Design and exploration of novel boronic acid inhibitors reveals important interactions with a clavulanic acid-resistant sulfhydryl-variable (SHV) β-lactamase

Journal of Medicinal Chemistry

Volumn 56, Issue 3, 2013, Pages 1084-1097

  Winkler, Marisa L ^a   Rodkey, Elizabeth A ^a   Taracila, Magdalena A ^a   Drawz, Sarah M ^a   Bethel, Christopher R ^b   Papp Wallace, Krisztina M ^a,b   Smith, Kerri M ^c   Xu, Yan ^c   Dwulit Smith, Jeffrey R ^a   Romagnoli, Chiara ^d   Caselli, Emilia ^d   Prati, Fabio ^d   Van Den Akker, Focco ^a   Bonomo, Robert A ^a,b  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

^c CLEVELAND STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

AMPICILLIN; BETA LACTAMASE SHV; BORONIC ACID DERIVATIVE; CLAVULANIC ACID;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; DRUG DESIGN; ESCHERICHIA COLI; HYDROGEN BOND; IMMUNOBLOTTING; NONHUMAN; PROTON TRANSPORT; X RAY CRYSTALLOGRAPHY;

EID: 84873917648     PISSN: 00222623     EISSN: 15204804     Source Type: Journal    
DOI: 10.1021/jm301490d     Document Type: Article

References (53)

1. Klevens, R. M.; Edwards, J. R.; Richards, C. L.; Horan, T. C.; Gaynes, R. P.; Pollock, D. A.; Cardo, D. M. Estimating Health Care-Associated Infections and Deaths in U.S. Hospitals, 2002 Public Health Rep. 2007, 122, 160-166
2. Drawz, S.; Bonomo, R. Three Decades of β-Lactamase Inhibitors Clin. Microbiol. Rev. 2010, 23, 160-201
3. Buynak, J. D. Cutting and Stitching: The Cross-linking of Peptidoglycan in the Assembly of the Bacterial Cell Wall ACS Chem. Biol. 2007, 2, 602-605
4. Meroueh, S. O.; Bencze, K. Z.; Hesek, D.; Lee, M.; Fisher, J. F.; Stemmler, T. L.; Mobashery, S. Three-Dmensional Structure of the Bacterial Cell Wall Peptidoglycan Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 4404-4409
5. Lakaye, B.; Dubus, A.; Lepage, S.; Groslambert, S.; Frere, J. M. When Drug Inactivation Renders the Target Irrelevant to Antibiotic Resistance: A Case Story with β-Lactams Mol. Microbiol. 1999, 31, 89-101
6. Lovering, A. L.; Safadi, S. S.; Strynadka, N. C. Structural Perspective of Peptidoglycan Biosynthesis and Assembly. Annu. Rev. Biochem. 81, 451-478.
7. Paterson, D. L.; Bonomo, R. A. Extended-Spectrum β-Lactamases: A Clinical Update Clin. Microbiol. Rev. 2005, 18, 657-686
8. Drawz, S.; Bethel, C. R.; Hujer, K. M.; Hurless, K. N.; Distler, A. M.; Caselli, E.; Prati, F.; Bonomo, R. A. The Role of a Second-Shell Residue in Modifying Substrate and Inhibitor Interactions in the SHV β-Lactamase: A Study of Ambler Position Asn276 Biochemistry 2009, 48, 4557-4566
9. Perez-Llarena, F. J.; Bou, G. β-Lactamase inhibitors: the story so far Curr. Med. Chem. 2009, 16, 3740-3765
10. Manageiro, V.; Ferreira, E.; Cougnoux, A.; Albuquerque, L.; Canica, M.; Bonnet, R. Characterization of the Inhibitor-Resistant SHV β-Lactamase SHV-107 in a Clinical Klebsiella pneumoniae Strain Coproducing GES-7 Enzyme Antimicrob. Agents Chemother. 2012, 56, 1042-1046
11. Manageiro, V.; Ferreira, E.; Albuquerque, L.; Bonnet, R.; Canica, M. Biochemical Study of a New Inhibitor-Resistant β-Lactamase, SHV-84, Produced by a Clinical Escherichia coli Strain Antimicrob. Agents Chemother. 2010, 54, 2271-2272
12. Mendonca, N.; Manageiro, V.; Robin, F.; Salgado, M. J.; Ferreira, E.; Canica, M.; Bonnet, R. The Lys234Arg Substitution in the Enzyme SHV-72 Is a Determinant for Resistance to Clavulanic Acid Inhibition Antimicrob. Agents Chemother. 2008, 52, 1806-1811
13. Prinarakis, E. E.; Miriagou, V.; Tzelepi, E.; Gazouli, M.; Tzouvelekis, L. S. Emergence of an Inhibitor-Resistant β-Lactamase (SHV-10) Derived from an SHV-5 Variant Antimicrob. Agents Chemother. 1997, 41, 838-840
14. Dubois, V.; Poirel, L.; Demarthe, F.; Aprin, C.; Coulange, L.; Minarini, L. A. R.; Bezian, M.-C.; Nordmann, P.; Quentin, C. Molecular and Biochemical Characterization of SHV-56, a Novel Inhibitor-Resistant β-Lactamase from Klebsiella pneumoniae Antimicrob. Agents Chemother. 2008, 52, 3792-3794
15. Dubois, V.; Poirel, L.; Arpin, C.; Coulange, L.; Bebear, C.; Nordmann, P.; Quentin, C. SHV-49, a Novel Inhibitor-Resistant β-Lactamase in a Clinical Isolate of Klebsiella pneumoniae Antimicrob. Agents Chemother. 2004, 48, 4466-4469
16. Sulton, D.; Pagan-Rodriguez, D.; Zhou, X.; Liu, Y.; Hujer, A. M.; Bethel, C. R.; Helfand, M. S.; Thomson, J. M.; Anderson, A. E.; Buynak, J. D.; Ng, L. M.; Bonomo, R. A. Clavulanic Acid Inactivation of SHV-1 and the Inhibitor-Resistant S130G SHV-1 β-Lactamase J. Biol. Chem. 2005, 280, 35528-35536
17. Thomson, J.; Distler, A. M.; Bonomo, R. A. Overcoming Resistance to β-Lactamase Inhibitors: Comparing Sulbactam to Novel Inhibitors against Clavulanate Resistant SHV Enzymes with Substitutions at Ambler Position 244 Biochemistry 2007, 46, 11361-11368
18. Thomson, J.; Distler, A. M.; Prati, F.; Bonomo, R. A. Probing Active Site Chemistry in SHV β-Lactamase Variants at Ambler Position 244 J. Biol. Chem. 2006, 281, 26734-26744
19. Sun, T.; Bethel, C. R.; Bonomo, R. A.; Knox, J. R. Inhibitor-Resistant Class A β-Lactamases: Consequences of the Ser130-to-Gly Mutation Seen in Apo and Tazobactam Structures of the SHV-1 Variant Biochemistry 2004, 43, 14111-14117
20. Helfand, M. S.; Taracila, M. A.; Totir, M. A.; Bonomo, R. A.; Buynak, J. D.; van den Akker, F.; Carey, P. R. Raman Crystallographic Studies of the Intermediates Formed by Ser130Gly SHV, a β-Lactamase that Confers Resistance to Clinical Inhibitors Biochemistry 2007, 46, 8689-8699
21. Helfand, M. S.; Bethel, C. R.; Hujer, A. M.; Hujer, K. M.; Anderson, V. E.; Bonomo, R. A. Understanding Resistance to β-Lactams and β-Lactamase Inhibitors in the SHV β-Lactamase: Lessons from the Mutagenesis of SER-130 J. Biol. Chem. 2003, 278, 52724-52729
22. Ambler, R. P.; Coulson, A. F. W.; Frere, J.-M.; Ghuysen, J.-M.; Joris, B.; Forsman, M.; Levesque, R. C.; Tiraby, G.; Waley, S. G. A Standard Numbering Scheme for the Class A β-lactamases Biochem. J. 1991, 276, 269-272
23. Ghuysen, J.-M. Serine β-Lactamases and Penicillin-Binding Proteins Annu. Rev. Microbiol. 1991, 45, 37-67
24. Huang, W.; Petrosino, J.; Hirsch, M.; Shenkin, P. S.; Palzkill, T. Amino acid sequence determinants of β-lactamase structure and activity J. Mol. Biol. 1996, 258, 688-703
25. Nukaga, M.; Mayama, K.; Hujer, A. M.; Bonomo, R. A.; Knox, J. R. Ultrahigh Resolution Structure of a Class A β-Lactamase: On the Mechanism and Specificity of the Extended-Spectrum SHV-2 Enzyme J. Mol. Biol. 2003, 328, 289-301
26. Thomson, J. M.; Prati, F.; Bethel, C. R.; Bonomo, R. A. Use of Novel Boronic Acid Transition State Inhibitors to Probe Substrate Affinity in SHV-Type Extended Spectrum β-Lactamases Antimicrob. Agents Chemother. 2007, 51, 1577-1579
27. Crompton, I. E.; Cuthbert, B. K.; Lowe, G.; Waley, S. G. The Inhibition of Serine β-lactamases by Specific Boronic Acids Biochem. J. 1988, 251, 453-459
28. Meroueh, S. O.; Fisher, J. F.; Schlegel, H. B.; Mobashery, S. Ab Initio QM/MM Study of Class A β-Lactamase Acylation: Dual Participation of Glu166 and Lys73 in a Concerted Base Promotion of Ser70 J. Am. Chem. Soc. 2005, 127, 15397-15407
29. Wang, X.; Minasov, G.; Shoichet, B. K. The Structural Bases of Antibiotic Resistance in the Clinically Derived Mutant β-Lactamases TEM-30, TEM-32, and TEM-34 J. Biol. Chem. 2002, 277, 32149-32156
30. Zafaralla, G.; Manavathu, E. K.; Lerner, S. A.; Mobashery, S. Elucidation of the Role of Arginine-244 in the Turnover Processes of Class A β-Lactamases Biochemistry 1992, 31, 3847-3852
31. Hujer, A. M.; Hujer, K. M.; Helfand, M. S.; Anderson, V. E.; Bonomo, R. A. Amino Acid Substitutions at Ambler Position Gly238 in the SHV-1 β-Lactamase: Exploring Sequence Requirements for Resistance to Penicillins and Cephalosporins Antimicrob. Agents Chemother. 2002, 46, 3971-3977
32. Hujer, A. M.; Bethel, C. R.; Bonomo, R. A. Antibody Mapping of the Linear Epitopes of CMY-2 and SHV-1 β-Lactamases Antimicrob. Agents Chemother. 2004, 48, 3980-3988
33. Papp-Wallace, K. M.; Taracila, M. A.; Smith, K. M.; Xu, Y.; Bonomo, R. A. Understanding the Molecular Determinants of Substrate and Inhibitor Specificities in the Carbapenemase KPC-2: Exploring the Roles of Arg220 and Glu276 Antimicrob. Agents Chemother. 2012, 56, 4428-4438
34. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically, 1st ed.; Approved Standard: Clinical and Laboratory Standards Institute: Wayne, PA, 2008.
35. Lin, S.; Thomas, M.; Shlaes, D. M.; Rudin, S. D.; Knox, J. R.; Anderson, V.; Bonomo, R. A. Kinetic Analysis of an Inhibitor-Resistant Variant of the OHIO-1 β-Lactamase, An SHV-Family Class A Enzyme Biochem. J. 1998, 333, 395-400
36. Morandi, F.; Caselli, E.; Morandi, S.; Focia, P. J.; Blazquez, J.; Shoichet, B. K.; Prati, F. Nanomolar Inhibitors of AmpC β-Lactamase J. Am. Chem. Soc. 2003, 125, 685-695
37. De Meester, F.; Joris, B.; Reckinger, G.; Bellefroid-Bourguignon, C.; Frere, J.-M.; Waley, S. G. Automated Analysis of Enzyme Inactivation Phenomena: Application to β-Lactamases and DD-Peptidases Biochem. Pharmacol. 1987, 36, 2393-2403
38. Papp-Wallace, K. M.; Taracila, M.; Wallace, C. J.; Hujer, K. M.; Bethel, C. R.; Hornick, J. M.; Bonomo, R. Elucidating the role of Trp105 in the KPC-2 β-lactamase Protein Sci. 2010, 19, 1714-1727
39. Papp-Wallace, K. M.; Taracila, M.; Hornick, J. M.; Hujer, A. M.; Hujer, K. M.; Distler, A. M.; Endimiani, A.; Bonomo, R. A. Substrate Selectivity and a Novel Role in Inhibitor Discrimination by Residue 237 in the KPC-2 β-Lactamase Antimicrob. Agents Chemother. 2010, 54, 2867-2877
40. Nagarajan, R.; Pratt, R. F. Thermodynamic Evaluation of a Covalently Bonded Transition State Analogue Inhibitor: Inhibition of β-Lactamases by Phosphonates Biochemistry 2004, 43, 9664-9673
41. Becktel, W.; Schellman, J. Protein Stability Curves Biopolymers 1987, 26, 1859-1877
42. Beadle, B. M.; McGovern, S. L.; Patera, A.; Shoichet, B. K. Functional Analyses of AmpC β-Lactamase through Differential Stability Protein Sci. 1999, 8, 1816-1824
43. Papp-Wallace, K. M.; Bethel, C. R.; Distler, A. M.; Kasuboski, C.; Taracila, M.; Bonomo, R. A. Inhibitor Resistance in the KPC-2 β-Lactamase, a Preeminent Property of This Class A β-Lactamase Antimicrob. Agents Chemother. 2010, 54, 890-897
44. Wu, G.; Robertson, D. H.; Brooks, C. L. R.; Vieth, M. Detailed Analysis of Grid-Based Molecular Docking: A Case Study of CDOCKER-A CHARMm-Based MD Docking Algorithm J. Comput. Chem. 2003, 24, 1549-1562
45. Drawz, S. M.; Taracila, M.; Caselli, E.; Prati, F.; Bonomo, R. A. Exploring Sequence Requirements for C3/C4 Carboxylate Recognition in the Pseudomonas aeruginosa Cephalosporinase: Insights into Plasticity of the AmpC β-Lactamase Protein Sci. 2011, 20, 941-958
46. Verlet, L. Computer "Experiments" on Classical Fluids. I. Thermodynamical Properties of Lennard-Jones Molecules Phys. Rev. 1967, 159, 98-103
47. Allen, M. P.; Tildesley, D. J. Periodic Boundary Conditions and Potential Truncation. In Computer Simulation of Liquids; Oxford University Press: Oxford, UK, 1987.
48. Haile, J. M. Molecular Dynamic Simulations: Elementary Methods; John Wiley & Sons: New York, 1992.
49. Eidam, O.; Romagnoli, C.; Caselli, E.; Babaoglu, K.; Teotico Pohlhaus, D.; Karpiak, J.; Bonnet, R.; Shoichet, B. K.; Prati, F. Design, Synthesis, Crystal Structures, and Antimicrobial Activity of Sulfonamide Boronic Acids as β-Lactamase Inhibitors J. Med. Chem. 2010, 53, 7852-7863
50. Otwinowski, Z.; Minor, W. [20] Processing of X-ray Diffraction Data Collected in Oscillation Mode Methods Enzymol. 1997, 276, 307-326
51. 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.; 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. 2011, 67, 235-242
52. Emsley, P.; Cowtan, K. Coot: Model-Building Tools for Molecular Graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 2126-2132
53. Shuttelkopf, A. W.; van Aalten, D. M. PRODRG: A Tool for High-Throughput Crystallography of Protein-Ligand Complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 1355-1363