Structural and Kinetic Studies of the Potent Inhibition of Metallo-β-lactamases by 6-Phosphonomethylpyridine-2-carboxylates

Biochemistry

Volumn 57, Issue 12, 2018, Pages 1880-1892

  Hinchliffe, Philip ^a   Tanner, Carol A ^b   Krismanich, Anthony P ^b   Labbé, Geneviève ^b   Goodfellow, Valerie J ^b   Marrone, Laura ^b   Desoky, Ahmed Y ^c   Calvopiña, Karina ^a   Whittle, Emily E ^a   Zeng, Fanxing ^b   Avison, Matthew B ^a   Bols, Niels C ^b   Siemann, Stefan ^d   Spencer, James ^a   Dmitrienko, Gary I ^b  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF WATERLOO   (Canada)

^c UNIVERSITY OF HAIL   (Saudi Arabia)

^d LAURENTIAN UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; CARBOXYLATION; ENZYMES; MOLECULES; NITROGEN; PYRIDINE;

CELLULAR ACTIVITIES; CLINICAL ISOLATES; GRAM-NEGATIVE BACTERIA; MINIMUM INHIBITORY CONCENTRATION; MULTIPLE INTERACTIONS; PHOSPHONATE GROUP; POTENT INHIBITION; PYRIDINE NITROGEN;

BACTERIA;

6 PHOSPHONOMETHYLPYRIDINE 2 CARBOXYLATE DERIVATIVE; ANTIINFECTIVE AGENT; ENZYME INHIBITOR; METALLO BETA LACTAMASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BETA LACTAMASE; BETA LACTAMASE INHIBITOR;

ANIMAL CELL; ANTIBACTERIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME INHIBITION; ENZYME KINETICS; ENZYME STRUCTURE; GROWTH INHIBITION; HUMAN; HUMAN CELL; HYDROPHOBICITY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; BACTERIUM; CHEMISTRY; ENZYMOLOGY;

BACTERIA; BACTERIAL PROTEINS; BETA-LACTAMASE INHIBITORS; BETA-LACTAMASES;

EID: 85044635223     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.7b01299     Document Type: Article

References (89)

1. Bush, K. (2013) Proliferation and significance of clinically relevant beta-lactamases. Ann. N. Y. Acad. Sci. 1277, 84-90, 10.1111/nyas.12023
2. Walsh, T. R. (2010) Emerging carbapenemases: a global perspective. Int. J. Antimicrob. Agents 36 (Suppl. 3), S8-S14, 10.1016/S0924-8579(10)70004-2
3. van Duin, D., Kaye, K. S., Neuner, E. A., and Bonomo, R. A. (2013) Carbapenem-resistant Enterobacteriaceae: a review of treatment and outcomes. Diagn. Microbiol. Infect. Dis. 75, 115-120, 10.1016/j.diagmicrobio.2012.11.009
4. Karsisiotis, A. I., Damblon, C. F., and Roberts, G. C. (2014) A variety of roles for versatile zinc in metallo-beta-lactamases, Metallomics 6, 1181-1197, 10.1039/C4MT00066H
5. Fisher, J. F., Meroueh, S. O., and Mobashery, S. (2005) Bacterial resistance to beta-lactam antibiotics: compelling opportunism, compelling opportunity. Chem. Rev. 105, 395-424, 10.1021/cr030102i
6. Bush, K. (2010) Alarming beta-lactamase-mediated resistance in multidrug-resistant Enterobacteriaceae. Curr. Opin. Microbiol. 13, 558-564, 10.1016/j.mib.2010.09.006
7. Palzkill, T. (2013) Metallo-beta-lactamase structure and function. Ann. N. Y. Acad. Sci. 1277, 91-104, 10.1111/j.1749-6632.2012.06796.x
8. Galleni, M., Lamotte-Brasseur, J., Rossolini, G. M., Spencer, J., Dideberg, O., and Frère, J. M. (2001) Standard numbering scheme for class B beta-lactamases. Antimicrob. Agents Chemother. 45, 660-663, 10.1128/AAC.45.3.660-663.2001
9. Bebrone, C. (2007) Metallo-beta-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem. Pharmacol. 74, 1686-1701, 10.1016/j.bcp.2007.05.021
10. Meini, M. R., Llarrull, L. I., and Vila, A. J. (2015) Overcoming differences: The catalytic mechanism of metallo-beta-lactamases, FEBS Lett. 589, 3419-3432, 10.1016/j.febslet.2015.08.015
11. Fonseca, F., Bromley, E. H., Saavedra, M. J., Correia, A., and Spencer, J. (2011) Crystal structure of Serratia fonticola Sfh-I: activation of the nucleophile in mono-zinc metallo-beta-lactamases. J. Mol. Biol. 411, 951-959, 10.1016/j.jmb.2011.06.043
12. Bush, K. and Jacoby, G. A. (2010) Updated functional classification of beta-lactamases. Antimicrob. Agents Chemother. 54, 969-976, 10.1128/AAC.01009-09
13. Fast, W. and Sutton, L. D. (2013) Metallo-beta-lactamase: inhibitors and reporter substrates. Biochim. Biophys. Acta, Proteins Proteomics 1834, 1648-1659, 10.1016/j.bbapap.2013.04.024
14. Brem, J., van Berkel, S. S., Zollman, D., Lee, S. Y., Gileadi, O., McHugh, P. J., Walsh, T. R., McDonough, M. A., and Schofield, C. J. (2016) Structural Basis of Metallo-beta-Lactamase Inhibition by Captopril Stereoisomers. Antimicrob. Agents Chemother. 60, 142-150, 10.1128/AAC.01335-15
15. Lienard, B. M., Garau, G., Horsfall, L., Karsisiotis, A. I., Damblon, C., Lassaux, P., Papamicael, C., Roberts, G. C., Galleni, M., Dideberg, O., Frère, J. M., and Schofield, C. J. (2008) Structural basis for the broad-spectrum inhibition of metallo-beta-lactamases by thiols. Org. Biomol. Chem. 6, 2282-2294, 10.1039/b802311e
16. González, M. M., Kosmopoulou, M., Mojica, M. F., Castillo, V., Hinchliffe, P., Pettinati, I., Brem, J., Schofield, C. J., Mahler, G., Bonomo, R. A., Llarrull, L. I., Spencer, J., and Vila, A. J. (2015) Bisthiazolidines: A Substrate-Mimicking Scaffold as an Inhibitor of the NDM-1 Carbapenemase. ACS Infect. Dis. 1, 544-554, 10.1021/acsinfecdis.5b00046
17. Mojica, M. F., Mahler, S. G., Bethel, C. R., Taracila, M. A., Kosmopoulou, M., Papp-Wallace, K. M., Llarrull, L. I., Wilson, B. M., Marshall, S. H., Wallace, C. J., Villegas, M. V., Harris, M. E., Vila, A. J., Spencer, J., and Bonomo, R. A. (2015) Exploring the Role of Residue 228 in Substrate and Inhibitor Recognition by VIM Metallo-beta-lactamases. Biochemistry 54, 3183-3196, 10.1021/acs.biochem.5b00106
18. Hinchliffe, P., Gonzalez, M. M., Mojica, M. F., Gonzalez, J. M., Castillo, V., Saiz, C., Kosmopoulou, M., Tooke, C. L., Llarrull, L. I., Mahler, G., Bonomo, R. A., Vila, A. J., and Spencer, J. (2016) Cross-class metallo-beta-lactamase inhibition by bisthiazolidines reveals multiple binding modes. Proc. Natl. Acad. Sci. U. S. A. 113, E3745-3754, 10.1073/pnas.1601368113
19. Spencer, J., Read, J., Sessions, R. B., Howell, S., Blackburn, G. M., and Gamblin, S. J. (2005) Antibiotic Recognition by Binuclear Metallo-β-Lactamases Revealed by X-ray Crystallography. J. Am. Chem. Soc. 127, 14439-14444, 10.1021/ja0536062
20. Feng, H., Ding, J., Zhu, D., Liu, X., Xu, X., Zhang, Y., Zang, S., Wang, D. C., and Liu, W. (2014) Structural and mechanistic insights into NDM-1 catalyzed hydrolysis of cephalosporins. J. Am. Chem. Soc. 136, 14694-14697, 10.1021/ja508388e
21. 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., McDonough, M. A., and Schofield, C. J. (2014) Rhodanine hydrolysis leads to potent thioenolate mediated metallo-beta-lactamase inhibition. Nat. Chem. 6, 1084-1090, 10.1038/nchem.2110
22. García-Sáez, I., Hopkins, J., Papamicael, C., Franceschini, N., Amicosante, G., Rossolini, G. M., Galleni, M., Frère, J. M., and Dideberg, O. (2003) The 1.5-A structure of Chryseobacterium meningosepticum zinc beta-lactamase in complex with the inhibitor, D-captopril, J. Biol. Chem. 278, 23868-23873, 10.1074/jbc.M301062200
23. Kurosaki, H., Yamaguchi, Y., Yasuzawa, H., Jin, W., Yamagata, Y., and Arakawa, Y. (2006) Probing, inhibition, and crystallographic characterization of metallo-beta-lactamase (IMP-1) with fluorescent agents containing dansyl and thiol groups. ChemMedChem 1, 969-972, 10.1002/cmdc.200600115
24. Yamaguchi, Y., Jin, W., Matsunaga, K., Ikemizu, S., Yamagata, Y., Wachino, J., Shibata, N., Arakawa, Y., and Kurosaki, H. (2007) Crystallographic investigation of the inhibition mode of a VIM-2 metallo-beta-lactamase from Pseudomonas aeruginosa by a mercaptocarboxylate inhibitor. J. Med. Chem. 50, 6647-6653, 10.1021/jm701031n
25. Wachino, J., Yamaguchi, Y., Mori, S., Kurosaki, H., Arakawa, Y., and Shibayama, K. (2013) Structural insights into the subclass B3 metallo-beta-lactamase SMB-1 and the mode of inhibition by the common metallo-beta-lactamase inhibitor mercaptoacetate. Antimicrob. Agents Chemother. 57, 101-109, 10.1128/AAC.01264-12
26. Nauton, L., Kahn, R., Garau, G., Hernandez, J. F., and Dideberg, O. (2008) Structural insights into the design of inhibitors for the L1 metallo-beta-lactamase from Stenotrophomonas maltophilia. J. Mol. Biol. 375, 257-269, 10.1016/j.jmb.2007.10.036
27. Lassaux, P., Hamel, M., Gulea, M., Delbruck, H., Mercuri, P. S., Horsfall, L., Dehareng, D., Kupper, M., Frère, J. M., Hoffmann, K., Galleni, M., and Bebrone, C. (2010) Mercaptophosphonate compounds as broad-spectrum inhibitors of the metallo-beta-lactamases. J. Med. Chem. 53, 4862-4876, 10.1021/jm100213c
28. Toney, J. H., Cleary, K. A., Hammond, G. G., Yuan, X., May, W. J., Hutchins, S. M., Ashton, W. T., and Vanderwall, D. E. (1999) Structure-activity relationships of biphenyl tetrazoles as metallo-beta-lactamase inhibitors. Bioorg. Med. Chem. Lett. 9, 2741-2746, 10.1016/S0960-894X(99)00458-8
29. Hiraiwa, Y., Saito, J., Watanabe, T., Yamada, M., Morinaka, A., Fukushima, T., and Kudo, T. (2014) X-ray crystallographic analysis of IMP-1 metallo-beta-lactamase complexed with a 3-aminophthalic acid derivative, structure-based drug design, and synthesis of 3,6-disubstituted phthalic acid derivative inhibitors. Bioorg. Med. Chem. Lett. 24, 4891-4894, 10.1016/j.bmcl.2014.08.039
30. Horsfall, L. E., Garau, G., Lienard, B. M., Dideberg, O., Schofield, C. J., Frère, J. M., and Galleni, M. (2007) Competitive inhibitors of the CphA metallo-beta-lactamase from Aeromonas hydrophila. Antimicrob. Agents Chemother. 51, 2136-2142, 10.1128/AAC.00866-06
31. Toney, J. H., Fitzgerald, P. M., Grover-Sharma, N., Olson, S. H., May, W. J., Sundelof, J. G., Vanderwall, D. E., Cleary, K. A., Grant, S. K., Wu, J. K., Kozarich, J. W., Pompliano, D. L., and Hammond, G. G. (1998) Antibiotic sensitization using biphenyl tetrazoles as potent inhibitors of Bacteroides fragilis metallo-beta-lactamase. Chem. Biol. 5, 185-196, 10.1016/S1074-5521(98)90632-9
32. Docquier, J. D., Benvenuti, M., Calderone, V., Stoczko, M., Menciassi, N., Rossolini, G. M., and Mangani, S. (2010) High-resolution crystal structure of the subclass B3 metallo-beta-lactamase BJP-1: rational basis for substrate specificity and interaction with sulfonamides. Antimicrob. Agents Chemother. 54, 4343-4351, 10.1128/AAC.00409-10
33. Brem, J., Cain, R., Cahill, S., McDonough, M. A., Clifton, I. J., Jimenez-Castellanos, J. C., Avison, M. B., Spencer, J., Fishwick, C. W., and Schofield, C. J. (2016) Structural basis of metallo-beta-lactamase, serine-beta-lactamase and penicillin-binding protein inhibition by cyclic boronates. Nat. Commun. 7, 12406, 10.1038/ncomms12406
34. Calvopina, K., Hinchliffe, P., Brem, J., Heesom, K. J., Johnson, S., Cain, R., Lohans, C. T., Fishwick, C. W. G., Schofield, C. J., Spencer, J., and Avison, M. B. (2017) Structural/mechanistic insights into the efficacy of nonclassical beta-lactamase inhibitors against extensively drug resistant Stenotrophomonas maltophilia clinical isolates. Mol. Microbiol. 106, 492-504, 10.1111/mmi.13831
35. Jacobsen, J. A., Major Jourden, J. L., Miller, M. T., and Cohen, S. M. (2010) To bind zinc or not to bind zinc: an examination of innovative approaches to improved metalloproteinase inhibition. Biochim. Biophys. Acta, Mol. Cell Res. 1803, 72-94, 10.1016/j.bbamcr.2009.08.006
36. Temperini, C., Innocenti, A., Guerri, A., Scozzafava, A., Rusconi, S., and Supuran, C. T. (2007) Phosph(on)ate as a zinc-binding group in metalloenzyme inhibitors: X-ray crystal structure of the antiviral drug foscarnet complexed to human carbonic anhydrase I. Bioorg. Med. Chem. Lett. 17, 2210-2215, 10.1016/j.bmcl.2007.01.113
37. Tronrud, D. E., Monzingo, A. F., and Matthews, B. W. (1986) Crystallographic structural analysis of phosphoramidates as inhibitors and transition-state analogs of thermolysin. Eur. J. Biochem. 157, 261-268, 10.1111/j.1432-1033.1986.tb09664.x
38. Maveyraud, L., Pratt, R. F., and Samama, J. P. (1998) Crystal structure of an acylation transition-state analog of the TEM-1 beta-lactamase. Mechanistic implications for class A beta-lactamases. Biochemistry 37, 2622-2628, 10.1021/bi972501b
39. Chen, C. C., Rahil, J., Pratt, R. F., and Herzberg, O. (1993) Structure of a phosphonate-inhibited beta-lactamase. An analog of the tetrahedral transition state/intermediate of beta-lactam hydrolysis. J. Mol. Biol. 234, 165-178, 10.1006/jmbi.1993.1571
40. Yang, K. W., Feng, L., Yang, S. K., Aitha, M., LaCuran, A. E., Oelschlaeger, P., and Crowder, M. W. (2013) New beta-phospholactam as a carbapenem transition state analog: Synthesis of a broad-spectrum inhibitor of metallo-beta-lactamases. Bioorg. Med. Chem. Lett. 23, 5855-5859, 10.1016/j.bmcl.2013.08.098
41. Lee, M., Hesek, D., and Mobashery, S. (2005) A practical synthesis of nitrocefin, J. Org. Chem. 70, 367-369, 10.1021/jo0487395
42. Labbé, G., Krismanich, A. P., de Groot, S., Rasmusson, T., Shang, M., Brown, M. D., Dmitrienko, G. I., and Guillemette, J. G. (2012) Development of metal-chelating inhibitors for the Class II fructose 1,6-bisphosphate (FBP) aldolase. J. Inorg. Biochem. 112, 49-58, 10.1016/j.jinorgbio.2012.02.032
43. Li, G. B., Brem, J., Lesniak, R., Abboud, M. I., Lohans, C. T., Clifton, I. J., Yang, S. Y., Jimenez-Castellanos, J. C., Avison, M. B., Spencer, J., McDonough, M. A., and Schofield, C. J. (2017) Crystallographic analyses of isoquinoline complexes reveal a new mode of metallo-beta-lactamase inhibition. Chem. Commun. (Cambridge, U. K.) 53, 5806-5809, 10.1039/C7CC02394D
44. King, A. M., Reid-Yu, S. A., Wang, W., King, D. T., De Pascale, G., Strynadka, N. C., Walsh, T. R., Coombes, B. K., and Wright, G. D. (2014) Aspergillomarasmine A overcomes metallo-beta-lactamase antibiotic resistance. Nature 510, 503-506, 10.1038/nature13445
45. Crossman, L. C., Gould, V. C., Dow, J. M., Vernikos, G. S., Okazaki, A., Sebaihia, M., Saunders, D., Arrowsmith, C., Carver, T., Peters, N., Adlem, E., Kerhornou, A., Lord, A., Murphy, L., Seeger, K., Squares, R., Rutter, S., Quail, M. A., Rajandream, M.-A., Harris, D., Churcher, C., Bentley, S. D., Parkhill, J., Thomson, N. R., and Avison, M. B. (2008) The complete genome, comparative and functional analysis of Stenotrophomonas maltophiliareveals an organism heavily shielded by drug resistance determinants, Genome Biol. 9, R74, 10.1186/gb-2008-9-4-r74
46. Gould, V. C. and Avison, M. B. (2006) SmeDEF-mediated antimicrobial drug resistance in Stenotrophomonas maltophilia clinical isolates having defined phylogenetic relationships. J. Antimicrob. Chemother. 57, 1070-1076, 10.1093/jac/dkl106
47. Gould, V. C., Okazaki, A., and Avison, M. B. (2013) Coordinate hyperproduction of SmeZ and SmeJK efflux pumps extends drug resistance in Stenotrophomonas maltophilia. Antimicrob. Agents Chemother. 57, 655-657, 10.1128/AAC.01020-12
48. CLSI (2014) Performance Standards for Antimicrobial Susceptibility Testing: Twenty-fourth Informational Supplement M100-S24. Technical Report, CLSI, Wayne, PA.
49. Dayeh, V. R., Schirmer, K., Lee, L. E. J., and Bols, N. C. (2003) The use of fish-derived cell lines for investigation of environmental contaminants. In Current Protocols in Toxicology, Unit 1.5, pp 1-17, Wiley, New York.
50. Ganassin, R. C., Schirmer, K., and Bols, N. C. (2000) Methods for the use of fish cell and tissue cultures as model systems in basic and toxicology research. In The Laboratory Fish (Ostrander, G. K., Ed.) pp 631-651, Academic Press, San Diego.
51. Ullah, J. H., Walsh, T. R., Taylor, I. A., Emery, D. C., Verma, C. S., Gamblin, S. J., and Spencer, J. (1998) The crystal structure of the L1 metallo-beta-lactamase from Stenotrophomonas maltophilia at 1.7 A resolution, J. Mol. Biol. 284, 125-136, 10.1006/jmbi.1998.2148
52. van Berkel, S. S., Brem, J., Rydzik, A. M., Salimraj, R., Cain, R., Verma, A., Owens, R. J., Fishwick, C. W., Spencer, J., and Schofield, C. J. (2013) Assay platform for clinically relevant metallo-beta-lactamases. J. Med. Chem. 56, 6945-6953, 10.1021/jm400769b
53. Ghavami, A., Labbé, G., Brem, J., Goodfellow, V. J., Marrone, L., Tanner, C. A., King, D. T., Lam, M., Strynadka, N. C., Pillai, D. R., Siemann, S., Spencer, J., Schofield, C. J., and Dmitrienko, G. I. (2015) Assay for drug discovery: Synthesis and testing of nitrocefin analogues for use as beta-lactamase substrates. Anal. Biochem. 486, 75-77, 10.1016/j.ab.2015.06.032
54. Morrison, J. F. and Walsh, C. T. (2006) The behavior and significance of slow-binding enzyme inhibitors, Adv. Enzymol. Relat. Areas Mol. Biol. 61, 201-301, 10.1002/9780470123072.ch5
55. Goličnik, M. and Stojan, J. (2004) Slow-binding inhibition: A theoretical and practical course for students, Biochem. Mol. Biol. Educ. 32, 228-235, 10.1002/bmb.2004.494032040358
56. Kabsch, W. (2010) Xds. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 125-132, 10.1107/S0907444909047337
57. Evans, P. R. (2011) An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr., Sect. D: Biol. Crystallogr. 67, 282-292, 10.1107/S090744491003982X
58. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674, 10.1107/S0021889807021206
59. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 486-501, 10.1107/S0907444910007493
60. Adams, P. D., Afonine, P. V., Bunkoczi, 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., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221, 10.1107/S0907444909052925
61. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 12-21, 10.1107/S0907444909042073
62. Roll, D. M., Yang, Y., Wildey, M. J., Bush, K., and Lee, M. D. (2010) Inhibition of metallo-beta-lactamases by pyridine monothiocarboxylic acid analogs. J. Antibiot. 63, 255-257, 10.1038/ja.2010.20
63. Siemann, S., Brewer, D., Clarke, A. J., Dmitrienko, G. I., Lajoie, G., and Viswanatha, T. (2002) IMP-1 metallo-beta-lactamase: effect of chelators and assessment of metal requirement by electrospray mass spectrometry. Biochim. Biophys. Acta, Gen. Subj. 1571, 190-200, 10.1016/S0304-4165(02)00258-1
64. Chen, A. Y., Thomas, P. W., Stewart, A. C., Bergstrom, A., Cheng, Z., Miller, C., Bethel, C. R., Marshall, S. H., Credille, C. V., Riley, C. L., Page, R. C., Bonomo, R. A., Crowder, M. W., Tierney, D. L., Fast, W., and Cohen, S. M. (2017) Dipicolinic Acid Derivatives as Inhibitors of New Delhi Metallo-beta-lactamase-1. J. Med. Chem. 60, 7267-7283, 10.1021/acs.jmedchem.7b00407
65. Meini, M.-R., Llarrull, L. I., and Vila, A. J. (2014) Evolution of Metallo-β-lactamases: Trends Revealed by Natural Diversity and in vitro Evolution. Antibiotics 3, 285-316, 10.3390/antibiotics3030285
66. Copeland, R. A. (2005) Evaluation of enzyme inhibitors in drug discovery. A guide for medicinal chemists and pharmacologists. Methods Biochem. Anal. 46, 1-265, 10.1002/9781118540398
67. Siemann, S., Clarke, A. J., Viswanatha, T., and Dmitrienko, G. I. (2003) Thiols as classical and slow-binding inhibitors of IMP-1 and other binuclear metallo-beta-lactamases. Biochemistry 42, 1673-1683, 10.1021/bi027072i
68. Badarau, A., Llinas, A., Laws, A. P., Damblon, C., and Page, M. I. (2005) Inhibitors of metallo-beta-lactamase generated from beta-lactam antibiotics. Biochemistry 44, 8578-8589, 10.1021/bi050302j
69. Mondal, J., Morrone, J. A., and Berne, B. J. (2013) How hydrophobic drying forces impact the kinetics of molecular recognition. Proc. Natl. Acad. Sci. U. S. A. 110, 13277-13282, 10.1073/pnas.1312529110
70. Copeland, R. A. (2010) The dynamics of drug-target interactions: drug-target residence time and its impact on efficacy and safety. Expert Opin. Drug Discovery 5, 305-310, 10.1517/17460441003677725
71. Copeland, R. A., Pompliano, D. L., and Meek, T. D. (2006) Drug-target residence time and its implications for lead optimization. Nat. Rev. Drug Discovery 5, 730-739, 10.1038/nrd2082
72. Dahl, G. and Akerud, T. (2013) Pharmacokinetics and the drug-target residence time concept. Drug Discovery Today 18, 697-707, 10.1016/j.drudis.2013.02.010
73. Walkup, G. K., You, Z., Ross, P. L., Allen, E. K., Daryaee, F., Hale, M. R., O'Donnell, J., Ehmann, D. E., Schuck, V. J., Buurman, E. T., Choy, A. L., Hajec, L., Murphy-Benenato, K., Marone, V., Patey, S. A., Grosser, L. A., Johnstone, M., Walker, S. G., Tonge, P. J., and Fisher, S. L. (2015) Translating slow-binding inhibition kinetics into cellular and in vivo effects. Nat. Chem. Biol. 11, 416-423, 10.1038/nchembio.1796
74. Papagiannitsis, C. C., Izdebski, R., Baraniak, A., Fiett, J., Herda, M., Hrabak, J., Derde, L. P., Bonten, M. J., Carmeli, Y., Goossens, H., Hryniewicz, W., Brun-Buisson, C., and Gniadkowski, M. (2015) Survey of metallo-beta-lactamase-producing Enterobacteriaceae colonizing patients in European ICUs and rehabilitation units, 2008-11. J. Antimicrob. Chemother. 70, 1981-1988, 10.1093/jac/dkv055
75. EUCAST (2017) The European Committee on Antimicrobial Susceptibility Testing. Breakpoint tables for interpretation of MICs and zone diameters, version 7.1 (http://www.eucast.org).
76. Walsh, F. (2007) Doripenem: A new carbapenem antibiotic a review of comparative antimicrobial and bactericidal activities. Ther. Clin. Risk Manage. 3, 789-794
77. Looney, W. J., Narita, M., and Muhlemann, K. (2009) Stenotrophomonas maltophilia: an emerging opportunist human pathogen. Lancet Infect. Dis. 9, 312-323, 10.1016/S1473-3099(09)70083-0
78. Waters, V., Yau, Y., Prasad, S., Lu, A., Atenafu, E., Crandall, I., Tom, S., Tullis, E., and Ratjen, F. (2011) Stenotrophomonas maltophilia in cystic fibrosis: serologic response and effect on lung disease. Am. J. Respir. Crit. Care Med. 183, 635-640, 10.1164/rccm.201009-1392OC
79. Freedman, L. D. and Doak, G. O. (1957) The Preparation And Properties Of Phosphonic Acids, Chem. Rev. 57, 479-523, 10.1021/cr50015a003
80. Yu, H., Kuhne, R., Ebert, R. U., and Schuurmann, G. (2010) Comparative analysis of QSAR models for predicting pK(a) of organic oxygen acids and nitrogen bases from molecular structure. J. Chem. Inf. Model. 50, 1949-1960, 10.1021/ci100306k
81. Giamarellou, H. and Antoniadou, A. (2001) Antipseudomonal antibiotics. Med. Clin. North Am. 85, 19-42, 10.1016/S0025-7125(05)70303-5
82. Garuti, L., Ferranti, A., Roberti, M., Katz, E., Budriesi, R., and Chiarini, A. (1992) Synthesis and biological evaluation of some new phosphonates. Pharmazie 47, 295-297
83. Martinez, C. R. and Iverson, B. L. (2012) Rethinking the term ″pi-stacking″. Chemical Science 3, 2191-2201, 10.1039/c2sc20045g
84. Gardonio, D. and Siemann, S. (2009) Chelator-facilitated chemical modification of IMP-1 metallo-beta-lactamase and its consequences on metal binding. Biochem. Biophys. Res. Commun. 381, 107-111, 10.1016/j.bbrc.2009.02.021
85. Toney, J. H., Hammond, G. G., Fitzgerald, P. M., Sharma, N., Balkovec, J. M., Rouen, G. P., Olson, S. H., Hammond, M. L., Greenlee, M. L., and Gao, Y. D. (2001) Succinic acids as potent inhibitors of plasmid-borne IMP-1 metallo-beta-lactamase. J. Biol. Chem. 276, 31913-31918, 10.1074/jbc.M104742200
86. Payne, D. J., Hueso-Rodríguez, J. A., Boyd, H., Concha, N. O., Janson, C. A., Gilpin, M., Bateson, J. H., Cheever, C., Niconovich, N. L., Pearson, S., Rittenhouse, S., Tew, D., Díez, E., Pérez, P., de la Fuente, J., Rees, M., and Rivera-Sagredo, A. (2002) Identification of a Series of Tricyclic Natural Products as Potent Broad-Spectrum Inhibitors of Metallo-β-Lactamases. Antimicrob. Agents Chemother. 46, 1880-1886, 10.1128/AAC.46.6.1880-1886.2002
87. Costello, A., Periyannan, G., Yang, K. W., Crowder, M. W., and Tierney, D. L. (2006) Site-selective binding of Zn(II) to metallo-beta-lactamase L1 from Stenotrophomonas maltophilia. JBIC, J. Biol. Inorg. Chem. 11, 351-358, 10.1007/s00775-006-0083-z
88. Griffin, D. H., Richmond, T. K., Sanchez, C., Möller, A. J., Breece, R. M., Tierney, D. L., Bennett, B., and Crowder, M. W. (2011) Structural and kinetic studies on metallo-beta-lactamase IMP-1. Biochemistry 50, 9125-9134, 10.1021/bi200839h
89. Calvopina, K., Umland, K. D., Rydzik, A. M., Hinchliffe, P., Brem, J., Spencer, J., Schofield, C. J., and Avison, M. B. (2016) Sideromimic Modification of Lactivicin Dramatically Increases Potency against Extensively Drug-Resistant Stenotrophomonas maltophilia Clinical Isolates. Antimicrob. Agents Chemother. 60, 4170-4175, 10.1128/AAC.00371-16