Identification of the β-Lactamase Inhibitor Protein-II (BLIP-II) interface residues essential for binding affinity and specificity for class A β-lactamases

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17156-17166

  Brown, Nicholas G ^a   Chow, Dar Chone ^a   Ruprecht, Kevin E ^a   Palzkill, Timothy ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE SUBSTITUTION; ALANINE-SCANNING MUTAGENESIS; AROMATIC AMINO ACID; BINDING AFFINITIES; INHIBITORY PROTEINS; INTERFACE RESIDUES; PROTEIN-PROTEIN INTERACTIONS; STRUCTURAL HOMOLOGY;

AMINO ACIDS; COMPLEXATION; PROTEINS;

BINDING ENERGY;

ALANINE; AROMATIC AMINO ACID; BETA LACTAMASE; BETA LACTAMASE INHIBITOR; BETA LACTAMASE INHIBITOR PROTEIN II; UNCLASSIFIED DRUG;

ALANINE SCANNING MUTAGENESIS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING KINETICS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME INHIBITION; ENZYME SPECIFICITY; INHIBITION KINETICS; LOW TEMPERATURE; MUTAGENESIS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; STRUCTURE ANALYSIS;

ALANINE SCANNING MUTAGENESIS; ANTIBIOTIC RESISTANCE; BETA-LACTAM ANTIBIOTIC; BETA-LACTAMASE; BINDING HOT SPOT; DRUG DISCOVERY; ENZYME INHIBITORS; ENZYME KINETICS; MOLECULAR RECOGNITION; PROTEIN-PROTEIN INTERACTIONS;

AMINO ACID SUBSTITUTION; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-LACTAM RESISTANCE; BETA-LACTAMASES; CATALYTIC DOMAIN; ESCHERICHIA COLI; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; STREPTOMYCES; THERMODYNAMICS;

EID: 84879066030     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.463521     Document Type: Article

References (51)

1. Jubb, H., Higueruelo, A. P., Winter, A., and Blundell, T. L. (2012) Structural biology and drug discovery for protein-protein interactions. Trends Pharm. Sci. 33, 241-248
2. Kuzu, G., Keskin, O., Gursoy, A., and Nussinov, R. (2012) Constructing structural networks of signaling pathways on the proteome scale. Curr. Opin. Struct. Biol. 22, 367-377
3. Schreiber, G., and Keating, A. E. (2011) Protein binding specificity versus promiscuity. Curr. Opin. Struct. Biol. 21, 50-61
4. Clackson, T., and Wells, J. A. (1995) A hot spot of binding energy in a hormone-receptor interface. Science 267, 383-386
5. Cunningham, B. C., and Wells, J. A. (1989) High-resolution epitope mapping of hGH-receptor interactions by alanine-scanning mutagenesis. Science 244, 1081-1085 (Pubitemid 19152300)
6. DeLano, W. L. (2002) Unraveling hot spots in binding interfaces. Progress and challenges. Curr. Opin. Struct. Biol. 12, 14-20
7. Bogan, A. A., and Thorn, K. S. (1998) Anatomy of hot spots in protein interfaces. J. Mol. Biol. 280, 1-9 (Pubitemid 28312802)
8. Zhang, Z., and Palzkill, T. (2004) Dissecting the protein-protein interface between β-lactamase inhibitory protein and class A β-lactamases. J. Biol. Chem. 279, 42860-42866 (Pubitemid 39372175)
9. Dutta, S., Gullá, 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. 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
11. Reichmann, D., Cohen, M., Abramovich, R., Dym, O., Lim, D., Strynadka, N. C., and Schreiber, G. (2007) Binding hot spots in the TEM1-BLIP interface in light of its modular architecture. J. Mol. Biol. 365, 663-679 (Pubitemid 44960349)
12. Fisher, J. F., Meroueh, S. O., and Mobashery, S. (2005) Bacterial resistance to β-lactam antibiotics. Compelling opportunism, compelling opportunity. Chem. Rev. 105, 395-424 (Pubitemid 40351628)
13. Ambler, R. P., Coulson, A. F., Frère, J.-M., Ghuysen, J.-M., Joris, B., Forsman, M., Levesque, R. C., Tiraby, G., and Waley, S. G. (1991) A standard numbering scheme for the class A β-lactamases. Biochem. J. 276, 269-270
14. Ishii, Y., Galleni, M., Ma, L., Frère, J.-M., and Yamaguchi, K. (2007) Biochemical characterisation of the CTX-M-14 β-lactamase. Int. J. Antimicrob. Agents 29, 159-164
15. 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 (Pubitemid 20281936)
16. Gretes, M., Lim, D. C., de Castro, L., Jensen, S. E., Kang, S. G., Lee, K. J., and Strynadka, N. C. (2009) Insights into positive and negative requirements for protein-protein interactions by crystallographic analysis of the β-lactamase inhibitory proteins BLIP, BLIP-I, and BLP. J. Mol. Biol. 389, 289-305
17. Kang, S. G., Park, H. U., Lee, H. S., Kim, H. T., and Lee, K. J. (2000) New β-lactamase inhibitory protein (BLIP-I) from Streptomyces exfoliatus SMF19 and its roles on the morphological differentiation. J. Biol. Chem. 275, 16851-16856 (Pubitemid 30398920)
18. Park, H. U., and Lee, K. J. (1998) Cloning and heterologous expression of the gene for BLIP-II, a β-lactamase-inhibitory protein from Streptomyces exfoliatus SMF19. Microbiology 144, 2161-2167 (Pubitemid 28403028)
19. 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 (Pubitemid 40094428)
20. Strynadka, N. C., Jensen, S. E., Alzari, P. M., and James, M. N. (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
21. Strynadka, N. C., Jensen, S. E., Johns, K., Blanchard, H., Page, M., Matagne, A., Frère, J.-M., and James, M. N. (1994) Structural and kinetic characterization of a β-lactamase-inhibitor protein. Nature 368, 657-660 (Pubitemid 24153393)
22. Wang, J., Zhang, Z., Palzkill, T., and Chow, D.-C. (2007) Thermodynamic investigation of the role of contact residues of β-lactamaseinhibitory protein for binding to TEM-1 β-lactamase. J. Biol. Chem. 282, 17676-17684 (Pubitemid 47100282)
23. Yuan, J., Huang, W., Chow, D. C., and Palzkill, T. (2009) Fine mapping of the sequence requirements for binding of β-lactamase inhibitory protein (BLIP) to TEM-1 β-lactamase using a genetic screen for BLIP function. J. Mol. Biol. 389, 401-412
24. Fülöp, V., and Jones, D. T. (1999) β propellers. Structural rigidity and functional diversity. Curr. Opin. Struct. Biol. 9, 715-721
25. Guruprasad, K., and Dhamayanthi, P. (2004) Structural plasticity associated with the β-propeller architecture. Int. J. Biol. Macromol. 34, 55-61 (Pubitemid 38721186)
26. Hadjebi, O., Casas-Terradellas, E., Garcia-Gonzalo, F. R., and Rosa, J. L. (2008) The RCC1 superfamily. From genes, to function, to disease. Biochim. Biophys. Acta 1783, 1467-1479
27. 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, 32723-32735
28. Lim, D., Park, H. U., De Castro, L., Kang, S. G., Lee, H. S., Jensen, S., Lee, K. J., and Strynadka, N. C. (2001) Crystal structure and kinetic analysis of β-lactamase inhibitor protein-II in complex with TEM-1 β-lactamase. Nat. Struct. Biol. 8, 848-852 (Pubitemid 32923602)
29. Brown, N. G., and Palzkill, T. (2010) Identification and characterization of β-lactamase inhibitor protein-II (BLIP-II) interactions with β-lactamases using phage display. Protein Eng. Des. Sel. 23, 469-478
30. Hanes, M. S., Reynolds, K. A., McNamara, C., Ghosh, P., Bonomo, R. A., Kirsch, J. F., and Handel, T. M. (2011) Specificity and cooperativity at β-lactamase position 104 in TEM-1/BLIP and SHV-1/BLIP interactions. Proteins 79, 1267-1276
31. Kühlmann, U. C., Pommer, A. J., Moore, G. R., James, R., and Kleanthous, C. (2000) Specificity in protein-protein interactions. The structural basis for dual recognition in endonuclease colicin-immunity protein complexes. J. Mol. Biol. 301, 1163-1178
32. Yuan, J., Chow, D. C., Huang, W., and Palzkill, T. (2011) Identification of a β-lactamase inhibitory protein variant that is a potent inhibitor of staphylococcus PC1 β-lactamase. J. Mol. Biol. 406, 730-744
33. 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 (Pubitemid 37432713)
34. Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2002) Multiple sequence alignment using ClustalW and ClustalX, in Current Protocols in Bioinformatics
35. 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 β-lactamase and β-lactamase inhibitor protein. Biochemistry 48, 9185-9193
36. Brown, N. G., Pennington, J. M., Huang, W., Ayvaz, T., and Palzkill, T. (2010) Multiple global suppressors of protein stability defects facilitate the evolution of extended-spectrum TEM β-lactamases. J. Mol. Biol. 404, 832-846
37. Materon, I. C., Queenan, A. M., Koehler, T. M., Bush, K., and Palzkill, T. (2003) Biochemical characterization of β-lactamases Bla1 and Bla2 from Bacillus anthracis. Antimicrob. Agents Chemother. 47, 2040-2042 (Pubitemid 36637842)
38. Stachyra, T., Levasseur, P., Péchereau, M. C., Girard, A. M., Claudon, M., Miossec, C., and Black, M. T. (2009) In vitro activity of the β-lactamase inhibitor NXL104 against KPC-2 carbapenemase and Enterobacteriaceae expressing KPC carbapenemases. J. Antimicrob. Chemother. 64, 326-329
39. Brown, N. G., Chow, D.-C., and Palzkill, T. (2013) BLIP-II is a highly potent inhibitor of the Klebsiella pneumoniae carbapenemase (KPC-2). Antimicrob. Agents Chemother., in press
40. Potapov, V., Reichmann, D., Abramovich, R., Filchtinski, D., Zohar, N., Ben Halevy, D., Edelman, M., Sobolev, V., and Schreiber, G. (2008) Computational redesign of a protein-protein interface for high affinity and binding sepcificity using modular architecture and naturally occurring template fragments. J. Mol. Biol. 384, 109-119
41. Thiel, P., Kaiser, M., and Ottmann, C. (2012) Small-molecule stabilization of protein-protein interactions. An underestimated concept in drug discovery? Angew. Chem. Int. Ed. Engl. 51, 2012-2018
42. Surade, S., and Blundell, T. L. (2012) Structural biology and drug discovery of difficult targets. The limits of ligandability. Chem. Biol. 19, 42-50
43. Scott, D. E., Ehebauer, M. T., Pukala, T., Marsh, M., Blundell, T. L., Venkitaraman, A. R., Abell, C., and Hyvönen, M. (2013) Using a fragmentbased approach to target protein-protein interactions. Chembiochem. 14, 332-342
44. Schreiber, G., Haran, G., and Zhou, H. X. (2009) Fundamental aspects of protein-protein association kinetics. Chem. Rev. 109, 839-860
45. Alsallaq, R., and Zhou, H.-X. (2008) Electrostatic rate enhancement and transient complex of protein-protein association. Proteins 71, 320-335 (Pubitemid 351358613)
46. Janin, J. (1997) The kinetics of protein-protein recognition. Proteins 28, 153-161
47. Schlosshauer, M., and Baker, D. (2004) Realistic protein-protein association rates from a simple diffusional model neglecting long-range interactions, free energy barriers, and landscape ruggedness. Protein Sci. 13, 1660-1669 (Pubitemid 38669253)
48. Zhou, H.-X. (1997) Enhancement of protein-protein association rate by interaction potential. Accuracy of prediction based on local Boltzmann factor. Biophys. J. 73, 2441-2445
49. Moreira, I. S., Fernandes, P. A., and Ramos, M. J. (2007) Hot spots-A review of the protein-protein interface determinant amino acid residues. Proteins 68, 803-812 (Pubitemid 47434705)
50. Clackson, T., Ultsch, M. H., Wells, J. A., and de Vos, A. M. (1998) Structural and functional analysis of the 1:1 growth hormone:receptor complex reveals the molecular basis for receptor affinity. J. Mol. Biol. 277, 1111-1128 (Pubitemid 28190850)
51. Curtis, M. D., and James, R. (1991) Investigation of the specificity of the interaction between colicin E9 and its immunity protein by site-directed mutagenesis. Mol. Microbiol. 5, 2727-2733 (Pubitemid 21896005)