Engineering Specificity from Broad to Narrow: Design of a β-Lactamase Inhibitory Protein (BLIP) Variant That Exclusively Binds and Detects KPC β-Lactamase

ACS Infectious Diseases

Volumn 2, Issue 12, 2016, Pages 969-979

  Chow, Dar Chone ^a   Rice, Kacie ^a   Huang, Wanzhi ^a   Atmar, Robert L ^a   Palzkill, Timothy ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

antibiotic resistance; diagnostics; enzyme inhibition; protein engineering; protein protein interactions; lactamase

Indexed keywords

BETA LACTAMASE; BETA LACTAMASE INHIBITORY PROTEIN; BETA LACTAMASE KPC 2; BETA LACTAMASE TEM 1; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BETA LACTAMASE INHIBITOR; BETA-LACTAMASE KPC-2; PROTEIN BINDING;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIUM ISOLATE; BINDING AFFINITY; DISSOCIATION RATE CONSTANT; ENZYME BINDING; ENZYME SPECIFICITY; ESCHERICHIA COLI; FEASIBILITY STUDY; GENETIC SCREENING; MOLECULAR LIBRARY; MULTIDRUG RESISTANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN EXPRESSION; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; MOLECULAR MODEL;

BACTERIAL PROTEINS; BETA-LACTAMASE INHIBITORS; BETA-LACTAMASES; ESCHERICHIA COLI; KINETICS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN ENGINEERING;

EID: 85003691647     PISSN: None     EISSN: 23738227     Source Type: Journal    
DOI: 10.1021/acsinfecdis.6b00160     Document Type: Article

References (49)

1. Bonsor, D. A. and Sundberg, E. J. (2011) Dissecting protein-protein interactions using directed evolution Biochemistry 50, 2394-2402 10.1021/bi102019c
2. Chen, T. S. and Keating, A. E. (2012) Designing specific protein-protein interactions using computation, experimental library screening, or integrated methods Protein Sci. 21, 949-963 10.1002/pro.2096
3. Schreiber, G. and Keating, A. E. (2011) Protein binding specificity versus promiscuity Curr. Opin. Struct. Biol. 21, 50-61 10.1016/j.sbi.2010.10.002
4. Collins, C. H., Leadbetter, J. R., and Arnold, F. H. (2006) Dual selection enhances the signaling specificity of a variant of the quorum-sensing transcriptional activator LuxR Nat. Biotechnol. 24, 708-712 10.1038/nbt1209
5. Dutta, S., Gulla, S., Chen, T. S., Fire, E., Grant, R. A., and Keating, A. E. (2010) Determinants of BH3 binding specificity for Mcl-1 versus Bcl-xL J. Mol. Biol. 398, 747-762 10.1016/j.jmb.2010.03.058
6. Havranek, J. J. and Harbury, P. B. (2003) Automated design of specificity in molecular recognition Nat. Struct. Biol. 10, 45-52 10.1038/nsb877
7. Levin, K. B., Dym, O., Albeck, S., Magdassi, S., Keeble, A. H., Kleanthous, C., and Tawfik, D. S. (2009) Following evolutionary paths to protein-protein interactions with high affinity and selectivity Nat. Struct. Mol. Biol. 16, 1049-1055 10.1038/nsmb.1670
8. Doran, J. L., Leskiw, B. K., Aippersbach, S., and Jensen, S. E. (1990) Isolation and characterization of a β-lactamase-inhibitory protein from Streptomyces clavuligerus and cloning and analysis of the corresponding gene J. Bacteriol. 172, 4909-4918
9. Hanes, M. S., Jude, K. M., Berger, J. M., Bonomo, R. A., and Handel, T. M. (2009) Structural and biochemical characterization of the interaction between KPC-2 beta-lactamase and beta-lactamase inhibitor protein Biochemistry 48, 9185-9193 10.1021/bi9007963
10. Strynadka, N. C. J., Jensen, S. E., Alzari, P. M., and James, M. N. G. (1996) A potent new mode of β-lactamase inhibition revealed by the 1.7Å X-ray crystallographic structure of the TEM-1-BLIP complex Nat. Struct. Biol. 3, 290-297 10.1038/nsb0396-290
11. Zhang, Z. and Palzkill, T. (2004) Dissecting the protein-protein interface between beta-lactamase inhibitory protein and class A beta-lactamases J. Biol. Chem. 279, 42860-42866 10.1074/jbc.M406157200
12. Liras, P. and Rodriguez-Garcia, A. (2000) Clavulanic acid, a beta-lactamase inhibitor: biosynthesis and molecular genetics Appl. Microbiol. Biotechnol. 54, 467-475 10.1007/s002530000420
13. Petrosino, J., Rudgers, G., Gilbert, H., and Palzkill, T. (1999) Contributions of aspartate 49 and phenylalanine 142 residues of a tight binding inhibitory protein of β-lactamases J. Biol. Chem. 274, 2394-2400 10.1074/jbc.274.4.2394
14. Reynolds, K. A., Thomson, J. M., Corbett, K. D., Bethel, C. R., Berger, J. M., Kirsch, J. F., Bonomo, R. A., and Handel, T. M. (2006) Structural and computational characterization of the SHV-1 beta-lactamase-beta-lactamase inhibitor protein interface J. Biol. Chem. 281, 26745-26753 10.1074/jbc.M603878200
15. Strynadka, N. C. J., Jensen, S. E., Johns, K., Blanchard, H., Page, M., Matagne, A., Frere, J.-M., and James, M. N. G. (1994) Structural and kinetic characterization of a β-lactamase-inhibitor protein Nature 368, 657-660 10.1038/368657a0
16. Reynolds, K. A., Hanes, M. S., Thomson, J. M., Antczak, A. J., Berger, J. M., Bonomo, R. A., Kirsch, J. F., and Handel, T. M. (2008) Computational redesign of the SHV-1 β-lactamase/β-lactamase inhibitor protein interface J. Mol. Biol. 382, 1265-1275 10.1016/j.jmb.2008.05.051
17. Yuan, J., Huang, W., Chow, D. C., and Palzkill, T. (2009) Fine mapping of the sequence requirements for binding of beta-lactamase inhibitory protein (BLIP) to TEM-1 beta-lactamase using a genetic screen for BLIP function J. Mol. Biol. 389, 401-412 10.1016/j.jmb.2009.04.028
18. Zhang, Z. and Palzkill, T. (2003) Determinants of binding affinity and specificity for the interaction of TEM-1 and SME-1 β-lactamase with β-lactamase inhibitory protein J. Biol. Chem. 278, 45706-45712 10.1074/jbc.M308572200
19. Arias, C. A. and Murray, B. E. (2009) Antibiotic-resistant bugs in the 21st century-a clinical super-challenge N. Engl. J. Med. 360, 439-443 10.1056/NEJMp0804651
20. Papp-Wallace, K. M., Endimiani, A., Taracila, M. A., and Bonomo, R. A. (2011) Carbapenems: past, present, and future Antimicrob. Agents Chemother. 55, 4943-4960 10.1128/AAC.00296-11
21. Nordmann, P., Cuzon, G., and Naas, T. (2009) The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria Lancet Infect. Dis. 9, 228-236 10.1016/S1473-3099(09)70054-4
22. Nordmann, P., Dortet, L., and Poirel, L. (2012) Carbapenem resistance in Enterobacteriaceae: here is the storm Trends Mol. Med. 18, 263-272 10.1016/j.molmed.2012.03.003
23. Yigit, H., Queenan, A. M., Anderson, G. J., Domenech-Sanchez, A., Biddle, J. W., Steward, C. D., Alberti, S., Bush, K., and Tenover, F. C. (2001) Novel carbapenem-hydrolyzing beta-lactamase, KPC-1, from a carbapenem- resistant strain of Klebsiella pneumoniae Antimicrob. Agents Chemother. 45, 1151-1161 10.1128/AAC.45.4.1151-1161.2001
24. Tzouvelekis, L. S., Markogiannakis, A., Psichogiou, M., Tassios, P. T., and Daikos, G. L. (2012) Carbapenemases in Klebsiella pneumoniae and other Enterobacteriaceae: an evolving crisis of global dimensions Clin. Microbiol. Rev. 25, 682-707 10.1128/CMR.05035-11
25. Queenan, A. M. and Bush, K. (2007) Carbapenemases: the versatile beta-lactamases Clin. Microbiol. Rev. 20, 440-458 10.1128/CMR.00001-07
26. Janin, J. (1997) The kinetics of protein-protein recognition Proteins: Struct., Funct., Genet. 28, 153-161 10.1002/(SICI)1097-0134(199706)28:2<153::AID-PROT4>3.0.CO;2-G
27. Schreiber, G., Haran, G., and Zhou, H. X. (2009) Fundamental aspects of protein-protein association kinetics Chem. Rev. 109, 839-860 10.1021/cr800373w
28. Yuan, J., Chow, D. C., Huang, W., and Palzkill, T. (2011) Identification of a beta-Lactamase Inhibitory Protein Variant That Is a Potent Inhibitor of Staphylococcus PC1 beta-Lactamase J. Mol. Biol. 406, 730-744 10.1016/j.jmb.2011.01.014
29. Reichmann, D., Rahat, O., Albeck, S., Meged, R., Dym, O., and Schreiber, G. (2005) The modular architecture of protein-protein binding interfaces Proc. Natl. Acad. Sci. U. S. A. 102, 57-62 10.1073/pnas.0407280102
30. Wells, J. A. (1990) Additivity of mutational effects in proteins Biochemistry 29, 8509-8517 10.1021/bi00489a001
31. Bernat, B., Pal, G., Sun, M., and Kossiakoff, A. A. (2003) Determination of the energetics governing the regulatory step in growth hormone-induced receptor homodimization Proc. Natl. Acad. Sci. U. S. A. 100, 952-957 10.1073/pnas.0235023100
32. Brown, N. G., Chow, D.-C., Ruprecht, K. E., and Palzkill, T. (2013) Identification of the β-lactamase inhibitor protein-II (BLIP-II) interface residues essential for binding affinity and specificity for class A β-lactamases J. Biol. Chem. 288, 17156-17166 10.1074/jbc.M113.463521
33. Joachimiak, L. A., Kortemme, T., Stoddard, B. L., and Baker, D. (2006) Computational design of a new hydrogen bond network and at least a 300-fold specificity switch at a protein-protein interface J. Mol. Biol. 361, 195-208 10.1016/j.jmb.2006.05.022
34. Kortemme, T., Joachimiak, L. A., Bullock, A. N., Schuler, A. D., Stoddard, B. L., and Baker, D. (2004) Computational redesign of protein-protein interaction specificity Nat. Struct. Mol. Biol. 11, 371-379 10.1038/nsmb749
35. Yosef, E., Politi, R., Choi, M. H., and Shifman, J. M. (2009) Computational design of calmodulin mutants with up to 900-fold increase in binding specificity J. Mol. Biol. 385, 1470-1480 10.1016/j.jmb.2008.09.053
36. Brown, N. G., Chow, D.-C., Sankaran, B., Zwart, P., Prasad, B. V., and Palzkill, T. (2011) Analysis of the binding forces driving the tight binding between β-lactamase inhibitory protein II (BLIP-II) and class A β-lactamases J. Biol. Chem. 286, 32723-32725 10.1074/jbc.M111.265058
37. Clackson, T. and Wells, J. A. (1995) A hot spot of binding energy in a hormone-receptor interface Science 267, 383-386 10.1126/science.7529940
38. Keeble, A. H., Joachimiak, L. A., Mate, M. J., Meenan, N., Kirkpatrick, N., Baker, D., and Kleanthous, C. (2008) Experimental and computational analyses of the energetic basis for dual recognition of immunity proteins by colicin endonucleases J. Mol. Biol. 379, 745-759 10.1016/j.jmb.2008.03.055
39. Li, Y., Urrutia, M., Smith-Gill, S. J., and Mariuzza, R. A. (2003) Dissection of binding interactions in the complex between the anti-lysozyme antibody HyHEL-63 and its antigen Biochemistry 42, 11-22 10.1021/bi020589+
40. Pons, J., Rajpal, A., and Kirsch, J. F. (1999) Energetic analysis of an antigen/antibody interface: alanine scanning mutagenesis and double mutant cycles on the HyHEL-10/lysozyme interaction Protein Sci. 8, 958-968 10.1110/ps.8.5.958
41. Dehouck, Y., Kwasigroch, J. M., Rooman, M., and Gilis, D. (2013) BeAtMuSiC: prediction of changes in the protein-protein binding affinity on mutations Nucleic Acids Res. 41, 333-339 10.1093/nar/gkt450
42. Hidalgo-Grass, C., Warburg, G., Temper, V., Benenson, S., Moses, A. E., and Block, C. et al. 2012, KPC-9, a novel carbapenemase from clinical specimens in Israel Antimicrob. Agents Chemother. 56, 6057-6059 10.1128/AAC.01156-12
43. Mehta, S. C., Rice, K., and Palzkill, T. (2015) Natural variants of the KPC-2 carbapenemase have evolved increased catalytic efficiency for ceftazidime hydrolysis at the cost of enzyme stability PLoS Pathog. 11, e1004949 10.1371/journal.ppat.1004949
44. Tseng, I. L., Liu, Y. M., Wang, S. J., Yeh, H. Y., Hsieh, C. L., Lu, H. L., Tseng, Y. C., and Mu, J. J. (2015) Emergence of carbapenemase producing Klebsiella pneumonia and spread of KPC-2 and KPC-17 in Taiwan: a nationwide study from 2011 to 2013 PLoS One 10, e0138471 10.1371/journal.pone.0138471
45. Wolter, D. J., Kurpiel, P. M., Woodford, N., Palepou, M. F., Goering, R. V., and Hanson, N. D. (2009) Phenotypic and comparative analysis of the novel KPC variant KPC-5 and its evolutionary variants KPC-2 and KPC-4 Antimicrob. Agents Chemother. 53, 557-562 10.1128/AAC.00734-08
46. Warming, S., Costantino, N., Court, D. L., Jenkins, N. A., and Copeland, N. G. (2005) Simple and highly efficient BAC recombineering using galK selection Nucleic Acids Res. 33, e36 10.1093/nar/gni035
47. Wang, J., Palzkill, T., and Chow, D. C. (2009) Structural insight into the kinetics and DeltaCp of interactions between TEM-1 beta-lactamase and beta-lactamase inhibitory protein (BLIP) J. Biol. Chem. 284, 595-609 10.1074/jbc.M804089200
48. Huang, W., Beharry, Z., Zhang, Z., and Palzkill, T. (2003) A broad-spectrum peptide inhibitor of beta-lactamase identified using phage display and peptide arrays Protein Eng., Des. Sel. 16, 853-860 10.1093/protein/gzg108
49. i values for tight-binding enzyme inhibitors: an in silico study of experimental error and assay design Anal. Biochem. 327, 61-67 10.1016/j.ab.2003.12.018