Allosteric inhibition of VIM metallo-β-lactamases by a camelid nanobody

Biochemical Journal

Volumn 450, Issue 3, 2013, Pages 477-486

  Sohier, Jean S ^a   Laurent, Clémentine ^a   Chevigné, Andy ^b   Pardon, Els ^c,d   Srinivasan, Vasundara ^c,d   Wernery, Ulrich ^e   Lassaux, Patricia ^a   Steyaert, Jan ^c,d   Galleni, Moreno ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

^b LUXEMBOURG INSTITUTE OF HEALTH   (Luxembourg)

^c DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^e CENTRAL VETERINARY RESEARCH LABORATORY   (United Arab Emirates)

Author keywords

Allosteric inhbition; Metallo lactamase; Nanobody

Indexed keywords

METALLO BETA LACTAMASE; NANOBODY;

ALLOSTERISM; ARTICLE; ARTIODACTYLA; BINDING AFFINITY; BINDING SITE; DRUG MECHANISM; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; EPITOPE MAPPING; HYDROPHOBICITY; KINETICS; PRIORITY JOURNAL; STEADY STATE;

ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; ANIMALS; BETA-LACTAMASES; CAMELIDS, NEW WORLD; CAMELS; CATALYTIC DOMAIN; ENZYME INHIBITORS; EPITOPE MAPPING; EPITOPES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; SINGLE-DOMAIN ANTIBODIES;

EID: 84874598106     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20121305     Document Type: Article

References (52)

1. Ambler, R. P. (1980) The structure of β-lactamases. Philos. Trans. R. Soc. London Ser. B 289, 321-331
2. Galleni, M., Lamotte-Brasseur, J., Rossolini, G. M., Spencer, J., Dideberg, O. and Frere, J. M. (2001) Standard numbering scheme for class B β-lactamases. Antimicrob. Agents Chemother. 45, 660-663
3. Carfi, A., Pares, S., Duee, E., Galleni, M., Duez, C., Frere, J. M. and Dideberg, O. (1995) The 3-D structure of a zinc metallo-β-lactamase from Bacillus cereus reveals a new type of protein fold. EMBO J. 14, 4914-4921
4. Bebrone, C. (2007) Metallo-β-lactamases (classification, activity, genetic organization, structure, zinc coordination) and their superfamily. Biochem. Pharmacol. 74, 1686-1701
5. Garau, G., Garcia-Saez, I., Bebrone, C., Anne, C., Mercuri, P., Galleni, M., Frere, J. M. and Dideberg, O. (2004) Update of the standard numbering scheme for class B β-lactamases. Antimicrob. Agents Chemother. 48, 2347-2349
6. Cornaglia, G., Giamarellou, H. and Rossolini, G. M. (2011) Metallo-β-lactamases: a last frontier for β-lactams? Lancet Infect. Dis. 11, 381-393
7. Walsh, T. R., Toleman, M. A., Poirel, L. and Nordmann, P. (2005) Metallo-β-lactamases: the quiet before the storm? Clin. Microbiol. Rev. 18, 306-325
8. Bush, K. and Fisher, J. F. (2011) Epidemiological expansion, structural studies, and clinical challenges of new β-lactamases from Gram-negative bacteria. Annu. Rev. Microbiol. 65, 455-478
9. Llarrull, L. I., Tioni, M. F. and Vila, A. J. (2008) Metal content and localization during turnover in B. cereus metallo-β-lactamase. J. Am. Chem. Soc. 130, 15842-15851
10. Gonzalez, J. M., Buschiazzo, A. and Vila, A. J. (2010) Evidence of adaptability in metal coordination geometry and active-site loop conformation among B1 metallo-β-lactamases. Biochemistry 49, 7930-7938
11. Bebrone, C., Lassaux, P., Vercheval, L., Sohier, J. S., Jehaes, A., Sauvage, E. and Galleni, M. (2010) Current challenges in antimicrobial chemotherapy: focus on β-lactamase inhibition. Drugs 70, 651-679
12. Drawz, S. M. and Bonomo, R. A. (2010) Three decades of β-lactamase inhibitors. Clin. Microbiol. Rev. 23, 160-201
13. Perez-Llarena, F. J. and Bou, G. (2009) β-Lactamase inhibitors: the story so far. Curr. Med. Chem. 16, 3740-3765
14. Conrath, K. E., Lauwereys, M., Galleni, M., Matagne, A., Frere, J. M., Kinne, J., Wyns, L. and Muyldermans, S. (2001) β-Lactamase inhibitors derived from single-domain antibody fragments elicited in the camelidae. Antimicrob. Agents Chemother. 45, 2807-2812
15. Muyldermans, S., Cambillau, C. and Wyns, L. (2001) Recognition of antigens by single-domain antibody fragments: the superfluous luxury of paired domains. Trends Biochem. Sci. 26, 230-235
16. De Genst, E., Silence, K., Decanniere, K., Conrath, K., Loris, R., Kinne, J., Muyldermans, S. and Wyns, L. (2006) Molecular basis for the preferential cleft recognition by dromedary heavy-chain antibodies. Proc. Natl. Acad. Sci. U.S.A. 103, 4586-4591
17. Conrath, K., Pereira, A. S., Martins, C. E., Timoteo, C. G., Tavares, P., Spinelli, S., Kinne, J., Flaudrops, C., Cambillau, C., Muyldermans, S. et al. (2009) Camelid nanobodies raised against an integral membrane enzyme, nitric oxide reductase. Protein Sci. 18, 619-628
18. Desmyter, A., Spinelli, S., Payan, F., Lauwereys, M., Wyns, L., Muyldermans, S. and Cambillau, C. (2002) Three camelid VHH domains in complex with porcine pancreatic α-amylase. Inhibition and versatility of binding topology. J. Biol. Chem. 277, 23645-23650
19. Lauwereys, M., Arbabi Ghahroudi, M., Desmyter, A., Kinne, J., Holzer, W., De Genst, E., Wyns, L. and Muyldermans, S. (1998) Potent enzyme inhibitors derived from dromedary heavy-chain antibodies. EMBO J. 17, 3512-3520
20. Transue, T. R., De Genst, E., Ghahroudi, M. A., Wyns, L. and Muyldermans, S. (1998) Camel single-domain antibody inhibits enzyme by mimicking carbohydrate substrate. Proteins 32, 515-522
21. Barlow, J. N., Conrath, K. and Steyaert, J. (2009) Substrate-dependent modulation of enzyme activity by allosteric effector antibodies. Biochim. Biophys. Acta 1794, 1259-1268
22. Oyen, D., Srinivasan, V., Steyaert, J. and Barlow, J. N. (2011) Constraining enzyme conformational change by an antibody leads to hyperbolic inhibition. J. Mol. Biol. 407, 138-148
23. Pournaras, S., Maniati, M., Petinaki, E., Tzouvelekis, L. S., Tsakris, A., Legakis, N. J. and Maniatis, A. N. (2003) Hospital outbreak of multiple clones of Pseudomonas aeruginosa carrying the unrelated metallo-β-lactamase gene variants blaVIM-2 and blaVIM-4. J. Antimicrob. Chemother. 51, 1409-1414
24. Studier, F. W. (2005) Protein production by auto-induction in high density shaking cultures. Protein Expression Purif. 41, 207-234
25. Lassaux, P., Traore, D. A., Loisel, E., Favier, A., Docquier, J. D., Sohier, J. S., Laurent, C., Bebrone, C., Frere, J. M., Ferrer, J. L. and Galleni, M. (2011) Biochemical and structural characterization of the subclass B1 metallo-β-lactamase VIM-4. Antimicrob. Agents Chemother. 55, 1248-1255
26. Arbabi Ghahroudi, M., Desmyter, A., Wyns, L., Hamers, R. and Muyldermans, S. (1997) Selection and identification of single domain antibody fragments from camel heavy-chain antibodies. FEBS Lett. 414, 521-526
27. Chames, P., Hoogenboom, H. R. and Henderikx, P. (2002) Selection of antibodies against biotinylated antigens. Methods Mol. Biol. 178, 147-157
28. Thys, B., Schotte, L., Muyldermans, S., Wernery, U., Hassanzadeh- Ghassabeh, G. and Rombaut, B. (2010) In vitro antiviral activity of single domain antibody fragments against poliovirus. Antiviral Res. 87, 257-264
29. Muyldermans, S., Baral, T. N., Retamozzo, V. C., De Baetselier, P., De Genst, E., Kinne, J., Leonhardt, H., Magez, S., Nguyen, V. K., Revets, H. et al. (2009) Camelid immunoglobulins and nanobody technology. Vet. Immunol. Immunopathol. 128, 178-183
30. Harmsen, M. M., Ruuls, R. C., Nijman, I. J., Niewold, T. A., Frenken, L. G. and de Geus, B. (2000) Llama heavy-chain V regions consist of at least four distinct subfamilies revealing novel sequence features. Mol. Immunol. 37, 579-590
31. Yanchak, M. P., Taylor, R. A. and Crowder, M. W. (2000) Mutational analysis of metallo-β-lactamase CcrA from Bacteroides fragilis. Biochemistry 39, 11330-11339
32. Simm, A. M., Higgins, C. S., Pullan, S. T., Avison, M. B., Niumsup, P., Erdozain, O., Bennett, P. M. and Walsh, T. R. (2001) A novel metallo-β-lactamase, Mbl1b, produced by the environmental bacterium Caulobacter crescentus. FEBS Lett. 509, 350-354
33. Oelschlaeger, P., Mayo, S. L. and Pleiss, J. (2005) Impact of remote mutations on metallo-β-lactamase substrate specificity: implications for the evolution of antibiotic resistance. Protein Sci. 14, 765-774
34. Muyldermans, S. and Lauwereys, M. (1999) Unique single-domain antigen binding fragments derived from naturally occurring camel heavy-chain antibodies. J. Mol. Recognit. 12, 131-140
35. Fenton, A. W. (2008) Allostery: an illustrated definition for the 'second secret of life'. Trends Biochem. Sci. 33, 420-425
36. Kern, D. and Zuiderweg, E. R. (2003) The role of dynamics in allosteric regulation. Curr. Opin. Struct. Biol. 13, 748-757
37. Garau, G., Bebrone, C., Anne, C., Galleni, M., Frere, J. M. and Dideberg, O. (2005) A metallo-β-lactamase enzyme in action: crystal structures of the monozinc carbapenemase CphA and its complex with biapenem. J. Mol. Biol. 345, 785-795
38. McManus-Munoz, S. and Crowder, M. W. (1999) Kinetic mechanism of metallo-β-lactamase L1 from Stenotrophomonas maltophilia. Biochemistry 38, 1547-1553
39. 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
40. 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. and Vila, A. J. (2008) Trapping and characterization of a reaction intermediate in carbapenem hydrolysis by B. cereus metallo-β-lactamase. J. Am. Chem. Soc. 130, 15852-15863
41. Wang, Z., Fast, W. and Benkovic, S. J. (1999) On the mechanism of the metallo-β-lactamase from Bacteroides fragilis. Biochemistry 38, 10013-10023
42. Oelschlaeger, P. and Pleiss, J. (2007) Hydroxyl groups in the ββ sandwich of metallo-β-lactamases favor enzyme activity: Tyr218 and Ser262 pull down the lid. J. Mol. Biol. 366, 316-329
43. Tomatis, P. E., Rasia, R. M., Segovia, L. and Vila, A. J. (2005) Mimicking natural evolution in metallo-β-lactamases through second-shell ligand mutations. Proc. Natl. Acad. Sci. U.S.A. 102, 13761-13766
44. Tomatis, P. E., Fabiane, S. M., Simona, F., Carloni, P., Sutton, B. J. and Vila, A. J. (2008) Adaptive protein evolution grants organismal fitness by improving catalysis and flexibility. Proc. Natl. Acad. Sci. U.S.A. 105, 20605-20610
45. Huntley, J. J., Fast, W., Benkovic, S. J., Wright, P. E. and Dyson, H. J. (2003) Role of a solvent-exposed tryptophan in the recognition and binding of antibiotic substrates for a metallo-β-lactamase. Protein Sci. 12, 1368-1375
46. Salsbury, Jr, F. R., Crowder, M. W., Kingsmore, S. F. and Huntley, J. J. (2009) Molecular dynamic simulations of the metallo-β-lactamase from Bacteroides fragilis in the presence and absence of a tight-binding inhibitor. J. Mol. Model. 15, 133-145
47. Scrofani, S. D., Chung, J., Huntley, J. J., Benkovic, S. J., Wright, P. E. and Dyson, H. J. (1999) NMR characterization of the metallo-β-lactamase from Bacteroides fragilis and its interaction with a tight-binding inhibitor: role of an active-site loop. Biochemistry 38, 14507-14514
48. Costello, A., Periyannan, G., Yang, K. W., Crowder, M. W. and Tierney, D. L. (2006) Site-selective binding of Zn(II) to metallo-β-lactamase L1 from Stenotrophomonas maltophilia. J. Biol. Inorg. Chem. 11, 351-358
49. Breece, R. M., Hu, Z., Bennett, B., Crowder, M. W. and Tierney, D. L. (2009) Motion of the zinc ions in catalysis by a dizinc metallo-β- lactamase. J. Am. Chem. Soc. 131, 11642-11643
50. 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-β-lactamase from Stenotrophomonas maltophilia at 1.7Å resolution. J. Mol. Biol. 284, 125-136
51. Zhang, H. and Hao, Q. (2011) Crystal structure of NDM-1 reveals a common β-lactam hydrolysis mechanism. FASEB J. 25, 2574-2582
52. King, D. and Strynadka, N. (2011) Crystal structure of New Delhi metallo-β-lactamase reveals molecular basis for antibiotic resistance. Protein Sci. 20, 1484-1491