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Structural and computational characterization of the SHV-1 beta-lactamase-beta-lactamase inhibitor protein interface.

Reynolds KA, Thomson JM, Corbett KD, Bethel CR, Berger JM, Kirsch JF, Bonomo RA, Handel TM
J Biol Chem 281 26745-53 (2006)
Cited: 37 times
EuropePMC logo PMID: 16809340

Abstract

Beta-lactamase inhibitor protein (BLIP) binds a variety of class A beta-lactamases with affinities ranging from micromolar to picomolar. Whereas the TEM-1 and SHV-1 beta-lactamases are almost structurally identical, BLIP binds TEM-1 approximately 1000-fold tighter than SHV-1. Determining the underlying source of this affinity difference is important for understanding the molecular basis of beta-lactamase inhibition and mechanisms of protein-protein interface specificity and affinity. Here we present the 1.6A resolution crystal structure of SHV-1.BLIP. In addition, a point mutation was identified, SHV D104E, that increases SHV.BLIP binding affinity from micromolar to nanomolar. Comparison of the SHV-1.BLIP structure with the published TEM-1.BLIP structure suggests that the increased volume of Glu-104 stabilizes a key binding loop in the interface. Solution of the 1.8A SHV D104K.BLIP crystal structure identifies a novel conformation in which this binding loop is removed from the interface. Using these structural data, we evaluated the ability of EGAD, a program developed for computational protein design, to calculate changes in the stability of mutant beta-lactamase.BLIP complexes. Changes in binding affinity were calculated within an error of 1.6 kcal/mol of the experimental values for 112 mutations at the TEM-1.BLIP interface and within an error of 2.2 kcal/mol for 24 mutations at the SHV-1.BLIP interface. The reasonable success of EGAD in predicting changes in interface stability is a promising step toward understanding the stability of the beta-lactamase.BLIP complexes and computationally assisted design of tight binding BLIP variants.

Reviews - 2g2u mentioned but not cited (1)

  1. Protein binding specificity versus promiscuity. Schreiber G, Keating AE. Curr Opin Struct Biol 21 50-61 (2011)

Articles - 2g2u mentioned but not cited (10)

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  2. Computational redesign of the SHV-1 beta-lactamase/beta-lactamase inhibitor protein interface. Reynolds KA, Hanes MS, Thomson JM, Antczak AJ, Berger JM, Bonomo RA, Kirsch JF, Handel TM. J Mol Biol 382 1265-1275 (2008)
  3. Modulating protein-protein interactions with small molecules: the importance of binding hotspots. Thangudu RR, Bryant SH, Panchenko AR, Madej T. J Mol Biol 415 443-453 (2012)
  4. Active site detection by spatial conformity and electrostatic analysis--unravelling a proteolytic function in shrimp alkaline phosphatase. Chakraborty S, Minda R, Salaye L, Bhattacharjee SK, Rao BJ. PLoS One 6 e28470 (2011)
  5. Specificity and cooperativity at β-lactamase position 104 in TEM-1/BLIP and SHV-1/BLIP interactions. Hanes MS, Reynolds KA, McNamara C, Ghosh P, Bonomo RA, Kirsch JF, Handel TM. Proteins 79 1267-1276 (2011)
  6. Composition of Overlapping Protein-Protein and Protein-Ligand Interfaces. Mohamed R, Degac J, Helms V. PLoS One 10 e0140965 (2015)
  7. The structure of BVU2987 from Bacteroides vulgatus reveals a superfamily of bacterial periplasmic proteins with possible inhibitory function. Das D, Finn RD, Carlton D, Miller MD, Abdubek P, Astakhova T, Axelrod HL, Bakolitsa C, Chen C, Chiu HJ, Chiu M, Clayton T, Deller MC, Duan L, Ellrott K, Ernst D, Farr CL, Feuerhelm J, Grant JC, Grzechnik A, Han GW, Jaroszewski L, Jin KK, Klock HE, Knuth MW, Kozbial P, Krishna SS, Kumar A, Marciano D, McMullan D, Morse AT, Nigoghossian E, Nopakun A, Okach L, Puckett C, Reyes R, Rife CL, Sefcovic N, Tien HJ, Trame CB, van den Bedem H, Weekes D, Wooten T, Xu Q, Hodgson KO, Wooley J, Elsliger MA, Deacon AM, Godzik A, Lesley SA, Wilson IA. Acta Crystallogr Sect F Struct Biol Cryst Commun 66 1265-1273 (2010)
  8. Enumerating pathways of proton abstraction based on a spatial and electrostatic analysis of residues in the catalytic site. Chakraborty S. PLoS One 7 e39577 (2012)
  9. Interdomain flexibility and interfacial integrity of β-lactamase inhibitory protein (BLIP) modulate its binding to class A β-lactamases. Huang L, So PK, Chen YW, Leung YC, Yao ZP. J Biol Chem 297 100980 (2021)
  10. The development of an affinity evaluation and prediction system by using protein-protein docking simulations and parameter tuning. Tsukamoto K, Yoshikawa T, Yokota K, Hourai Y, Fukui K. Adv Appl Bioinform Chem 2 1-15 (2009)


Reviews citing this publication (5)

  1. Three decades of beta-lactamase inhibitors. Drawz SM, Bonomo RA. Clin Microbiol Rev 23 160-201 (2010)
  2. Membrane protein architects: the role of the BAM complex in outer membrane protein assembly. Knowles TJ, Scott-Tucker A, Overduin M, Henderson IR. Nat Rev Microbiol 7 206-214 (2009)
  3. The molecular architecture of protein-protein binding sites. Reichmann D, Rahat O, Cohen M, Neuvirth H, Schreiber G. Curr Opin Struct Biol 17 67-76 (2007)
  4. Tackling the Antibiotic Resistance Caused by Class A β-Lactamases through the Use of β-Lactamase Inhibitory Protein. Eiamphungporn W, Schaduangrat N, Malik AA, Nantasenamat C. Int J Mol Sci 19 E2222 (2018)
  5. Evolution: a guide to perturb protein function and networks. Lichtarge O, Wilkins A. Curr Opin Struct Biol 20 351-359 (2010)

Articles citing this publication (21)

  1. Binding hot spots in the TEM1-BLIP interface in light of its modular architecture. Reichmann D, Cohen M, Abramovich R, Dym O, Lim D, Strynadka NC, Schreiber G. J Mol Biol 365 663-679 (2007)
  2. Insights into positive and negative requirements for protein-protein interactions by crystallographic analysis of the beta-lactamase inhibitory proteins BLIP, BLIP-I, and BLP. Gretes M, Lim DC, de Castro L, Jensen SE, Kang SG, Lee KJ, Strynadka NC. J Mol Biol 389 289-305 (2009)
  3. Structural and biochemical characterization of the interaction between KPC-2 beta-lactamase and beta-lactamase inhibitor protein. Hanes MS, Jude KM, Berger JM, Bonomo RA, Handel TM. Biochemistry 48 9185-9193 (2009)
  4. Structural insight into the kinetics and DeltaCp of interactions between TEM-1 beta-lactamase and beta-lactamase inhibitory protein (BLIP). Wang J, Palzkill T, Chow DC. J Biol Chem 284 595-609 (2009)
  5. A Machine Learning Approach for Hot-Spot Detection at Protein-Protein Interfaces. Melo R, Fieldhouse R, Melo A, Correia JD, Cordeiro MN, Gümüş ZH, Costa J, Bonvin AM, Moreira IS. Int J Mol Sci 17 E1215 (2016)
  6. The solution structure of the outer membrane lipoprotein OmlA from Xanthomonas axonopodis pv. citri reveals a protein fold implicated in protein-protein interaction. Vanini MM, Spisni A, Sforça ML, Pertinhez TA, Benedetti CE. Proteins 71 2051-2064 (2008)
  7. Identification and characterization of beta-lactamase inhibitor protein-II (BLIP-II) interactions with beta-lactamases using phage display. Brown NG, Palzkill T. Protein Eng Des Sel 23 469-478 (2010)
  8. Identification of a β-lactamase inhibitory protein variant that is a potent inhibitor of Staphylococcus PC1 β-lactamase. Yuan J, Chow DC, Huang W, Palzkill T. J Mol Biol 406 730-744 (2011)
  9. An evolutionarily conserved allosteric site modulates beta-lactamase activity. Avci FG, Altinisik FE, Vardar Ulu D, Ozkirimli Olmez E, Sariyar Akbulut B. J Enzyme Inhib Med Chem 31 33-40 (2016)
  10. 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. Yuan J, Huang W, Chow DC, Palzkill T. J Mol Biol 389 401-412 (2009)
  11. Role of β-lactamase residues in a common interface for binding the structurally unrelated inhibitory proteins BLIP and BLIP-II. Fryszczyn BG, Adamski CJ, Brown NG, Rice K, Huang W, Palzkill T. Protein Sci 23 1235-1246 (2014)
  12. Engineering Specificity from Broad to Narrow: Design of a β-Lactamase Inhibitory Protein (BLIP) Variant That Exclusively Binds and Detects KPC β-Lactamase. Chow DC, Rice K, Huang W, Atmar RL, Palzkill T. ACS Infect Dis 2 969-979 (2016)
  13. Weighted protein residue networks based on joint recurrences between residues. Karain WI, Qaraeen NI. BMC Bioinformatics 16 173 (2015)
  14. Protein-protein binding affinities by pulse proteolysis: application to TEM-1/BLIP protein complexes. Hanes MS, Ratcliff K, Marqusee S, Handel TM. Protein Sci 19 1996-2000 (2010)
  15. An active site loop toggles between conformations to control antibiotic hydrolysis and inhibition potency for CTX-M β-lactamase drug-resistance enzymes. Lu S, Hu L, Lin H, Judge A, Rivera P, Palaniappan M, Sankaran B, Wang J, Prasad BVV, Palzkill T. Nat Commun 13 6726 (2022)
  16. BLIP-II Employs Differential Hotspot Residues To Bind Structurally Similar Staphylococcus aureus PBP2a and Class A β-Lactamases. Adamski CJ, Palzkill T. Biochemistry 56 1075-1084 (2017)
  17. Efficient production of secretory Streptomyces clavuligerus β-lactamase inhibitory protein (BLIP) in Pichia pastoris. Law KH, Tsang MW, Wong YK, Tsang MS, Lau PY, Wong KY, Ho KP, Leung YC. AMB Express 8 64 (2018)
  18. Properties that rank protein:protein docking poses with high accuracy. Simões ICM, Coimbra JTS, Neves RPP, Costa IPD, Ramos MJ, Fernandes PA. Phys Chem Chem Phys 20 20927-20942 (2018)
  19. Studies on amino acid replacement and inhibitory activity of a beta-lactamase inhibitory peptide. Xie L, Xu M, Yang T, Zhu C, Zhu B, Hu Y. Biochemistry (Mosc) 75 336-341 (2010)
  20. Use of periplasmic target protein capture for phage display engineering of tight-binding protein-protein interactions. Fryszczyn BG, Brown NG, Huang W, Balderas MA, Palzkill T. Protein Eng Des Sel 24 819-828 (2011)
  21. Comment The molecular epidemiology of extended-spectrum beta-lactamase producing organisms. Paterson DL. Enferm Infecc Microbiol Clin 26 403 (2008)


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