A biophysical study with carbohydrate derivatives explains the molecular basis of monosaccharide selectivity of the Pseudomonas aeruginosa lectin lecB

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Sommer, Roman ^a,b   Exner, Thomas E ^b,c   Titz, Alexer ^a,b  

^a SAARLAND UNIVERSITY   (Germany)

^b UNIVERSITY OF KONSTANZ   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE DERIVATIVE; LECB PROTEIN; LECTIN; UNCLASSIFIED DRUG; CARBOHYDRATE; LECB PROTEIN, PSEUDOMONAS AERUGINOSA; MONOSACCHARIDE;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPETITIVE BINDING ASSAY; COMPLEX FORMATION; CONTROLLED STUDY; HYDROGEN BOND; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PROTEIN BINDING; QUANTITATIVE ANALYSIS; THERMODYNAMICS; BINDING COMPETITION; BIOFILM; BIOPHYSICS; CALORIMETRY; CHEMISTRY; LIQUID CHROMATOGRAPHY; NUCLEAR MAGNETIC RESONANCE; PSEUDOMONAS AERUGINOSA;

PSEUDOMONAS AERUGINOSA;

BINDING, COMPETITIVE; BIOFILMS; BIOPHYSICS; CALORIMETRY; CARBOHYDRATES; CHROMATOGRAPHY, LIQUID; LECTINS; MONOSACCHARIDES; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PSEUDOMONAS AERUGINOSA;

EID: 84912033992     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112822     Document Type: Article

References (56)

1. Cross A, Allen JR, Burke J, Ducel G, Harris A, et al. (1983) Nosocomial infections due to Pseudomonas aeruginosa: review of recent trends. Clin Infect Dis 5 Suppl 5: S837-45.
2. Peleg AY, Hooper DC (2010) Hospital-Acquired Infections Due to Gram-Negative Bacteria. New Engl J Med 362: 1804-1813.
3. Tümmler B, Kiewitz C (1999) Cystic fibrosis: an inherited susceptibility to bacterial respiratory infections. Mol Med Today 5: 351-8.
4. Davies D (2003) Understanding biofilm resistance to antibacterial agents. Nat Rev Drug Discov 2: 114-22.
5. Poole K (2011) Pseudomonas aeruginosa: resistance to the max. Front Microbiol 2: 65.
6. Sommer R, Joachim I, Wagner S, Titz A (2013) New approaches to control infections: anti-biofilm strategies against gram-negative bacteria. CHIMIA 67: 286-90.
7. Tielker D, Hacker S, Loris R, Strathmann M, Wingender J, et al. (2005) Pseudomonas aeruginosa lectin LecB is located in the outer membrane and is involved in biofilm formation. Microbiology 151: 1313-23.
8. Johansson EMV, Crusz SA, Kolomiets E, Buts L, Kadam RU, et al. (2008) Inhibition and dispersion of Pseudomonas aeruginosa biofilms by glycopeptide dendrimers targeting the fucose-specific lectin LecB. Chem Biol 15: 1249-57.
9. Loris R, Tielker D, Jaeger K, Wyns L (2003) Structural basis of carbohydrate recognition by the lectin LecB from Pseudomonas aeruginosa. J Mol Biol 331: 861-70.
10. Mitchell E, Houles C, Sudakevitz D, Wimmerova M, Gautier C, et al. (2002) Structural basis for oligosaccharide-mediated adhesion of Pseudomonas aeruginosa in the lungs of cystic fibrosis patients. Nat Struct Biol 9: 918-21.
11. Sabin C, Mitchell EP, Pokorná M, Gautier C, Utille J, et al. (2006) Binding of different monosaccharides by lectin PA-IIL from Pseudomonas aeruginosa: thermodynamics data correlated with X-ray structures. FEBS Lett 580: 982-7.
12. Gilboa-Garber N (1982) Pseudomonas aeruginosa lectins. Methods Enzymol 83: 378-385.
13. Titz A. (2014) Carbohydrate-Based Anti-Virulence Compounds Against Chronic Pseudomonas aeruginosa Infections with a Focus on Small Molecules. In: Topics in Medicinal Chemistry Springer Berlin Heidelberg. p. doi: 10.1007/7355-2014-44.
14. Bernardi A, Jiménez-Barbero J, Casnati A, De Castro C, Darbre T, et al. (2012) Multivalent glycoconjugates as anti-pathogenic agents. Chem Soc Rev 42: 4709-4727.
15. Hauck D, Joachim I, Frommeyer B, Varrot A, Philipp B, et al. (2013) Discovery of Two Classes of Potent Glycomimetic Inhibitors of Pseudomonas aeruginosa LecB with Distinct Binding Modes. ACS Chem Biol 8: 1775-84.
16. Gottlieb HE, Kotlyar V, Nudelman A (1997) NMR Chemical Shifts of Common Laboratory Solvents as Trace Impurities. J Org Chem 62: 7512-7515.
17. Bordoni A, Lima C, Mariño K, de Lederkremer RM, Marino C (2008) Facile synthesis of methyl alphaand beta-D-[6-(3)H]galactofuranosides from D-galacturonic acid. Substrates for the detection of galactofuranosidases. Carbohydr Res 343: 1863-9.
18. Kondo H, Aoki S, Ichikawa Y, Halcomb RL, Ritzen H, et al. (1994) Glycosyl Phosphites as Glycosylation Reagents: Scope and Mechanism. J Org Chem 59: 864-877.
19. Guo Z, Hui Y (1996) A New Strategy for the Stereoselective Syntheses of C-Glycosyl Compounds of b- Pentapyranoses. Synth Commun 26: 2067-2073.
20. Phiasivongsa P, Samoshin V, Gross P (2003) Henry condensations with 4,6-O-benzylidenylated and non-protected D-glucose and L-fucose via DBU-catalysis. Tetrahedron Lett 44: 5495-5498.
21. Nishi Y, Tanimoto T (2009) Preparation and characterization of branched beta-cyclodextrins having alpha-L-fucopyranose and a study of their functions. Biosci Biotechnol Biochem 73: 562-9.
22. Daniellou R, Le Narvor C (2005) Synthesis of GDP-Fucose on a Soluble Support: A Donor Substrate for the Fucosyltransferases. Adv Synth Catal 347: 1863-1868.
23. Carpintero M, Bastida A, García-Junceda E, Jiménez-Barbero J, Fernández-Mayoralas A (2001) Synthesis of Carba- and C-Fucopyranosides and Their Evaluation as a-Fucosidase Inhibitors 2 Analysis of an Unusual Conformation Adopted by an Amino-C-fucopyranoside. Eur J Org Chem 2001: 4127-4135.
24. Wilkins MR, Gasteiger E, Bairoch A, Sanchez JC, Williams KL, et al. (1999) Protein identification and analysis tools in the ExPASy server. Methods Mol Biol 112: 531-52.
25. Turnbull WB, Precious BL, Homans SW (2004) Dissecting the cholera toxin-ganglioside GM1 interaction by isothermal titration calorimetry. J Am Chem Soc 126: 1047-54.
26. Sigurskjold BW (2000) Exact analysis of competition ligand binding by displacement isothermal titration calorimetry. Anal Biochem 277: 260-6.
27. Case DA, Darden TA, Cheatham ITE, Simmerling CL, Wang J, et al. (2012) AMBER 12, Computer Program. University of California, San Francisco.
28. Darden T, York D, Pedersen L (1993) Particle mesh Ewald: An N [center-dot] log(N) method for Ewald sums in large systems. J Chem Phys 98: 10089-10092.
29. Ryckaert J, Ciccotti G, Berendsen HJC (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23: 327-341.
30. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, et al. (1995) A Second Generation Force Field for the Simulation of Proteins, Nucleic Acids, and Organic Molecules. J Am Chem Soc 117: 5179-5197.
31. Li P, Roberts BP, Chakravorty DK, Merz KM Jr (2013) Rational Design of Particle Mesh Ewald Compatible Lennard-Jones Parameters for +2 Metal Cations in Explicit Solvent. J Chem Theory Comput 9: 2733-2748.
32. Wang J, Wang W, Kollman PA, Case DA (2006) Automatic atom type and bond type perception in molecular mechanical calculations. J Mol Graph Model 25: 247-60.
33. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, et al. (2004) Gaussian 03 (Revision C.2). Wallingford CT, Gaussian, Inc.
34. Singh UC, Kollman PA (1984) An approach to computing electrostatic charges for molecules. J Comput Chem 5: 129-145.
35. Wang J, Wolf RM, Caldwell JW, Kollman PA, Case DA (2004) Development and testing of a general amber force field. J Comput Chem 25: 1157-74.
36. Horn HW, Swope WC, Pitera JW, Madura JD, Dick TJ, et al. (2004) Development of an improved foursite water model for biomolecular simulations: TIP4P-Ew. J Chem Phys 120: 9665-78.
37. Kirkwood JG (1935) Statistical Mechanics of Fluid Mixtures. J Chem Phys 3: 300-313.
38. Steinbrecher T, Mobley DL, Case DA (2007) Nonlinear scaling schemes for Lennard-Jones interactions in free energy calculations. J Chem Phys 127: 214108.
39. Simonson T (1993) Free energy of particle insertion. Mol Phys 80: 441-447.
40. Carchon G, Chré tien F, Delannoy P, Verbert A, Chapleur Y (2001) Synthesis of a non-charged analogue of guanosyldiphosphofucose. Tetrahedron Lett 42: 8821-8824.
41. Bihovsky R, Selick C, Giusti I (1988) Synthesis of C-glucosides by reactions of glucosyl halides with organocuprates. J Org Chem 53: 4026-4031.
42. Langer AW. (1974) Some Mechanistic Aspects of N-Chelated Organolithium Catalysis. In: Langer AW, ed., Advances in Chemistry, Polyamine-Chelated Alkali Metal Compounds Vol. 130. American Chemical Society. p. 1-22.
43. Polakova M, Petrusova M, Barath M, Petrus L (2005) Denitration of primary nitromethyl groups in Cglycopyranosylnitromethanes via C-glycopyranosylmethanal diethyl dithioacetals. Chem Pap 59: 289-290.
44. Mitchell EP, Sabin C, Snajdrová L, Pokorná M, Perret S, et al. (2005) High affinity fucose binding of Pseudomonas aeruginosa lectin PA-IIL: 1.0 A resolution crystal structure of the complex combined with thermodynamics and computational chemistry approaches. Proteins 58: 735-46.
45. Wu AM, Gong Y, Li C, Gilboa-Garber N (2010) Duality of the carbohydrate-recognition system of Pseudomonas aeruginosa-II lectin (PA-IIL). FEBS Lett 584: 2371-5.
46. Kollman PA, Massova I, Reyes C, Kuhn B, Huo S, et al. (2000) Calculating structures and free energies of complex molecules: combining molecular mechanics and continuum models. Acc Chem Res 33: 889-97.
47. Srinivasan J, Cheatham TE, Cieplak P, Kollman PA, Case DA (1998) Continuum Solvent Studies of the Stability of DNA, RNA, and Phosphoramidate2DNA Helices. J Am Chem Soc 120: 9401-9409.
48. Homeyer N, Gohlke H (2012) Free Energy Calculations by the Molecular Mechanics Poisson2Boltzmann Surface Area Method. Molecular Informatics 31: 114-122.
49. Nguyen CN, Young TK, Gilson MK (2012) Grid inhomogeneous solvation theory: hydration structure and thermodynamics of the miniature receptor cucurbit [7] uril. J Chem Phys 137: 044101.
50. Lazaridis T (1998) Inhomogeneous Fluid Approach to Solvation Thermodynamics. 1. Theory. J Phys Chem B 102: 3531-3541.
51. Roe DR, Cheatham TE (2013) PTRAJ and CPPTRAJ: Software for Processing and Analysis of Molecular Dynamics Trajectory Data. J Chem Theory Comput 9: 3084-3095.
52. Mishra NK, Kríz Z, Wimmerová M, Koca J (2010) Recognition of selected monosaccharides by Pseudomonas aeruginosa Lectin II analyzed by molecular dynamics and free energy calculations. Carbohydr Res 345: 1432-41.
53. Sudakevitz D, Kostlánová N, Blatman-Jan G, Mitchell EP, Lerrer B, et al. (2004) A new Ralstonia solanacearum high-affinity mannose-binding lectin RS-IIL structurally resembling the Pseudomonas aeruginosa fucose-specific lectin PA-IIL. Mol Microbiol 52: 691-700.
54. Lameignere E, Malinovská L, Sláviková M, Duchaud E, Mitchell EP, et al. (2008) Structural basis for mannose recognition by a lectin from opportunistic bacteria Burkholderia cenocepacia. Biochem J 411: 307-18.
55. Adam J, Pokorná M, Sabin C, Mitchell EP, Imberty A, et al. (2007) Engineering of PA-IIL lectin from Pseudomonas aeruginosa - Unravelling the role of the specificity loop for sugar preference. BMC Struct Biol 7: 36.
56. Perret S, Sabin C, Dumon C, Pokorná M, Gautier C, et al. (2005) Structural basis for the interaction between human milk oligosaccharides and the bacterial lectin PA-IIL of Pseudomonas aeruginosa. Biochem. J. 389: 325-332.