Role of β-lactamase residues in a common interface for binding the structurally unrelated inhibitory proteins BLIP and BLIP-II

Protein Science

Volumn 23, Issue 9, 2014, Pages 1235-1246

  Fryszczyn, Bartlomiej G ^a   Adamski, Carolyn J ^a   Brown, Nicholas G ^a   Rice, Kacie ^a   Huang, Wanzhi ^a   Palzkill, Timothy ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Antibiotic resistance; Beta lactamase; Binding kinetics; Molecular recognition; Protein protein interactions

Indexed keywords

BETA LACTAMASE; BETA LACTAMASE INHIBITOR; BETA-LACTAMASE TEM-1; PROTEIN BINDING;

CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; KINETICS; METABOLISM; MUTATION; PROTEIN CONFORMATION;

BETA-LACTAMASE INHIBITORS; BETA-LACTAMASES; KINETICS; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 84906886142     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2505     Document Type: Article

References (42)

1. Perkins JR, Diboun I, Dessailly BH, Lees JG, Orengo C (2010) Transient protein-protein interactions: structural, functional, and network properties. Structure 18: 1233-1243.
2. Khan SH, Ahmad F, Ahmad N, Flynn DC, Kumar R (2011) Protein-protein interactions: principles, techniques, and their potential role in new drug development. J Biomol Struct Dyn 28:929-938.
3. Schreiber G, Keating AE (2011) Protein binding specificity versus promiscuity. Curr Opin Struc Biol 21:50- 61.
4. Zhang Z, 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.
5. Zhang Z, Palzkill T (2004) Dissecting the proteinprotein interface between beta-lactamase inhibitory protein and class A beta-lactamases. J Biol Chem 279: 42860-42866.
6. Reichmann D, Rahat O, Albeck S, Meged R, Dym O, Schreiber G (2005) The modular architecture of protein-protein binding interfaces. Proc Natl Acad Sci USA 102:57-62.
7. Reynolds KA, Thomson JM, Corbett KD, Bethel CR, Berger JM, Kirsch JF, Bonomo RA, Handel TM (2006) Structural and computational characterization of the SHV-1 beta-lactamase-beta-lactamase inhibitor protein interface. J Biol Chem 281:26745-26753.
8. Reichmann D, Cohen M, Abramovich R, Dym O, Lim D, Strynadka NCJ, Schreiber G (2007) Binding hot spots in the TEM1-BLIP interface in light of its modular architecture. J Mol Biol 365:663-679.
9. Gretes M, Lim DC, de Castro L, Jensen S, Kang SG, Lee KJ, Strynadka NCJ (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.
10. Brown NG, Chow D-C, Sankaran B, Zwart P, Prasad BV, 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.
11. Keskin O, Ma B, Nussinov R (2005) Hot regions in protein- protein interactions: The organization and contribution of structurally conserved hot spot residues. J Mol Biol 345:1281-1294.
12. Moreira IS, Fernandes PA, Ramos MJ (2007) Hot spots-A review of the protein-protein interface determinant amino acid residues. Proteins 68:803-812.
13. Kozakov D, Hall DR, Chuang GY, Cencic R, Brenke R, Grove LE, Beglov D, Pelletier J, Whitty A, Vajda S (2011) Structural conservation of druggable hot spots in protein-protein interfaces. Proc Natl Acad Sci U.S.A 108:13528-13533.
14. De Lano WL (2002) Unraveling hot spots in binding interfaces: progress and challenges. Curr Opin Struct Biol 12:14-20.
15. Bush K, Fisher JF (2011) Epidemiological expansion, structural studies, and clinical challenges of new blactamases from Gram-negative bacteria. Ann Rev Microbiol 65:455-478.
16. Strynadka NCJ, Jensen SE, Alzari PM, James MNG (1996) A potent new mode of β-lactamase inhibition revealed by the 1.7A ° X-ray crystallographic structure of the TEM-1-BLIP complex. Nature Struct Biol 3:290-297.
17. Lim D, Park HU, De Castro L, Kang SG, Lee HS, Jensen S, Lee KJ, Strynadka NCJ (2001) Crystal structure and kinetic analysis of b-lactamase inhibitor protein-II in complex with TEM-1 β-lactamase. Nat Struct Biol 8:848-852.
18. Doran JL, Leskiw BK, Aippersbach S, Jensen SE (1990) Isolation and characterization of a β-lactamaseinhibitory protein from Streptomyces clavuligerus and cloning and analysis of the corresponding gene. J Bacteriol 172:4909-4918.
19. Strynadka NCJ, Jensen SE, Johns K, Blanchard H, Page M, Matagne A, Frere J-M, James MNG (1994) Structural and kinetic characterization of a blactamase- inhibitor protein. Nature 368:657-660.
20. Reichmann D, Rahat O, Cohen M, Neuvirth H, Schreiber G (2007) The molecular architecture of protein-protein binding sites. Curr Opin Struct Biol 17:67-76.
21. Brown NG, Palzkill T (2010) Identification and characterization of beta-lactamase inhibitor protein-II (BLIPII) interactions with beta-lactamases using phage display. Protein Eng Des Sel 23:469-478.
22. Brown NG, Chow D-C, Ruprecht KE, Palzkill T (2013) Identification of the β-lactamase inhibitor protein-II (BLIP-II) interface residues essential for binding affinity and specificity for class A b-lactamases. J Biol Chem 288:17156-17166.
23. Petrosino J, Rudgers G, Gilbert H, 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.
24. Hanes MS, Jude KM, Berger JM, Bonomo RA, Handel TM (2009) Structural and biochemical characterization of the interaction between KPC-2 beta-lactamase and beta-lactamase inhibitor protein. Biochemistry 48: 9185-9193.
25. Wang J, Palzkill T, Chow DC (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.
26. Selzer T, Schreiber G (1999) Predicting the rate enhancement of protein complex formation from the electrostatic energy of interaction. J Mol Biol 287:409-419.
27. Kozer N, Schreiber G (2004) Effect of crowding on protein-protein association rates: fundamental differences between low and high mass crowding agents. J Mol Biol 336:763-774.
28. Kim DE, Chivian D, Baker D (2004) Protein structure prediction and analysis using the Robetta server. Nucleic Acids Res 32:526-531.
29. Dehouck Y, Kwasigroch JM, Rooman M, Gilis D (2013) BeAtMuSiC: prediction of changes in the proteinprotein binding affinity on mutations. Nucleic Acids Res 41:333-339.
30. Colledge M, Scott JD (1999) AKAPs: from structure to function. Trends Cell Biol 9:916-921.
31. DeLano WL, Ultsch MH, de Vos AM, Wells JA (2000) Convergent solution to binding at a protein-protein interface. Science 287:1279-1283.
32. Stewart M (2007) Molecular mechanism of the nuclear protein import cycle. Nat Rev Mol Cell Biol 8:195-208.
33. Chang CA, McLaughlin WA, Baron R, Wang W, McCammon JA (2008) Entropic contributions and the influence of the hydrophobic environment in promiscuous protein-protein association. Proc Natl Acad Sci USA 105:7456-7461.
34. Fromer M, Shifman JM (2009) Tradeoff between stability and multispecificity in the design of promiscuous proteins. PLOS Comp Biol 5:e1000627.
35. Zhao H, Naganathan S, Beckett D (2009) Thermodynamic and structural investigation of bispecificity in protein-protein interactions. J Mol Biol 389:336-348.
36. Adikaram PR, Beckett D (2012) Functional versatility of a single protein surface in two protein:protein interactions. J Mol Biol 419:223-233.
37. Martin J-F (2010) Beauty is in the eye of the beholder: proteins can recognize binding sites of homologous proteins in more than one way. PLOS Comp Biol 6:e1000821.
38. Perez F, Endimiani A, Hujer KM, Bonomo RA (2007) The continuing challenge of ESBLs. Curr Opin Pharmacol 7:459-469.
39. Papp-Wallace KM, Endimiani A, Taracila MA, Bonomo RA (2011) Carbapenems: past, present, and future. Antimicrob Agents Chemother 55:4943-4960.
40. Marciano DC, Brown NG, Palzkill T (2009) Analysis of the plasticity of location of positive charge within the active site of the TEM-1 b-lactamase. Protein Sci 18: 2080-2089.
41. Marciano DC, Pennington JM, Wang X, Wang J, Chen Y, Thomas VL, Shoichet BK, Palzkill T (2008) Genetic and structural characterization of an L201P global suppressor substitution in TEM-1 beta-lactamase. J Mol Biol 384:151-164.
42. Murphy DJ (2004) Determination of accurate Ki values for tight-binding enzyme inhibitors: An in silico study of experimental error and assay design. Anal Biochem 327: 61-67.