Fragment-guided design of subnanomolar β-lactamase inhibitors active in vivo

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 43, 2012, Pages 17448-17453

  Eidam, Oliv ^a   Romagnoli, Chiara ^b   Dalmasso, Guillaume ^c   Barelier, Sarah ^a   Caselli, Emilia ^b   Bonnet, Richard ^c,d   Shoichet, Brian K ^a   Prati, Fabio ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^c CRNH Auvergne   (France)

^d UNIVERSITY HOSPITAL OF CLERMONT FERRAND   (France)

Author keywords

Antibiotic resistance; Antimicrobial; Boronic acid; Drug discovery; Structure based

Indexed keywords

BETA LACTAMASE AMPC; BORONIC ACID DERIVATIVE; CEFOTAXIME; CEFTAZIDIME; IMIPENEM;

ANIMAL MODEL; ANTIBIOTIC RESISTANCE; ANTIBIOTIC THERAPY; ANTIMICROBIAL ACTIVITY; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG DESIGN; DRUG STRUCTURE; DRUG SYNTHESIS; DRUG TREATMENT FAILURE; ESCHERICHIA COLI; IN VIVO STUDY; MINIMUM INHIBITORY CONCENTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANTI-BACTERIAL AGENTS; BACTERIA; BETA-LACTAMASES; DRUG DESIGN; ENZYME INHIBITORS; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; X-RAY DIFFRACTION;

EID: 84867919842     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1208337109     Document Type: Article

References (41)

1. Frere JM (1995) Beta-lactamases and bacterial resistance to antibiotics. Mol Microbiol 16:385-395.
2. Bush K (1999) Beta-lactamases of increasing clinical importance. Curr Pharm Des 5:839-845.
3. Nukaga M, Kumar S, Nukaga K, Pratt RF, Knox JR (2004) Hydrolysis of third-generation cephalosporins by class C beta-lactamases: Structures of a transition state analog of cefotaxime in wild-type and extended spectrum enzymes. J Biol Chem 279:9344-9352. (Pubitemid 38295999)
4. Fisher JF, Meroueh SO, Mobashery S (2005) Bacterial resistance to beta-lactam antibiotics: Compelling opportunism, compelling opportunity. Chem Rev 105:395-424. (Pubitemid 40351628)
5. Drawz SM, Bonomo RA (2010) Three decades of beta-lactamase inhibitors. Clin Microbiol Rev 23:160-201.
6. Caselli E, et al. (2001) Energetic, structural, and antimicrobial analyses of beta-lactam side chain recognition by beta-lactamases. Chem Biol 8:17-31. (Pubitemid 32165809)
7. Powers RA, Caselli E, Focia PJ, Prati F, Shoichet BK (2001) Structures of ceftazidime and its transition-state analogue in complex with AmpC beta-lactamase: Implications for resistance mutations and inhibitor design. Biochemistry 40:9207-9214. (Pubitemid 32730042)
8. Morandi F, et al. (2003) Nanomolar inhibitors of AmpC beta-lactamase. J Am Chem Soc 125:685-695.
9. Morandi S, Morandi F, Caselli E, Shoichet BK, Prati F (2008) Structure-based optimization of cephalothin-analogue boronic acids as beta-lactamase inhibitors. Bioorg Med Chem 16:1195-1205. (Pubitemid 351191778)
10. Wang X, et al. (2003) Recognition and resistance in TEM beta-lactamase. Biochemistry 42:8434-8444.
11. Eidam O, et al. (2010) Design, synthesis, crystal structures, and antimicrobial activity of sulfonamide boronic acids as beta-lactamase inhibitors. J Med Chem 53:7852-7863.
12. Tondi D, Morandi F, Bonnet R, Costi MP, Shoichet BK (2005) Structure-based optimization of a non-beta-lactam lead results in inhibitors that do not up-regulate betalactamase expression in cell culture. J Am Chem Soc 127:4632-4639. (Pubitemid 40489619)
13. Rees DC, Congreve M, Murray CW, Carr R (2004) Fragment-based lead discovery. Nat Rev Drug Discovery 3:660-672. (Pubitemid 39173507)
14. Murray CW, Blundell TL (2010) Structural biology in fragment-based drug design. Curr Opin Struct Biol 20:497-507.
15. Fischer M, Hubbard RE (2009) Fragment-based ligand discovery. Mol Interventions 9:22-30.
16. Ciulli A, Williams G, Smith AG, Blundell TL, Abell C (2006) Probing hot spots at protein-ligand binding sites: A fragment-based approach using biophysical methods. J Med Chem 49:4992-5000. (Pubitemid 44201057)
17. Allen KN, et al. (1996) An experimental approach to mapping the binding surfaces of crystalline proteins. J Phys Chem 100:2605-2611. (Pubitemid 126793213)
18. Landon MR, et al. (2009) Detection of ligand binding hot spots on protein surfaces via fragment-based methods: Application to DJ-1 and glucocerebrosidase. J Comput Aided Mol Des 23:491-500.
19. Hann MM, Leach AR, Harper G (2001) Molecular complexity and its impact on the probability of finding leads for drug discovery. J Chem Inf Comput Sci 41:856-864.
20. Fink T, Bruggesser H, Reymond JL (2005) Virtual exploration of the small-molecule chemical universe below 160 daltons. Angew Chem Int Ed Engl 44:1504-1508. (Pubitemid 40460043)
21. Fink T, Reymond JL (2007) Virtual exploration of the chemical universe up to 11 atoms of C, N, O, F: Assembly of 26.4 million structures (110.9 million stereoisomers) and analysis for new ring systems, stereochemistry, physicochemical properties, compound classes, and drug discovery. J Chem Inf Model 47:342-353. (Pubitemid 46615939)
22. Teotico DG, et al. (2009) Docking for fragment inhibitors of AmpC beta-lactamase. Proc Natl Acad Sci USA 106:7455-7460.
23. Babaoglu K, Shoichet BK (2006) Deconstructing fragment-based inhibitor discovery. Nat Chem Biol 2:720-723. (Pubitemid 44764214)
24. Weston GS, Blazquez J, Baquero F, Shoichet BK (1998) Structure-based enhancement of boronic acid-based inhibitors of AmpC beta-lactamase. J Med Chem 41:4577-4586. (Pubitemid 28516456)
25. Morrison JF, Walsh CT (1988) The behavior and significance of slow-binding enzyme inhibitors. Adv Enzymol Relat Areas Mol Biol 61:201-301.
26. Strynadka NC, Martin R, Jensen SE, GoldM, Jones JB (1996) Structure-based design of a potent transition state analogue for TEM-1 beta-lactamase. Nat Struct Biol 3:688-695. (Pubitemid 26260059)
27. Chen Y, Minasov G, Roth TA, Prati F, Shoichet BK (2006) The deacylation mechanism of AmpC beta-lactamase at ultrahigh resolution. J Am Chem Soc 128:2970-2976.
28. Lemke TL, Williams DA (2007) Foye's Principles of Medicinal Chemistry (Lippincott Williams & Wilkins, Philadelphia), 6th Ed.
29. Overington JP, Al-Lazikani B, Hopkins AL (2006) How many drug targets are there? Nat Rev Drug Discovery 5:993-996. (Pubitemid 44835126)
30. Pouvreau L, et al. (1998) Effect of pea and bovine trypsin inhibitors on wild-type and modified trypsins. FEBS Lett 423:167-172. (Pubitemid 28343202)
31. Del Mar EG, Largman C, Brodrick JW, Fassett M, Geokas MC (1980) Substrate specificity of human pancreatic elastase 2. Biochemistry 19:468-472. (Pubitemid 10103799)
32. Rodriguez-Martinez JA, Rivera-Rivera I, Sola RJ, Griebenow K (2009) Enzymatic activity and thermal stability of PEG-alpha-chymotrypsin conjugates. Biotechnol Lett 31:883-887.
33. Chen Y, Delmas J, Sirot J, Shoichet B, Bonnet R (2005) Atomic resolution structures of CTX-M beta-lactamases: Extended spectrum activities from increased mobility and decreased stability. J Mol Biol 348:349-362. (Pubitemid 40462101)
34. Clinical and Laboratory Standards Institute (2010) Performance standards for antimicrobial susceptibility testing. 20th Informational Supplement pp M100-S20.
35. Meanwell NA (2011) Synopsis of some recent tactical application of bioisosteres in drug design. J Med Chem 54:2529-2591.
36. Bohm HJ (1992) The computer program Ludi: A new method for the de novo design of enzyme inhibitors. J Comput Aided Mol Des 6:61-78.
37. Eisen MB, Wiley DC, Karplus M, Hubbard RE (1994) HOOK: A program for finding novel molecular architectures that satisfy the chemical and steric requirements of a macromolecule binding site. Proteins 19:199-221. (Pubitemid 24215048)
38. Bohacek RS, McMartin C (1994) Multiple highly diverse structures complementary to enzyme binding sites: Results of extensive application of a de novo design method incorporating combinatorial growth. J Am Chem Soc 116:5560-5571.
39. Joseph-McCarthy D, Hogle JM, KarplusM(1997) Use of the multiple copy simultaneous search (MCSS) method to design a new class of picornavirus capsid binding drugs. Proteins 29:32-58. (Pubitemid 27377417)
40. Barelier S, Pons J, Marcillat O, Lancelin JM, Krimm I (2010) Fragment-based deconstruction of Bcl-x(L) inhibitors. J Med Chem 53:2577-2588.
41. Kalyanaraman C, Bernacki K, Jacobson MP (2005) Virtual screening against highly charged active sites: Identifying substrates of alpha-beta barrel enzymes. Biochemistry 44:2059-2071. (Pubitemid 40223633)