Crystal structures of penicillin-binding protein 3 (PBP3) from methicillin-resistant staphylococcus aureus in the Apo and cefotaxime-bound forms

Journal of Molecular Biology

Volumn 423, Issue 3, 2012, Pages 351-364

  Yoshida, Hisashi ^a   Kawai, Fumihiro ^a,c   Obayashi, Eiji ^a,d   Akashi, Satoko ^a   Roper, David I ^b   Tame, Jeremy R H ^a   Park, Sam Yong ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c University of Houston   (United States)

^d SHIMANE UNIVERSITY FACULTY OF MEDICINE   (Japan)

Author keywords

analytical ultracentrifugation; antibiotic; mass spectrometry; MRSA; protein complex

Indexed keywords

AMINO TERMINAL TELOPEPTIDE; CARBOXY TERMINAL TELOPEPTIDE; CEFOTAXIME; DIMER; GAMMA GLUTAMYLTRANSFERASE; PENICILLIN BINDING PROTEIN; PENICILLIN BINDING PROTEIN 3; PENICILLIN DERIVATIVE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DRUG PROTEIN BINDING; ELECTROSPRAY MASS SPECTROMETRY; GENE EXPRESSION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS;

METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 84867082602     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.07.012     Document Type: Article

References (52)

1. W. Vollmer, D. Blanot, and M.A. de Pedro Peptidoglycan structure and architecture FEMS Microbiol. Rev. 32 2008 149 167
2. E. Sauvage, F. Kerff, M. Terrak, J.A. Ayala, and P. Charlier The penicillin-binding proteins: structure and role in peptidoglycan biosynthesis FEMS Microbiol. Rev. 32 2008 234 258
3. K. Ubukata, R. Nonoguchi, M. Matsuhashi, and M. Konno Expression and inducibility in Staphylococcus aureus of the mecA gene, which encodes a methicillin-resistant S. aureus-specific penicillin-binding protein J. Bacteriol. 171 1989 2882 2885
4. E.A. Morell, and D.M. Balkin Methicillin-resistant Staphylococcus aureus: a pervasive pathogen highlights the need for new antimicrobial development Yale J. Biol. Med. 83 2010 223 233
5. R. Banerjee, M. Gretes, C. Harlem, L. Basuino, and H.F. Chambers A mecA-negative strain of methicillin-resistant Staphylococcus aureus with high-level β-lactam resistance contains mutations in three genes Antimicrob. Agents Chemother. 54 2010 4900 4902
6. D.J. Tipper, and J.L. Strominger Mechanism of action of penicillins: a proposal based on their structural similarity to acyl-D-alanyl-D-alanine Proc. Natl Acad. Sci. USA 54 1965 1133 1141
7. C. Contreras-Martel, C. Dahout-Gonzalez, S. Martins Ados, M. Kotnik, and A. Dessen PBP active site flexibility as the key mechanism for β-lactam resistance in pneumococci J. Mol. Biol. 387 2009 899 909
8. C. Goffin, and J.M. Ghuysen Multimodular penicillin-binding proteins: an enigmatic family of orthologs and paralogs Microbiol. Mol. Biol. Rev. 62 1998 1079 1093
9. A.S. Ghosh, C. Chowdhury, and D.E. Nelson Physiological functions of D-alanine carboxypeptidases in Escherichia coli Trends Microbiol. 16 2008 309 317
10. G. Memmi, S.R. Filipe, M.G. Pinho, Z. Fu, and A. Cheung Staphylococcus aureus PBP4 is essential for β-lactam resistance in community-acquired methicillin-resistant strains Antimicrob. Agents Chemother. 52 2008 3955 3966
11. V. Navratna, S. Nadig, V. Sood, K. Prasad, G. Arakere, and B. Gopal Molecular basis for the role of Staphylococcus aureus penicillin binding protein 4 in antimicrobial resistance J. Bacteriol. 192 2010 134 144
12. M.G. Pinho, H. de Lencastre, and A. Tomasz Cloning, characterization, and inactivation of the gene pbpC, encoding penicillin-binding protein 3 of Staphylococcus aureus J. Bacteriol. 182 2000 1074 1079
13. C. Fraipont, S. Alexeeva, B. Wolf, R. van der Ploeg, M. Schloesser, T. den Blaauwen, and M. Nguyen-Disteche The integral membrane FtsW protein and peptidoglycan synthase PBP3 form a subcomplex in Escherichia coli Microbiology 157 2011 251 259
14. A. Piette, C. Fraipont, T. Den Blaauwen, M.E. Aarsman, S. Pastoret, and M. Nguyen-Disteche Structural determinants required to target penicillin-binding protein 3 to the septum of Escherichia coli J. Bacteriol. 186 2004 6110 6117
15. M. Nguyen-Disteche, C. Fraipont, N. Buddelmeijer, and N. Nanninga The structure and function of Escherichia coli penicillin-binding protein 3 Cell. Mol. Life Sci. 54 1998 309 316
16. N.H. Georgopapadakou, B.A. Dix, and Y.R. Mauriz Possible physiological functions of penicllin-binding proteins in Staphylococcus aureus Antimicrob. Agents Chemother. 29 1986 333 336
17. M.T. Sung, Y.T. Lai, C.Y. Huang, L.Y. Chou, H.W. Shih, and W.C. Cheng Crystal structure of the membrane-bound bifunctional transglycosylase PBP1b from Escherichia coli Proc. Natl Acad. Sci. USA 106 2009 8824 8829
18. A.J. Powell, J. Tomberg, A.M. Deacon, R.A. Nicholas, and C. Davies Crystal structures of penicillin-binding protein 2 from penicillin-susceptible and -resistant strains of Neisseria gonorrhoeae reveal an unexpectedly subtle mechanism for antibiotic resistance J. Biol. Chem. 284 2009 1202 1212
19. S. Sainsbury, L. Bird, V. Rao, S.M. Shepherd, D.I. Stuart, and W.N. Hunter Crystal structures of penicillin-binding protein 3 from Pseudomonas aeruginosa: comparison of native and antibiotic-bound forms J. Mol. Biol. 405 2011 173 184
20. S. Han, R.P. Zaniewski, E.S. Marr, B.M. Lacey, A.P. Tomaras, and A. Evdokimov Structural basis for effectiveness of siderophore-conjugated monocarbams against clinically relevant strains of Pseudomonas aeruginosa Proc. Natl Acad. Sci. USA 107 2010 22002 22007
21. C. Contreras-Martel, V. Job, A.M. Di Guilmi, T. Vernet, O. Dideberg, and A. Dessen Crystal structure of penicillin-binding protein 1a (PBP1a) reveals a mutational hotspot implicated in β-lactam resistance in Streptococcus pneumoniae J. Mol. Biol. 355 2006 684 696
22. S. Pares, N. Mouz, Y. Petillot, R. Hakenbeck, and O. Dideberg X-ray structure of Streptococcus pneumoniae PBP2x, a primary penicillin target enzyme Nat. Struct. Biol. 3 1996 284 289
23. A.L. Lovering, L.H. de Castro, D. Lim, and N.C. Strynadka Structural insight into the transglycosylation step of bacterial cell-wall biosynthesis Science 315 2007 1402 1405
24. D. Lim, and N.C. Strynadka Structural basis for the β lactam resistance of PBP2a from methicillin-resistant Staphylococcus aureus Nat. Struct. Biol. 9 2002 870 876
25. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, and N. Echols PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 213 221
26. P. Gouet, E. Courcelle, D.I. Stuart, and F. Metoz ESPript: multiple sequence alignments in PostScript Bioinformatics 15 1999 305 308
27. A.L. Lovering, L. De Castro, and N.C. Strynadka Identification of dynamic structural motifs involved in peptidoglycan glycosyltransfer J. Mol. Biol. 383 2008 167 177
28. C. Goffin, C. Fraipont, J. Ayala, M. Terrak, M. Nguyen-Disteche, and J.M. Ghuysen The non-penicillin-binding module of the tripartite penicillin-binding protein 3 of Escherichia coli is required for folding and/or stability of the penicillin-binding module and the membrane-anchoring module confers cell septation activity on the folded structure J. Bacteriol. 178 1996 5402 5409
29. M. Punta, P.C. Coggill, R.Y. Eberhardt, J. Mistry, J. Tate, and C. Boursnell The Pfam protein families database Nucleic Acids Res. 40 2012 D290 D301
30. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2256 2268
31. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
32. J.R.H. Tame Scoring functions: a view from the bench J. Comput.-Aided Mol. Des. 13 1999 99 108
33. J.R.H. Tame Scoring functions - the first 100 years J. Comput.-Aided Mol. Des. 19 2005 445 451
34. H. Kishida, S. Unzai, D.I. Roper, A. Lloyd, S.Y. Park, and J.R.H. Tame Crystal structure of penicillin binding protein 4 (dacB) from Escherichia coli, both in the native form and covalently linked to various antibiotics Biochemistry 45 2006 783 792
35. N.H. Georgopapadakou, S.A. Smith, and D.P. Bonner Penicillin-binding proteins in a Staphylococcus aureus strain resistant to specific β-lactam antibiotics Antimicrob. Agents Chemother. 22 1982 172 175
36. C. Contreras-Martel, A. Amoroso, E.C. Woon, A. Zervosen, S. Inglis, and A. Martins Structure-guided design of cell wall biosynthesis inhibitors that overcome β-lactam resistance in Staphylococcus aureus (MRSA) ACS Chem. Biol. 6 2011 943 951
37. J. Tomberg, M. Unemo, C. Davies, and R.A. Nicholas Molecular and structural analysis of mosaic variants of penicillin-binding protein 2 conferring decreased susceptibility to expanded-spectrum cephalosporins in Neisseria gonorrhoeae: role of epistatic mutations Biochemistry 49 2010 8062 8070
38. H.R. Josephine, P. Charlier, C. Davies, R.A. Nicholas, and R.F. Pratt Reactivity of penicillin-binding proteins with peptidoglycan-mimetic β-lactams: what's wrong with these enzymes? Biochemistry 45 2006 15873 15883
39. M.G.P. Page Beta-lactam antibiotics T.J. Dougherty, M.J. Pucci, Antibiotic Discovery and Development 2012 Springer Berlin, Germany
40. T.B. Clarke, F. Kawai, S.Y. Park, J.R.H. Tame, C.G. Dowson, and D.I. Roper Mutational analysis of the substrate specificity of Escherichia coli penicillin binding protein 4 Biochemistry 48 2009 2675 2683
41. R.F. Pratt Substrate specificity of bacterial DD-peptidases (penicillin-binding proteins) Cell. Mol. Life Sci. 65 2008 2138 2155
42. E. Sauvage, R. Herman, S. Petrella, C. Duez, F. Bouillenne, J.M. Frere, and P. Charlier Crystal structure of the Actinomadura R39 DD-peptidase reveals new domains in penicillin-binding proteins J. Biol. Chem. 29 2005 29
43. R.A. Nicholas, S. Krings, J. Tomberg, G. Nicola, and C. Davies Crystal structure of wild-type penicillin-binding protein 5 from Escherichia coli: implications for deacylation of the acyl-enzyme complex J. Biol. Chem. 278 2003 52826 52833
44. G. Nicola, J. Tomberg, R.F. Pratt, R.A. Nicholas, and C. Davies Crystal structures of covalent complexes of β-lactam antibiotics with Escherichia coli penicillin-binding protein 5: toward an understanding of antibiotic specificity Biochemistry 49 2010 8094 8104
45. E. Sauvage, A.J. Powell, J. Heilemann, H.R. Josephine, P. Charlier, C. Davies, and R.F. Pratt Crystal structures of complexes of bacterial dd-peptidases with peptidoglycan-mimetic ligands: the substrate specificity puzzle J. Mol. Biol. 381 2008 383 393
46. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
47. T.R. Schneider, and G.M. Sheldrick Substructure solution with SHELXD Acta Crystallogr., Sect. D: Biol. Crystallogr. 58 2002 1772 1779
48. C. Vonrhein, E. Blanc, P. Roversi, and G. Bricogne Automated structure solution with autoSHARP Methods Mol. Biol. 364 2007 215 230
49. J.-P. Abrahams, and A.G.W. Leslie Methods used in the structure determination of bovine mitochondrial F1 ATPase Acta Crystallogr., Sect. D: Biol. Crystallogr. 52 1996 30 42
50. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 486 501
51. G.N. Murshudov, A.A. Vagin, and E.J. Dodson Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 1997 240 255
52. P.H. Brown, and P. Schuck A new adaptive grid-size algorithm for the simulation of sedimentation velocity profiles in analytical ultracentrifugation Comput. Phys. Commun. 178 2008 105 120