Exploring the potential of boronic acids as inhibitors of OXA-24/40 β-lactamase

Protein Science

Volumn 26, Issue 3, 2017, Pages 515-526

  Werner, Josephine P ^a   Mitchell, Joshua M ^a   Taracila, Magdalena A ^b,c   Bonomo, Robert A ^b,c   Powers, Rachel A ^a  

^a GRAND VALLEY STATE UNIVERSITY   (United States)

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

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

Author keywords

boronic acid; CHDL; inhibitor; OXA; X ray structure; lactamase

Indexed keywords

AMPICILLIN; BETA LACTAM ANTIBIOTIC; BETA LACTAMASE; BETA LACTAMASE INHIBITOR; BORONIC ACID DERIVATIVE; CARBAPENEM HYDROLYZING CLASS D BETA LACTAMASE; IMIPENEM; UNCLASSIFIED DRUG; BETA-LACTAMASE OXA-24;

ANTIBIOTIC RESISTANCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; COVALENT BOND; CRYSTAL STRUCTURE; CRYSTALLIZATION; ENZYME ACTIVITY; ENZYME INACTIVATION; ENZYME INHIBITION; ESCHERICHIA COLI; HYDROGEN BOND; HYDROLYSIS; HYDROPHOBICITY; IC50; MINIMUM INHIBITORY CONCENTRATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STRUCTURE ANALYSIS; SUBSTRATE CONCENTRATION; X RAY CRYSTALLOGRAPHY; CHEMISTRY; PROTEIN DOMAIN;

BETA-LACTAMASE INHIBITORS; BETA-LACTAMASES; BORONIC ACIDS; CRYSTALLOGRAPHY, X-RAY; PROTEIN DOMAINS;

EID: 85013654812     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.3100     Document Type: Article

References (54)

1. Bonomo RA, Szabo D (2006) Mechanisms of multidrug resistance in Acinetobacter species and Pseudomonas aeruginosa. Clin Infect Dis 43 Suppl 2:S49–S56.
2. Perez F, Hujer AM, Hujer KM, Decker BK, Rather PN, Bonomo RA (2007) Global challenge of multidrug-resistant Acinetobacter baumannii. Antimicrob Agents Chemother 51:3471–3484.
3. Perez F, Endimiani A, Bonomo RA (2008) Why are we afraid of Acinetobacter baumannii? Expert Rev Anti Infect Ther 6:269–271.
4. Hujer KM, Hujer AM, Hulten EA, Bajaksouzian S, Adams JM, Donskey CJ, Ecker DJ, Massire C, Eshoo MW, Sampath R, Thomson JM, Rather PN, Craft DW, Fishbain JT, Ewell AJ, Jacobs MR, Paterson DL, Bonomo RA (2006) Analysis of antibiotic resistance genes in multidrug-resistant Acinetobacter sp. isolates from military and civilian patients treated at the Walter Reed Army Medical Center. Antimicrob Agents Chemother 50:4114–4123.
5. Bou G, Martinez-Beltran J (2000) Cloning, nucleotide sequencing, and analysis of the gene encoding an AmpC β-lactamase in Acinetobacter baumannii. Antimicrob Agents Chemother 44:428–432.
6. Poirel L, Naas T, Nordmann P (2009) Diversity, epidemiology, and genetics of class D β-lactamases. Antimicrob Agents Chemother 54:24–38.
7. Bush K, Jacoby GA (2010) Updated functional classification of β-lactamases. Antimicrob Agents Chemother 54:969–976.
8. Paton R, Miles RS, Hood J, Amyes SG (1993) ARI 1: β-lactamase-mediated imipenem resistance in Acinetobacter baumannii. Int J Antimicrob Agents 2:81–87.
9. Hujer KM, Hamza NS, Hujer AM, Perez F, Helfand MS, Bethel CR, Thomson JM, Anderson VE, Barlow M, Rice LB, Tenover FC, Bonomo RA (2005) Identification of a new allelic variant of the Acinetobacter baumannii cephalosporinase, ADC-7 β-lactamase: defining a unique family of class C enzymes. Antimicrob Agents Chemother 49:2941–2948.
10. Drawz SM, Bonomo RA (2010) Three decades of β-lactamase inhibitors. Clin Microbiol Rev 23:160–201.
11. Page MG (2000) β Lactamase inhibitors. Drug Resist Updat 3:109–125.
12. Queenan AM, Bush K (2007) Carbapenemases: the versatile β-lactamases. Clin Microbiol Rev 20:440–458.
13. Beesley T, Gascoyne N, Knott-Hunziker V, Petursson S, Waley SG, Jaurin B, Grundstrom T (1983) The inhibition of class C β-lactamases by boronic acids. Biochem J 209:229–233.
14. Adediran SA, Nukaga M, Baurin S, Frere JM, Pratt RF (2005) Inhibition of class D β-lactamases by acyl phosphates and phosphonates. Antimicrob Agents Chemother 49:4410–4412.
15. Wyrembak PN, Babaoglu K, Pelto RB, Shoichet BK, Pratt RF (2007) O-aryloxycarbonyl hydroxamates: new β-lactamase inhibitors that cross-link the active site. J Am Chem Soc 129:9548–9549.
16. Endimiani A, Choudhary Y, Bonomo RA (2009) In vitro activity of NXL104 in combination with β-lactams against Klebsiella pneumoniae isolates producing KPC carbapenemases. Antimicrob Agents Chemother 53:3599–3601.
17. Ehmann DE, Jahic H, Ross PL, Gu RF, Hu J, Kern G, Walkup GK, Fisher SL (2012) Avibactam is a covalent, reversible, non-β-lactam β-lactamase inhibitor. Proc Natl Acad Sci U S A 109:11663–11668.
18. Ehmann DE, Jahic H, Ross PL, Gu RF, Hu J, Durand-Reville TF, Lahiri S, Thresher J, Livchak S, Gao N, Palmer T, Walkup GK, Fisher SL (2013) Kinetics of avibactam inhibition against Class A, C, and D β-lactamases. J Biol Chem 288:27960–27971.
19. Griffith DC, Loutit JS, Morgan EE, Durso S, Dudley MN (2016) Phase 1 study of the safety, tolerability, and pharmacokinetics of the β-lactamase inhibitor Vaborbactam (RPX7009) in healthy adult subjects. Antimicrob Agents Chemother 60:6326–6332.
20. Ness S, Martin R, Kindler AM, Paetzel M, Gold M, Jensen SE, Jones JB, Strynadka NC (2000) Structure-based design guides the improved efficacy of deacylation transition state analogue inhibitors of TEM-1 β-lactamase. Biochemistry 39:5312–5321.
21. Morandi F, Caselli E, Morandi S, Focia PJ, Blazquez J, Shoichet BK, Prati F (2003) Nanomolar inhibitors of AmpC β-lactamase. J Am Chem Soc 125:685–695.
22. Tan Q, Ogawa AM, Painter RE, Park YW, Young K, DiNinno FP (2010) 4,7-Dichloro benzothien-2-yl sulfonylaminomethyl boronic acid: first boronic acid-derived β-lactamase inhibitor with class A, C, and D activity. Bioorg Med Chem Lett 20:2622–2624.
23. Hecker SJ, Reddy KR, Totrov M, Hirst GC, Lomovskaya O, Griffith DC, King P, Tsivkovski R, Sun D, Sabet M, Tarazi Z, Clifton MC, Atkins K, Raymond A, Potts KT, Abendroth J, Boyer SH, Loutit JS, Morgan EE, Durso S, Dudley MN (2015) Discovery of a cyclic boronic acid β-lactamase inhibitor (RPX7009) with utility vs class A serine carbapenemases. J Med Chem 58:3682–3692.
24. McKinney DC, Zhou F, Eyermann CJ, Ferguson AD, Prince DB, Breen J, Giacobbe RA, Lahiri S, Verheijen JC (2015) 4,5-Disubstituted 6-aryloxy-1,3-dihydrobenzo[c][1,2]oxaboroles are broad-spectrum serine β-lactamase inhibitors. ACS Infect Dis 1:310–316.
25. Strynadka NC, Martin R, Jensen SE, Gold M, Jones JB (1996) Structure-based design of a potent transition state analogue for TEM-1 β-lactamase. Nat Struct Biol 3:688–695.
26. Powers RA, Swanson HC, Taracila MA, Florek NW, Romagnoli C, Caselli E, Prati F, Bonomo RA, Wallar BJ (2014) Biochemical and structural analysis of inhibitors targeting the ADC-7 cephalosporinase of Acinetobacter baumannii. Biochemistry 53:7670–7679.
27. Tondi D, Venturelli A, Bonnet R, Pozzi C, Shoichet BK, Costi MP (2014) Targeting class A and C serine β-lactamases with a broad-spectrum boronic acid derivative. J Med Chem 57:5449–5458.
28. Powers RA, Shoichet BK (2002) Structure-based approach for binding site identification on AmpC β-lactamase. J Med Chem 45:3222–3234.
29. Leonard DA, Bonomo RA, Powers RA (2013) Class D β-lactamases: a reappraisal after five decades. Acc Chem Res 46:2407–2415.
30. Chen VB, Arendall WB, III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Cryst D66:12–21.
31. Eidam O, Romagnoli C, Dalmasso G, Barelier S, Caselli E, Bonnet R, Shoichet BK, Prati F (2012) Fragment-guided design of subnanomolar β-lactamase inhibitors active in vivo. Proc Natl Acad Sci U S A 109:17448–17453.
32. Usher KC, Blaszczak LC, Weston GS, Shoichet BK, Remington SJ (1998) Three-dimensional structure of AmpC β-lactamase from Escherichia coli bound to a transition-state analogue: possible implications for the oxyanion hypothesis and for inhibitor design. Biochemistry 37:16082–16092.
33. Xia Y, Cao K, Zhou Y, Alley MR, Rock F, Mohan M, Meewan M, Baker SJ, Lux S, Ding CZ, Jia G, Kully M, Plattner JJ (2011) Synthesis and SAR of novel benzoxaboroles as a new class of β-lactamase inhibitors. Bioorg Med Chem Lett 21:2533–2536.
34. Burley SK, Petsko GA (1985) Aromatic-aromatic interaction: a mechanism of protein structure stabilization. Science 229:23–28.
35. McGaughey GB, Gagne M, Rappe AK (1998) pi-Stacking interactions. Alive and well in proteins. J Biol Chem 273:15458–15463.
36. Madhusudan Makwana K, Mahalakshmi R (2015) Implications of aromatic-aromatic interactions: From protein structures to peptide models. Protein Sci 24:1920–1933.
37. Lanzarotti E, Biekofsky RR, Estrin DA, Marti MA, Turjanski AG (2011) Aromatic-aromatic interactions in proteins: beyond the dimer. J Chem Inf Model 51:1623–1633.
38. Kaitany KC, Klinger NV, June CM, Ramey ME, Bonomo RA, Powers RA, Leonard DA (2013) Structures of the class D carbapenemases OXA-23 and OXA-146: Mechanistic basis of activity against carbapenems, extended-spectrum cephalosporins and aztreonam. Antimicrob Agents Chemother 57:4848–4855.
39. Docquier JD, Calderone V, De Luca F, Benvenuti M, Giuliani F, Bellucci L, Tafi A, Nordmann P, Botta M, Rossolini GM, Mangani S (2009) Crystal structure of the OXA-48 β-lactamase reveals mechanistic diversity among class D carbapenemases. Chem Biol 16:540–547.
40. Smith CA, Antunes NT, Stewart NK, Frase H, Toth M, Kantardjieff KA, Vakulenko S (2015) Structural basis for enhancement of carbapenemase activity in the OXA-51 family of class D β-lactamases. ACS Chem Biol 10:1791–1796.
41. June CM, Muckenthaler TJ, Schroder EC, Klamer ZL, Wawrzak Z, Powers RA, Szarecka A, Leonard DA (2016) The structure of a doripenem-bound OXA-51 class D β-lactamase variant with enhanced carbapenemase activity. Protein Sci 25:2152–2163.
42. Smith CA, Antunes NT, Toth M, Vakulenko SB (2014) Crystal structure of carbapenemase OXA-58 from Acinetobacter baumannii. Antimicrob Agents Chemother 58:2135–2143.
43. June CM, Muckenthaler TJ, Schroder EC, Klamer ZL, Wawrzak Z, Powers RA, Szarecka A, Leonard DA (2016) The structure of a doripenem-bound OXA-51 class D β-lactamase variant with enhanced carbapenemase activity. Protein Sci 25:2152–2163.
44. Schneider KD, Ortega CJ, Renck NA, Bonomo RA, Powers RA, Leonard DA (2011) Structures of the class D carbapenemase OXA-24 from Acinetobacter baumannii in complex with doripenem. J Mol Biol 406:583–594.
45. Cheng Y, Prusoff WH (1973) Relationship between the inhibition constant (KI) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharmacol 22:3099–3108.
46. Vonrhein C, Flensburg C, Keller P, Sharff A, Smart O, Paciorek W, Womack T, Bricogne G (2011) Data processing and analysis with the autoPROC toolbox. Acta Cryst D67:293–302.
47. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ (2007) Phaser crystallographic software. J Appl Cryst 40:658–674.
48. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Cryst D53:240–255.
49. Winn MD, Ballard CC, Cowtan KD, Dodson EJ, Emsley P, Evans PR, Keegan RM, Krissinel EB, Leslie AG, McCoy A, McNicholas SJ, Murshudov GN, Pannu NS, Potterton EA, Powell HR, Read RJ, Vagin A, Wilson KS (2011) Overview of the CCP4 suite and current developments. Acta Cryst D67:235–242.
50. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Cryst D66:486–501.
51. Joosten RP, Joosten K, Murshudov GN, Perrakis A (2012) PDB_REDO: constructive validation, more than just looking for errors. Acta Cryst D68:484–496.
52. Joosten RP, Long F, Murshudov GN, Perrakis A (2014) The PDB_REDO server for macromolecular structure model optimization. IUCrJ 1:213–220.
53. National Committee for Clinical Laboratory Standards. (1997). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved Standard M7-A4, Villanova, PA.
54. Schrodinger LLC (2010) The PyMOL Molecular Graphics System, Version 1.3r1.