Optimizing the Multivalent Binding of the Bacterial Lectin LecA by Glycopeptide Dendrimers for Therapeutic Purposes

Journal of Chemical Information and Modeling

Volumn 56, Issue 6, 2016, Pages 1193-1204

  Bouvier, Benjamin ^a  

^a UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DENDRIMERS; PEPTIDES;

AMINO ACID SEQUENCE; COARSE-GRAINED; FUNCTIONALIZED; LECTIN AFFINITY; MULTIVALENT BINDING; MULTIVALENT LIGANDS; SUGAR-BINDING PROTEIN; THERAPEUTIC COMPOUNDS;

FUNCTIONAL POLYMERS;

ADHESIN; DENDRIMER; GLYCOPEPTIDE; LECA PROTEIN, BACTERIA; PROTEIN BINDING;

AMINO ACID SEQUENCE; CHEMISTRY; DRUG DESIGN; ENZYME ACTIVE SITE; METABOLISM; MOLECULAR DYNAMICS;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; CATALYTIC DOMAIN; DENDRIMERS; DRUG DESIGN; GLYCOPEPTIDES; MOLECULAR DYNAMICS SIMULATION; PROTEIN BINDING;

EID: 84976448216     PISSN: 15499596     EISSN: 1549960X     Source Type: Journal    
DOI: 10.1021/acs.jcim.6b00146     Document Type: Article

References (58)

1. Gabius, H.-J. J.; André, S.; Jiménez-Barbero, J.; Romero, A.; Solís, D. From Lectin Structure to Functional Glycomics: Principles of the Sugar Code Trends Biochem. Sci. 2011, 36, 298-313 10.1016/j.tibs.2011.01.005
2. Pinho, S. S.; Reis, C. A. Glycosylation in Cancer: Mechanisms and Clinical Implications Nat. Rev. Cancer 2015, 15, 540-555 10.1038/nrc3982
3. Paleček, E.; Tkáč, J.; Bartǒsík, M.; Bertók, T. s.; Ostatná, V.; Paleček, J. Electrochemistry of Nonconjugated Proteins and Glycoproteins. Toward Sensors for Biomedicine and Glycomics Chem. Rev. 2015, 115, 2045-2108 10.1021/cr500279h
4. André, S.; Kaltner, H.; Manning, J. C.; Murphy, P. V.; Gabius, H.-J. J. Lectins: Getting Familiar with Translators of the Sugar Code Molecules 2015, 20, 1788-1823 10.3390/molecules20021788
5. Buckeridge, M. S.; de Souza, A. P. Breaking the Glycomic Code of Cell Wall Polysaccharides May Improve Second-Generation Bioenergy Production from Biomass BioEnergy Res. 2014, 7, 1065-1073 10.1007/s12155-014-9460-6
6. Mason, C. P.; Tarr, A. W. Human Lectins and their Roles in Viral Infections Molecules 2015, 20, 2229-2271 10.3390/molecules20022229
7. Jo, E.-K. K. Mycobacterial Interaction with Innate Receptors: TLRs, C-Type Lectins, and NLRs Curr. Opin. Infect. Dis. 2008, 21, 279-286 10.1097/QCO.0b013e3282f88b5d
8. Jiménez Blanco, J. L.; Ortiz Mellet, C.; García Fernández, J. M. Multivalency in Heterogeneous Glycoenvironments: Hetero-Glycoclusters, -Glycopolymers and -Glycoassemblies Chem. Soc. Rev. 2013, 42, 4518-4531 10.1039/C2CS35219B
9. Lundquist, J. J.; Toone, E. J. The Cluster Glycoside Effect Chem. Rev. 2002, 102, 555-578 10.1021/cr000418f
10. Levine, P. M.; Carberry, T. P.; Holub, J. M.; Kirshenbaum, K. Crafting Precise Multivalent Architectures MedChemComm 2013, 4, 493-509 10.1039/c2md20338c
11. Compain, P.; Bodlenner, A. The Multivalent Effect in Glycosidase Inhibition: a New, Rapidly Emerging Topic in Glycoscience ChemBioChem 2014, 15, 1239-1251 10.1002/cbic.201402026
12. Cecioni, S.; Imberty, A.; Vidal, S. Glycomimetics Versus Multivalent Glycoconjugates for the Design of High Affinity Lectin Ligands Chem. Rev. 2015, 115, 525-561 10.1021/cr500303t
13. Kiessling, L. L.; Gestwicki, J. E.; Strong, L. E. Synthetic Multivalent Ligands in the Exploration of Cell-Surface Interactions Curr. Opin. Chem. Biol. 2000, 4, 696-703 10.1016/S1367-5931(00)00153-8
14. Wittmann, V.; Pieters, R. J. Bridging Lectin Binding Sites by Multivalent Carbohydrates Chem. Soc. Rev. 2013, 42, 4492-4503 10.1039/c3cs60089k
15. Bernardi, A. et al. Multivalent Glycoconjugates as Anti-Pathogenic Agents Chem. Soc. Rev. 2013, 42, 4709-4727 10.1039/C2CS35408J
16. Giuliani, A.; Rinaldi, A. C. Beyond Natural Antimicrobial Peptides: Multimeric Peptides and Other Peptidomimetic Approaches Cell. Mol. Life Sci. 2011, 68, 2255-2266 10.1007/s00018-011-0717-3
17. Sommer, P.; Fluxa, V. S.; Darbre, T.; Reymond, J.-L. L. Proteolysis of Peptide Dendrimers ChemBioChem 2009, 10, 1527-1536 10.1002/cbic.200900060
18. Stach, M.; Siriwardena, T. N.; Köhler, T.; van Delden, C.; Darbre, T.; Reymond, J.-L. L. Combining Topology and Sequence Design for the Discovery of Potent Antimicrobial Peptide Dendrimers Against Multidrug-Resistant Pseudomonas Aeruginosa Angew. Chem., Int. Ed. 2014, 53, 12827-12831 10.1002/anie.201409270
19. Ravi, H. K.; Stach, M.; Soares, T. A.; Darbre, T.; Reymond, J.-L. L.; Cascella, M. Electrostatics and Flexibility Drive Membrane Recognition and Early Penetration by the Antimicrobial Peptide Dendrimer Bh1 Chem. Commun. (Cambridge, U. K.) 2013, 49, 8821-8823 10.1039/c3cc44912b
20. Novoa, A.; Eierhoff, T.; Topin, J.; Varrot, A.; Barluenga, S.; Imberty, A.; Römer, W.; Winssinger, N. A LecA Ligand Identified from a Galactoside-Conjugate Array Inhibits Host Cell Invasion by Pseudomonas Aeruginosa Angew. Chem., Int. Ed. 2014, 53, 8885-8889 10.1002/anie.201402831
21. Kadam, R. U.; Bergmann, M.; Hurley, M.; Garg, D.; Cacciarini, M.; Swiderska, M. A.; Nativi, C.; Sattler, M.; Smyth, A. R.; Williams, P.; Cámara, M.; Stocker, A.; Darbre, T.; Reymond, J.-L. L. A Glycopeptide Dendrimer Inhibitor of the Galactose-Specific Lectin LecA and of Pseudomonas Aeruginosa Biofilms Angew. Chem., Int. Ed. 2011, 50, 10631-10635 10.1002/anie.201104342
22. Kilpatrick, D. C. Animal Lectins: a Historical Introduction and Overview Biochim. Biophys. Acta, Gen. Subj. 2002, 1572, 187-197 10.1016/S0304-4165(02)00308-2
23. Mitchell, E.; Houles, C.; Sudakevitz, D.; Wimmerova, M.; Gautier, C.; Pérez, S.; Wu, A. M.; Gilboa-Garber, N.; Imberty, A. Structural Basis for Oligosaccharide-Mediated Adhesion of Pseudomonas Aeruginosa in the Lungs of Cystic Fibrosis Patients Nat. Struct. Biol. 2002, 9, 918-921 10.1038/nsb865
24. Filipe, L. C. S.; Machuqueiro, M.; Baptista, A. M. Unfolding the Conformational Behavior of Peptide Dendrimers: Insights from Molecular Dynamics Simulations J. Am. Chem. Soc. 2011, 133, 5042-5052 10.1021/ja111001v
25. Filipe, L. C.; Machuqueiro, M.; Darbre, T.; Baptista, A. n. M. Unraveling the Conformational Determinants of Peptide Dendrimers Using Molecular Dynamics Simulations Macromolecules 2013, 46, 9427-9436 10.1021/ma401574b
26. Johansson, E. M.; Kolomiets, E.; Rosenau, F.; Jaeger, K.-E. E.; Darbre, T.; Reymond, J.-L. L. Combinatorial Variation of Branching Length and Multivalency in a Large (390625 Member) Glycopeptide Dendrimer Library: Ligands for Fucose-Specific Lectins New J. Chem. 2007, 31, 1291-1299 10.1039/b616051b
27. Fritz, D.; Koschke, K.; Harmandaris, V. A.; van der Vegt, N. F. A.; Kremer, K. Multiscale Modeling of Soft Matter: Scaling of Dynamics Phys. Chem. Chem. Phys. 2011, 13, 10412-10420 10.1039/c1cp20247b
28. Monticelli, L.; Kandasamy, S. K.; Periole, X.; Larson, R. G.; Tieleman, D. P.; Marrink, S.-J. J. The MARTINI Coarse-Grained Force Field: Extension to Proteins J. Chem. Theory Comput. 2008, 4, 819-834 10.1021/ct700324x
29. Marrink, S. J.; Risselada, H. J.; Yefimov, S.; Tieleman, D. P.; de Vries, A. H. The MARTINI Force Field: Coarse Grained Model for Biomolecular Simulations J. Phys. Chem. B 2007, 111, 7812-7824 10.1021/jp071097f
30. Zhao, J.; Zhao, C.; Liang, G.; Zhang, M.; Zheng, J. Engineering Antimicrobial Peptides with Improved Antimicrobial and Hemolytic Activities J. Chem. Inf. Model. 2013, 53, 3280-3296 10.1021/ci400477e
31. Zhao, X.; Yu, H.; Yang, L.; Li, Q.; Huang, X. Simulating the Antimicrobial Mechanism of Human β-Defensin-3 with Coarse-Grained Molecular Dynamics J. Biomol. Struct. Dyn. 2015, 33, 2522-2529 10.1080/07391102.2014.1002424
32. Horn, J. N.; Sengillo, J. D.; Lin, D.; Romo, T. D.; Grossfield, A. Characterization of a Potent Antimicrobial Lipopeptide via Coarse-Grained Molecular Dynamics Biochim. Biophys. Acta, Biomembr. 2012, 1818, 212-218 10.1016/j.bbamem.2011.07.025
33. Cohen, F. E.; Sternberg, M. J. On the Prediction of Protein Structure: the Significance of the Root-Mean-Square Deviation J. Mol. Biol. 1980, 138, 321-333 10.1016/0022-2836(80)90289-2
34. Yazici, B.; Yolacan, S. A Comparison of Various Tests of Normality J. Statist. Comput. Simulation 2007, 77, 175-183 10.1080/10629360600678310
35. Frey, B. J.; Dueck, D. Clustering by passing Messages Between Data Points Science 2007, 315, 972-976 10.1126/science.1136800
36. Schneider, T. D.; Stephens, R. M. Sequence Logos: a New Way to Display Consensus Sequences Nucleic Acids Res. 1990, 18, 6097-6100 10.1093/nar/18.20.6097
37. Pronk, S.; Páll, S.; Schulz, R.; Larsson, P.; Bjelkmar, P.; Apostolov, R.; Shirts, M. R.; Smith, J. C.; Kasson, P. M.; van der Spoel, D.; Hess, B.; Lindahl, E. GROMACS 4.5: a High-Throughput and Highly Parallel Open Source Molecular Simulation Toolkit Bioinformatics 2013, 29, 845-854 10.1093/bioinformatics/btt055
38. Pall, S.; Abraham, M. J.; Kutzner, C.; Hess, B.; Lindahl, E. Solving Software Challenges for Exascale; Springer: Cham, Switzerland, 2014; pp 3-27.
39. López, C. A.; Rzepiela, A. J.; De Vries, A. H.; Dijkhuizen, L.; Hünenberger, P. H.; Marrink, S. J. Martini Coarse-Grained Force Field: Extension to Carbohydrates J. Chem. Theory Comput. 2009, 5, 3195-3210 10.1021/ct900313w
40. Fuhrmans, M.; Sanders, B. P.; Marrink, S.-J.; de Vries, A. H. Effects of Bundling on the Properties of the SPC Water Model Theor. Chem. Acc. 2010, 125, 335-344 10.1007/s00214-009-0590-4
41. Cioci, G.; Mitchell, E. P.; Gautier, C.; Wimmerová, M.; Sudakevitz, D.; Pérez, S.; Gilboa-Garber, N.; Imberty, A. Structural Basis of Calcium and Galactose Recognition by the Lectin PA-IL of Pseudomonas Aeruginosa FEBS Lett. 2003, 555, 297-301 10.1016/S0014-5793(03)01249-3
42. Van Der Walt, S.; Colbert, S. C.; Varoquaux, G. The NumPy Array: a Structure for Efficient Numerical Computation Comput. Sci. Eng. 2011, 13, 22-30 10.1109/MCSE.2011.37
43. Pedregosa, F.; Varoquaux, G.; Gramfort, A.; Michel, V.; Thirion, B.; Grisel, O.; Blondel, M.; Prettenhofer, P.; Weiss, R.; Dubourg, V. Scikit-learn: Machine Learning in Python J. Mach. Learn. Res. 2011, 12, 2825-2830
44. Humphrey, W.; Dalke, A.; Schulten, K. VMD: Visual Molecular Dynamics J. Mol. Graphics 1996, 14, 33-38 10.1016/0263-7855(96)00018-5
45. Crooks, G. E.; Hon, G.; Chandonia, J.-M. M.; Brenner, S. E. WebLogo: a Sequence Logo Generator Genome Res. 2004, 14, 1188-1190 10.1101/gr.849004
46. Huerta-Cepas, J.; Dopazo, J.; Gabaldón, T. ETE: a Python Environment for Tree Exploration BMC Bioinf. 2010, 11, 24-30 10.1186/1471-2105-11-24
47. Hunter, J. D. Matplotlib: a 2D Graphics Environment Comput. Sci. Eng. 2007, 9, 90-95 10.1109/MCSE.2007.55
48. Kolomiets, E.; Swiderska, M. A.; Kadam, R. U.; Johansson, E. M. V.; Jaeger, K.-E. E.; Darbre, T.; Reymond, J.-L. L. Glycopeptide Dendrimers with High Affinity for the Fucose-Binding Lectin LecB from Pseudomonas Aeruginosa ChemMedChem 2009, 4, 562-569 10.1002/cmdc.200800380
49. Zamyatnin, A. A. Protein Volume in Solution Prog. Biophys. Mol. Biol. 1972, 24, 107-123 10.1016/0079-6107(72)90005-3
50. Kyte, J.; Doolittle, R. F. A Simple Method for Displaying the Hydropathic Character of a Protein J. Mol. Biol. 1982, 157, 105-132 10.1016/0022-2836(82)90515-0
51. Visini, R. et al. Structural Insight into Multivalent Galactoside Binding to Pseudomonas Aeruginosa Lectin LecA ACS Chem. Biol. 2015, 10, 2455-2462 10.1021/acschembio.5b00302
52. Sicard, D.; Chevolot, Y.; Souteyrand, E.; Imberty, A.; Vidal, S.; Phaner-Goutorbe, M. Molecular Arrangement Between Multivalent Glycocluster and Pseudomonas Aeruginosa LecA (PA-IL) by Atomic Force Microscopy: Influence of the Glycocluster Concentration J. Mol. Recognit. 2013, 26, 694-699 10.1002/jmr.2333
53. Stark, A. C.; Andrews, C. T.; Elcock, A. H. Toward Optimized Potential Functions for Protein-Protein Interactions in Aqueous Solutions: Osmotic Second Virial Coefficient Calculations Using the MARTINI Coarse-Grained Force Field J. Chem. Theory Comput. 2013, 9, 4176-4185 10.1021/ct400008p
54. Bohacek, R. S.; McMartin, C.; Guida, W. C. The Art and Practice of Structure-Based Drug Design: a Molecular Modeling Perspective Med. Res. Rev. 1996, 16, 3-50 10.1002/(SICI)1098-1128(199601)16:1<3::AID-MED1>3.0.CO;2-6
55. Bergmann, M.; Michaud, G.; Visini, R.; Jin, X.; Gillon, E.; Stocker, A.; Imberty, A.; Darbre, T.; Reymond, J.-L. L. Multivalency Effects on Pseudomonas Aeruginosa Biofilm Inhibition and Dispersal by Glycopeptide Dendrimers Targeting Lectin LecA Org. Biomol. Chem. 2016, 14, 138-148 10.1039/C5OB01682G
56. Gestwicki, J. E.; Strong, L. E.; Kiessling, L. L. Tuning Chemotactic Responses with Synthetic Multivalent Ligands Chem. Biol. 2000, 7, 583-591 10.1016/S1074-5521(00)00002-8
57. Mullen, D. G.; Fang, M.; Desai, A.; Baker, J. R.; Orr, B. G.; Banaszak Holl, M. M. A Quantitative Assessment of Nanoparticle-Ligand Distributions: Implications for Targeted Drug and Imaging Delivery in Dendrimer Conjugates ACS Nano 2010, 4, 657-670 10.1021/nn900999c
58. Schreiber, G.; Haran, G.; Zhou, H.-X. X. Fundamental Aspects of Protein-Protein Association Kinetics Chem. Rev. 2009, 109, 839-860 10.1021/cr800373w