A close look onto structural models and primary ligands of metallo-β-lactamases

Drug Resistance Updates

Volumn 40, Issue , 2018, Pages 1-12

  Raczynska, Joanna E ^a   Shabalin, Ivan G ^b,c   Minor, Wladek ^b,c   Wlodawer, Alexander ^d   Jaskolski, Mariusz ^a,e  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

^b UNIVERSITY OF VIRGINIA   (United States)

^c Center for Structural Genomics of Infectious Diseases   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e ADAM MICKIEWICZ UNIVERSITY   (Poland)

Author keywords

Antibiotic resistance; Data mining; Drug design target; Metal coordination; Metallo Lactamase; Model validation; New Delhi metallo lactamase (NDM); Protein Data Bank (PDB); Reproducibility; Structural databases; Structure re deposition

Indexed keywords

ANTIBIOTIC AGENT; BACTERIAL PROTEIN; CAPTOPRIL; CEFALEXIN; ETHYLENE GLYCOL; FEZ 1 PROTEIN; FROPENEM; LIGAND; METALLO BETA LACTAMASE; METALLO BETA LACTAMASE NDM 1; TIOPRONIN; UNCLASSIFIED DRUG; BETA LACTAM; BETA LACTAMASE; BETA LACTAMASE INHIBITOR; BETA-LACTAMASE NDM-1;

BACILLUS CEREUS; CRYSTAL STRUCTURE; ELECTRON; LEGIONELLA; LEGIONELLA GORMANII; MACROMOLECULE; NONHUMAN; PH; PRIORITY JOURNAL; REVIEW; STRUCTURAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; ENZYME SPECIFICITY; MEDICAL RESEARCH; MOLECULAR MODEL; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

BETA-LACTAMASE INHIBITORS; BETA-LACTAMASES; BETA-LACTAMS; BIOMEDICAL RESEARCH; CRYSTALLOGRAPHY, X-RAY; LIGANDS; MODELS, MOLECULAR; MODELS, STRUCTURAL; MOLECULAR STRUCTURE; PROTEIN CONFORMATION; SUBSTRATE SPECIFICITY;

EID: 85052652298     PISSN: 13687646     EISSN: 15322084     Source Type: Journal    
DOI: 10.1016/j.drup.2018.08.001     Document Type: Review

References (52)

1. Adams, P.D., Afonine, P.V., Bunkóczi, G., Chen, V.B., Davis, I.W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W., McCoy, A.J., Moriarty, N.W., Oeffner, R., Read, R.J., Richardson, D.C., Richardson, J.S., Terwilliger, T.C., Zwart, P.H., PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. Sect. D Biol. Crystallogr. 66 (2010), 213–221, 10.1107/S0907444909052925.
2. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E., The protein data bank. Nucleic Acids Res. 28 (2000), 235–242, 10.1093/nar/28.1.235.
3. Brem, J., van Berkel, S.S., Aik, W., Rydzik, A.M., Avison, M.B., Pettinati, I., Umland, K.-D., Kawamura, A., Spencer, J., Claridge, T.D.W., McDonough, M.A., Schofield, C.J., Rhodanine hydrolysis leads to potent thioenolate mediated metallo-β-lactamase inhibition. Nat. Chem. 6 (2014), 1084–1090, 10.1038/nchem.2110.
4. Brem, J., Van Berkel, S.S., Zollman, D., Lee, S.Y., Gileadi, O., McHugh, P.J., Walsh, T.R., McDonough, M.A., Schofield, C.J., Structural basis of metallo-β-lactamase inhibition by captopril stereoisomers. Antimicrob. Agents Chemother. 60 (2016), 142–150, 10.1128/AAC.01335-15.
5. Brünger, A.T., Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature, 355, 1992, 472.
6. Chen, V.B., Arendall, W.B., Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., Murray, L.W., Richardson, J.S., Richardson, D.C., MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 66 (2010), 12–21, 10.1107/S0907444909042073.
7. Das, C.K., Nair, N.N., Hydrolysis of cephalexin and meropenem by New Delhi metallo-β-lactamase: the substrate protonation mechanism is drug dependent. Phys. Chem. Chem. Phys. 19 (2017), 13111–13121, 10.1039/C6CP08769H.
8. Davies, J., Davies, D., Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 74 (2010), 417–433, 10.1128/MMBR.00016-10.
9. Docquier, J.-D., Mangani, S., An update on β-lactamase inhibitor discovery and development. Drug Resist. Update 36 (2018), 13–29, 10.1016/j.drup.2017.11.002.
10. Docquier, J.D., Benvenuti, M., Calderone, V., Stoczko, M., Menciassi, N., Rossolini, G.M., Mangani, S., High-resolution crystal structure of the subclass B3 metallo-β-lactamase BJP-1: rational basis for substrate specificity and interaction with sulfonamides. Antimicrob. Agents Chemother. 54 (2010), 4343–4351, 10.1128/AAC.00409-10.
11. Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of coot. Acta Crystallogr. Sect. D Biol. Crystallogr. 66 (2010), 486–501, 10.1107/S0907444910007493.
12. Faraci, W.S., Pratt, R.F., Elimination of a good leaving group from the 3’-position of a cephalosporin need not be concerted with β-lactam ring opening: TEM-2 β-lactamase-catalyzed hydrolysis of pyridine-2-azo-4’-(”,N’-dimethylaniline) cephalosporin (PADAC) and of cephaloridine. J. Am. Chem. Soc. 106 (1984), 1489–1490.
13. Feng, H., Ding, J., Zhu, D., Liu, X., Xu, X., Zhang, Y., Zang, S., Wang, D.C., Liu, W., Structural and mechanistic insights into NDM-1 catalyzed hydrolysis of cephalosporins. J. Am. Chem. Soc. 136 (2014), 14694–14697, 10.1021/ja508388e.
14. Freedman, L.P., Cockburn, I.M., Simcoe, T.S., The economics of reproducibility in preclinical research. PLoS Biol. 13 (2015), 1–9, 10.1371/journal.pbio.1002165.
15. Frère, J.-M., Sauvage, E., Kerff, F., From « an enzyme able to destroy penicillin » to carbapenemases: 70 years of β-lactamase misbehavior. Curr. Drug Targets 17 (2016), 974–982.
16. García-Sáez, I., Mercuri, P.S., Papamicael, C., Kahn, R., Frère, J.M., Galleni, M., Rossolini, G.M., Dideberg, O., Three-dimensional structure of FEZ-1, a monomeric subclass B3 metallo-β-lactamase from Fluoribacter gormanii, in native form and in complex with D-captopril. J. Mol. Biol. 325 (2003), 651–660, 10.1016/S0022-2836(02)01271-8.
17. Goto, M., Takahashi, T., Yamashita, F., Koreeda, A., Mori, H., Ohta, M., Arakawa, Y., Inhibition of the metallo-beta-lactamase produced from Serratia marcescens by thiol compounds. Biol. Pharm. Bull. 20 (1997), 1136–1140.
18. Grabowski, M., Langner, K.M., Cymborowski, M., Porebski, P.J., Sroka, P., Zheng, H., Cooper, D.R., Zimmerman, M.D., Elsliger, M.A., Burley, S.K., Minor, W., A public database of macromolecular diffraction experiments. Acta Crystallogr. Sect. D Struct. Biol. 72 (2016), 1181–1193, 10.1107/S2059798316014716.
19. Greenlee, M.L., Laub, J.B., Balkovec, J.M., Hammond, M.L., Hammond, G.G., Pompliano, D.L., Epstein-Toney, J.H., Synthesis and SAR of thioester and thiol inhibitors of IMP-1 metallo-β-lactamase. Bioorganic Med. Chem. Lett. 9 (1999), 2549–2554, 10.1016/S0960-894X(99)00425-4.
20. Jaskolski, M., On the propagation of errors. Acta Crystallogr. Sect. D Biol. Crystallogr. 69 (2013), 1865–1866, 10.1107/S090744491301528X.
21. Kim, Y., Cunningham, M.A., Mire, J., Tesar, C., Sacchettini, J., Joachimiak, A., NDM-1, the ultimate promiscuous enzyme: substrate recognition and catalytic mechanism. FASEB J. 27 (2013), 1917–1927, 10.1096/fj.12-224014.
22. King, D.T., Worrall, L.J., Gruninger, R., Strynadka, N.C.J., New Delhi Metallo-β-lactamase: structural insights into β-lactam recognition and inhibition. J. Am. Chem. Soc. 134 (2012), 11362–11365, 10.1021/ja303579d.
23. Kleywegt, G.J., Harris, M.R., Zou, J.Y., Taylor, T.C., Wählby, A., Jones, T.A., The Uppsala electron-density server. Acta Crystallogr. Sect. D Biol. Crystallogr. 60 (2004), 2240–2249, 10.1107/S0907444904013253.
24. Klingler, F.M., Wichelhaus, T.A., Frank, D., Cuesta-Bernal, J., El-Delik, J., Müller, H.F., Sjuts, H., Göttig, S., Koenigs, A., Pos, K.M., Pogoryelov, D., Proschak, E., Approved drugs containing thiols as inhibitors of metallo-β-lactamases: Strategy to combat multidrug-resistant bacteria. J. Med. Chem. 58 (2015), 3626–3630, 10.1021/jm501844d.
25. Kowiel, M., Jaskolski, M., Dauter, Z., ACHESYM: an algorithm and server for standardized placement of macromolecular models in the unit cell. Acta Crystallogr. Sect. D Biol. Crystallogr. 70 (2014), 3290–3298, 10.1107/S1399004714024572.
26. Liebschner, D., Afonine, P.V., Moriarty, N.W., Poon, B.K., Sobolev, O.V., Terwilliger, T.C., Adams, P.D., Polder maps: improving OMIT maps by excluding bulk solvent. Acta Crystallogr. Sect. D Struct. Biol. 73 (2017), 148–157, 10.1107/S2059798316018210.
27. Majorek, K.A., Kuhn, M.L., Chruszcz, M., Anderson, W.F., Minor, W., Double trouble - Buffer selection and his-tag presence may be responsible for nonreproducibility of biomedical experiments. Protein Sci. 23 (2014), 1359–1368, 10.1002/pro.2520.
28. McKenna, M., Antibiotic resistance: the last resort. Nature 499 (2013), 394–396, 10.1038/499394a.
29. Merritt, E.A., To B or not to B: a question of resolution?. Acta Crystallogr. Sect. D Biol. Crystallogr. 68 (2012), 468–477, 10.1107/S0907444911028320.
30. Minor, W., Cymborowski, M., Otwinowski, Z., Chruszcz, M., HKL-3000: the integration of data reduction and structure solution - from diffraction images to an initial model in minutes. Acta Crystallogr. Sect. D Biol. Crystallogr. 62 (2006), 859–866, 10.1107/S0907444906019949.
31. Minor, W., Dauter, Z., Helliwell, J.R., Jaskolski, M., Wlodawer, A., Safeguarding structural data repositories against bad apples. Structure 24 (2016), 216–220, 10.1016/j.str.2015.12.010.
32. Mojica, M.F., Bonomo, R.A., Fast, W., B1-metallo-β-Lactamases: where do we stand?. Curr. Drug Targets 17 (2016), 1029–1050.
33. Murshudov, G.N., Skubák, P., Lebedev, A.A., Pannu, N.S., Steiner, R.A., Nicholls, R.A., Winn, M.D., Long, F., Vagin, A.A., REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. Sect. D Biol. Crystallogr. 67 (2011), 355–367, 10.1107/S0907444911001314.
34. Naas, T., Oueslati, S., Bonnin, R.A., Dabos, M.L., Zavala, A., Dortet, L., Retailleau, P., Iorga, B.I., Beta-lactamase database (BLDB)–structure and function. J. Enzym. Inhib. Med. Chem. 32 (2017), 917–919, 10.1080/14756366.2017.1344235.
35. Otwinowski, Z., Minor, W., Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997), 307–326, 10.1016/S0076-6879(97)76066-X.
36. Painter, J., Merritt, E.A., Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr. Sect. D Biol. Crystallogr. 62 (2006), 439–450, 10.1107/S0907444906005270.
37. Porebski, P.J., Sroka, P., Zheng, H., Cooper, D.R., Minor, W., Molstack—interactive visualization tool for presentation, interpretation, and validation of macromolecules and electron density maps. Protein Sci. 27 (2018), 86–94, 10.1002/pro.3272.
38. Pozharski, E., Weichenberger, C.X., Rupp, B., Techniques, tools and best practices for ligand electron-density analysis and results from their application to deposited crystal structures. Acta Crystallogr. Sect. D Biol. Crystallogr. 69 (2013), 150–167, 10.1107/S0907444912044423.
39. Prinz, F., Schlange, T., Asadullah, K., Believe it or not: how much can we rely on published data on potential drug targets?. Nat. Rev. Drug Discov. 10 (2011), 712–713, 10.1038/nrd3439-c1.
40. Read, R.J., Adams, P.D., Arendall, W.B., Brunger, A.T., Emsley, P., Joosten, R.P., Kleywegt, G.J., Krissinel, E.B., Lütteke, T., Otwinowski, Z., Perrakis, A., Richardson, J.S., Sheffler, W.H., Smith, J.L., Tickle, I.J., Vriend, G., Zwart, P.H., A new generation of crystallographic validation tools for the Protein Data Bank. Structure 19 (2011), 1395–1412, 10.1016/j.str.2011.08.006.
41. Rupp, B., Wlodawer, A., Minor, W., Helliwell, J.R., Jaskolski, M., Correcting the record of structural publications requires joint effort of the community and journal editors. FEBS J. 283 (2016), 4452–4457, 10.1111/febs.13765.
42. Shabalin, I., Dauter, Z., Jaskolski, M., Minor, W., Wlodawer, A., Crystallography and chemistry should always go together: a cautionary tale of protein complexes with cisplatin and carboplatin. Acta Crystallogr. Sect. D Biol. Crystallogr. 71 (2015), 1965–1979, 10.1107/S139900471500629X.
43. Siemann, S., Clarke, A.J., Viswanatha, T., Dmitrienko, G.I., Thiols as classical and slow-binding inhibitors of IMP-1 and other binuclear metallo-β-lactamases. Biochemistry 42 (2003), 1673–1683, 10.1021/bi027072i.
44. Tioni, M.F., Llarrull, L.I., Poeylaut-Palena, A.A., Marti, M.A., Saggu, M., Periyannan, G.R., Mata, E.G., Bennett, B., Murgida, D.H., Vila, A.J., Trapping and characterization of a reaction intermediate in carbapenem hydrolysis by B. Cereus Metallo-β-lactamase. J. Am. Chem. Soc. 130 (2008), 15852–15863, 10.1007/s11103-011-9767-z.Plastid.
45. Walsh, T.R., Toleman, M.A., Poirel, L., Nordmann, P., Metallo-β-lactamases: the quiet before the storm?. Clin. Microbiol. Rev. 18 (2005), 306–325, 10.1128/CMR.18.2.306-325.2005.
46. Winn, M.D., Ballard, C.C., Cowtan, K.D., Dodson, E.J., Emsley, P., Evans, P.R., Keegan, R.M., Krissinel, E.B., Leslie, A.G.W., McCoy, A., McNicholas, S.J., Murshudov, G.N., Pannu, N.S., Potterton, E.A., Powell, H.R., Read, R.J., Vagin, A., Wilson, K.S., Overview of the CCP4 suite and current developments. Acta Crystallogr. Sect. D Biol. Crystallogr. 67 (2011), 235–242, 10.1107/S0907444910045749.
47. Wlodawer, A., Minor, W., Dauter, Z., Jaskolski, M., Protein crystallography for non-crystallographers, or how to get the best (but not more) from published macromolecular structures. FEBS J. 275 (2008), 1–21, 10.1111/j.1742-4658.2007.06178.x.
48. Wlodawer, A., Minor, W., Dauter, Z., Jaskolski, M., Protein crystallography for aspiring crystallographers or how to avoid pitfalls and traps in macromolecular structure determination. FEBS J. 280 (2013), 5705–5736, 10.1111/febs.12495.
49. Wlodawer, A., Dauter, Z., Porebski, P.J., Minor, W., Stanfield, R., Jaskolski, M., Pozharski, E., Weichenberger, C.X., Rupp, B., Detect, Correct, Retract: how to manage incorrect structural models. FEBS J. 285 (2018), 444–466, 10.1111/FEBS.14320.
50. World Health Organization, Prioritization of Pathogens to Guide Discovery, Research and Development of New Antibiotics for Drug-resistant Bacterial Infections, Including Tuberculosis. 2017.
51. Zheng, H., Chordia, M.D., Cooper, D.R., Chruszcz, M., Müller, P., Sheldrick, G.M., Minor, W., Validation of metal-binding sites in macromolecular structures with the CheckMyMetal web server. Nat. Protoc. 9 (2014), 156–170, 10.1038/nprot.2013.172.
52. Zheng, H., Cooper, D.R., Porebski, P.J., Shabalin, I.G., Handing, K.B., Minor, W., CheckMyMetal: a macromolecular metal-binding validation tool. Acta Crystallogr. Sect. D Struct. Biol. 73 (2017), 223–233, 10.1107/S2059798317001061.