Molecular insight into pseudolysin inhibition using the MM-PBSA and LIE methods

Journal of Structural Biology

Volumn 153, Issue 2, 2006, Pages 129-144

  Adekoya, Olayiwola A ^a   Willassen, Nils Peder ^a   Sylte, Ingebrigt ^a  

^a UNIVERSITY OF TROMSØ   (Norway)

Author keywords

Computational alanine scanning; Free energy of binding; LIE calculations; MM PBSA calculations; Molecular dynamics simulations; Protein protein interactions; Pseudolysin; Pseudolysin inhibition; SMPI

Indexed keywords

BACTERIAL ENZYME; ELASTASE; METALLOPROTEINASE INHIBITOR; PSEUDOLYSIN; UNCLASSIFIED DRUG;

ARTICLE; DATA ANALYSIS; ENZYME INHIBITION; GRAM NEGATIVE INFECTION; HYDROGEN BOND; IMAGING; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; STREPTOMYCES; TECHNIQUE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; BINDING SITES; COMPUTER SIMULATION; CRYSTALLOGRAPHY, X-RAY; ELECTROSTATICS; ENTROPY; HYDROGEN BONDING; KINETICS; LIGANDS; METALLOENDOPEPTIDASES; MODELS, MOLECULAR; MOLECULAR CONFORMATION; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MONTE CARLO METHOD; PROTEIN BINDING; SEQUENCE ALIGNMENT; THERMODYNAMICS; THERMOLYSIN; ZINC;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS AERUGINOSA; STREPTOMYCES;

EID: 31344452474     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsb.2005.11.003     Document Type: Article

References (69)

1. R. Abagyan, T. Maxim, and D. Kuznetsov ICM-A new method for protein modelling and design: applications to docking and structure prediction from the distorted native conformation J. Comp. Chem. 15 1994 488 506
2. O.A. Adekoya, N.P. Willassen, and I. Sylte The protein-protein interactions between SMPI and thermolysin studied by molecular dynamics and MM/PBSA calculations J. Biomol. Struct. Dyn. 22 2005 521 532
3. I.L. Alberts, K. Nadassy, and S.J. Wodak Analysis of zinc binding sites in protein crystal structures Protein Sci. 7 1998 1700 1716
4. J. Åqvist Calculation of absolute binding free energies for charged ligands and effects of long-range electrostatic interactions J. Comput. Chem. 17 1996 1587 1597
5. J. Åqvist, V.B. Luzhkov, and B.O. Brandsdal Ligand binding affinities from MD simulations Acc. Chem. Res. 35 2002 358 365
6. J. Åqvist, C. Medina, and J.E. Samuelsson A new method for predicting binding affinity in computer-aided drug design Protein Eng. 7 1994 385 391
7. C.I. Bayly, P. Cieplak, W.D. Cornell, and P.A. Kollman A well-behaved electrostatic potential based method using charge restraints for deriving atomic charges-the RESP model J. Phys. Chem. 97 1993 10269 10280
8. F.R. Burns, C.A. Paterson, R.D. Gray, and J.T. Wells Inhibition of Pseudomonas aeruginosa elastase and Pseudomonas keratitis using a thiol-based peptide Antimicrob. Agents Chemother. 34 1990 2065 2069
9. Case, D.A., Pearlman, D.A., Caldwell, J.W., Cheatham III, T.E., Wang, J., Ross, W.S., Simmerling, C., Darden, T., Merz, K.M., Stanton, R.V., et al., 2002. AMBER 7. AMBER 7. University of California, San Francisco.
10. T.E. Cheatham III, J. Srinivasan, D.A. Case, and P.A. Kollman Molecular dynamics and continuum solvent studies of the stability of polyG-polyC and polyA-polyT DNA duplexes in solution J. Biomol. Struct. Dyn. 16 1998 265 280
11. T. Clackson, M.H. Ultsch, J.A. Wells, and A.M. deVos Structural and functional analysis of the 1:1 growth hormone:receptor complex reveals the molecular basis for receptor affinity J. Mol. Biol. 277 1998 1111 1128
12. W.D. Cornell, P. Cieplak, C.I. Bayly, I.R. Gould, K.M. Merz, D.M. Ferguson, D.C. Spellmeyer, T. Fox, J.W. Caldwell, and P.A. Kollman A 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules J. Am. Chem. Soc. 117 1995 5179 5197
13. W.D. Cornell, P. Cieplak, C.I. Bayly, and P.A. Kollman Application of RESP charges to calculate conformational energies, hydrogen-bond energies, and free-energies of solvation J. Am. Chem. Soc. 115 1993 9620 9631
14. T. Darden, D. York, and L. Pedersen Particle mesh Ewald: An N • log (N) method for Ewald sums in large systems J. Chem. Phys. 98 1993 10089 10092
15. G. Doring, H.J. Obernesser, and K. Botzenhart Extracellular toxins of Pseudomonas aeruginosa. II. Effect of two proteases on human immunoglobulins IgG, IgA and secretory IgA (author's transl.) Zentralbl. Bakteriol. A 249 1981 89 98
16. O.A.T. Donini, and P.A. Kollman Calculation and prediction of binding free energies for the matrix metalloproteinases J. Med. Chem. 43 2000 4180 4188
17. U. Essmann, Perera Lalith, M.L. Berkowitz, T. Darden, Lee Hsing, and L.G. Pedersen A smooth particle mesh Ewald method J. Chem. Phys. 103 1995 8577 8593
18. P. Ferrara, H. Gohlke, D.J. Price, G. Klebe, and C.L. Brooks 3rd Assessing scoring functions for protein-ligand interactions J. Med. Chem. 47 2004 3032 3047
19. Frisch, M.J., Trucks, G.W., Schlegel, H.B., Scuseria, G.E., Robb, M.A., Cheeseman, J.R., Zakrzewski, V.G., Montgomery, J.A.J., Stratmann, R.E., Burant, J.C., et al., 2001. Gaussian 98 (Revision A.11). Gaussian, Pittsburgh, PA.
20. M.K. Gilson, and B. Honig Calculation of the total electrostatic energy of a macromolecular system: solvation energies, binding energies, and conformational analysis Proteins 4 1988 7 18
21. W.F.v. Gunsteren, and H.T.C. Berendsen Algorithms for macromolecular dynamics and contraints dynamics Mol. Phys. 34 1977 1311
22. T. Hansson, J. Marelius, and J. Åqvist Ligand binding affinity prediction by linear interaction energy methods J. Comput.-Aid. Mol. Des. 12 1998 27 35
23. L.W. Heck, K. Morihara, W.B. McRae, and E.J. Miller Specific cleavage of human type III and IV collagens by Pseudomonas aeruginosa elastase Infect. Immun. 51 1986 115 118
24. K. Hiraga, S.S. Seeram, S. Tate, N. Tanaka, M. Kainosho, and K. Oda Mutational analysis of the reactive site loop of Streptomyces metalloproteinase inhibitor, SMPI J. Biochem. (Tokyo) 125 1999 202 209
25. J. Hobden Pseudomonas aeruginosa proteases and corneal virulence DNA Cell Biol. 21 2002 391 396
26. H.M. Holden, and B.W. Matthews The binding of l-valyl-l-tryptophan to crystalline thermolysin illustrates the mode of interaction of a product of peptide hydrolysis J. Biol. Chem. 263 1988 3256 3260
27. I.A. Holder, and R. Wheeler Experimental studies of the pathogenesis of infections owing to Pseudomonas aeruginosa: elastase, an IgG protease Can. J. Microbiol. 30 1984 1118 1124
28. B. Honig, and A. Nicholls Classical electrostatics in biology and chemistry Science 268 1995 1144 1149
29. T. Hou, S. Guo, and X. Xu Predictions of binding of a diverse set of ligands to gelatinase-A by a combination of molecular dynamics and continuum solvent models J. Phys. Chem. B 106 2002 5527 5535
30. T.J. Hou, W. Zhang, and X.J. Xu Binding affinities for a series of selective inhibitors of gelatinase-A using molecular dynamics with a linear interaction energy approach J. Phys. Chem. B 105 2001 5304 5315
31. M. Izquierdo-Martin, and R.L. Stein Mechanistic studies on the inhibition of thermolysin by a peptide hydroxamic acid J. Am. Chem. Soc. 114 1992 325 331
32. D.A. Johnson, B. Carter-Hamm, and W.M. Dralle Inactivation of human bronchial mucosal proteinase inhibitor by Pseudomonas aeruginosa elastase Am. Rev. Respir. Dis. 126 1982 1070 1073
33. W.L. Jorgensen Revised TIPS for simulations of liquid water and aqueous solutions J. Chem. Phys. 77 1982 4156
34. E. Kessler, and S. Blumberg Specific inhibitors of Pseudomonas aeruginosa elastase as potential drugs for the treatment of Pseudomonas keratitis Antibiot. Chemother. 39 1987 102 112
35. E. Kessler, M. Israel, N. Landshman, A. Chechick, and S. Blumberg In vitro inhibition of Pseudomonas aeruginosa elastase by metal-chelating peptide derivatives Infect. Immun. 38 1982 716 723
36. E. Kessler, and A. Spierer Inhibition by phosphoramidon of Pseudomonas aeruginosa elastase injected intracorneally in rabbit eyes Curr. Eye Res. 3 1984 1075 1078
37. P.A. Kollman, I. Massova, C. Reyes, B. Kuhn, S. Huo, L. Chong, M. Lee, T. Lee, Y. Duan, W. Wang, O. Donini, P. Cieplak, J. Srinivasan, D.A. Case, and T.E. Cheatham Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models Acc. Chem. Res. 33 2000 889 897
38. Y. Komori, T. Nonogaki, and T. Nikai Hemorrhagic activity and muscle damaging effect of Pseudomonas aeruginosa metalloproteinase (elastase) Toxicon 39 2001 1327 1332
39. T. Kortemme, and D. Baker A simple physical model for binding energy hot spots in protein-protein complexes PNAS 99 2002 14116 14121
40. Kortemme, T., Kim, D.E., Baker, D., 2004. Computational alanine scanning of protein-protein interfaces. Sci. STKE 2004, pl2.
41. J. Kottalam, and D.A. Case Langevin modes of macromolecules-applications to Crambin and DNA hexamers Biopolymers 29 1990 1409 1421
42. G. Lamm, and A. Szabo Langevin modes of macromolecules Biophys. J. 49 1986 A57
43. K.B. Ljungberg, J. Marelius, D. Musil, P. Svensson, B. Norden, and J. Åqvist Computational modelling of inhibitor binding to human thrombin Eur. J. Pharm. Sci. 12 2001 441 446
44. J. Marelius, T. Hansson, and J. Åqvist Calculation of ligand binding free energies from molecular dynamics simulations Int. J. Quant. Chem. 69 1998 77 88
45. W.I. Mariencheck, J.F. Alcorn, S.M. Palmer, and J.R. Wright Pseudomonas aeruginosa elastase degrades surfactant proteins A and D Am. J. Respir. Cell Mol. Biol. 28 2003 528 537
46. B.W. Matthews Structural basis of the action of thermolysin and related zinc peptidases Acc. Chem. Res. 21 1988 333 340
47. K. Morihara Pseudolysin and other pathogen endopeptidases of thermolysin family Methods Enzymol. 248 1995 242 253
48. K. Morihara, H. Tsuzuki, and K. Oda Protease and elastase of Pseudomonas aeruginosa: inactivation of human plasma alpha 1-proteinase inhibitor Infect. Immun. 24 1979 188 193
49. N. Nishino, and J.C. Powers Pseudomonas aeruginosa elastase. Development of a new substrate, inhibitors, and an affinity ligand J. Biol. Chem. 255 1980 3482 3486
50. K. Oda, T. Koyama, and S. Murao Purification and properties of a proteinaceous metallo-proteinase inhibitor from Streptomyces nigrescens TK-23 Biochim. Biophys. Acta 571 1979 147 156
51. A. Ohno, S. Tate, S.S. Seeram, K. Hiraga, M.B. Swindells, K. Oda, and M. Kainosho NMR structure of the Streptomyces metalloproteinase inhibitor, SMPI, isolated from Streptomyces nigrescens TK-23: another example of an ancestral beta gamma-crystallin precursor structure J. Mol. Biol. 282 1998 421 433
52. D.A. Pearlman, D.A. Case, J.W. Caldwell, W.S. Ross, T.E. Cheatham III, S. DeBolt, D.M. Ferguson, G.L. Seibel, and P. Kollman AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules Comput. Phys. Commun. 91 1995 1 41
53. D. Rasnick, and J.C. Powers Active site directed irreversible inhibition of thermolysin Biochemistry 17 1978 4363 4369
54. W. Rocchia, S. Sridharan, A. Nicholls, E. Alexov, A. Chiabrera, and B. Honig Rapid grid-based construction of the molecular surface and the use of induced surface charge to calculate reaction field energies: applications to the molecular systems and geometric objects J. Comp. Chem. 23 2002 128 137
55. M. Sanner, A.J. Olson, and J.C. Spehner Reduced surface: An efficient way to compute molecular surfaces Biopolymers 38 1996 305 320
56. I. Schechter, and A. Berger On the size of the active site in proteases. I. Papain Biochem. Biophys. Res. Commun. 27 1967 157 162
57. A. Schmidtchen, E. Holst, H. Tapper, and L. Bjorck Elastase-producing Pseudomonas aeruginosa degrade plasma proteins and extracellular products of human skin and fibroblasts, and inhibit fibroblast growth Microb. Pathogen. 34 2003 47 55
58. S.S. Seeram, K. Hiraga, and K. Oda Resynthesis of reactive site peptide bond and temporary inhibition of Streptomyces metalloproteinase inhibitor J. Biochem. (Tokyo) 122 1997 788 794
59. S.S. Seeram, K. Hiraga, A. Saji, M. Tashiro, and K. Oda Identification of reactive site of a proteinaceous metalloproteinase inhibitor from Streptomyces nigrescens TK-23 J. Biochem. (Tokyo) 121 1997 1088 1095
60. D. Sitkoff, A. Kim, Sharp, and B. Honig Accurate calculation of hydration free energies using macroscopic solvent models J. Phys. Chem. 98 1994 1978 1988
61. V. Sobolev, A. Sorokine, J. Prilusky, E.E. Abola, and M. Edelman Automated analysis of interatomic contacts in proteins Bioinformatics 15 1999 327 332
62. S. Tate, A. Ohno, S.S. Seeram, K. Hiraga, K. Oda, and M. Kainosho Elucidation of the mode of interaction of thermolysin with a proteinaceous metalloproteinase inhibitor, SMPI, based on a model complex structure and a structural dynamics analysis J. Mol. Biol. 282 1998 435 446
63. G.E. Terp, I.T. Christensen, and F.S. Jorgensen Structural differences of matrix metalloproteinases. Homology modeling and energy minimization of enzyme-substrate complexes J. Biomol. Struct. Dyn. 17 2000 933 946
64. M.M. Thayer, K.M. Flaherty, and D.B. McKay Three-dimensional structure of the elastase of Pseudomonas aeruginosa at 1.5-Å resolution J. Biol. Chem. 266 1991 2864 2871
65. D.E. Tronrud, H.M. Holden, and B.W. Matthews Structures of two thermolysin-inhibitor complexes that differ by a single hydrogen bond Science 235 1987 571 574
66. D.E. Tronrud, A.F. Monzingo, and B.W. Matthews Crystallographic structural analysis of phosphoramidates as inhibitors and transition-state analogs of thermolysin Eur. J. Biochem. 157 1986 261 268
67. A.C. Wallace, R.A. Laskowski, and J.M. Thornton LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions Protein Eng. 8 1995 127 134
68. W. Wang, J. Wang, and P.A. Kollmann What determine the van der Waals coefficient β in the LIE (Linear Interaction Energy) method to estimate binding free energies using molecular dynamics simulations? Proteins: Struct. Funct. Gen. 34 1999 395 402
69. Z.R. Wasserman, and C.N. Hodge Fitting an inhibitor into the active site of thermolysin: a molecular dynamics case study Proteins 24 1996 227 237