtilis encodes 16 penicillin-binding proteins (PBPs) involved in the synthesis and/or remodelling of the peptidoglycan during the complex life cycle of this sporulating Gram-positive rod-shaped bacterium. PBP4a (encoded by the dacC gene) is a low-molecular mass PBP clearly exhibiting in vitro DD-carboxypeptidase activity. We have solved the crystal structure of this protein alone and in complex with a peptide (D-alpha-aminopymelyl-epsilon-D-alanyl-D-alanine) that mimics the C-terminal end of the Bacillus peptidoglycan stem peptide. PBP4a is composed of three domains: the penicillin-binding domain with a fold similar to the class A beta-lactamase structure and two domains inserted between the conserved motifs 1 and 2 characteristic of the penicillin-recognizing enzymes. The soaking of PBP4a in a solution of D-alpha-aminopymelyl-epsilon-D-alanyl-D-alanine resulted in an adduct between PBP4a and a D-alpha-aminopimelyl-epsilon-D-alanine dipeptide and an unbound D-alanine, i.e. the products of acylation of PBP4a by D-alpha-aminopymelyl-epsilon-D-alanyl-D-alanine with the release of a D-alanine. The adduct also reveals a binding pocket specific to the diaminopimelic acid, the third residue of the peptidoglycan stem pentapeptide of B. subtilis. This pocket is specific for this class of PBPs.

Reviews - 2j9p mentioned but not cited (1)

  1. Structural Insights for β-Lactam Antibiotics. Kim D, Kim S, Kwon Y, Kim Y, Park H, Kwak K, Lee H, Lee JH, Jang KM, Kim D, Lee SH, Kang LW. Biomol Ther (Seoul) 31 141-147 (2023)

Articles - 2j9p mentioned but not cited (6)

  1. ZBTB7A mutations in acute myeloid leukaemia with t(8;21) translocation. Hartmann L, Dutta S, Opatz S, Vosberg S, Reiter K, Leubolt G, Metzeler KH, Herold T, Bamopoulos SA, Bräundl K, Zellmeier E, Ksienzyk B, Konstandin NP, Schneider S, Hopfner KP, Graf A, Krebs S, Blum H, Middeke JM, Stölzel F, Thiede C, Wolf S, Bohlander SK, Preiss C, Chen-Wichmann L, Wichmann C, Sauerland MC, Büchner T, Berdel WE, Wörmann BJ, Braess J, Hiddemann W, Spiekermann K, Greif PA. Nat Commun 7 11733 (2016)
  2. Investigation of the mechanism of the cell wall DD-carboxypeptidase reaction of penicillin-binding protein 5 of Escherichia coli by quantum mechanics/molecular mechanics calculations. Shi Q, Meroueh SO, Fisher JF, Mobashery S. J Am Chem Soc 130 9293-9303 (2008)
  3. In vivo functional and molecular characterization of the Penicillin-Binding Protein 4 (DacB) of Pseudomonas aeruginosa. Aguilera Rossi CG, Gómez-Puertas P, Ayala Serrano JA. BMC Microbiol 16 234 (2016)
  4. Subfamily-specific adaptations in the structures of two penicillin-binding proteins from Mycobacterium tuberculosis. Prigozhin DM, Krieger IV, Huizar JP, Mavrici D, Waldo GS, Hung LW, Sacchettini JC, Terwilliger TC, Alber T. PLoS One 9 e116249 (2014)
  5. Synthesis and biological evaluation of the progenitor of a new class of cephalosporin analogues, with a particular focus on structure-based computational analysis. Verdino A, Vigliotta G, Giordano D, Caputo I, Soriente A, De Rosa M, Marabotti A. PLoS One 12 e0181563 (2017)
  6. Comparative Modeling and Analysis of Extremophilic D-Ala-D-Ala Carboxypeptidases. Diessner EM, Takahashi GR, Martin RW, Butts CT. Biomolecules 13 328 (2023)


Reviews citing this publication (7)

  1. The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis. Sauvage E, Kerff F, Terrak M, Ayala JA, Charlier P. FEMS Microbiol Rev 32 234-258 (2008)
  2. Bacterial peptidoglycan (murein) hydrolases. Vollmer W, Joris B, Charlier P, Foster S. FEMS Microbiol Rev 32 259-286 (2008)
  3. Bridging cell wall biosynthesis and bacterial morphogenesis. Matteï PJ, Neves D, Dessen A. Curr Opin Struct Biol 20 749-755 (2010)
  4. Chemical Reporters for Bacterial Glycans: Development and Applications. Banahene N, Kavunja HW, Swarts BM. Chem Rev 122 3336-3413 (2022)
  5. β-Lactam antibiotic targets and resistance mechanisms: from covalent inhibitors to substrates. Mora-Ochomogo M, Lohans CT. RSC Med Chem 12 1623-1639 (2021)
  6. Fortifying the wall: synthesis, regulation and degradation of bacterial peptidoglycan. Sobhanifar S, King DT, Strynadka NC. Curr Opin Struct Biol 23 695-703 (2013)
  7. Penicillin-binding proteins: evergreen drug targets. Frère JM, Page MG. Curr Opin Pharmacol 18 112-119 (2014)

Articles citing this publication (15)

  1. Specialized peptidoglycan hydrolases sculpt the intra-bacterial niche of predatory Bdellovibrio and increase population fitness. Lerner TR, Lovering AL, Bui NK, Uchida K, Aizawa S, Vollmer W, Sockett RE. PLoS Pathog 8 e1002524 (2012)
  2. Crystal structure of cefditoren complexed with Streptococcus pneumoniae penicillin-binding protein 2X: structural basis for its high antimicrobial activity. Yamada M, Watanabe T, Miyara T, Baba N, Saito J, Takeuchi Y, Ohsawa F. Antimicrob Agents Chemother 51 3902-3907 (2007)
  3. Secreted-protein response to sigmaU activity in Streptomyces coelicolor. Gordon ND, Ottaviano GL, Connell SE, Tobkin GV, Son CH, Shterental S, Gehring AM. J Bacteriol 190 894-904 (2008)
  4. An Activity-Based Probe for Studying Crosslinking in Live Bacteria. Gautam S, Kim T, Shoda T, Sen S, Deep D, Luthra R, Ferreira MT, Pinho MG, Spiegel DA. Angew Chem Int Ed Engl 54 10492-10496 (2015)
  5. Crystal structures of complexes of bacterial DD-peptidases with peptidoglycan-mimetic ligands: the substrate specificity puzzle. Sauvage E, Powell AJ, Heilemann J, Josephine HR, Charlier P, Davies C, Pratt RF. J Mol Biol 381 383-393 (2008)
  6. Identification and characterization of a novel serine protease, VvpS, that contains two functional domains and is essential for autolysis of Vibrio vulnificus. Lim MS, Kim JA, Lim JG, Kim BS, Jeong KC, Lee KH, Choi SH. J Bacteriol 193 3722-3732 (2011)
  7. A computational evaluation of the mechanism of penicillin-binding protein-catalyzed cross-linking of the bacterial cell wall. Shi Q, Meroueh SO, Fisher JF, Mobashery S. J Am Chem Soc 133 5274-5283 (2011)
  8. Metal nitrite: a powerful oxidizing reagent. Baidya M, Yamamoto H. J Am Chem Soc 133 13880-13882 (2011)
  9. 4-quinolones as noncovalent inhibitors of high molecular mass penicillin-binding proteins. Shilabin AG, Dzhekieva L, Misra P, Jayaram B, Pratt RF. ACS Med Chem Lett 3 592-595 (2012)
  10. Trapping of an acyl-enzyme intermediate in a penicillin-binding protein (PBP)-catalyzed reaction. Macheboeuf P, Lemaire D, Teller N, Martins Ados S, Luxen A, Dideberg O, Jamin M, Dessen A. J Mol Biol 376 405-413 (2008)
  11. Inhibition of DD-peptidases by a specific trifluoroketone: crystal structure of a complex with the Actinomadura R39 DD-peptidase. Dzhekieva L, Adediran SA, Herman R, Kerff F, Duez C, Charlier P, Sauvage E, Pratt RF. Biochemistry 52 2128-2138 (2013)
  12. A Lysine Cluster in Domain II of Bacillus subtilis PBP4a Plays a Role in the Membrane Attachment of This C1-PBP. Vanden Broeck A, Van der Heiden E, Sauvage E, Dauvin M, Joris B, Duez C. PLoS One 10 e0140082 (2015)
  13. Biochemical and crystallographic studies of L,D-transpeptidase 2 from Mycobacterium tuberculosis with its natural monomer substrate. de Munnik M, Lang PA, Calvopiña K, Rabe P, Brem J, Schofield CJ. Commun Biol 7 1173 (2024)
  14. Proteomic analysis and optimized production of Alkalihalobacillus patagoniensis PAT 05T extracellular proteases. Olivera NL, Sequeiros C, Iglesias M, Nievas M. Bioprocess Biosyst Eng 44 225-234 (2021)
  15. Structural Insights into the Penicillin-Binding Protein 4 (DacB) from <i>Mycobacterium tuberculosis</i>. Kang SM, Kim DH. Int J Mol Sci 25 983 (2024)


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